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    Through the doors of perception to function in arbuscular mycorrhizal symbioses. Bucher Marcel,Hause Bettina,Krajinski Franziska,Küster Helge The New phytologist The formation of an arbuscular mycorrhizal (AM) symbiosis is initiated by the bidirectional exchange of diffusible molecules. While strigolactone hormones, secreted from plant roots,stimulate hyphal branching and fungal metabolism, fungal short-chain chitin oligomers as well assulfated and nonsulfated lipochitooligosaccharides (s/nsMyc-LCOs) elicit pre-symbiosis responses in the host. Fungal LCO signals are structurally related to rhizobial Nod-factor LCOs. Genome-wide expression studies demonstrated that defined sets of genes were induced by Nod-, sMyc- and nsMyc-LCOs, indicating LCO-specific perception in the pre-symbiosis phase. During hyphopodium formation and the subsequent root colonization, cross-talk between plant roots and AM fungi also involves phytohormones. Notably, gibberellins control arbuscule formation via DELLA proteins, which themselves serve as positive regulators of arbuscule formation. The establishment of arbuscules is accompanied by a substantial transcriptional and post-transcriptional reprogramming of host roots, ultimately defining the unique protein composition of arbuscule-containing cells. Based on cellular expression profiles, key check points of AM development as well as candidate genes encoding transcriptional regulators and regulatory microRNAs were identified. Detailed functional analyses of promoters specified short motifs sufficient for cell-autonomous gene regulation in cells harboring arbuscules, and suggested simultaneous, multi-level regulation of the mycorrhizal phosphate uptake pathway by integrating AM symbiosis and phosphate starvation response signaling. 10.1111/nph.12862
    Arbuscular mycorrhizal dialogues: do you speak 'plantish' or 'fungish'? Bonfante Paola,Genre Andrea Trends in plant science Plants rely on their associated microbiota for crucial physiological activities; realization of this interaction drives research to understand inter-domain communication. This opinion article focuses on the arbuscular mycorrhizal (AM) symbiosis, which involves the Glomeromycota, fungi that can form a symbiosis with most plants. Here we propose the hypothesis that the molecules involved in inter-kingdom symbiotic signaling, such as strigolactones, cutin monomers, and chitin-related molecules, also have key roles in development, originally unrelated to symbiosis. Thus, the symbiotic role of these molecules relies on the co-evolved capacity of the AM partners to perceive and interpret them as symbiotic signals. 10.1016/j.tplants.2014.12.002
    Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. Walder Florian,Brulé Daphnée,Koegel Sally,Wiemken Andres,Boller Thomas,Courty Pierre-Emmanuel The New phytologist In a preceding microcosm study, we found huge differences in phosphorus (P) acquisition in sorghum (Sorghum bicolor) and flax (Linum usitatissimum) sharing a common mycorrhizal network (CMN). Is the transcriptional regulation of arbuscular mycorrhizal (AM)-induced inorganic orthophosphate (Pi) transporters responsible for these differences? We characterized and analyzed the expression of Pi transporters of the Pht1 family in both plant species, and identified two new AM-inducible Pi transporters in flax. Mycorrhizal Pi acquisition was strongly affected by the combination of plant and AM fungal species. A corresponding change in the expression of two AM-inducible Pht1 transporters was noticed in both plants (SbPT9, SbPT10, LuPT5 and LuPT8), but the effect was very weak. Overall, the expression level of these genes did not explain why flax took up more Pi from the CMN than did sorghum. The post-transcriptional regulation of the transporters and their biochemical properties may be more important for their function than the fine-tuning of their gene expression. 10.1111/nph.13292
    Suppression of Arbuscule Degeneration in Medicago truncatula phosphate transporter4 Mutants is Dependent on the Ammonium Transporter 2 Family Protein AMT2;3. Breuillin-Sessoms Florence,Floss Daniela S,Gomez S Karen,Pumplin Nathan,Ding Yi,Levesque-Tremblay Veronique,Noar Roslyn D,Daniels Dierdra A,Bravo Armando,Eaglesham James B,Benedito Vagner A,Udvardi Michael K,Harrison Maria J The Plant cell During arbuscular mycorrhizal (AM) symbiosis, the plant gains access to phosphate (Pi) and nitrogen delivered by its fungal symbiont. Transfer of mineral nutrients occurs at the interface between branched hyphae called arbuscules and root cortical cells. In Medicago truncatula, a Pi transporter, PT4, is required for symbiotic Pi transport, and in pt4, symbiotic Pi transport fails, arbuscules degenerate prematurely, and the symbiosis is not maintained. Premature arbuscule degeneration (PAD) is suppressed when pt4 mutants are nitrogen-deprived, possibly the result of compensation by PT8, a second AM-induced Pi transporter. However, PAD is also suppressed in nitrogen-starved pt4 pt8 double mutants, negating this hypothesis and furthermore indicating that in this condition, neither of these symbiotic Pi transporters is required for symbiosis. In M. truncatula, three AMT2 family ammonium transporters are induced during AM symbiosis. To test the hypothesis that suppression of PAD involves AMT2 transporters, we analyzed double and triple Pi and ammonium transporter mutants. ATM2;3 but not AMT2;4 was required for suppression of PAD in pt4, while AMT2;4, but not AMT2;3, complemented growth of a yeast ammonium transporter mutant. In summary, arbuscule life span is influenced by PT4 and ATM2;3, and their relative importance varies with the nitrogen status of the plant. 10.1105/tpc.114.131144
    Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Gutjahr Caroline,Sawers Ruairidh J H,Marti Guillaume,Andrés-Hernández Liliana,Yang Shu-Yi,Casieri Leonardo,Angliker Herbert,Oakeley Edward J,Wolfender Jean-Luc,Abreu-Goodger Cei,Paszkowski Uta Proceedings of the National Academy of Sciences of the United States of America Root systems consist of different root types (RTs) with distinct developmental and functional characteristics. RTs may be individually reprogrammed in response to their microenvironment to maximize adaptive plasticity. Molecular understanding of such specific remodeling--although crucial for crop improvement--is limited. Here, RT-specific transcriptomes of adult rice crown, large and fine lateral roots were assessed, revealing molecular evidence for functional diversity among individual RTs. Of the three rice RTs, crown roots displayed a significant enrichment of transcripts associated with phytohormones and secondary cell wall (SCW) metabolism, whereas lateral RTs showed a greater accumulation of transcripts related to mineral transport. In nature, arbuscular mycorrhizal (AM) symbiosis represents the default state of most root systems and is known to modify root system architecture. Rice RTs become heterogeneously colonized by AM fungi, with large laterals preferentially entering into the association. However, RT-specific transcriptional responses to AM symbiosis were quantitatively most pronounced for crown roots despite their modest physical engagement in the interaction. Furthermore, colonized crown roots adopted an expression profile more related to mycorrhizal large lateral than to noncolonized crown roots, suggesting a fundamental reprogramming of crown root character. Among these changes, a significant reduction in SCW transcripts was observed that was correlated with an alteration of SCW composition as determined by mass spectrometry. The combined change in SCW, hormone- and transport-related transcript profiles across the RTs indicates a previously overlooked switch of functional relationships among RTs during AM symbiosis, with a potential impact on root system architecture and functioning. 10.1073/pnas.1504142112
    Difference in Striga-susceptibility is reflected in strigolactone secretion profile, but not in compatibility and host preference in arbuscular mycorrhizal symbiosis in two maize cultivars. Yoneyama Kaori,Arakawa Ryota,Ishimoto Keiko,Kim Hyun Il,Kisugi Takaya,Xie Xiaonan,Nomura Takahito,Kanampiu Fred,Yokota Takao,Ezawa Tatsuhiro,Yoneyama Koichi The New phytologist Strigolactones released from plant roots trigger both seed germination of parasitic weeds such as Striga spp. and hyphal branching of the symbionts arbuscular mycorrhizal (AM) fungi. Generally, strigolactone composition in exudates is quantitatively and qualitatively different among plants, which may be involved in susceptibility and host specificity in the parasite-plant interactions. We hypothesized that difference in strigolactone composition would have a significant impact on compatibility and host specificity/preference in AM symbiosis. Strigolactones in root exudates of Striga-susceptible (Pioneer 3253) and -resistant (KST 94) maize (Zea mays) cultivars were characterized by LC-MS/MS combined with germination assay using Striga hermonthica seeds. Levels of colonization and community compositions of AM fungi in the two cultivars were investigated in field and glasshouse experiments. 5-Deoxystrigol was exuded exclusively by the susceptible cultivar, while the resistant cultivar mainly exuded sorgomol. Despite the distinctive difference in strigolactone composition, the levels of AM colonization and the community compositions were not different between the cultivars. The present study demonstrated that the difference in strigolactone composition has no appreciable impact on AM symbiosis, at least in the two maize cultivars, and further suggests that the traits involved in Striga-resistance are not necessarily accompanied by reduction in compatibility to AM fungi. 10.1111/nph.13375
    EXO70I Is Required for Development of a Sub-domain of the Periarbuscular Membrane during Arbuscular Mycorrhizal Symbiosis. Zhang Xinchun,Pumplin Nathan,Ivanov Sergey,Harrison Maria J Current biology : CB In eukaryotic cells, polarized secretion mediated by exocytotic fusion of membrane vesicles with the plasma membrane is essential for spatially restricted expansion of the plasma membrane and for the delivery of molecules to specific locations at the membrane and/or cell surface. The EXOCYST complex is central to this process, and in yeast, regulation of the EXO70 subunit influences exocytosis and cargo specificity. In contrast to yeast and mammalian cells, plants have upwards of 23 EXO70 genes with largely unknown roles. During arbuscular mycorrhizal (AM) symbiosis, deposition of the plant periarbuscular membrane (PAM) around the fungal arbuscule creates an intracellular membrane interface between the symbionts. The PAM has two major membrane sub-domains, and symbiosis-specific transporter proteins are localized in the branch domain. Currently, the mechanisms and cellular machinery involved in biogenesis of the PAM are largely unknown. Here, we identify an EXO70I protein present exclusively in plants forming AM symbiosis. Medicago truncatula exo70i mutants are unable to support normal arbuscule development, and incorporation of two PAM-resident ABC transporters, STR and STR2, is limited. During arbuscule branching, EXO70I is located in spatially restricted zones adjacent to the PAM around the arbuscule hyphal tips where it interacts with Vapyrin, a plant-specific protein required for arbuscule development. We conclude that EXO70I provides a specific exocytotic capacity necessary for development of the main functional sub-domain of the PAM. Furthermore, in contrast to other eukaryotes, plant EXO70s have evolved distinct specificities and interaction partners to fulfill their specialized secretory requirements. 10.1016/j.cub.2015.06.075
    Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. Garcia Kevin,Delaux Pierre-Marc,Cope Kevin R,Ané Jean-Michel The New phytologist Ectomycorrhizal (ECM) symbioses are among the most widespread associations between roots of woody plants and soil fungi in forest ecosystems. These associations contribute significantly to the sustainability and sustainagility of these ecosystems through nutrient cycling and carbon sequestration. Unfortunately, the molecular mechanisms controlling the mutual recognition between both partners are still poorly understood. Elegant work has demonstrated that effector proteins from ECM and arbuscular mycorrhizal (AM) fungi regulate host defenses by manipulating plant hormonal pathways. In parallel, genetic and evolutionary studies in legumes showed that a 'common symbiosis pathway' is required for the establishment of the ancient AM symbiosis and has been recruited for the rhizobia-legume association. Given that genes of this pathway are present in many angiosperm trees that develop ectomycorrhizas, we propose their potential involvement in some but not all ECM associations. The maintenance of a successful long-term relationship seems strongly regulated by resource allocation between symbiotic partners, suggesting that nutrients themselves may serve as signals. This review summarizes our current knowledge on the early and late signal exchanges between woody plants and ECM fungi, and we suggest future directions for decoding the molecular basis of the underground dance between trees and their favorite fungal partners. 10.1111/nph.13423
