The Auxin-Regulated Protein ZmAuxRP1 Coordinates the Balance between Root Growth and Stalk Rot Disease Resistance in Maize.
Ye Jianrong,Zhong Tao,Zhang Dongfeng,Ma Chuanyu,Wang Lina,Yao Lishan,Zhang Qianqian,Zhu Mang,Xu Mingliang
Molecular plant
To optimize fitness, plants must efficiently allocate their resources between growth and defense. Although phytohormone crosstalk has emerged as a major player in balancing growth and defense, the genetic basis by which plants manage this balance remains elusive. We previously identified a quantitative disease-resistance locus, qRfg2, in maize (Zea mays) that protects against the fungal disease Gibberella stalk rot. Here, through map-based cloning, we demonstrate that the causal gene at qRfg2 is ZmAuxRP1, which encodes a plastid stroma-localized auxin-regulated protein. ZmAuxRP1 responded quickly to pathogen challenge with a rapid yet transient reduction in expression that led to arrested root growth but enhanced resistance to Gibberella stalk rot and Fusarium ear rot. ZmAuxRP1 was shown to promote the biosynthesis of indole-3-acetic acid (IAA), while suppressing the formation of benzoxazinoid defense compounds. ZmAuxRP1 presumably acts as a resource regulator modulating indole-3-glycerol phosphate and/or indole flux at the branch point between the IAA and benzoxazinoid biosynthetic pathways. The concerted interplay between IAA and benzoxazinoids can regulate the growth-defense balance in a timely and efficient manner to optimize plant fitness.
10.1016/j.molp.2018.10.005
Integrating Hormone- and Micromolecule-Mediated Signaling with Plasmodesmal Communication.
Han Xiao,Kim Jae-Yean
Molecular plant
Intercellular and supracellular communications through plasmodesmata are involved in vital processes for plant development and physiological responses. Micro- and macromolecules, including hormones, RNA, and proteins, serve as biological information vectors that traffic through the plasmodesmata between cells. Previous studies demonstrated that the plasmodesmata are elaborately regulated, whereby a long queue of multiple signaling molecules forms. However, the mechanism by which these signals are coupled or coordinated in terms of simultaneous transport in a single channel remains a puzzle. In the last few years, several phytohormones that could function as both non-cell-autonomous signals and plasmodesmal regulators have been disclosed. Plasmodesmal regulators such as auxin, salicylic acid, reactive oxygen species, gibberellic acids, chitin, and jasmonic acid could regulate intercellular trafficking by adjusting plasmodesmal permeability. Here, callose, along with β-glucan synthase and β-glucanase, plays a critical role in regulating plasmodesmal permeability. Interestingly, most of the previously identified regulators are capable of diffusing through the plasmodesmata. Given the small sizes of these molecules, the plasmodesmata are prominent intercellular channels that allow diffusion-based movement of those signaling molecules. Obviously, intercellular communication is under the control of a major mechanism, named a feedback loop, at the plasmodesmata, which mediates complicated biological behaviors. Prospective research on the mechanism of coupling micromolecules at the plasmodesmata for developmental signaling and nutrient provision will help us to understand how plants coordinate their development and photosynthetic assimilation, which is important for agriculture.
10.1016/j.molp.2015.08.015
Roles of Defense Hormones in the Regulation of Ozone-Induced Changes in Gene Expression and Cell Death.
Xu Enjun,Vaahtera Lauri,Brosché Mikael
Molecular plant
Apoplast, the diffusional space between plant cell plasma membranes, is an important medium for signaling within and between the cells. Apoplastic reactive oxygen species (ROS) are crucial signaling molecules in various biological processes. ROS signaling is interconnected with the response to several hormones, including jasmonic acid (JA), salicylic acid (SA) and ethylene. Using ozone (O3) to activate apoplastic ROS signaling, we performed global and targeted analysis of transcriptional changes and cell death assays to dissect the contribution of hormone signaling and various transcription factors (TFs) in the regulation of gene expression and cell death. The contributions of SA, JA, and ethylene were assessed through analysis of single, double, and triple mutants deficient in biosynthesis or signaling for all three hormones. Even in the triple mutant, the global gene expression responses to O3 were mostly similar to the wild-type. Cell death in the JA receptor mutant coi1-16 was suppressed by impairment of the NADPH oxidase RBOHF, suggesting a role for a ROS signal in limiting the spread of cell death. In response to apoplastic ROS, there is not a single signaling pathway that regulates gene expression or cell death. Instead, several pathways regulate the apoplastic ROS response via combinatorial or overlapping mechanisms.
10.1016/j.molp.2015.08.008
Suppression of Jasmonic Acid-Mediated Defense by Viral-Inducible MicroRNA319 Facilitates Virus Infection in Rice.
