Biologia plantarum 67:322-333, 2023 | DOI: 10.32615/bp.2023.037
Could a cuticle be an active component of plant immunity?
- Department of Experimental Plant Biology, Faculty of Science, University of South Bohemia in České Budějovice, Branišovská 1645/31a, CZ-37005, České Budějovice, Czech Republic
The cuticle is the first physical barrier between the plant and the outer environment. The cuticle is no longer viewed as a rigid "inert sealer". Components of the cuticle were found to be responsive in their function and chemical composition to environmental signals. Cuticle creation is energy-consuming and complicated. Thus, cuticle composition and renewal dynamics are precisely regulated. Activated plant immunity is also energy "expensive". We briefly summarised our knowledge of the involvement of cuticle in plant-microbe interactions. Changes in cuticle amount and composition affect plant resistance to pathogens and treatment with cutin monomers triggers plant immunity. However, our knowledge about the effects of activated plant immunity on cuticle is scarce. We hypothesise that activated immunity influences cuticle dynamics. Our in-silico gene expression analysis revealed that cuticle biosynthetic genes are modulated under conditions simulating activated immunity. The analysis indicates that the cuticle is not just a rigid component of a plant reaction to the pathogen attack. Strengthening of the cuticle could prevent pathogen penetration. However, inhibition of cuticle production could save the energy needed for plant immunity. We propose questions which should be addressed in future research. Answering them would lead to a better understanding of plant defence against pathogens.
Keywords: cuticle dynamics, gene expression, microbe penetration, plant immunity, wax.
Received: August 14, 2023; Revised: October 30, 2023; Accepted: November 7, 2023; Published online: December 14, 2023 Show citation
References
- Aragón W., Formey D., Aviles-Baltazar N.Y. et al.: Arabidopsis thaliana cuticle composition contributes to differential defense response to Botrytis cinerea. - Front. Plant Sci. 12: 738949, 2021.
Go to original source... - Aragón W., Reina-Pinto J.J., Serrano M.: The intimate talk between plants and microorganisms at the leaf surface. - J. Exp. Bot. 68: 5339-5350, 2017.
Go to original source... - Arya G.C., Cohen H.: The multifaceted roles of fungal cutinases during infection. - J. Fungi 8: 199, 2022.
Go to original source... - Atkin D.S.J., Hamilton R.J.: The changes with age in the epicuticular wax of Sorghum bicolor. - J. Nat. Prod. 45: 697-703, 1982.
Go to original source... - Barthlott W., Neinhuis C.: Purity of the sacred lotus, or escape from contamination in biological surfaces. - Planta 202: 1-8, 1997.
Go to original source... - Bernard A., Domergue F., Pascal S. et al.: Reconstitution of plant alkane biosynthesis in yeast demonstrates that Arabidopsis ECERIFERUM1 and ECERIFERUM3 are core components of a very-long-chain alkane synthesis complex. - Plant Cell 24: 3106-3118, 2012.
Go to original source... - Bernard A., Joubès J.: Arabidopsis cuticular waxes: Advances in synthesis, export and regulation. - Prog. Lipid Res. 52: 110-129, 2013.
Go to original source... - Bessire M., Borel S., Fabre G. et al.: A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. - Plant Cell 23: 1958-1970, 2011.
Go to original source... - Bessire M., Chassot C., Jacquat A.-C. et al.: A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. - EMBO J. 26: 2158-2168, 2007.
Go to original source... - Bhanot V., Fadanavis S.V., Panwar J.: Revisiting the architecture, biosynthesis and functional aspects of the plant cuticle: There is more scope. - Environ. Exp. Bot. 183: 104364, 2021.
Go to original source... - Blanc C., Coluccia F., L'Haridon F. et al.: The cuticle mutant eca2 modifies plant defense responses to biotrophic and necrotrophic pathogens and herbivory insects. - Mol. Plant Microbe. Interact. 31: 344-355, 2018.
Go to original source... - Bourdenx B., Bernard A., Domergue F. et al.: Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. - Plant Physiol. 156: 29-45, 2011.
Go to original source... - Boutrot F., Zipfel C.: Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. - Annu. Rev. Phytopathol. 55: 257-286, 2017.
Go to original source... - Cameron K.D., Teece M.A., Smart L.B.: Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. - Plant Physiol. 140: 176-183, 2006.
Go to original source... - Cassagne C., Lessire R., Bessoule J.J. et al.: Biosynthesis of very long chain fatty acids in higher plants. - Prog. Lipid Res. 33: 55-69, 1994.