    Combined genetic and transcriptomic analysis reveals three major signalling pathways activated by Myc-LCOs in Medicago truncatula. Camps Céline,Jardinaud Marie-Françoise,Rengel David,Carrère Sébastien,Hervé Christine,Debellé Frédéric,Gamas Pascal,Bensmihen Sandra,Gough Clare The New phytologist Myc-LCOs are newly identified symbiotic signals produced by arbuscular mycorrhizal (AM) fungi. Like rhizobial Nod factors, they are lipo-chitooligosaccharides that activate the common symbiotic signalling pathway (CSSP) in plants. To increase our limited understanding of the roles of Myc-LCOs we aimed to analyse Myc-LCO-induced transcriptional changes and their genetic control. Whole genome RNA sequencing (RNA-seq) was performed on roots of Medicago truncatula wild-type plants, and dmi3 and nsp1 symbiotic mutants affected in nodulation and mycorrhizal signalling. Plants were treated separately with the two major types of Myc-LCOs, sulphated and nonsulphated. Generalized linear model analysis identified 2201 differentially expressed genes and classified them according to genotype and/or treatment effects. Three genetic pathways for Myc-LCO-regulation of transcriptomic reprogramming were highlighted: DMI3- and NSP1-dependent; DMI3-dependent and NSP1-independent; and DMI3- and NSP1-independent. Comprehensive analysis revealed overlaps with previous AM studies, and highlighted certain functions, especially signalling components and transcription factors. These data provide new insights into mycorrhizal signalling mechanisms, supporting a role for NSP1, and specialisation for NSP1-dependent and -independent pathways downstream of DMI3. Our data also indicate significant Myc-LCO-activated signalling upstream of DMI3 and/or parallel to the CSSP and some constitutive activity of the CSSP. 10.1111/nph.13427
    Rice responds to endophytic colonization which is independent of the common symbiotic signaling pathway. Chen Xi,Miché Lucie,Sachs Sabrina,Wang Qi,Buschart Anna,Yang Haiyuan,Vera Cruz Casiana M,Hurek Thomas,Reinhold-Hurek Barbara The New phytologist As molecular interactions of plants with N2 -fixing endophytes are largely uncharacterized, we investigated whether the common signaling pathway (CSP) shared by root nodule symbioses (RNS) and arbuscular mycorrhizal (AM) symbioses may have been recruited for the endophytic Azoarcus sp.-rice (Oryza sativa) interaction, and combined this investigation with global approaches to characterize rice root responses to endophytic colonization. Putative homologs of genes required for the CSP were analyzed for their putative role in endophytic colonization. Proteomic and suppressive subtractive hybridization (SSH) approaches were also applied, and a comparison of defense-related processes was carried out by setting up a pathosystem for flooded roots with Xanthomonas oryzae pv. oryzae strain PXO99 (Xoo). All tested genes were expressed in rice roots seedlings but not induced upon Azoarcus sp. inoculation, and the oscyclops and oscastor mutants were not impaired in endophytic colonization. Global approaches highlighted changes in rice metabolic activity and Ca(2+) -dependent signaling in roots colonized by endophytes, including some stress proteins. Marker genes for defense responses were induced to a lesser extent by the endophytes than by the pathogen, indicating a more compatible interaction. Our results thus suggest that rice roots respond to endophytic colonization by inducing metabolic shifts and signaling events, for which the CSP is not essential. 10.1111/nph.13458
    Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Walder Florian,van der Heijden Marcel G A Nature plants Arbuscular mycorrhizal (AM) fungi are one of the most important groups of plant symbionts. These fungi provide mineral nutrients to plants in exchange for carbon. Although substantial amounts of resources are exchanged, the factors that regulate trade in the AM symbiosis are poorly understood. Recent evidence for the reciprocally regulated exchange of resources by AM fungi and plants has led to the suggestion that these symbioses operate according to biological market dynamics, in which interactions are viewed from an economic perspective, and the most beneficial partners are favoured. Here we present five arguments that challenge the importance of reciprocally regulated exchange, and thereby market dynamics, for resource exchange in the AM symbiosis, and suggest that such reciprocity is only found in a subset of symbionts, under specific conditions. We instead propose that resource exchange in the AM symbiosis is determined by competition for surplus resources, functional diversity and sink strength. 10.1038/nplants.2015.159
    A symbiosis-dedicated SYNTAXIN OF PLANTS 13II isoform controls the formation of a stable host-microbe interface in symbiosis. Huisman Rik,Hontelez Jan,Mysore Kirankumar S,Wen Jiangqi,Bisseling Ton,Limpens Erik The New phytologist Arbuscular mycorrhizal (AM) fungi and rhizobium bacteria are accommodated in specialized membrane compartments that form a host-microbe interface. To better understand how these interfaces are made, we studied the regulation of exocytosis during interface formation. We used a phylogenetic approach to identify target soluble N-ethylmaleimide-sensitive factor-attachment protein receptors (t-SNAREs) that are dedicated to symbiosis and used cell-specific expression analysis together with protein localization to identify t-SNAREs that are present on the host-microbe interface in Medicago truncatula. We investigated the role of these t-SNAREs during the formation of a host-microbe interface. We showed that multiple syntaxins are present on the peri-arbuscular membrane. From these, we identified SYNTAXIN OF PLANTS 13II (SYP13II) as a t-SNARE that is essential for the formation of a stable symbiotic interface in both AM and rhizobium symbiosis. In most dicot plants, the SYP13II transcript is alternatively spliced, resulting in two isoforms, SYP13IIα and SYP13IIβ. These splice-forms differentially mark functional and degrading arbuscule branches. Our results show that vesicle traffic to the symbiotic interface is specialized and required for its maintenance. Alternative splicing of SYP13II allows plants to replace a t-SNARE involved in traffic to the plasma membrane with a t-SNARE that is more stringent in its localization to functional arbuscules. 10.1111/nph.13973
    Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. Kikuchi Yusuke,Hijikata Nowaki,Ohtomo Ryo,Handa Yoshihiro,Kawaguchi Masayoshi,Saito Katsuharu,Masuta Chikara,Ezawa Tatsuhiro The New phytologist Arbuscular mycorrhizal fungi translocate polyphosphate through hyphae over a long distance to deliver to the host. More than three decades ago, suppression of host transpiration was found to decelerate phosphate delivery of the fungal symbiont, leading us to hypothesize that transpiration provides a primary driving force for polyphosphate translocation, probably via creating hyphal water flow in which fungal aquaporin(s) may be involved. The impact of transpiration suppression on polyphosphate translocation through hyphae of Rhizophagus clarus was evaluated. An aquaporin gene expressed in intraradical mycelia was characterized and knocked down by virus-induced gene silencing to investigate the involvement of the gene in polyphosphate translocation. Rhizophagus clarus aquaporin 3 (RcAQP3) that was most highly expressed in intraradical mycelia encodes an aquaglyceroporin responsible for water transport across the plasma membrane. Knockdown of RcAQP3 as well as the suppression of host transpiration decelerated polyphosphate translocation in proportion to the levels of knockdown and suppression, respectively. These results provide the first insight into the mechanism underlying long-distance polyphosphate translocation in mycorrhizal associations at the molecular level, in which host transpiration and the fungal aquaporin play key roles. A hypothetical model of the translocation is proposed for further elucidation of the mechanism. 10.1111/nph.14016
    An Autophagy-Related Kinase Is Essential for the Symbiotic Relationship between and Both Rhizobia and Arbuscular Mycorrhizal Fungi. Estrada-Navarrete Georgina,Cruz-Mireles Neftaly,Lascano Ramiro,Alvarado-Affantranger Xóchitl,Hernández-Barrera Alejandra,Barraza Aarón,Olivares Juan E,Arthikala Manoj-Kumar,Cárdenas Luis,Quinto Carmen,Sanchez Federico The Plant cell Eukaryotes contain three types of lipid kinases that belong to the phosphatidylinositol 3-kinase (PI3K) family. In plants and , only PI3K class III family members have been identified. These enzymes regulate the innate immune response, intracellular trafficking, autophagy, and senescence. Here, we report that RNAi-mediated downregulation of common bean () severely impaired symbiosis in composite plants with endosymbionts such as and Downregulation of Pv was associated with a marked decrease in root hair growth and curling. Additionally, infection thread growth, root-nodule number, and symbiosome formation in root nodule cells were severely affected. Interestingly, root colonization by AM fungi and the formation of arbuscules were also abolished in PI3K loss-of-function plants. Furthermore, the transcript accumulation of genes encoding proteins known to interact with PI3K to form protein complexes involved in autophagy was drastically reduced in these transgenic roots. RNAi-mediated downregulation of one of these genes, /, resulted in a similar phenotype as observed for transgenic roots in which Pv had been downregulated. Our findings show that an autophagy-related process is crucial for the mutualistic interactions of with beneficial microorganisms. 10.1105/tpc.15.01012
    Chromium immobilization by extra- and intraradical fungal structures of arbuscular mycorrhizal symbioses. Wu Songlin,Zhang Xin,Sun Yuqing,Wu Zhaoxiang,Li Tao,Hu Yajun,Lv Jitao,Li Gang,Zhang Zhensong,Zhang Jing,Zheng Lirong,Zhen Xiangjun,Chen Baodong Journal of hazardous materials Arbuscular mycorrhizal (AM) fungi can enhance plant Cr tolerance through immobilizing Cr in mycorrhizal roots. However, the detailed processes and mechanisms are unclear. The present study focused on cellular distribution and speciation of Cr in both extraradical mycelium (ERM) and mycorrhizal roots exposed to Cr(VI) by using field emission scanning electron microscopy equipped with energy dispersive X-ray spectrometer (FE-SEM-EDS), scanning transmission soft X-ray microscopy (STXM) and X-ray absorption fine structure (XAFS) spectroscopy techniques. We found that amounts of particles (possibly extracellular polymeric substances, EPS) were produced on the AM fungal surface upon Cr(VI) stress, which contributed greatly to Cr(VI) reduction and immobilization. With EDS of the surface of AM fungi exposed to various Cr(VI) levels, a positive correlation between Cr and P was revealed, suggesting that phosphate groups might act as counter ions of Cr(III), which was also confirmed by the XAFS analysis. Besides, STXM and XAFS analyses showed that Cr(VI) was reduced to Cr(III) in AM fungal structures (arbuscules, intraradical mycelium, etc.) and cell walls in mycorrhizal roots, and complexed possibly with carboxyl groups or histidine analogues. The present work provided evidence of Cr immobilization on fungal surface and in fungal structures in mycorrhizal roots at a cellular level, and thus unraveled the underlying mechanisms by which AM symbiosis immobilize Cr. 10.1016/j.jhazmat.2016.05.017
    Arbuscular Mycorrhizal Symbiosis Requires a Phosphate Transceptor in the Gigaspora margarita Fungal Symbiont. Xie Xianan,Lin Hui,Peng Xiaowei,Xu Congrui,Sun Zhongfeng,Jiang Kexin,Huang Antian,Wu Xiaohui,Tang Nianwu,Salvioli Alessandra,Bonfante Paola,Zhao Bin Molecular plant The majority of terrestrial vascular plants are capable of forming mutualistic associations with obligate biotrophic arbuscular mycorrhizal (AM) fungi from the phylum Glomeromycota. This mutualistic symbiosis provides carbohydrates to the fungus, and reciprocally improves plant phosphate uptake. AM fungal transporters can acquire phosphate from the soil through the hyphal networks. Nevertheless, the precise functions of AM fungal phosphate transporters, and whether they act as sensors or as nutrient transporters, in fungal signal transduction remain unclear. Here, we report a high-affinity phosphate transporter GigmPT from Gigaspora margarita that is required for AM symbiosis. Host-induced gene silencing of GigmPT hampers the development of G. margarita during AM symbiosis. Most importantly, GigmPT functions as a phosphate transceptor in G. margarita regarding the activation of the phosphate signaling pathway as well as the protein kinase A signaling cascade. Using the substituted-cysteine accessibility method, we identified residues A (in transmembrane domain [TMD] IV) and Val (in TMD VIII) of GigmPT, both of which are critical for phosphate signaling and transport in yeast during growth induction. Collectively, our results provide significant insights into the molecular functions of a phosphate transceptor from the AM fungus G. margarita. 10.1016/j.molp.2016.08.011
    Biology and evolution of arbuscular mycorrhizal symbiosis in the light of genomics. Kamel Laurent,Keller-Pearson Michelle,Roux Christophe,Ané Jean-Michel The New phytologist 531 I. 531 II. 532 III. 532 IV. 534 V. 534 535 References 535 SUMMARY: Arbuscular mycorrhizal (AM) fungi associate with the vast majority of land plants, providing mutual nutritional benefits and protecting hosts against biotic and abiotic stresses. Significant progress was made recently in our understanding of the genomic organization, the obligate requirements, and the sexual nature of these fungi through the release and subsequent mining of genome sequences. Genomic and genetic approaches also improved our understanding of the signal repertoire used by AM fungi and their plant hosts to recognize each other for the initiation and maintenance of this association. Evolutionary and bioinformatic analyses of host and nonhost plant genomes represent novel ways with which to decipher host mechanisms controlling these associations and shed light on the stepwise acquisition of this genetic toolkit during plant evolution. Mining fungal and plant genomes along with evolutionary and genetic approaches will improve understanding of these symbiotic associations and, in the long term, their usefulness in agricultural settings. 10.1111/nph.14263
