Cutinsomes and CUTIN SYNTHASE1 Function Sequentially in Tomato Fruit Cutin Deposition.
Plant physiology
The aerial parts of plants, including the leaves, fruits and non-lignified stems, are covered with a protective cuticle, largely composed of the polyester cutin. Two mechanisms of cutin deposition have been identified in tomato () fruit. The contribution of each mechanism to cutin synthesis and deposition has shown a temporal and coordinated sequence that correlates with the two periods of organ growth, cell division and cell expansion. Cutinsomes, self-assembled particles composed of esterified cutin monomers, are involved in the synthesis of the procuticle during cell division and provide a template for further cutin deposition. CUTIN SYNTHASE1 (CUS1), an acyl transferase enzyme that links cutin monomers, contributes to massive cuticle deposition during the early stages of the cell expansion period by incorporating additional cutin to the procuticle template. However, cutin deposition and polymerization appear to be part of a more complex biological scenario, which is yet not fully understood. CUS1 is also associated with the coordinated growth of the cutinized and non-cutinized domains of the outer epidermal wall, and affects cell size. A dynamic and complex interplay linking cutin synthesis with cell wall development and epidermal cell size has been identified.
10.1104/pp.20.00516
Glandular trichomes: micro-organs with model status?
The New phytologist
Glandular trichomes are epidermal outgrowths that are the site of biosynthesis and storage of large quantities of specialized metabolites. Besides their role in the protection of plants against biotic and abiotic stresses, they have attracted interest owing to the importance of the compounds they produce for human use; for example, as pharmaceuticals, flavor and fragrance ingredients, or pesticides. Here, we review what novel concepts investigations on glandular trichomes have brought to the field of specialized metabolism, particularly with respect to chemical and enzymatic diversity. Furthermore, the next challenges in the field are understanding the metabolic network underlying the high productivity of glandular trichomes and the transport and storage of metabolites. Another emerging area is the development of glandular trichomes. Studies in some model species, essentially tomato, tobacco, and Artemisia, are now providing the first molecular clues, but many open questions remain: How is the distribution and density of different trichome types on the leaf surface controlled? When is the decision for an epidermal cell to differentiate into one type of trichome or another taken? Recent advances in gene editing make it now possible to address these questions and promise exciting discoveries in the near future.
10.1111/nph.16283
Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking.
Horticulture research
Fruit cracking is an important problem in horticultural crop production. Polygalacturonase (SlPG) and expansin (SlEXP1) proteins cooperatively disassemble the polysaccharide network of tomato fruit cell walls during ripening and thereby, enable softening. A Golden 2-like (GLK2) transcription factor, SlGLK2 regulates unripe fruit chloroplast development and results in elevated soluble solids and carotenoids in ripe fruit. To determine whether SlPG, SlEXP1, or SlGLK2 influence the rate of tomato fruit cracking, the incidence of fruit epidermal cracking was compared between wild-type, Ailsa Craig (WT) and fruit with suppressed and expression () or expressing a truncated nonfunctional Slglk2 (). Treating plants with exogenous ABA increases xylemic flow into fruit. Our results showed that ABA treatment of tomato plants greatly increased cracking of fruit from WT and mutant, but not from genotypes. The fruit were firmer, had higher total soluble solids, denser cell walls and thicker cuticles than fruit of the other genotypes. Fruit from the ABA treated fruit had cell walls with less water-soluble and more ionically and covalently-bound pectins than fruit from the other lines, demonstrating that ripening-related disassembly of the fruit cell wall, but not elimination of SlGLK2, influences cracking. Cracking incidence was significantly correlated with cell wall and wax thickness, and the content of cell wall protopectin and cellulose, but not with Ca content.
10.1038/s41438-018-0105-3
Glycerol-3-phosphate acyltransferase 6 controls filamentous pathogen interactions and cell wall properties of the tomato and Nicotiana benthamiana leaf epidermis.