Go to original source... - Chassot C., Buchala A., Schoonbeek H. et al.: Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. - Plant J. 55: 555-567, 2008.
Go to original source... - Chassot C., Nawrath C., Métraux J.-P.: Cuticular defects lead to full immunity to a major plant pathogen. - Plant J. 49: 972-980, 2007.
Go to original source... - Dodds P.N., Rathjen J.P.: Plant immunity: Towards an integrated view of plant-pathogen interactions. - Nat. Rev. Genet. 11: 539-548, 2010.
Go to original source... - Edqvist J., Blomqvist K., Nieuwland J., Salminen T.A.: Plant lipid transfer proteins: Are we finally closing in on the roles of these enigmatic proteins? - J. Lipid Res. 59: 1374-1382, 2018.
Go to original source... - Edstam M.M., Viitanen L., Salminen T.A., Edqvist J.: Evolutionary history of the non-specific lipid transfer proteins. - Mol. Plant 4: 947-964, 2011.
Go to original source... - Edwards D.: Cells and tissues in the vegetative sporophytes of early land plants. - New Phytol. 125: 225-247, 1993.
Go to original source... - Fauth M., Schweizer P., Buchala A. et al.: Cutin monomers and surface wax constituents elicit H2O2 in conditioned cucumber hypocotyl segments and enhance the activity of other H2O2 elicitors. - Plant Physiol. 117: 1373-1380, 1998.
Go to original source... - Fich E.A., Segerson N.A., Rose J.K.C.: The plant polyester cutin: biosynthesis, structure, and biological roles. - Annu. Rev. Plant Biol. 67: 207-233, 2016.
Go to original source... - Francis S.A., Dewey F.M., Gurr S.J.: The role of cutinase in germling development and infection by Erysiphe graminis f. sp. hordei. - Physiol. Mol. Plant Pathol. 49: 201-211, 1996.
Go to original source... - Gao L., Burnier A., Huang Y.: Quantifying instantaneous regeneration rates of plant leaf waxes using stable hydrogen isotope labeling. - Rapid Commun. Mass Spectrom. 26: 115-122, 2012.
Go to original source... - Gilbert R.D., Johnson A.M., Dean R.A.: Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. - Physiol. Mol. Plant Pathol. 48: 335-346, 1996.
Go to original source... - Go Y.S., Kim H., Kim H.J. et al.: Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-type transcription factor. - Plant Cell 26: 1666-1680, 2014.
Go to original source... - Greer S., Wen M., Bird D. et al.: The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. - Plant Physiol. 145: 653-667, 2007.
Go to original source... - Hansjakob A., Bischof S., Bringmann G. et al.: Very-long-chain aldehydes promote in vitro prepenetration processes of Blumeria graminis in a dose- and chain length-dependent manner. - New Phytol. 188: 1039-1054, 2010.
Go to original source... - Hansjakob A., Riederer M., Hildebrandt U.: Wax matters: absence of very-long-chain aldehydes from the leaf cuticular wax of the glossy11 mutant of maize compromises the prepenetration processes of Blumeria graminis. - Plant Pathol. 60: 1151-1161, 2011.
Go to original source... - Heredia-Guerrero J.A., Benítez J.J., Heredia A.: Self-assembled polyhydroxy fatty acids vesicles: a mechanism for plant cutin synthesis. - BioEssays 30: 273-277, 2008.
Go to original source... - Hou S., Liu Z., Shen H., Wu D.: Damage-associated molecular pattern-triggered immunity in plants. - Front. Plant Sci. 10: 646, 2019.
Go to original source... - Inada N., Savory E.A.: Inhibition of prepenetration processes of the powdery mildew Golovinomyces orontii on host inflorescence stems is reduced in the Arabidopsis cuticular mutant cer3 but not in cer1. - J. Gen. Plant Pathol. 77: 273-281, 2011.
Go to original source... - Ingram G., Nawrath C.: The roles of the cuticle in plant development: organ adhesions and beyond. - J. Exp. Bot. 68: 5307-5321, 2017.
Go to original source... - Jenks M.A., Tuttle H.A., Feldmann K.A.: Changes in epicuticular waxes on wildtype and eceriferum mutants in Arabidopsis during development. - Phytochemistry 42: 29-34, 1996.
Go to original source... - Jessen D., Roth C., Wiermer M., Fulda M.: Two activities of long-chain acyl-coenzyme A synthetase are involved in lipid trafficking between the endoplasmic reticulum and the plastid in Arabidopsis. - Plant Physiol. 167: 351-366, 2015.