    Positive Gene Regulation by a Natural Protective miRNA Enables Arbuscular Mycorrhizal Symbiosis. Couzigou Jean-Malo,Lauressergues Dominique,André Olivier,Gutjahr Caroline,Guillotin Bruno,Bécard Guillaume,Combier Jean-Philippe Cell host & microbe Arbuscular mycorrhizal (AM) symbiosis associates most plants with fungi of the phylum Glomeromycota. The fungus penetrates into roots and forms within cortical cell branched structures called arbuscules for nutrient exchange. We discovered that miR171b has a mismatched cleavage site and is unable to downregulate the miR171 family target gene, LOM1 (LOST MERISTEMS 1). This mismatched cleavage site is conserved among plants that establish AM symbiosis, but not in non-mycotrophic plants. Unlike other members of the miR171 family, miR171b stimulates AM symbiosis and is expressed specifically in root cells that contain arbuscules. MiR171b protects LOM1 from negative regulation by other miR171 family members. These findings uncover a unique mechanism of positive post-transcriptional regulation of gene expression by miRNAs and demonstrate its relevance for the establishment of AM symbiosis. 10.1016/j.chom.2016.12.001
    Sl-IAA27 regulates strigolactone biosynthesis and mycorrhization in tomato (var. MicroTom). Guillotin Bruno,Etemadi Mohammad,Audran Corinne,Bouzayen Mondher,Bécard Guillaume,Combier Jean-Philippe The New phytologist Root colonization by arbuscular mycorrhizal (AM) fungi is a complex and finely tuned process. Previous studies have shown that, among other plant hormones, auxin plays a role in this process but the specific involvement of Aux/IAAs, the key regulators of auxin responses, is still unknown. In this study, we addressed the role of the tomato Sl-IAA27 during AM symbiosis by using Sl-IAA27-RNAi and pSL-IAA27::GUS stable tomato lines. The data show that Sl-IAA27 expression is up-regulated by the AM fungus and that silencing of Sl-IAA27 has a negative impact on AM colonization. Sl-IAA27-silencing resulted in down-regulation of three genes involved in strigolactone synthesis, NSP1, D27 and MAX1, and treatment of Sl-IAA27-silenced plants with the strigolactone analog GR24 complemented their mycorrhizal defect phenotype. Overall, the study identified an Aux/IAA gene as a new component of the signaling pathway controlling AM fungal colonization in tomato. This gene is proposed to control strigolactone biosynthesis via the regulation of NSP1. 10.1111/nph.14246
    Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. Sawers Ruairidh J H,Svane Simon F,Quan Clement,Grønlund Mette,Wozniak Barbara,Gebreselassie Mesfin-Nigussie,González-Muñoz Eliécer,Chávez Montes Ricardo A,Baxter Ivan,Goudet Jerome,Jakobsen Iver,Paszkowski Uta The New phytologist Plant interactions with arbuscular mycorrhizal fungi have long attracted interest for their potential to promote more efficient use of mineral resources in agriculture. Their use, however, remains limited by a lack of understanding of the processes that determine the outcome of the symbiosis. In this study, the impact of host genotype on growth response to mycorrhizal inoculation was investigated in a panel of diverse maize lines. A panel of 30 maize lines was evaluated with and without inoculation with arbuscular mycorrhizal fungi. The line Oh43 was identified to show superior response and, along with five other reference lines, was characterized in greater detail in a split-compartment system, using P to quantify mycorrhizal phosphorus uptake. Changes in relative growth indicated variation in host capacity to profit from the symbiosis. Shoot phosphate content, abundance of root-internal and -external fungal structures, mycorrhizal phosphorus uptake, and accumulation of transcripts encoding plant PHT1 family phosphate transporters varied among lines. Superior response in Oh43 is correlated with extensive development of root-external hyphae, accumulation of specific Pht1 transcripts and high phosphorus uptake by mycorrhizal plants. The data indicate that host genetic factors influence fungal growth strategy with an impact on plant performance. 10.1111/nph.14403
    A Transcriptional Program for Arbuscule Degeneration during AM Symbiosis Is Regulated by MYB1. Floss Daniela S,Gomez S Karen,Park Hee-Jin,MacLean Allyson M,Müller Lena M,Bhattarai Kishor K,Lévesque-Tremblay Veronique,Maldonado-Mendoza Ignacio E,Harrison Maria J Current biology : CB During the endosymbiosis formed between plants and arbuscular mycorrhizal (AM) fungi, the root cortical cells are colonized by branched hyphae called arbuscules, which function in nutrient exchange with the plant [1]. Despite their positive function, arbuscules are ephemeral structures, and their development is followed by a degeneration phase, in which the arbuscule and surrounding periarbuscular membrane and matrix gradually disappear from the root cell [2, 3]. Currently, the root cell's role in this process and the underlying regulatory mechanisms are unknown. Here, by using a Medicago truncatula pt4 mutant in which arbuscules degenerate prematurely [4], we identified arbuscule degeneration-associated genes, of which 38% are predicted to encode secreted hydrolases, suggesting a role in disassembly of the arbuscule and interface. Through RNAi and analysis of an insertion mutant, we identified a symbiosis-specific MYB-like transcription factor (MYB1) that suppresses arbuscule degeneration in mtpt4. In myb1, expression of several degeneration-associated genes is reduced. Conversely, in roots constitutively overexpressing MYB1, expression of degeneration-associated genes is increased and subsequent development of symbiosis is impaired. MYB1-regulated gene expression is enhanced by DELLA proteins and is dependent on NSP1 [5], but not NSP2 [6]. Furthermore, MYB1 interacts with DELLA and NSP1. Our data identify a transcriptional program for arbuscule degeneration and reveal that its regulators include MYB1 in association with two transcriptional regulators, NSP1 and DELLA, both of which function in preceding phases of the symbiosis. We propose that the combinatorial use of transcription factors enables the sequential expression of transcriptional programs for arbuscule development and degeneration. 10.1016/j.cub.2017.03.003
    Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth. Koch Alexander M,Antunes Pedro M,Maherali Hafiz,Hart Miranda M,Klironomos John N The New phytologist Although arbuscular mycorrhizal (AM) fungi are obligate symbionts that can influence plant growth, the magnitude and direction of these effects are highly variable within fungal genera and even among isolates within species, as well as among plant taxa. To determine whether variability in AM fungal morphology and growth is correlated with AM fungal effects on plant growth, we established a common garden experiment with 56 AM fungal isolates comprising 17 genera and six families growing with three plant host species. Arbuscular mycorrhizal fungal morphology and growth was highly conserved among isolates of the same species and among species within a family. By contrast, plant growth response to fungal inoculation was highly variable, with the majority of variation occurring among different isolates of the same AM fungal species. Our findings show that host performance cannot be predicted from AM fungal morphology and growth traits. Divergent effects on plant growth among isolates within an AM fungal species may be caused by coevolution between co-occurring fungal and plant populations. 10.1111/nph.14465
    The rice LysM receptor-like kinase OsCERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling. Carotenuto Gennaro,Chabaud Mireille,Miyata Kana,Capozzi Martina,Takeda Naoya,Kaku Hanae,Shibuya Naoto,Nakagawa Tomomi,Barker David G,Genre Andrea The New phytologist The rice lysin-motif (LysM) receptor-like kinase OsCERK1 is now known to have a dual role in both pathogenic and symbiotic interactions. Following the recent discovery that the Oscerk1 mutant is unable to host arbuscular mycorrhizal (AM) fungi, we have examined whether OsCERK1 is directly involved in the perception of the short-chain chitin oligomers (Myc-COs) identified in AM fungal exudates and shown to activate nuclear calcium (Ca ) spiking in the rice root epidermis. An Oscerk1 knockout mutant expressing the cameleon NLS-YC2.60 was used to monitor nuclear Ca signaling following root treatment with either crude fungal exudates or purified Myc-COs. Compared with wild-type rice, Ca spiking responses to AM fungal elicitation were absent in root atrichoblasts of the Oscerk1 mutant. By contrast, rice lines mutated in OsCEBiP, encoding the LysM receptor-like protein which associates with OsCERK1 to perceive chitin elicitors of the host immune defense pathway, responded positively to Myc-COs. These findings provide direct evidence that the bi-functional OsCERK1 plays a central role in perceiving short-chain Myc-CO signals and activating the downstream conserved symbiotic signal transduction pathway. 10.1111/nph.14539
    Strigolactones in Plant Interactions with Beneficial and Detrimental Organisms: The Yin and Yang. López-Ráez Juan A,Shirasu Ken,Foo Eloise Trends in plant science Strigolactones (SLs) are plant hormones that have important roles as modulators of plant development. They were originally described as ex planta signaling molecules in the rhizosphere that induce the germination of parasitic plants, a role that was later linked to encouraging the beneficial symbiosis with arbuscular mycorrhizal (AM) fungi. Recently, the focus has shifted to examining the role of SLs in plant-microbe interactions, and has revealed roles for SLs in the association of legumes with nitrogen-fixing rhizobacteria and in interactions with disease-causing pathogens. Here, we examine the role of SLs in plant interactions with beneficial and detrimental organisms, and propose possible future biotechnological applications. 10.1016/j.tplants.2017.03.011
    Diet of Arbuscular Mycorrhizal Fungi: Bread and Butter? Rich Mélanie K,Nouri Eva,Courty Pierre-Emmanuel,Reinhardt Didier Trends in plant science Most plants entertain mutualistic interactions known as arbuscular mycorrhiza (AM) with soil fungi (Glomeromycota) which provide them with mineral nutrients in exchange for reduced carbon from the plant. Mycorrhizal roots represent strong carbon sinks in which hexoses are transferred from the plant host to the fungus. However, most of the carbon in AM fungi is stored in the form of lipids. The absence of the type I fatty acid synthase (FAS-I) complex from the AM fungal model species Rhizophagus irregularis suggests that lipids may also have a role in nutrition of the fungal partner. This hypothesis is supported by the concerted induction of host genes involved in lipid metabolism. We explore the possible roles of lipids in the light of recent literature on AM symbiosis. 10.1016/j.tplants.2017.05.008
    Nutrient Exchange and Regulation in Arbuscular Mycorrhizal Symbiosis. Wang Wanxiao,Shi Jincai,Xie Qiujin,Jiang Yina,Yu Nan,Wang Ertao Molecular plant Most land plants form symbiotic associations with arbuscular mycorrhizal (AM) fungi. These are the most common and widespread terrestrial plant symbioses, which have a global impact on plant mineral nutrition. The establishment of AM symbiosis involves recognition of the two partners and bidirectional transport of different mineral and carbon nutrients through the symbiotic interfaces within the host root cells. Intriguingly, recent discoveries have highlighted that lipids are transferred from the plant host to AM fungus as a major carbon source. In this review, we discuss the transporter-mediated transfer of carbon, nitrogen, phosphate, potassium and sulfate, and present hypotheses pertaining to the potential regulatory mechanisms of nutrient exchange in AM symbiosis. Current challenges and future perspectives on AM symbiosis research are also discussed. 10.1016/j.molp.2017.07.012
    Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis. MacLean Allyson M,Bravo Armando,Harrison Maria J The Plant cell Plants have lived in close association with arbuscular mycorrhizal (AM) fungi for over 400 million years. Today, this endosymbiosis occurs broadly in the plant kingdom where it has a pronounced impact on plant mineral nutrition. The symbiosis develops deep within the root cortex with minimal alterations in the external appearance of the colonized root; however, the absence of macroscopic alterations belies the extensive signaling, cellular remodeling, and metabolic alterations that occur to enable accommodation of the fungal endosymbiont. Recent research has revealed the involvement of a novel -acetyl glucosamine transporter and an alpha/beta-fold hydrolase receptor at the earliest stages of AM symbiosis. Calcium channels required for symbiosis signaling have been identified, and connections between the symbiosis signaling pathway and key transcriptional regulators that direct AM-specific gene expression have been established. Phylogenomics has revealed the existence of genes conserved for AM symbiosis, providing clues as to how plant cells fine-tune their biology to enable symbiosis, and an exciting coalescence of genome mining, lipid profiling, and tracer studies collectively has led to the conclusion that AM fungi are fatty acid auxotrophs and that plants provide their fungal endosymbionts with fatty acids. Here, we provide an overview of the molecular program for AM symbiosis and discuss these recent advances. 10.1105/tpc.17.00555