Zhang Chao,Ding Zuomei,Wu Kangcheng,Yang Liang,Li Yang,Yang Zhen,Shi Shan,Liu Xiaojuan,Zhao Shanshan,Yang Zhirui,Wang Yu,Zheng Luping,Wei Juan,Du Zhenguo,Zhang Aihong,Miao Hongqin,Li Yi,Wu Zujian,Wu Jianguo
Molecular plant
MicroRNAs (miRNAs) are pivotal modulators of plant development and host-virus interactions. However, the roles and action modes of specific miRNAs involved in viral infection and host susceptibility remain largely unclear. In this study, we show that Rice ragged stunt virus (RRSV) infection caused increased accumulation of miR319 but decreased expression of miR319-regulated TCP (TEOSINTE BRANCHED/CYCLOIDEA/PCF) genes, especially TCP21, in rice plants. Transgenic rice plants overexpressing miR319 or downregulating TCP21 exhibited disease-like phenotypes and showed significantly higher susceptibility to RRSV in comparison with the wild-type plants. In contrast, only mild disease symptoms were observed in RRSV-infected lines overexpressing TCP21 and especially in the transgenic plants overexpressing miR319-resistant TCP21. Both RRSV infection and overexpression of miR319 caused the decreased endogenous jasmonic acid (JA) levels along with downregulated expression of JA biosynthesis and signaling-related genes in rice. However, treatment of rice plants with methyl jasmonate alleviated disease symptoms caused by RRSV and reduced virus accumulation. Taken together, our results suggest that the induction of miR319 by RRSV infection in rice suppresses JA-mediated defense to facilitate virus infection and symptom development.
10.1016/j.molp.2016.06.014
Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs.
Nature communications
Plants resist infection and herbivory with innate immune responses that are often associated with reduced growth. Despite the importance of growth-defense tradeoffs in shaping plant productivity in natural and agricultural ecosystems, the molecular mechanisms that link growth and immunity are poorly understood. Here, we demonstrate that growth-defense tradeoffs mediated by the hormone jasmonate are uncoupled in an Arabidopsis mutant (jazQ phyB) lacking a quintet of Jasmonate ZIM-domain transcriptional repressors and the photoreceptor phyB. Analysis of epistatic interactions between jazQ and phyB reveal that growth inhibition associated with enhanced anti-insect resistance is likely not caused by diversion of photoassimilates from growth to defense but rather by a conserved transcriptional network that is hardwired to attenuate growth upon activation of jasmonate signalling. The ability to unlock growth-defense tradeoffs through relief of transcription repression provides an approach to assemble functional plant traits in new and potentially useful ways.
10.1038/ncomms12570
Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals.
Kong Chui-Hua,Zhang Song-Zhu,Li Yong-Hua,Xia Zhi-Chao,Yang Xue-Fang,Meiners Scott J,Wang Peng
Nature communications
Plant neighbor detection and response strategies are important mediators of interactions among species. Despite increasing knowledge of neighbor detection and response involving plant volatiles, less is known about how soil-borne signaling chemicals may act belowground in plant-plant interactions. Here, we experimentally demonstrate neighbor detection and allelopathic responses between wheat and 100 other plant species via belowground signaling. Wheat can detect both conspecific and heterospecific neighbors and responds by increasing allelochemical production. Furthermore, we show that (-)-loliolide and jasmonic acid are present in root exudates from a diverse range of species and are able to trigger allelochemical production in wheat. These findings suggest that root-secreted (-)-loliolide and jasmonic acid are involved in plant neighbor detection and allelochemical response and may be widespread mediators of belowground plant-plant interactions.
10.1038/s41467-018-06429-1
A fungal monooxygenase-derived jasmonate attenuates host innate immunity.
Patkar Rajesh N,Benke Peter I,Qu Ziwei,Chen Yuan Yi Constance,Yang Fan,Swarup Sanjay,Naqvi Naweed I
Nature chemical biology
Distinct modifications fine-tune the activity of jasmonic acid (JA) in regulating plant growth and immunity. Hydroxylated JA (12OH-JA) promotes flower and tuber development but prevents induction of JA signaling, plant defense or both. However, biosynthesis of 12OH-JA has remained elusive. We report here an antibiotic biosynthesis monooxygenase (Abm) that converts endogenous free JA into 12OH-JA in the model rice blast fungus Magnaporthe oryzae. Such fungal 12OH-JA is secreted during host penetration and helps evade the defense response. Loss of Abm in M. oryzae led to accumulation of methyl JA (MeJA), which induces host defense and blocks invasive growth. Exogenously added 12OH-JA markedly attenuated abmΔ-induced immunity in rice. Notably, Abm itself is secreted after invasion and most likely converts plant JA into 12OH-JA to facilitate host colonization. This study sheds light on the chemical arms race during plant-pathogen interaction, reveals Abm as an antifungal target and outlines a synthetic strategy for transformation of a versatile small-molecule phytohormone.