The New phytologist
The leaf outer epidermal cell wall acts as a barrier against pathogen attack and desiccation, and as such is covered by a cuticle, composed of waxes and the polymer cutin. Cutin monomers are formed by the transfer of fatty acids to glycerol by glycerol-3-phosphate acyltransferases, which facilitate their transport to the surface. The extent to which cutin monomers affect leaf cell wall architecture and barrier properties is not known. We report a dual functionality of pathogen-inducible GLYCEROL-3-PHOSPHATE ACYLTRANSFERASE 6 (GPAT6) in controlling pathogen entry and cell wall properties affecting dehydration in leaves. Silencing of Nicotiana benthamiana NbGPAT6a increased leaf susceptibility to infection by the oomycetes Phytophthora infestans and Phytophthora palmivora, whereas overexpression of NbGPAT6a-GFP rendered leaves more resistant. A loss-of-function mutation in tomato SlGPAT6 similarly resulted in increased susceptibility of leaves to Phytophthora infection, concomitant with changes in haustoria morphology. Modulation of GPAT6 expression altered the outer wall diameter of leaf epidermal cells. Moreover, we observed that tomato gpat6-a mutants had an impaired cell wall-cuticle continuum and fewer stomata, but showed increased water loss. This study highlights a hitherto unknown role for GPAT6-generated cutin monomers in influencing epidermal cell properties that are integral to leaf-microbe interactions and in limiting dehydration.
10.1111/nph.15846
The Tomato Genome Encodes SPCH, MUTE, and FAMA Candidates That Can Replace the Endogenous Functions of Their Orthologs.
Frontiers in plant science
Stomatal abundance determines the maximum potential for gas exchange between the plant and the atmosphere. In , it is set during organ development through complex genetic networks linking epidermal differentiation programs with environmental response circuits. Three related bHLH transcription factors, SPCH, MUTE, and FAMA, act as positive drivers of stomata differentiation. Mutant alleles of some of these genes sustain different stomatal numbers in the mature organs and have potential to modify plant performance under different environmental conditions. However, knowledge about stomatal genes in dicotyledoneous crops is scarce. In this work, we identified the putative orthologs of these three master regulators and assessed their functional orthology by their ability to complement loss-of-function mutants, the epidermal phenotypes elicited by their conditional overexpression, and the expression patterns of their promoter regions in . Our results indicate that the tomato proteins are functionally equivalent to their counterparts and that the tomato putative promoter regions display temporal and spatial expression domains similar to those reported for the genes. tracking of tomato stomatal lineages in developing cotyledons revealed cell division and differentiation histories similar to those of . Interestingly, the genome harbors a gene, expressed in leaves but functionally distinct from the true orthologue. Thus, the basic program for stomatal development in uses key conserved genetic determinants. This opens the possibility of modifying stomatal abundance in tomato through previously tested alleles conferring altered stomata abundance phenotypes that correlate with physiological traits related to water status, leaf cooling, or photosynthesis.
10.3389/fpls.2019.01300
The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning.
Shi Jian Xin,Adato Avital,Alkan Noam,He Yonghua,Lashbrooke Justin,Matas Antonio J,Meir Sagit,Malitsky Sergey,Isaacson Tal,Prusky Dov,Leshkowitz Dena,Schreiber Lukas,Granell Antonio R,Widemann Emilie,Grausem Bernard,Pinot Franck,Rose Jocelyn K C,Rogachev Ilana,Rothan Christophe,Aharoni Asaph
The New phytologist
Fleshy tomato fruit typically lacks stomata; therefore, a proper cuticle is particularly vital for fruit development and interaction with the surroundings. Here, we characterized the tomato SlSHINE3 (SlSHN3) transcription factor to extend our limited knowledge regarding the regulation of cuticle formation in fleshy fruits. We created SlSHN3 overexpressing and silenced plants, and used them for detailed analysis of cuticular lipid compositions, phenotypic characterization, and the study on the mode of SlSHN3 action. Heterologous expression of SlSHN3 in Arabidopsis phenocopied overexpression of the Arabidopsis SHNs. Silencing of SlSHN3 results in profound morphological alterations of the fruit epidermis and significant reduction in cuticular lipids. We demonstrated that SlSHN3 activity is mediated by control of genes associated with cutin metabolism and epidermal cell patterning. As with SlSHN3 RNAi lines, mutation in the SlSHN3 target gene, SlCYP86A69, resulted in severe cutin deficiency and altered fruit surface architecture. In vitro activity assays demonstrated that SlCYP86A69 possesses NADPH-dependent ω-hydroxylation activity, particularly of C18:1 fatty acid to the 18-hydroxyoleic acid cutin monomer. This study provided insights into transcriptional mechanisms mediating fleshy fruit cuticle formation and highlighted the link between cutin metabolism and the process of fruit epidermal cell patterning.
10.1111/nph.12032