    Root-associated fungal microbiota of nonmycorrhizal and its contribution to plant phosphorus nutrition. Almario Juliana,Jeena Ganga,Wunder Jörg,Langen Gregor,Zuccaro Alga,Coupland George,Bucher Marcel Proceedings of the National Academy of Sciences of the United States of America Most land plants live in association with arbuscular mycorrhizal (AM) fungi and rely on this symbiosis to scavenge phosphorus (P) from soil. The ability to establish this partnership has been lost in some plant lineages like the Brassicaceae, which raises the question of what alternative nutrition strategies such plants have to grow in P-impoverished soils. To understand the contribution of plant-microbiota interactions, we studied the root-associated fungal microbiome of (Brassicaceae) with the hypothesis that some of its components can promote plant P acquisition. Using amplicon sequencing of the fungal internal transcribed spacer 2, we studied the root and rhizosphere fungal communities of growing under natural and controlled conditions including low-P soils and identified a set of 15 fungal taxa consistently detected in its roots. This cohort included a Helotiales taxon exhibiting high abundance in roots of wild growing in an extremely P-limited soil. Consequently, we isolated and subsequently reintroduced a specimen from this taxon into its native P-poor soil in which it improved plant growth and P uptake. The fungus exhibited mycorrhiza-like traits including colonization of the root endosphere and P transfer to the plant. Genome analysis revealed a link between its endophytic lifestyle and the expansion of its repertoire of carbohydrate-active enzymes. We report the discovery of a plant-fungus interaction facilitating the growth of a nonmycorrhizal plant under native P-limited conditions, thus uncovering a previously underestimated role of root fungal microbiota in P cycling. 10.1073/pnas.1710455114
    Independent signalling cues underpin arbuscular mycorrhizal symbiosis and large lateral root induction in rice. Chiu Chai Hao,Choi Jeongmin,Paszkowski Uta The New phytologist Perception of arbuscular mycorrhizal fungi (AMF) triggers distinct plant signalling responses for parallel establishment of symbiosis and induction of lateral root formation. Rice receptor kinase CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) and α/β-fold hydrolase DWARF14-LIKE (D14L) are involved in pre-symbiotic fungal perception. After 6 wk post-inoculation with Rhizophagus irregularis, root developmental responses, fungal colonization and transcriptional responses were monitored in two independent cerk1 null mutants; a deletion mutant lacking D14L, and with D14L complemented as well as their respective wild-type cultivars (cv Nipponbare and Nihonmasari). Here we show that although essential for symbiosis, D14L is dispensable for AMF-induced root architectural modulation, which conversely relies on CERK1. Our results demonstrate uncoupling of symbiosis and the symbiotic root developmental signalling during pre-symbiosis with CERK1 required for AMF-induced root architectural changes. 10.1111/nph.14936
    Microbiome and ecotypic adaption of Holcus lanatus (L.) to extremes of its soil pH range, investigated through transcriptome sequencing. Young Ellen,Carey Manus,Meharg Andrew A,Meharg Caroline Microbiome BACKGROUND:Plants can adapt to edaphic stress, such as nutrient deficiency, toxicity and biotic challenges, by controlled transcriptomic responses, including microbiome interactions. Traditionally studied in model plant species with controlled microbiota inoculation treatments, molecular plant-microbiome interactions can be functionally investigated via RNA-Seq. Complex, natural plant-microbiome studies are limited, typically focusing on microbial rRNA and omitting functional microbiome investigations, presenting a fundamental knowledge gap. Here, root and shoot meta-transcriptome analyses, in tandem with shoot elemental content and root staining, were employed to investigate transcriptome responses in the wild grass Holcus lanatus and its associated natural multi-species eukaryotic microbiome. A full factorial reciprocal soil transplant experiment was employed, using plant ecotypes from two widely contrasting natural habitats, acid bog and limestone quarry soil, to investigate naturally occurring, and ecologically meaningful, edaphically driven molecular plant-microbiome interactions. RESULTS:Arbuscular mycorrhizal (AM) and non-AM fungal colonization was detected in roots in both soils. Staining showed greater levels of non-AM fungi, and transcriptomics indicated a predominance of Ascomycota-annotated genes. Roots in acid bog soil were dominated by Phialocephala-annotated transcripts, a putative growth-promoting endophyte, potentially involved in N nutrition and ion homeostasis. Limestone roots in acid bog soil had greater expression of other Ascomycete genera and Oomycetes and lower expression of Phialocephala-annotated transcripts compared to acid ecotype roots, which corresponded with reduced induction of pathogen defense processes, particularly lignin biosynthesis in limestone ecotypes. Ascomycota dominated in shoots and limestone soil roots, but Phialocephala-annotated transcripts were insignificant, and no single Ascomycete genus dominated. Fusarium-annotated transcripts were the most common genus in shoots, with Colletotrichum and Rhizophagus (AM fungi) most numerous in limestone soil roots. The latter coincided with upregulation of plant genes involved in AM symbiosis initiation and AM-based P acquisition in an environment where P availability is low. CONCLUSIONS:Meta-transcriptome analyses provided novel insights into H. lanatus transcriptome responses, associated eukaryotic microbiota functions and taxonomic community composition. Significant edaphic and plant ecotype effects were identified, demonstrating that meta-transcriptome-based functional analysis is a powerful tool for the study of natural plant-microbiome interactions. 10.1186/s40168-018-0434-3
    Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species. Martín-Robles Nieves,Lehmann Anika,Seco Erica,Aroca Ricardo,Rillig Matthias C,Milla Rubén The New phytologist The arbuscular mycorrhizal (AM) symbiosis is key to plant nutrition, and hence is potentially key in sustainable agriculture. Fertilization and other agricultural practices reduce soil AM fungi and root colonization. Such conditions might promote the evolution of low mycorrhizal responsive crops. Therefore, we ask if and how evolution under domestication has altered AM symbioses of crops. We measured the effect of domestication on mycorrhizal responsiveness across 27 crop species and their wild progenitors. Additionally, in a subset of 14 crops, we tested if domestication effects differed under contrasting phosphorus (P) availabilities. The response of AM symbiosis to domestication varied with P availability. On average, wild progenitors benefited from the AM symbiosis irrespective of P availability, while domesticated crops only profited under P-limited conditions. Magnitudes and directions of response were diverse among the 27 crops, and were unrelated to phylogenetic affinities or to the coordinated evolution with fine root traits. Our results indicate disruptions in the efficiency of the AM symbiosis linked to domestication. Under high fertilization, domestication could have altered the regulation of resource trafficking between AM fungi and associated plant hosts. Provided that crops are commonly raised under high fertilization, this result has important implications for sustainable agriculture. 10.1111/nph.14962
    Anthropogenic disturbance equalizes diversity levels in arbuscular mycorrhizal fungal communities. García de León David,Davison John,Moora Mari,Öpik Maarja,Feng Huyuan,Hiiesalu Inga,Jairus Teele,Koorem Kadri,Liu Yongjun,Phosri Cherdchai,Sepp Siim-Kaarel,Vasar Martti,Zobel Martin Global change biology The arbuscular mycorrhizal (AM) symbiosis is a key plant-microbe interaction in sustainable functioning ecosystems. Increasing anthropogenic disturbance poses a threat to AM fungal communities worldwide, but there is little empirical evidence about its potential negative consequences. In this global study, we sequenced AM fungal DNA in soil samples collected from pairs of natural (undisturbed) and anthropogenic (disturbed) plots in two ecosystem types (10 naturally wooded and six naturally unwooded ecosystems). We found that ecosystem type had stronger directional effects than anthropogenic disturbance on AM fungal alpha and beta diversity. However, disturbance increased alpha and beta diversity at sites where natural diversity was low and decreased diversity at sites where natural diversity was high. Cultured AM fungal taxa were more prevalent in anthropogenic than natural plots, probably due to their efficient colonization strategies and ability to recover from disturbance. We conclude that anthropogenic disturbance does not have a consistent directional effect on AM fungal diversity; rather, disturbance equalizes levels of diversity at large scales and causes changes in community functional structure. 10.1111/gcb.14131
    Non-Mycorrhizal Plants: The Exceptions that Prove the Rule. Cosme Marco,Fernández Ivan,Van der Heijden Marcel G A,Pieterse Corné M J Trends in plant science The widespread symbiotic interaction between plants and arbuscular mycorrhizal (AM) fungi relies on a complex molecular dialog with reciprocal benefits in terms of nutrition, growth, and protection. Approximately 29% of all vascular plant species do not host AM symbiosis, including major crops. Under certain conditions, however, presumed non-host plants can become colonized by AM fungi and develop rudimentary AM (RAM) phenotypes. Here we zoom in on the mustard family (Brassicaceae), which harbors AM hosts, non-hosts, and presumed non-host species such as Arabidopsis thaliana, for which conditional RAM colonization has been described. We advocate that RAM phenotypes and redundant genomic elements of the symbiotic 'toolkit' are missing links that can help to unravel genetic constraints that drive the evolution of symbiotic incompatibility. 10.1016/j.tplants.2018.04.004
    Mechanisms Underlying Establishment of Arbuscular Mycorrhizal Symbioses. Choi Jeongmin,Summers William,Paszkowski Uta Annual review of phytopathology Most land plants engage in mutually beneficial interactions with arbuscular mycorrhizal (AM) fungi, the fungus providing phosphate and nitrogen in exchange for fixed carbon. During presymbiosis, both organisms communicate via oligosaccharides and butenolides. The requirement for a rice chitin receptor in symbiosis-induced lateral root development suggests that cell division programs operate in inner root tissues during both AM and nodule symbioses. Furthermore, the identification of transcription factors underpinning arbuscule development and degeneration reemphasized the plant's regulatory dominance in AM symbiosis. Finally, the finding that AM fungi, as lipid auxotrophs, depend on plant fatty acids (FAs) to complete their asexual life cycle revealed the basis for fungal biotrophy. Intriguingly, lipid metabolism is also central for asexual reproduction and interaction of the fungal sister clade, the Mucoromycotina, with endobacteria, indicative of an evolutionarily ancient role for lipids in fungal mutualism. 10.1146/annurev-phyto-080516-035521
    Medicago AP2-Domain Transcription Factor WRI5a Is a Master Regulator of Lipid Biosynthesis and Transfer during Mycorrhizal Symbiosis. Jiang Yina,Xie Qiujin,Wang Wanxiao,Yang Jun,Zhang Xiaowei,Yu Nan,Zhou Yun,Wang Ertao Molecular plant Most land plants have evolved a mutualistic symbiosis with arbuscular mycorrhiza (AM) fungi that improve nutrient acquisition from the soil. In return, up to 20% of host plant photosynthate is transferred to the mycorrhizal fungus in the form of lipids and sugar. Nutrient exchange must be regulated by both partners in order to maintain a reliable symbiotic relationship. However, the mechanisms underlying the regulation of lipid transfer from the plant to the AM fungus remain elusive. Here, we show that the Medicago truncatula AP2/EREBP transcription factor WRI5a, and likely its two homologs WRI5b/Erf1 and WRI5c, are master regulators of AM symbiosis controlling lipid transfer and periarbuscular membrane formation. We found that WRI5a binds AW-box cis-regulatory elements in the promoters of M. truncatula STR, which encodes a periarbuscular membrane-localized ABC transporter required for lipid transfer from the plant to the AM fungus, and MtPT4, which encodes a phosphate transporter required for phosphate transfer from the AM fungus to the plant. The hairy roots of the M. truncatula wri5a mutant and RNAi composite plants displayed impaired arbuscule formation, whereas overexpression of WRI5a resulted in enhanced expression of STR and MtPT4, suggesting that WRI5a regulates bidirectional symbiotic nutrient exchange. Moreover, we found that WRI5a and RAM1 (Required for Arbuscular Mycorrhization symbiosis 1), which encodes a GRAS-domain transcription factor, regulate each other at the transcriptional level, forming a positive feedback loop for regulating AM symbiosis. Collectively, our data suggest a role for WRI5a in controlling bidirectional nutrient exchange and periarbuscular membrane formation via the regulation of genes involved in the biosynthesis of fatty acids and phosphate uptake in arbuscule-containing cells. 10.1016/j.molp.2018.09.006
    A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane. Roth Ronelle,Chiapello Marco,Montero Héctor,Gehrig Peter,Grossmann Jonas,O'Holleran Kevin,Hartken Denise,Walters Fergus,Yang Shu-Yi,Hillmer Stefan,Schumacher Karin,Bowden Sarah,Craze Melanie,Wallington Emma J,Miyao Akio,Sawers Ruairidh,Martinoia Enrico,Paszkowski Uta Nature communications In terrestrial ecosystems most plant species live in mutualistic symbioses with nutrient-delivering arbuscular mycorrhizal (AM) fungi. Establishment of AM symbioses includes transient, intracellular formation of fungal feeding structures, the arbuscules. A plant-derived peri-arbuscular membrane (PAM) surrounds the arbuscules, mediating reciprocal nutrient exchange. Signaling at the PAM must be well coordinated to achieve this dynamic cellular intimacy. Here, we identify the PAM-specific Arbuscular Receptor-like Kinase 1 (ARK1) from maize and rice to condition sustained AM symbiosis. Mutation of rice ARK1 causes a significant reduction in vesicles, the fungal storage structures, and a concomitant reduction in overall root colonization by the AM fungus Rhizophagus irregularis. Arbuscules, although less frequent in the ark1 mutant, are morphologically normal. Co-cultivation with wild-type plants restores vesicle and spore formation, suggesting ARK1 function is required for the completion of the fungal life-cycle, thereby defining a functional stage, post arbuscule development. 10.1038/s41467-018-06865-z
    Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. Rivero Javier,Álvarez Domingo,Flors Víctor,Azcón-Aguilar Concepción,Pozo María J The New phytologist Arbuscular mycorrhizal (AM) symbioses can improve plant tolerance to multiple stresses. We compared three AM fungi (AMF) from different genera, one of them isolated from a dry and saline environment, in terms of their ability to increase tomato tolerance to moderate or severe drought or salt stress. Plant physiological parameters and metabolic profiles were compared in order to find the molecular mechanisms underlying plant protection against stress. Mycorrhizal growth response was determined, and ultrahigh-performance LC-MS was used to compare the metabolic profile of plants under the different treatments. All AMF increased plant tolerance to stress, and the positive effects of the symbiosis were correlated with the severity of the stress. The AMF isolated from the stressful environment was the most effective in improving plant tolerance to salt stress. Differentially accumulated compounds were identified and the antistress properties of some of them were confirmed. We demonstrate that AM symbioses increase plant metabolic plasticity to cope with stress. Some responses were common to all AMF tested, while others were specifically related to particular isolates. Important metabolism reprograming was evidenced upon salt stress, and we identified metabolic pathways and compounds differentially accumulated in mycorrhizas that may underlie their enhanced tolerance to stress. 10.1111/nph.15295
    The role of plant mycorrhizal type and status in modulating the relationship between plant and arbuscular mycorrhizal fungal communities. Neuenkamp Lena,Moora Mari,Öpik Maarja,Davison John,Gerz Maret,Männistö Minna,Jairus Teele,Vasar Martti,Zobel Martin The New phytologist Interactions between communities of plants and arbuscular mycorrhizal (AM) fungi shape fundamental ecosystem properties. Experimental evidence suggests that compositional changes in plant and AM fungal communities should be correlated, but empirical data from natural ecosystems are scarce. We investigated the dynamics of covariation between plant and AM fungal communities during three stages of grassland succession, and the biotic and abiotic factors shaping these dynamics. Plant communities were characterised using vegetation surveys. AM fungal communities were characterised by 454-sequencing of the small subunit rRNA gene and identification against the AM fungal reference database MaarjAM. AM fungal abundance was estimated using neutral-lipid fatty acids (NLFAs). Multivariate correlation analysis (Procrustes) revealed a significant relationship between plant and AM fungal community composition. The strength of plant-AM fungal correlation weakened during succession following cessation of grassland management, reflecting changes in the proportion of plants exhibiting different AM status. Plant-AM fungal correlation was strong when the abundance of obligate AM plants was high, and declined as the proportion of facultative AM plants increased. We conclude that the extent to which plants rely on AM symbiosis can determine how tightly communities of plants and AM fungi are interlinked, regulating community assembly of both symbiotic partners. 10.1111/nph.14995
    The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: insights from genetics and genomics. Sawers Ruairidh J H,Ramírez-Flores M Rosario,Olalde-Portugal Víctor,Paszkowski Uta The New phytologist Contents Summary 1135 I. Introduction 1135 II. Recruitment of plant metabolites and hormones as signals in AM symbiosis 1136 III. Phytohormones are regulators of AM symbiosis and targets of plant breeding 1137 IV. Variation in host response to AM symbiosis 1137 V. Outlook 1137 Acknowledgements 1139 References 1139 SUMMARY: Cereals (rice, maize, wheat, sorghum and the millets) provide over 50% of the world's caloric intake, a value that rises to > 80% in developing countries. Since domestication, cereals have been under artificial selection, largely directed towards higher yield. Throughout this process, cereals have maintained their capacity to interact with arbuscular mycorrhizal (AM) fungi, beneficial symbionts that associate with the roots of most terrestrial plants. It has been hypothesized that the shift from the wild to cultivation, and above all the last c. 50 years of intensive breeding for high-input farming systems, has reduced the capacity of the major cereal crops to gain full benefit from AM interactions. Recent studies have shed further light on the molecular basis of establishment and functioning of AM symbiosis in cereals, providing insight into where the breeding process might have had an impact. Classic phytohormones, targets of artificial selection during the generation of Green Revolution semi-dwarf varieties, have emerged as important regulators of AM symbiosis. Although there is still much to be learnt about the mechanistic basis of variation in symbiotic outcome, these advances are providing an insight into the role of arbuscular mycorrhiza in agronomic systems. 10.1111/nph.15152
    Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. Lanfranco Luisa,Fiorilli Valentina,Gutjahr Caroline The New phytologist Contents Summary 1031 I. Introduction 1031 II. Interkingdom communication enabling symbiosis 1032 III. Nutritional and regulatory roles for key metabolites in the AM symbiosis 1035 IV. The plant-fungus genotype combination determines the outcome of the symbiosis 1039 V. Perspectives 1039 Acknowledgements 1041 References 1041 SUMMARY: The evolutionary and ecological success of the arbuscular mycorrhizal (AM) symbiosis relies on an efficient and multifactorial communication system for partner recognition, and on a fine-tuned and reciprocal metabolic regulation of each symbiont to reach an optimal functional integration. Besides strigolactones, N-acetylglucosamine-derivatives released by the plant were recently suggested to trigger fungal reprogramming at the pre-contact stage. Remarkably, N-acetylglucosamine-based diffusible molecules also are symbiotic signals produced by AM fungi (AMF) and clues on the mechanisms of their perception by the plant are emerging. AMF genomes and transcriptomes contain a battery of putative effector genes that may have conserved and AMF- or host plant-specific functions. Nutrient exchange is the key feature of AM symbiosis. A mechanism of phosphate transport inside fungal hyphae has been suggested, and first insights into the regulatory mechanisms of root colonization in accordance with nutrient transfer and status were obtained. The recent discovery of the dependency of AMF on fatty acid transfer from the host has offered a convincing explanation for their obligate biotrophism. Novel studies highlighted the importance of plant and fungal genotypes for the outcome of the symbiosis. These findings open new perspectives for fundamental research and application of AMF in agriculture. 10.1111/nph.15230
    Ectopic activation of cortical cell division during the accommodation of arbuscular mycorrhizal fungi. Russo Giulia,Carotenuto Gennaro,Fiorilli Valentina,Volpe Veronica,Chiapello Marco,Van Damme Daniel,Genre Andrea The New phytologist Arbuscular mycorrhizas (AMs) between plants and soil fungi are widespread symbioses with a major role in soil nutrient uptake. In this study we investigated the induction of root cortical cell division during AM colonization by combining morphometric and gene expression analyses with promoter activation and protein localization studies of the cell-plate-associated exocytic marker TPLATE. Our results show that TPLATE promoter is activated in colonized cells of the root cortex where we also observed the appearance of cells that are half the size of the surrounding cells. Furthermore, TPLATE-green fluorescent protein recruitment to developing cell plates highlighted ectopic cell division events in the inner root cortex during early AM colonization. Lastly, transcripts of TPLATE, KNOLLE and Cyclinlike 1 (CYC1) are all upregulated in the same context, alongside endocytic markers Adaptor-Related Protein complex 2 alpha 1 subunit (AP2A1) and Clathrin Heavy Chain 2 (CHC2), known to be active during cell plate formation. This pattern of gene expression was recorded in wild-type Medicago truncatula roots, but not in a common symbiotic signalling pathway mutant where fungal colonization is blocked at the epidermal level. Altogether, these results suggest the activation of cell-division-related mechanisms by AM hosts during the accommodation of the symbiotic fungus. 10.1111/nph.15398
    Arbuscular mycorrhizal phenotyping: the dos and don'ts. Montero Hector,Choi Jeongmin,Paszkowski Uta The New phytologist 10.1111/nph.15489
    Plant-mediated effects of soil phosphorus on the root-associated fungal microbiota in Arabidopsis thaliana. Fabiańska Izabela,Gerlach Nina,Almario Juliana,Bucher Marcel The New phytologist Plants respond to phosphorus (P) limitation through an array of morphological, physiological and metabolic changes which are part of the phosphate (Pi) starvation response (PSR). This response influences the establishment of the arbuscular mycorrhizal (AM) symbiosis in most land plants. It is, however, unknown to what extent available P and the PSR redefine plant interactions with the fungal microbiota in soil. Using amplicon sequencing of the fungal taxonomic marker ITS2, we examined the changes in root-associated fungal communities in the AM nonhost species Arabidopsis thaliana in response to soil amendment with P and to genetic perturbations in the plant PSR. We observed robust shifts in root-associated fungal communities of P-replete plants in comparison with their P-deprived counterparts, while bulk soil communities remained unaltered. Moreover, plants carrying mutations in the phosphate signaling network genes, phr1, phl1 and pho2, exhibited similarly altered root fungal communities characterized by the depletion of the chytridiomycete taxon Olpidium brassicae specifically under P-replete conditions. This study highlights the nutritional status and the underlying nutrient signaling network of an AM nonhost plant as previously unrecognized factors influencing the assembly of the plant fungal microbiota in response to P in nonsterile soil. 10.1111/nph.15538
    Accumulation of phosphoinositides in distinct regions of the periarbuscular membrane. Ivanov Sergey,Harrison Maria J The New phytologist Phosphoinositides and phosphatidic acid are small anionic lipids that comprise a minor proportion of total membrane lipids in eukaryotic cells but influence a broad range of cellular processes including endomembrane trafficking, signaling, exocytosis and endocytosis. To investigate the spatial distribution of phosphoinositides during arbuscular mycorrhizal symbiosis, we generated fluorescent reporters of PI(4,5)P and PI4P, as well as phosphatidic acid and diacylglycerol and used them to monitor lipid distribution on the cytoplasmic side of membrane bilayers in colonized cortical cells. The PI4P reporter accumulated strongly on the periarbuscular membrane (PAM) and transiently labeled Golgi bodies, while the PA reporter showed differential labeling of endomembranes and the PAM. Surprisingly, the PI(4,5)P reporter accumulated in small, discrete regions of the PAM on the arbuscule trunks, frequently in two regions on opposing sides of the hypha. A mutant reporter with reduced PI(4,5)P binding capacity did not show these accumulations. The PI(4,5)P -rich regions were detected at all phases of arbuscule development following branching, co-localized with membrane marker proteins potentially indicating high membrane bilayer content, and were associated with an alteration in morphology of the hypha. A possible analogy to the biotrophic interfacial membrane complex formed in rice infected with Magnaporthe orzyae is discussed. 10.1111/nph.15553
    Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view. Dreyer Ingo,Spitz Olivia,Kanonenberg Kerstin,Montag Karolin,Handrich Maria R,Ahmad Sabahuddin,Schott-Verdugo Stephan,Navarro-Retamal Carlos,Rubio-Meléndez María E,Gomez-Porras Judith L,Riedelsberger Janin,Molina-Montenegro Marco A,Succurro Antonella,Zuccaro Alga,Gould Sven B,Bauer Petra,Schmitt Lutz,Gohlke Holger The New phytologist To obtain insights into the dynamics of nutrient exchange in arbuscular mycorrhizal (AM) symbiosis, we modelled mathematically the two-membrane system at the plant-fungus interface and simulated its dynamics. In computational cell biology experiments, the full range of nutrient transport pathways was tested for their ability to exchange phosphorus (P)/carbon (C)/nitrogen (N) sources. As a result, we obtained a thermodynamically justified, independent and comprehensive model of the dynamics of the nutrient exchange at the plant-fungus contact zone. The predicted optimal transporter network coincides with the transporter set independently confirmed in wet-laboratory experiments previously, indicating that all essential transporter types have been discovered. The thermodynamic analyses suggest that phosphate is released from the fungus via proton-coupled phosphate transporters rather than anion channels. Optimal transport pathways, such as cation channels or proton-coupled symporters, shuttle nutrients together with a positive charge across the membranes. Only in exceptional cases does electroneutral transport via diffusion facilitators appear to be plausible. The thermodynamic models presented here can be generalized and adapted to other forms of mycorrhiza and open the door for future studies combining wet-laboratory experiments with computational simulations to obtain a deeper understanding of the investigated phenomena. 10.1111/nph.15646