10.1038/nchembio.1885
Stressed Out About Hormones: How Plants Orchestrate Immunity.
Bürger Marco,Chory Joanne
Cell host & microbe
Plants are under relentless challenge by pathogenic bacteria, fungi, and oomycetes, for whom they provide a resource of living space and nutrients. Upon detection of pathogens, plants carry out multiple layers of defense response, orchestrated by a tightly organized network of hormones. In this review, we provide an overview of the phytohormones involved in immunity and the ways pathogens manipulate their biosynthesis and signaling pathways. We highlight recent developments, including the discovery of a defense signaling molecule, new insights into hormone biosynthesis, and the increasing importance of signaling hubs at which hormone pathways intersect.
10.1016/j.chom.2019.07.006
CATALASE2 Coordinates SA-Mediated Repression of Both Auxin Accumulation and JA Biosynthesis in Plant Defenses.
Yuan Hong-Mei,Liu Wen-Cheng,Lu Ying-Tang
Cell host & microbe
Plants defend against pathogen attack by modulating auxin signaling and activating the salicylic acid (SA) and jasmonic acid (JA) signaling pathways. SA and JA act antagonistically in resistance to specific pathogen types, yet how plants coordinate these phytohormones remains elusive. Here we report that biotrophic-pathogen-induced SA accumulation dampens both auxin and JA synthesis by inhibiting CATALASE2 (CAT2) activity in the model plant Arabidopsis. SA suppression of CAT2 results in increased HO levels and subsequent sulfenylation of tryptophan synthetase β subunit 1, thus depleting the auxin biosynthetic precursor tryptophan. In addition, we find that CAT2 promotes JA biosynthesis by facilitating direct interaction of the JA biosynthetic enzymes ACX2 and ACX3, and thus SA repression of CAT2 inhibits JA accumulation. As such, the cat2-1 mutant exhibits increased resistance to biotrophic pathogens and increased susceptibility to necrotrophic pathogens. Our study illustrates how CAT2 coordinates SA repression of auxin accumulation and JA biosynthesis in plant defense.
10.1016/j.chom.2017.01.007
Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity.
Liu Lijing,Sonbol Fathi-Mohamed,Huot Bethany,Gu Yangnan,Withers John,Mwimba Musoki,Yao Jian,He Sheng Yang,Dong Xinnian
Nature communications
It is an apparent conundrum how plants evolved effector-triggered immunity (ETI), involving programmed cell death (PCD), as a major defence mechanism against biotrophic pathogens, because ETI-associated PCD could leave them vulnerable to necrotrophic pathogens that thrive on dead host cells. Interestingly, during ETI, the normally antagonistic defence hormones, salicylic acid (SA) and jasmonic acid (JA) associated with defence against biotrophs and necrotrophs respectively, both accumulate to high levels. In this study, we made the surprising finding that JA is a positive regulator of RPS2-mediated ETI. Early induction of JA-responsive genes and de novo JA synthesis following SA accumulation is activated through the SA receptors NPR3 and NPR4, instead of the JA receptor COI1. We provide evidence that NPR3 and NPR4 may mediate this effect by promoting degradation of the JA transcriptional repressor JAZs. This unique interplay between SA and JA offers a possible explanation of how plants can mount defence against a biotrophic pathogen without becoming vulnerable to necrotrophic pathogens.
10.1038/ncomms13099
Metabolic Basis of Pathogenesis and Host Adaptation in Rice Blast.
Deng Yi Zhen,Naqvi Naweed I
Annual review of microbiology
The blast disease, caused by the ascomycete , poses a great threat to rice production worldwide. Increasing use of fungicides and/or blast-resistant varieties of rice () has proved to be ineffective in long-term control of blast disease under field conditions. To develop effective and durable resistance to blast, it is important to understand the cellular mechanisms underlying pathogenic development in . In this review, we summarize the latest research in phototropism, autophagy, nutrient and redox signaling, and intrinsic phytohormone mimics in for cellular and metabolic adaptation(s) during its interactions with the host plants.
10.1146/annurev-micro-020518-115810
Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice.