Go to original source... - Jetter R., Schäffer S.: Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. - Plant Physiol. 126: 1725-1737, 2001.
Go to original source... - Jones J.D.G., Dangl J.L.: The plant immune system. - Nature 444: 323-329, 2006.
Go to original source... - Ju S., Go Y.S., Choi H.J. et al.: DEWAX transcription factor is involved in resistance to Botrytis cinerea in Arabidopsis thaliana and Camelina sativa. - Front. Plant Sci. 8: 1210, 2017.
Go to original source... - Kachroo A., Kachroo P.: Salicylic acid-, jasmonic acid- and ethylenemediated regulation of plant defense signaling. - In: Setlow J.K. (ed.): Genetic Engineering. Vol. 28. Pp. 55-83. Springer, Boston 2007.
Go to original source... - Kachroo A., Kachroo P.: Fatty acid-derived signals in plant defense. - Annu. Rev. Phytopathol. 47: 153-176, 2009.
Go to original source... - Kahmen A., Dawson T.E., Vieth A., Sachse D.: Leaf wax n-alkane δD values are determined early in the ontogeny of Populus trichocarpa leaves when grown under controlled environmental conditions. - Plant Cell Environ. 34: 1639-1651, 2011.
Go to original source... - Kamtsikakis A., Baales J., Zeisler-Diehl V.V. et al.: Asymmetric water transport in dense leaf cuticles and cuticle-inspired compositionally graded membranes. - Nat. Commun. 12: 1267, 2021.
Go to original source... - Karbulková J., Schreiber L., Macek P., Šantrůček J.: Differences between water permeability of astomatous and stomatous cuticular membranes: effects of air humidity in two species of contrasting drought-resistance strategy. - J. Exp. Bot. 59: 3987-3995, 2008.
Go to original source... - Kerstiens G.: Cuticular water permeability and its physiological significance. - J. Exp. Bot. 47: 1813-1832, 1996.
Go to original source... - Koch K., Hartmann K.D., Schreiber L. et al.: Influences of air humidity during the cultivation of plants on wax chemical composition, morphology and leaf surface wettability. - Environ. Exp. Bot. 56: 1-9, 2006.
Go to original source... - Kolattukudy E.P., Rogers M.L., Li D. et al.: Surface signaling in pathogenesis. - PNAS 92: 4080-4087, 1995.
Go to original source... - Kong L., Chang C.: Suppression of wheat TaCDK8/TaWIN1 interaction negatively affects germination of Blumeria graminis f. sp. tritici by interfering with very-long-chain aldehyde biosynthesis. - Plant Mol. Biol. 96: 165-178, 2018.
Go to original source... - Kosma D.K., Bourdenx B., Bernard A. et al.: The impact of water deficiency on leaf cuticle lipids of Arabidopsis. - Plant Physiol. 151: 1918-1929, 2009.
Go to original source... - Kubásek J., Kalistová T., Janová J. et al.: 13CO2 labelling as a tool for elucidating the mechanism of cuticle development: a case of Clusia rosea. - New Phytol. 238: 202-215, 2023.
Go to original source... - Kunst L., Samuels A.L.: Biosynthesis and secretion of plant cuticular wax. - Prog. Lipid Res. 42: 51-80, 2003.
Go to original source... - L'Haridon F., Besson-Bard A., Binda M. et al.: A permeable cuticle is associated with the release of reactive oxygen species and induction of innate immunity. - PLoS Pathog. 7: e1002148, 2011.
Go to original source... - Lee S., Fu F., Xu S. et al.: Global regulation of plant immunity by histone lysine methyl transferases. - Plant Cell 28: 1640-1661, 2016.
Go to original source... - Lewandowska M., Keyl A., Feussner I.: Wax biosynthesis in response to danger: its regulation upon abiotic and biotic stress. - New Phytol. 227: 698-713, 2020.
Go to original source... - Li N., Xu C., Li-Beisson Y. et al.: Fatty acid and lipid transport in plant cells. - Trends Plant Sci. 21: 145-158, 2016.
Go to original source... - Li X., Liu N., Sun Y. et al.: The cotton GhWIN2 gene activates the cuticle biosynthesis pathway and influences the salicylic and jasmonic acid biosynthesis pathways. - BMC Plant Biol. 19: 379, 2019.
Go to original source... - Lim G.H., Liu H., Yu K. et al.: The plant cuticle regulates apoplastic transport of salicylic acid during systemic acquired resistance. - Sci. Adv. 6: eeaz0478, 2020.