    First evidence for the joint dispersal of mycorrhizal fungi and plant diaspores by birds. Correia Marta,Heleno Ruben,da Silva Luís Pascoal,Costa José Miguel,Rodríguez-Echeverría Susana The New phytologist Seed dispersal allows plants to colonise new sites and escape from pathogens and intraspecific competition, maintaining plant genetic diversity and regulating plant distribution. Conversely, most plant species form mutualistic associations with arbuscular mycorrhizal (AM) fungi in a symbiosis established immediately after seed germination. Because AM fungi are obligate symbionts, using the same dispersal vector as their host should be highly advantageous for their survival, but the co-dispersal of seeds and AM fungal spores has never been confirmed. We aim to clarify the potential role of European birds, essential dispersers for many plant species, as co-dispersers of seeds and AM fungal spores. In total, 63 bird droppings with intact seeds were placed in sterilised soil and maintained for 4 months in a protected environment to avoid contamination. Additionally, 173 bird droppings and 729 gauze swabs used to clean birds' feet were inspected for AM fungal spores. Although no spores were detected by direct observation of these samples, seven Rubus ulmifolius seedlings obtained from four independent droppings of Erithacus rubecula and Sylvia melanocephala were colonised by AM fungi. Our results show that birds can effectively co-disperse viable seeds and AM fungal spores, potentially over long distances, providing a pivotal mechanism to understand the cosmopolitan distribution of AM fungi. 10.1111/nph.15571
    Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region-related gene that positively regulates symbiosis. Le Marquer Morgane,Bécard Guillaume,Frei Dit Frey Nicolas The New phytologist The arbuscular mycorrhizal (AM) symbiosis is a beneficial association established between land plants and the members of a subphylum of fungi, the Glomeromycotina. How the two symbiotic partners regulate their association is still enigmatic. Secreted fungal peptides are candidates for regulating this interaction. We searched for fungal peptides with similarities with known plant signalling peptides. We identified CLAVATA (CLV)/EMBRYO SURROUNDING REGION (ESR)-RELATED PROTEIN (CLE) genes in phylogenetically distant AM fungi: four Rhizophagus species and one Gigaspora species. These CLE genes encode a signal peptide for secretion and the conserved CLE C-terminal motif. They seem to be absent in the other fungal clades. Rhizophagus irregularis and Gigaspora rosea CLE genes (RiCLE1 and GrCLE1) are transcriptionally induced in symbiotic vs asymbiotic conditions. Exogenous application of synthetic RiCLE1 peptide on Medicago truncatula affects root architecture, by slowing the apical growth of primary roots and stimulating the formation of lateral roots. In addition, pretreatment of seedlings with RiCLE1 peptide stimulates mycorrhization. Our findings demonstrate for the first time that in addition to plants and nematodes, AM fungi also possess CLE genes. These results pave the way for deciphering new mechanisms by which AM fungi modulate plant cellular responses during the establishment of AM symbiosis. 10.1111/nph.15643
    Comparative genomics of Rhizophagus irregularis, R. cerebriforme, R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina. Morin Emmanuelle,Miyauchi Shingo,San Clemente Hélène,Chen Eric C H,Pelin Adrian,de la Providencia Ivan,Ndikumana Steve,Beaudet Denis,Hainaut Mathieu,Drula Elodie,Kuo Alan,Tang Nianwu,Roy Sébastien,Viala Julie,Henrissat Bernard,Grigoriev Igor V,Corradi Nicolas,Roux Christophe,Martin Francis M The New phytologist Glomeromycotina is a lineage of early diverging fungi that establish arbuscular mycorrhizal (AM) symbiosis with land plants. Despite their major ecological role, the genetic basis of their obligate mutualism remains largely unknown, hindering our understanding of their evolution and biology. We compared the genomes of Glomerales (Rhizophagus irregularis, Rhizophagus diaphanus, Rhizophagus cerebriforme) and Diversisporales (Gigaspora rosea) species, together with those of saprotrophic Mucoromycota, to identify gene families and processes associated with these lineages and to understand the molecular underpinning of their symbiotic lifestyle. Genomic features in Glomeromycotina appear to be very similar with a very high content in transposons and protein-coding genes, extensive duplications of protein kinase genes, and loss of genes coding for lignocellulose degradation, thiamin biosynthesis and cytosolic fatty acid synthase. Most symbiosis-related genes in R. irregularis and G. rosea are specific to Glomeromycotina. We also confirmed that the present species have a homokaryotic genome organisation. The high interspecific diversity of Glomeromycotina gene repertoires, affecting all known protein domains, as well as symbiosis-related orphan genes, may explain the known adaptation of Glomeromycotina to a wide range of environmental settings. Our findings contribute to an increasingly detailed portrait of genomic features defining the biology of AM fungi. 10.1111/nph.15687
    Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism. Fernández Iván,Cosme Marco,Stringlis Ioannis A,Yu Ke,de Jonge Ronnie,van Wees SaskiaC M,Pozo Maria J,Pieterse Corné M J,van der Heijden Marcel G A The New phytologist Approximately 29% of all vascular plant species are unable to establish an arbuscular mycorrhizal (AM) symbiosis. Despite this, AM fungi (Rhizophagus spp.) are enriched in the root microbiome of the nonhost Arabidopsis thaliana, and Arabidopsis roots become colonized when AM networks nurtured by host plants are available. Here, we investigated the nonhost-AM fungus interaction by analyzing transcriptional changes in Rhizophagus, Arabidopsis and the host plant Medicago truncatula while growing in the same mycorrhizal network. In early interaction stages, Rhizophagus activated the Arabidopsis strigolactone biosynthesis genes CCD7 and CCD8, suggesting that detection of AM fungi is not completely impaired. However, in colonized Arabidopsis roots, fungal nutrient transporter genes GintPT, GintAMT2, GintMST2 and GintMST4, essential for AM symbiosis, were not activated. RNA-seq transcriptome analysis pointed to activation of costly defenses in colonized Arabidopsis roots. Moreover, Rhizophagus colonization caused a 50% reduction in shoot biomass, but also led to enhanced systemic immunity against Botrytis cinerea. This suggests that early signaling between AM fungi and Arabidopsis is not completely impaired and that incompatibility appears at later interaction stages. Moreover, Rhizophagus-mediated defenses coincide with reduced Arabidopsis growth, but also with systemic disease resistance, highlighting the multifunctional role of AM fungi in host and nonhost interactions. 10.1111/nph.15798
    Local endoreduplication as a feature of intracellular fungal accommodation in arbuscular mycorrhizas. Carotenuto Gennaro,Volpe Veronica,Russo Giulia,Politi Mara,Sciascia Ivan,de Almeida-Engler Janice,Genre Andrea The New phytologist The intracellular accommodation of arbuscular mycorrhizal (AM) fungi is a paradigmatic feature of this plant symbiosis that depends on the activation of a dedicated signaling pathway and the extensive reprogramming of host cells, including striking changes in nuclear size and transcriptional activity. By combining targeted sampling of early root colonization sites, detailed confocal imaging, flow cytometry and gene expression analyses, we demonstrate that local, recursive events of endoreduplication are triggered in the Medicago truncatula root cortex during AM colonization. AM colonization induces an increase in ploidy levels and the activation of endocycle specific markers. This response anticipates the progression of fungal colonization and is limited to arbusculated and neighboring cells in the cortical tissue. Furthermore, endoreduplication is not induced in M. truncatula mutants for symbiotic signaling pathway genes. On this basis, we propose endoreduplication as part of the host cell prepenetration responses that anticipate AM fungal accommodation in the root cortex. 10.1111/nph.15763
    Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. Wipf Daniel,Krajinski Franziska,van Tuinen Diederik,Recorbet Ghislaine,Courty Pierre-Emmanuel The New phytologist Arbuscular mycorrhiza (AM) symbiosis occurs between obligate biotrophic fungi of the phylum Glomeromycota and most land plants. The exchange of nutrients between host plants and AM fungi (AMF) is presumed to be the main benefit for the two symbiotic partners. In this review article, we outline the current concepts of nutrient exchanges within this symbiosis (mechanisms and regulation). First, we focus on phosphorus and nitrogen transfer from the fungal partner to the host plant, and on the reciprocal transfer of carbon compounds, with a highlight on a possible interplay between nitrogen and phosphorus nutrition during AM symbiosis. We further discuss potential mechanisms of regulation of these nutrient exchanges linked to membrane dynamics. The review finally addresses the common mycorrhizal networks formed AMF, which interconnect plants from similar and/or different species. Finally the best way to integrate this knowledge and the ensuing potential benefits of AM into sustainable agriculture is discussed. 10.1111/nph.15775
    The Medicago truncatula LysM receptor-like kinase LYK9 plays a dual role in immunity and the arbuscular mycorrhizal symbiosis. Gibelin-Viala Chrystel,Amblard Emilie,Puech-Pages Virginie,Bonhomme Maxime,Garcia Magali,Bascaules-Bedin Adeline,Fliegmann Judith,Wen Jiangqi,Mysore Kirankumar S,le Signor Christine,Jacquet Christophe,Gough Clare The New phytologist Plant -specific lysin-motif receptor-like kinases (LysM-RLKs) are implicated in the perception of N-acetyl glucosamine-containing compounds, some of which are important signal molecules in plant-microbe interactions. Among these, both lipo-chitooligosaccharides (LCOs) and chitooligosaccharides (COs) are proposed as arbuscular mycorrhizal (AM) fungal symbiotic signals. COs can also activate plant defence, although there are scarce data about CO production by pathogens, especially nonfungal pathogens. We tested Medicago truncatula mutants in the LysM-RLK MtLYK9 for their abilities to interact with the AM fungus Rhizophagus irregularis and the oomycete pathogen Aphanomyces euteiches. This prompted us to analyse whether A. euteiches can produce COs. Compared with wild-type plants, Mtlyk9 mutants had fewer infection events and were less colonised by the AM fungus. By contrast, Mtlyk9 mutants were more heavily infected by A. euteiches and showed more disease symptoms. Aphanomyces euteiches was also shown to produce short COs, mainly CO II, but also CO III and CO IV, and traces of CO V, both ex planta and in planta. MtLYK9 thus has a dual role in plant immunity and the AM symbiosis, which raises questions about the functioning and the ancestral origins of such a receptor protein. 10.1111/nph.15891
    Dysfunction in the arbuscular mycorrhizal symbiosis has consistent but small effects on the establishment of the fungal microbiota in Lotus japonicus. Xue Li,Almario Juliana,Fabiańska Izabela,Saridis Georgios,Bucher Marcel The New phytologist Most land plants establish mutualistic interactions with arbuscular mycorrhizal (AM) fungi. Intracellular accommodation of AM fungal symbionts remodels important host traits like root morphology and nutrient acquisition. How mycorrhizal colonization impacts plant microbiota is unclear. To understand the impact of AM symbiosis on fungal microbiota, ten Lotus japonicus mutants impaired at different stages of AM formation were grown in non-sterile natural soil and their root-associated fungal communities were studied. Plant mutants lacking the capacity to form mature arbuscules (arb ) exhibited limited growth performance associated with altered phosphorus (P) acquisition and reduction-oxidation (redox) processes. Furthermore, arb plants assembled moderately but consistently different root-associated fungal microbiota, characterized by the depletion of Glomeromycota and the concomitant enrichment of Ascomycota, including Dactylonectria torresensis. Single and co-inoculation experiments showed a strong reduction of root colonization by D. torresensis in the presence of AM fungus Rhizophagus irregularis, particularly in arbuscule-forming plants. Our results suggest that impairment of central symbiotic functions in AM host plants leads to specific changes in root microbiomes and in tripartite interactions between the host plant, AM and non-AM fungi. This lays the foundation for mechanistic studies on microbe-microbe and microbe-host interactions in AM symbiosis of the model L. japonicus. 10.1111/nph.15958
    A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. An Jianyong,Zeng Tian,Ji Chuanya,de Graaf Sanne,Zheng Zijun,Xiao Ting Ting,Deng Xiuxin,Xiao Shunyuan,Bisseling Ton,Limpens Erik,Pan Zhiyong The New phytologist Plants form a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula. We show that M. truncatula SWEET1b transporter is strongly upregulated in arbuscule-containing cells compared to roots and localizes to the peri-arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule-specific overexpression of MtSWEET1b , which are considered to act in a dominant-negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis. 10.1111/nph.15975