Guo Jianping,Xu Chunxue,Wu Di,Zhao Yan,Qiu Yongfu,Wang Xiaoxiao,Ouyang Yidan,Cai Baodong,Liu Xin,Jing Shengli,Shangguan Xinxin,Wang Huiying,Ma Yinhua,Hu Liang,Wu Yan,Shi Shaojie,Wang Wenliang,Zhu Lili,Xu Xun,Chen Rongzhi,Feng Yuqi,Du Bo,He Guangcun
Nature genetics
The brown planthopper (BPH) and white-backed planthopper (WBPH) are the most destructive insect pests of rice, and they pose serious threats to rice production throughout Asia. Thus, there are urgent needs to identify resistance-conferring genes and to breed planthopper-resistant rice varieties. Here we report the map-based cloning and functional analysis of Bph6, a gene that confers resistance to planthoppers in rice. Bph6 encodes a previously uncharacterized protein that localizes to exocysts and interacts with the exocyst subunit OsEXO70E1. Bph6 expression increases exocytosis and participates in cell wall maintenance and reinforcement. A coordinated cytokinin, salicylic acid and jasmonic acid signaling pathway is activated in Bph6-carrying plants, which display broad resistance to all tested BPH biotypes and to WBPH without sacrificing yield, as these plants were found to maintain a high level of performance in a field that was heavily infested with BPH. Our results suggest that a superior resistance gene that evolved long ago in a region where planthoppers are found year round could be very valuable for controlling agricultural insect pests.
10.1038/s41588-018-0039-6
Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae.
Yang Chun-Lin,Liang Shan,Wang Hai-Yun,Han Li-Bo,Wang Fu-Xin,Cheng Huan-Qing,Wu Xiao-Min,Qu Zhan-Liang,Wu Jia-He,Xia Gui-Xian
Molecular plant
In this study, we identified a defense-related major latex protein (MLP) from upland cotton (designated GhMLP28) and investigated its functional mechanism. GhMLP28 transcripts were ubiquitously present in cotton plants, with higher accumulation in the root. Expression of the GhMLP28 gene was induced by Verticillium dahliae inoculation and was responsive to defense signaling molecules, including ethylene, jasmonic acid, and salicylic acid. Knockdown of GhMLP28 expression by virus-induced gene silencing resulted in increased susceptibility of cotton plants to V. dahliae infection, while ectopic overexpression of GhMLP28 in tobacco improved the disease tolerance of the transgenic plants. Further analysis revealed that GhMLP28 interacted with cotton ethylene response factor 6 (GhERF6) and facilitated the binding of GhERF6 to GCC-box element. Transient expression assay demonstrated that GhMLP28 enhanced the transcription factor activity of GhERF6, which led to the augmented expression of some GCC-box genes. GhMLP28 proteins were located in both the nucleus and cytoplasm and their nuclear distribution was dependent on the presence of GhERF6. Collectively, these results demonstrate that GhMLP28 acts as a positive regulator of GhERF6, and synergetic actions of the two proteins may contribute substantially to protection against V. dahliae infection in cotton plants.
10.1016/j.molp.2014.11.023
Jasmonic Acid Oxidase 2 Hydroxylates Jasmonic Acid and Represses Basal Defense and Resistance Responses against Botrytis cinerea Infection.
Smirnova Ekaterina,Marquis Valentin,Poirier Laure,Aubert Yann,Zumsteg Julie,Ménard Rozenn,Miesch Laurence,Heitz Thierry
Molecular plant
Jasmonates (JAs) orchestrate immune responses upon wound/herbivore injury or infection by necrotrophic pathogens. Elucidation of catabolic routes has revealed new complexity in jasmonate metabolism. Two integrated pathways attenuate signaling by turning over the active hormone jasmonoyl-isoleucine (JA-Ile) through ω-oxidation or deconjugation, and define an indirect route forming the derivative 12OH-JA. Here, we provide evidence for a second 12OH-JA formation pathway by direct jasmonic acid (JA) oxidation. Three jasmonic acid oxidases (JAOs) of the 2-oxoglutarate dioxygenase family catalyze specific oxidation of JA to 12OH-JA, and their genes are induced by wounding or infection by the fungus Botrytis cinerea. JAO2 exhibits the highest basal expression, and its deficiency in jao2 mutants strongly enhanced antifungal resistance. The resistance phenotype resulted from constitutive expression of antimicrobial markers rather than from their higher induction in infected jao2 plants and could be reversed by ectopic expression of any of the three JAOs in jao2. Elevated defense in jao2 was dependent on the activity of JASMONATE RESPONSE 1 (JAR1) and CORONATINE-INSENSITIVE 1 (COI1) but was not correlated with enhanced JA-Ile accumulation. Instead, jao2 mutant lines displayed altered accumulation of several JA species in healthy and challenged plants, suggesting elevated metabolic flux through JA-Ile. Collectively, these data identify the missing enzymes hydroxylating JA and uncover an important metabolic diversion mechanism for repressing basal JA defense responses.
10.1016/j.molp.2017.07.010