Go to original source... - Liu J., Chen S., Chen L. et al.: BIK1 cooperates with BAK1 to regulate constitutive immunity and cell death in Arabidopsis. - J. Integr. Plant Biol. 59: 234-239, 2017.
Go to original source... - Macková J., Vašková M., Macek P. et al.: Plant response to drought stress simulated by ABA application: Changes in chemical composition of cuticular waxes. - Environ. Exp. Bot. 86: 70-75, 2013.
Go to original source... - Neinhuis C., Koch K., Barthlott W.: Movement and regeneration of epicuticular waxes through plant cuticles. - Planta 213: 427-434, 2001.
Go to original source... - Niklas K.J., Cobb E.D., Matas A.J.: The evolution of hydrophobic cell wall biopolymers: from algae to angiosperms. - J. Exp. Bot. 68: 5261-5269, 2017.
Go to original source... - Niklas K.J., Kutschera U.: The evolution of the land plant life cycle. - New Phytol. 185: 27-41, 2010.
Go to original source... - Ohlrogge J., Browse J., Jaworski J. et al.: Lipids. - In: Buchanan B.B., Gruissem W., Jones R.L. (ed.): Biochemistry and Molecular Biology of Plants. Pp. 337-400. American Society of Plant Biologists, Hoboken 2015.
- Pascal S., Bernard A., Deslous P. et al.: Arabidopsis CER1-LIKE1 functions in a cuticular very-long-chain alkane-forming complex. - Plant Physiol. 179: 415-432, 2019.
Go to original source... - Pfeilmeier S., Caly D.L., Malone J.G.: Bacterial pathogenesis of plants: future challenges from a microbial perspective. Challenges in bacterial molecular plant pathology. - Mol. Plant Pathol. 17: 1298-1313, 2016.
Go to original source... - Philippe G., Sørensen I., Jiao C. et al.: Cutin and suberin: assembly and origins of specialized lipidic cell wall scaffolds. - Curr. Opin. Plant Biol. 55: 11-20, 2020.
Go to original source... - Podila G.K., Rogers L.M., Kolattukudy P.E.: Chemical signals from avocado surface wax trigger germination and appressorium formation in Colletotrichum gloeosporioides. - Plant Physiol. 103: 267-272, 1993.
Go to original source... - Pollard M., Beisson F., Li Y., Ohlrogge J.B.: Building lipid barriers: biosynthesis of cutin and suberin. - Trends Plant Sci. 13: 236-246, 2008.
Go to original source... - Post-Beittenmiller D.: Biochemistry and molecular biology of wax production in plants. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 405-430, 1996.
Go to original source... - Reis H., Pfiffi S., Hahn M.: Molecular and functional characterization of a secreted lipase from Botrytis cinerea. - Mol. Plant Pathol. 6: 257-267, 2005.
Go to original source... - Richardson A., Franke R., Kerstiens G. et al.: Cuticular wax deposition in growing barley (Hordeum vulgare) leaves commences in relation to the point of emergence of epidermal cells from the sheaths of older leaves. - Planta 222: 472-483, 2005.
Go to original source... - Riederer M., Schreiber L.: Protecting against water loss: analysis of the barrier properties of plant cuticles. - J. Exp. Bot. 52: 2023-2032, 2001.
Go to original source... - Ringelmann A., Riedel M., Riederer M. et al.: Two sides of a leaf blade: Blumeria graminis needs chemical cues in cuticular waxes of Lolium perenne for germination and differentiation. - Planta 230: 95-105, 2009.
Go to original source... - Rowland O., Zheng H., Hepworth S.R. et al.: CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. - Plant Physiol. 142: 866-877, 2006.
Go to original source... - Sachse D., Kahmen A., Gleixner G.: Significant seasonal variation in the hydrogen isotopic composition of leaf-wax lipids for two deciduous tree ecosystems (Fagus sylvativa and Acer pseudoplatanus). - Org. Geochem. 40: 732-742, 2009.
Go to original source... - Samuels L., Kunst L., Jetter R.: Sealing plant surfaces: cuticular wax formation by epidermal cells. - Annu. Rev. Plant Biol. 59: 683-707, 2008.
Go to original source... - Samuels L., McFarlane H.E.: Plant cell wall secretion and lipid traffic at membrane contact sites of the cell cortex. - Protoplasma 249: 19-23, 2012.