    A LysM Receptor Heteromer Mediates Perception of Arbuscular Mycorrhizal Symbiotic Signal in Rice. He Jiangman,Zhang Chi,Dai Huiling,Liu Huan,Zhang Xiaowei,Yang Jun,Chen Xi,Zhu Yayun,Wang Dapeng,Qi Xiaofeng,Li Weichao,Wang Zhihui,An Guoyong,Yu Nan,He Zuhua,Wang Yong-Fei,Xiao Youli,Zhang Peng,Wang Ertao Molecular plant Symbiotic microorganisms improve nutrient uptake by plants. To initiate mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, plants perceive Myc factors, including lipochitooligosaccharides (LCOs) and short-chain chitooligosaccharides (CO4/CO5), secreted by AM fungi. However, the molecular mechanism of Myc factor perception remains elusive. In this study, we identified a heteromer of LysM receptor-like kinases consisting of OsMYR1/OsLYK2 and OsCERK1 that mediates the perception of AM fungi in rice. CO4 directly binds to OsMYR1, promoting the dimerization and phosphorylation of this receptor complex. Compared with control plants, Osmyr1 and Oscerk1 mutant rice plants are less sensitive to Myc factors and show decreased AM colonization. We engineered transgenic rice by expressing chimeric receptors that respectively replaced the ectodomains of OsMYR1 and OsCERK1 with those from the homologous Nod factor receptors MtNFP and MtLYK3 of Medicago truncatula. Transgenic plants displayed increased calcium oscillations in response to Nod factors compared with control rice. Our study provides significant mechanistic insights into AM symbiotic signal perception in rice. Expression of chimeric Nod/Myc receptors achieves a potentially important step toward generating cereals that host nitrogen-fixing bacteria. 10.1016/j.molp.2019.10.015
    Transcriptomic analysis of field-droughted sorghum from seedling to maturity reveals biotic and metabolic responses. Varoquaux Nelle,Cole Benjamin,Gao Cheng,Pierroz Grady,Baker Christopher R,Patel Dhruv,Madera Mary,Jeffers Tim,Hollingsworth Joy,Sievert Julie,Yoshinaga Yuko,Owiti Judith A,Singan Vasanth R,DeGraaf Stephanie,Xu Ling,Blow Matthew J,Harrison Maria J,Visel Axel,Jansson Christer,Niyogi Krishna K,Hutmacher Robert,Coleman-Derr Devin,O'Malley Ronan C,Taylor John W,Dahlberg Jeffery,Vogel John P,Lemaux Peggy G,Purdom Elizabeth Proceedings of the National Academy of Sciences of the United States of America Drought is the most important environmental stress limiting crop yields. The C4 cereal sorghum [ (L.) Moench] is a critical food, forage, and emerging bioenergy crop that is notably drought-tolerant. We conducted a large-scale field experiment, imposing preflowering and postflowering drought stress on 2 genotypes of sorghum across a tightly resolved time series, from plant emergence to postanthesis, resulting in a dataset of nearly 400 transcriptomes. We observed a fast and global transcriptomic response in leaf and root tissues with clear temporal patterns, including modulation of well-known drought pathways. We also identified genotypic differences in core photosynthesis and reactive oxygen species scavenging pathways, highlighting possible mechanisms of drought tolerance and of the delayed senescence, characteristic of the stay-green phenotype. Finally, we discovered a large-scale depletion in the expression of genes critical to arbuscular mycorrhizal (AM) symbiosis, with a corresponding drop in AM fungal mass in the plants' roots. 10.1073/pnas.1907500116
    LCO Receptors Involved in Arbuscular Mycorrhiza Are Functional for Rhizobia Perception in Legumes. Girardin Ariane,Wang Tongming,Ding Yi,Keller Jean,Buendia Luis,Gaston Mégane,Ribeyre Camille,Gasciolli Virginie,Auriac Marie-Christine,Vernié Tatiana,Bendahmane Abdelhafid,Ried Martina Katharina,Parniske Martin,Morel Patrice,Vandenbussche Michiel,Schorderet Martine,Reinhardt Didier,Delaux Pierre-Marc,Bono Jean-Jacques,Lefebvre Benoit Current biology : CB Bacterial lipo-chitooligosaccharides (LCOs) are key mediators of the nitrogen-fixing root nodule symbiosis (RNS) in legumes. The isolation of LCOs from arbuscular mycorrhizal fungi suggested that LCOs are also signaling molecules in arbuscular mycorrhiza (AM). However, the corresponding plant receptors have remained uncharacterized. Here we show that petunia and tomato mutants in the LysM receptor-like kinases LYK10 are impaired in AM formation. Petunia and tomato LYK10 proteins have a high affinity for LCOs (Kd in the nM range) comparable to that previously reported for a legume LCO receptor essential for the RNS. Interestingly, the tomato and petunia LYK10 promoters, when introduced into a legume, were active in nodules similarly to the promoter of the legume orthologous gene. Moreover, tomato and petunia LYK10 coding sequences restored nodulation in legumes mutated in their orthologs. This combination of genetic and biochemical data clearly pinpoints Solanaceous LYK10 as part of an ancestral LCO perception system involved in AM establishment, which has been directly recruited during evolution of the RNS in legumes. 10.1016/j.cub.2019.11.038
    A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. Zeng Tian,Rodriguez-Moreno Luis,Mansurkhodzaev Artem,Wang Peng,van den Berg Willy,Gasciolli Virginie,Cottaz Sylvain,Fort Sébastien,Thomma Bart P H J,Bono Jean-Jacques,Bisseling Ton,Limpens Erik The New phytologist Arbuscular mycorrhizal (AM) fungi greatly improve mineral uptake by host plants in nutrient-depleted soil and can intracellularly colonize root cortex cells in the vast majority of higher plants. However, AM fungi possess common fungal cell wall components such as chitin that can be recognized by plant chitin receptors to trigger immune responses, raising the question as to how AM fungi effectively evade chitin-triggered immune responses during symbiosis. In this study, we characterize a secreted lysin motif (LysM) effector identified from the model AM fungal species Rhizophagus irregularis, called RiSLM. RiSLM is one of the highest expressed effector proteins in intraradical mycelium during the symbiosis. In vitro binding assays show that RiSLM binds chitin-oligosaccharides and can protect fungal cell walls from chitinases. Moreover, RiSLM efficiently interferes with chitin-triggered immune responses, such as defence gene induction and reactive oxygen species production in Medicago truncatula. Although RiSLM also binds to symbiotic (lipo)chitooligosaccharides it does not interfere significantly with symbiotic signalling in Medicago. Host-induced gene silencing of RiSLM greatly reduces fungal colonization levels. Taken together, our results reveal a key role for AM fungal LysM effectors to subvert chitin-triggered immunity in symbiosis, pointing to a common role for LysM effectors in both symbiotic and pathogenic fungi. 10.1111/nph.16245
    The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice. Choi Jeongmin,Lee Tak,Cho Jungnam,Servante Emily K,Pucker Boas,Summers William,Bowden Sarah,Rahimi Mehran,An Kyungsook,An Gynheung,Bouwmeester Harro J,Wallington Emma J,Oldroyd Giles,Paszkowski Uta Nature communications Most plants associate with beneficial arbuscular mycorrhizal (AM) fungi that facilitate soil nutrient acquisition. Prior to contact, partner recognition triggers reciprocal genetic remodelling to enable colonisation. The plant Dwarf14-Like (D14L) receptor conditions pre-symbiotic perception of AM fungi, and also detects the smoke constituent karrikin. D14L-dependent signalling mechanisms, underpinning AM symbiosis are unknown. Here, we present the identification of a negative regulator from rice, which operates downstream of the D14L receptor, corresponding to the homologue of the Arabidopsis thaliana Suppressor of MAX2-1 (AtSMAX1) that functions in karrikin signalling. We demonstrate that rice SMAX1 is a suppressor of AM symbiosis, negatively regulating fungal colonisation and transcription of crucial signalling components and conserved symbiosis genes. Similarly, rice SMAX1 negatively controls strigolactone biosynthesis, demonstrating an unexpected crosstalk between the strigolactone and karrikin signalling pathways. We conclude that removal of SMAX1, resulting from D14L signalling activation, de-represses essential symbiotic programmes and increases strigolactone hormone production. 10.1038/s41467-020-16021-1
    Functional analysis of the OsNPF4.5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants. Wang Shuangshuang,Chen Aiqun,Xie Kun,Yang Xiaofeng,Luo Zhenzhen,Chen Jiadong,Zeng Dechao,Ren Yuhan,Yang Congfan,Wang Lingxiao,Feng Huimin,López-Arredondo Damar Lizbeth,Herrera-Estrella Luis Rafael,Xu Guohua Proceedings of the National Academy of Sciences of the United States of America Low availability of nitrogen (N) is often a major limiting factor to crop yield in most nutrient-poor soils. Arbuscular mycorrhizal (AM) fungi are beneficial symbionts of most land plants that enhance plant nutrient uptake, particularly of phosphate. A growing number of reports point to the substantially increased N accumulation in many mycorrhizal plants; however, the contribution of AM symbiosis to plant N nutrition and the mechanisms underlying the AM-mediated N acquisition are still in the early stages of being understood. Here, we report that inoculation with AM fungus remarkably promoted rice () growth and N acquisition, and about 42% of the overall N acquired by rice roots could be delivered via the symbiotic route under N-NO supply condition. Mycorrhizal colonization strongly induced expression of the putative nitrate transporter gene in rice roots, and its orthologs in and in OsNPF4.5 is exclusively expressed in the cells containing arbuscules and displayed a low-affinity NO transport activity when expressed in oocytes. Moreover, knockout of resulted in a 45% decrease in symbiotic N uptake and a significant reduction in arbuscule incidence when NO was supplied as an N source. Based on our results, we propose that the NPF4.5 plays a key role in mycorrhizal NO acquisition, a symbiotic N uptake route that might be highly conserved in gramineous species. 10.1073/pnas.2000926117
    Plant nutrient-acquisition strategies drive topsoil microbiome structure and function. Bahram Mohammad,Netherway Tarquin,Hildebrand Falk,Pritsch Karin,Drenkhan Rein,Loit Kaire,Anslan Sten,Bork Peer,Tedersoo Leho The New phytologist Plant nutrient-acquisition strategies drive soil processes and vegetation performance, but their effect on the soil microbiome remains poorly understood. This knowledge is important to predict the shifts in microbial diversity and functions due to increasing changes in vegetation traits under global change. Here we documented the topsoil microbiomes of 145 boreal and temperate terrestrial sites in the Baltic region that broadly differed in vegetation type and nutritional traits, such as mycorrhizal types and symbiotic nitrogen-fixation. We found that sites dominated by arbuscular mycorrhizal (AM) vegetation harbor relatively more AM fungi, bacteria, fungal saprotrophs, and pathogens in the topsoil compared with sites dominated by ectomycorrhizal (EM) plants. These differences in microbiome composition reflect the rapid nutrient cycling and negative plant-soil feedback in AM soils. Lower fungal diversity and bacteria : fungi ratios in EM-dominated habitats are driven by monodominance of woody vegetation as well as soil acidification by EM fungi, which are associated with greater diversity and relative abundance of carbohydrate-active enzymes. Our study suggests that shifts in vegetation related to global change and land use may strongly alter the topsoil microbiome structure and function. 10.1111/nph.16598
    Myristate and the ecology of AM fungi: significance, opportunities, applications and challenges. Rillig Matthias C,Aguilar-Trigueros Carlos A,Anderson Ian C,Antonovics Janis,Ballhausen Max-Bernhard,Bergmann Joana,Bielcik Milos,Chaudhary V Bala,Deveautour Coline,Grünfeld Leonie,Hempel Stefan,Lakovic Milica,Lammel Daniel R,Lehmann Anika,Lehmann Johannes,Leifheit Eva F,Liang Yun,Li Erqin,Lozano Yudi M,Manntschke Annette,Mansour India,Oviatt Peter,Pinek Liliana,Powell Jeff R,Roy Julien,Ryo Masahiro,Sosa-Hernández Moisés A,Veresoglou Stavros D,Wang Dongwei,Yang Gaowen,Zhang Haiyang The New phytologist A recent study by Sugiura and coworkers reported the non-symbiotic growth and spore production of an arbuscular mycorrhizal (AM) fungus, Rhizophagus irregularis, when the fungus received an external supply of certain fatty acids, myristates (C:14). This discovery follows the insight that AM fungi receive fatty acids from their hosts when in symbiosis. If this result holds up and can be repeated under nonsterile conditions and with a broader range of fungi, it has numerous consequences for our understanding of AM fungal ecology, from the level of the fungus, at the plant community level, and to functional consequences in ecosystems. In addition, myristate may open up several avenues from a more applied perspective, including improved fungal culture and supplementation of AM fungi or inoculum in the field. We here map these potential opportunities, and additionally offer thoughts on potential risks of this potentially new technology. Lastly, we discuss the specific research challenges that need to be overcome to come to an understanding of the potential role of myristate in AM ecology. 10.1111/nph.16527
    Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi. Sugiura Yuta,Akiyama Rei,Tanaka Sachiko,Yano Koji,Kameoka Hiromu,Marui Shiori,Saito Masanori,Kawaguchi Masayoshi,Akiyama Kohki,Saito Katsuharu Proceedings of the National Academy of Sciences of the United States of America Arbuscular mycorrhizal (AM) fungi, forming symbiotic associations with land plants, are obligate symbionts that cannot complete their natural life cycle without a host. The fatty acid auxotrophy of AM fungi is supported by recent studies showing that lipids synthesized by the host plants are transferred to the fungi, and that the latter lack genes encoding cytosolic fatty acid synthases. Therefore, to establish an asymbiotic cultivation system for AM fungi, we tried to identify the fatty acids that could promote biomass production. To determine whether AM fungi can grow on medium supplied with fatty acids or lipids under asymbiotic conditions, we tested eight saturated or unsaturated fatty acids (C12 to C18) and two β-monoacylglycerols. Only myristate (C14:0) led to an increase in the biomass of , inducing extensive hyphal growth and formation of infection-competent secondary spores. However, such spores were smaller than those generated symbiotically. Furthermore, we demonstrated that can take up fatty acids in its branched hyphae and use myristate as a carbon and energy source. Myristate also promoted the growth of and Finally, mixtures of myristate and palmitate accelerated fungal growth and induced a substantial change in fatty acid composition of triacylglycerol compared with single myristate application, although palmitate was not used as a carbon source for cell wall biosynthesis in this culture system. Our findings demonstrate that myristate boosts the asymbiotic growth of AM fungi and can also serve as a carbon and energy source. 10.1073/pnas.2006948117
    Codependency between plant and arbuscular mycorrhizal fungal communities: what is the evidence? Kokkoris Vasilis,Lekberg Ylva,Antunes Pedro M,Fahey Catherine,Fordyce James A,Kivlin Stephanie N,Hart Miranda M The New phytologist That arbuscular mycorrhizal (AM) fungi covary with plant communities is clear, and many papers report nonrandom associations between symbiotic partners. However, these studies do not test the causal relationship, or 'codependency', whereby the composition of one guild affects the composition of the other. Here we outline underlying requirements for codependency, compare important drivers for both plant and AM fungal communities, and assess how host preference - a pre-requisite for codependency - changes across spatiotemporal scales and taxonomic resolution for both plants and AM fungi. We find few examples in the literature designed to test for codependency and those that do have been conducted within plots or mesocosms. Also, while plants and AM fungi respond similarly to coarse environmental filters, most variation remains unexplained, with host identity explaining less than 30% of the variation in AM fungal communities. These results combined question the likelihood of predictable co-occurrence, and therefore evolution of codependency, between plant and AM fungal taxa across locations. We argue that codependency is most likely to occur in homogeneous environments where specific plant - AM fungal pairings have functional consequences for the symbiosis. We end by outlining critical aspects to consider moving forward. 10.1111/nph.16676
    Mycorrhizal symbiosis modulates the rhizosphere microbiota to promote rhizobia-legume symbiosis. Wang Xiaolin,Feng Huan,Wang Yayu,Wang Mingxing,Xie Xingguang,Chang Huizhong,Wang Like,Qu Jicheng,Sun Kai,He Wei,Wang Chunyan,Dai Chuanchao,Chu Zhaohui,Tian Changfu,Yu Nan,Zhang Xuebin,Liu Huan,Wang Ertao Molecular plant Plants establish symbioses with mutualistic fungi, such as arbuscular mycorrhizal (AM) fungi, and bacteria, such as rhizobia, to exchange key nutrients and thrive. Plants and symbionts have coevolved and represent vital components of terrestrial ecosystems. Plants employ an ancestral AM signaling pathway to establish intracellular symbioses, including the legume-rhizobia symbiosis, in their roots. Nevertheless, the relationship between the AM and rhizobial symbioses in native soil is poorly understood. Here, we examined how these distinct symbioses affect root-associated bacterial communities in Medicago truncatula by performing quantitative microbiota profiling (QMP) of 16S rRNA genes. We found that M. truncatula mutants that cannot establish AM or rhizobia symbiosis have an altered microbial load (quantitative abundance) in the rhizosphere and roots, and in particular that AM symbiosis is required to assemble a normal quantitative root-associated microbiota in native soil. Moreover, quantitative microbial co-abundance network analyses revealed that AM symbiosis affects Rhizobiales hubs among plant microbiota and benefits the plant holobiont. Through QMP of rhizobial rpoB and AM fungal SSU rRNA genes, we revealed a new layer of interaction whereby AM symbiosis promotes rhizobia accumulation in the rhizosphere of M. truncatula. We further showed that AM symbiosis-conditioned microbial communities within the M. truncatula rhizosphere could promote nodulation in different legume plants in native soil. Given that the AM and rhizobial symbioses are critical for crop growth, our findings might inform strategies to improve agricultural management. Moreover, our work sheds light on the co-evolution of these intracellular symbioses during plant adaptation to native soil conditions. 10.1016/j.molp.2020.12.002
    Light availability and light demand of plants shape the arbuscular mycorrhizal fungal communities in their roots. Neuenkamp Lena,Zobel Martin,Koorem Kadri,Jairus Teele,Davison John,Öpik Maarja,Vasar Martti,Moora Mari Ecology letters Plants involved in the arbuscular mycorrhizal (AM) symbiosis trade photosynthetically derived carbon for fungal-provided soil nutrients. However, little is known about how plant light demand and ambient light conditions influence root-associating AM fungal communities. We conducted a manipulative field experiment to test whether plants' shade-tolerance influences their root AM fungal communities in open and shaded grassland sites. We found similar light-dependent shifts in AM fungal community structure for experimental bait plant roots and the surrounding soil. Yet, deviation from the surrounding soil towards lower AM fungal beta-diversity in the roots of shade-intolerant plants in shade suggested preferential carbon allocation to specific AM fungi in conditions where plant-assimilated carbon available to fungi was limited. We conclude that favourable environmental conditions widen the plant biotic niche, as demonstrated here with optimal light availability reducing plants' selectivity for specific AM fungi, and promote compatibility with a larger number of AM fungal taxa. 10.1111/ele.13656
    VAPYRIN attenuates defence by repressing PR gene induction and localized lignin accumulation during arbuscular mycorrhizal symbiosis of Petunia hybrida. Chen Min,Bruisson Sébastien,Bapaume Laure,Darbon Geoffrey,Glauser Gaëtan,Schorderet Martine,Reinhardt Didier The New phytologist The intimate association of host and fungus in arbuscular mycorrhizal (AM) symbiosis can potentially trigger induction of host defence mechanisms against the fungus, implying that successful symbiosis requires suppression of defence. We addressed this phenomenon by using AM-defective vapyrin (vpy) mutants in Petunia hybrida, including a new allele (vpy-3) with a transposon insertion close to the ATG start codon. We explore whether abortion of fungal infection in vpy mutants is associated with the induction of defence markers, such as cell wall alterations, accumulation of reactive oxygen species (ROS), defence hormones and induction of pathogenesis-related (PR) genes. We show that vpy mutants exhibit a strong resistance against intracellular colonization, which is associated with the generation of cell wall appositions (papillae) with lignin impregnation at fungal entry sites, while no accumulation of defence hormones, ROS or callose was observed. Systematic analysis of PR gene expression revealed that several PR genes are induced in mycorrhizal roots of the wild-type, and even more in vpy plants. Some PR genes are induced exclusively in vpy mutants. Our results suggest that VPY is involved in avoiding or suppressing the induction of a cellular defence syndrome that involves localized lignin deposition and PR gene induction. 10.1111/nph.17109
    Mycology: Rediscovery of a lost model fungus highlights the origin of mycorrhizal symbioses. Current biology : CB Arbuscular mycorrhizae (AM) are the most frequent symbioses of land plants. By reisolating a long-lost fungus from nature, a new study cracks the genomics of an enigmatic fungal-cyanobacterial partnership and reestablishes a valuable model for understanding the AM symbiosis. 10.1016/j.cub.2021.02.006
    Host identity influences nuclear dynamics in arbuscular mycorrhizal fungi. Kokkoris Vasilis,Chagnon Pierre-Luc,Yildirir Gökalp,Clarke Kelsey,Goh Dane,MacLean Allyson M,Dettman Jeremy,Stefani Franck,Corradi Nicolas Current biology : CB The arbuscular mycorrhizal fungi (AMF) are involved in one of the most ecologically important symbioses on the planet, occurring within the roots of most land plants. Knowledge of even basic elements of AM fungal biology is still poor, with the discovery that AMF may in fact have a sexual life cycle being only very recently reported. AMF produce asexual spores that contain up to several thousand individual haploid nuclei of either largely uniform genotypes (AMF homokaryons) or nuclei originating from two parental genotypes (AMF dikaryons or heterokaryons). In contrast to the sexual dikaryons in the phyla Ascomycota and Basidiomycota, in which pairs of nuclei coexist in single hyphal compartments, AMF dikaryons carry several thousand nuclei in a coenocytic mycelium. Here, we set out to better understand the dynamics of this unique multinucleate condition by combining molecular analyses with advanced microscopy and modeling. Herein, we report that select AMF dikaryotic strains carry the distinct nucleotypes in equal proportions to one another, whereas others show an unequal distribution of parental nucleotypes. In both cases, the relative proportions within a given strain are inherently stable. Simulation models suggest that AMF dikaryons may be maintained through nuclear cooperation dynamics. Remarkably, we report that these nuclear ratios shift dramatically in response to plant host identity, revealing a previously unknown layer of genetic complexity and dynamism within the intimate interactions that occur between the partners of a prominent terrestrial symbiosis. 10.1016/j.cub.2021.01.035
    A nuclear-targeted effector of Rhizophagus irregularis interferes with histone 2B mono-ubiquitination to promote arbuscular mycorrhisation. Wang Peng,Jiang Henan,Boeren Sjef,Dings Harm,Kulikova Olga,Bisseling Ton,Limpens Erik The New phytologist Arguably, symbiotic arbuscular mycorrhizal (AM) fungi have the broadest host range of all fungi, being able to intracellularly colonise root cells in the vast majority of all land plants. This raises the question how AM fungi effectively deal with the immune systems of such a widely diverse range of plants. Here, we studied the role of a nuclear-localisation signal-containing effector from Rhizophagus irregularis, called Nuclear Localised Effector1 (RiNLE1), that is highly and specifically expressed in arbuscules. We showed that RiNLE1 is able to translocate to the host nucleus where it interacts with the plant core nucleosome protein histone 2B (H2B). RiNLE1 is able to impair the mono-ubiquitination of H2B, which results in the suppression of defence-related gene expression and enhanced colonisation levels. This study highlights a novel mechanism by which AM fungi can effectively control plant epigenetic modifications through direct interaction with a core nucleosome component. Homologues of RiNLE1 are found in a range of fungi that establish intimate interactions with plants, suggesting that this type of effector may be more widely recruited to manipulate host defence responses. 10.1111/nph.17236
    How and where do disturbances promote the establishment of nonnative mycorrhizal plants at high elevations? Bueno C Guillermo,Hiiesalu Inga,Koorem Kadri The New phytologist 10.1111/nph.17274
    A mycorrhiza-associated receptor-like kinase with an ancient origin in the green lineage. Montero Héctor,Lee Tak,Pucker Boas,Ferreras-Garrucho Gabriel,Oldroyd Giles,Brockington Samuel F,Miyao Akio,Paszkowski Uta Proceedings of the National Academy of Sciences of the United States of America Receptor-like kinases (RLKs) are key cell signaling components. The rice ARBUSCULAR RECEPTOR-LIKE KINASE 1 (OsARK1) regulates the arbuscular mycorrhizal (AM) association postarbuscule development and belongs to an undefined subfamily of RLKs. Our phylogenetic analysis revealed that has an ancient paralogue in spermatophytes, Single and double mutants in rice showed a nonredundant AM symbiotic function for Global transcriptomics identified a set of genes coregulated by the two RLKs, suggesting that and orchestrate symbiosis in a common pathway. ARK lineage proteins harbor a newly identified SPARK domain in their extracellular regions, which underwent parallel losses in ARK1 and ARK2 in monocots. This protein domain has ancient origins in streptophyte algae and defines additional overlooked groups of putative cell surface receptors. 10.1073/pnas.2105281118
    Arsenic transformation and volatilization by arbuscular mycorrhizal symbiosis under axenic conditions. Li Jinglong,Chen Baodong,Zhang Xin,Hao Zhipeng,Zhang Xuemeng,Zhu Yongguan Journal of hazardous materials It is well known that arbuscular mycorrhizal (AM) fungi can enhance plant arsenic (As) resistance by influencing As uptake, translocation, and speciation; however, As transformation and volatilization by an entire plant inoculated with AM fungus remains uninvestigated. In the present study, AM symbiosis of Rhizophagus irregularis with unbroken Medicago sativa was successfully established in vitro. Afterwards, five concentrations of arsenate were applied to the culture media. The results showed that AM inoculation could methylate inorganic As into dimethylarsinic acid (DMA), dimethylarsine (DMAsH), and trimethylarsine (TMAs), which were detected in the plants, media, or air. Volatile As, accounting for a small proportion of total organic As, appeared under high arsenate exposure, accompanied by remarkable upregulation of root RiMT-11, an arsenite methyltransferase gene in R. irregularis. In addition, AM colonization significantly increased arsenite percentages in plant tissues and external media. Regardless of As species, AM inoculation tended to release the transformed As into the environment rather than transfer them to plant tissues. Our present study, for the first time, comprehensively verified As methylation, volatilization, and reduction by AM fungus associated with the entire plant under absolute axenic conditions and gained a deeper insight into As metabolism in AM symbionts. 10.1016/j.jhazmat.2021.125390