Go to original source... - Schreiber L., Skrabs M., Hartmann K.D. et al.: Effect of humidity on cuticular water permeability of isolated cuticular membranes and leaf disks. - Planta 214: 274-282, 2001.
Go to original source... - Schreiber L.: Effect of temperature on cuticular transpiration of isolated cuticular membranes and leaf discs. - J. Exp. Bot. 52: 1893-1900, 2001.
Go to original source... - Schweizer P., Felix G., Buchala A. et al.: Perception of free cutin monomers by plant cells. - Plant J. 10: 331-341, 1996.
Go to original source... - Segado P., Heredia-Guerrero J.A., Heredia A., Domínguez E.: Cutinsomes and CUTIN SYNTHASE1 function sequentially in tomato fruit cutin deposition. - Plant Physiol. 183: 1622-1637, 2020.
Go to original source... - Seo P.J., Park C.-M.: MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. - New Phytol. 186: 471-483, 2010.
Go to original source... - Serrano M., Coluccia F., Torres M. et al.: The cuticle and plant defense to pathogens. - Front. Plant Sci. 5: 274, 2014.
Go to original source... - Shellakkutti N., Thangamani P.D., Suresh K. et al.: Cuticular transpiration is not affected by enhanced wax and cutin amounts in response to osmotic stress in barley. - Physiol. Plantarum 174: e13735, 2022.
Go to original source... - Sieber P., Schorderet M., Ryser U. et al.: Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. - Plant Cell 12: 721-737, 2000.
Go to original source... - Skamnioti P., Gurr S.J.: Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. - Plant Cell 19: 2674-2689, 2007.
Go to original source... - Stępiński D., Kwiatkowska M., Wojtczak A. et al.: The role of cutinsomes in plant cuticle formation. - Cells 9: 1778, 2020.
Go to original source... - Szczuka E., Szczuka A.: Cuticle fluorescence during embryogenesis of Arabidopsis thaliana (L.) Heynh. - Acta Biol. Cracov. Bot. 45: 63-67, 2003.
- Tang D., Simonich M.T., Innes R.W.: Mutations in LACS2, a long-chain acyl-coenzyme A synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. - Plant Physiol. 144: 1093-1103, 2007.
Go to original source... - Voisin D., Nawrath C., Kurdyukov S. et al.: Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator. - PLoS Genet. 5: e1000703, 2009.
Go to original source... - Wang F., Zhang P., Qiang S. et al.: Effects of epicuticular wax from Digitaria sanguinalis and Festuca arundinacea on infection by Curvularia eragrostidis. - Australas. Plant Path. 37: 43-52, 2008.
Go to original source... - Wang X., Kong L., Zhi P., Chang C.: Update on cuticular wax biosynthesis and its roles in plant disease resistance. - Int. J. Mol. Sci. 21: 5514, 2020.
Go to original source... - Wang X., Zhi P., Fan Q. et al.: Wheat CHD3 protein TaCHR729 regulates the cuticular wax biosynthesis required for stimulating germination of Blumeria graminis f. sp. tritici. - J. Exp. Bot. 70: 701-713, 2019.
Go to original source... - Watson G.S., Gellender M., Watson J.A.: Self-propulsion of dew drops on lotus leaves: a potential mechanism for self cleaning. - Biofouling 30: 427-434, 2014.
Go to original source... - Weidenbach D., Jansen M., Franke R.B. et al.: Evolutionary conserved function of barley and Arabidopsis 3-KETOACYL-CoA SYNTHASES in providing wax signals for germination of powdery mildew fungi. - Plant Physiol. 166: 1621-1633, 2014.
Go to original source... - Xia Y., Gao Q.M., Yu K. et al.: An intact cuticle in distal tissues is essential for the induction of systemic acquired resistance in plants. - Cell Host Microbe 5: 151-165, 2009.
Go to original source... - Xiao F., Goodwin S.M., Xiao Y. et al.: Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. - EMBO J. 23: 2903-2913, 2004.
Go to original source... - Xin A., Herburger K.: Mini review: Transport of hydrophobic polymers into the plant apoplast. - Front. Plant Sci. 11: 990, 2021.
Go to original source... - Yang X., Zhao H., Kosma D.K. et al.: The acyl desaturase CER17 is involved in producing wax unsaturated primary alcohols and cutin monomers. - Plant Physiol. 173: 1109-1124, 2017.
Go to original source... - Yeats T.H., Rose J.K.C.: The formation and function of plant cuticles. - Plant Physiol. 163: 5-20, 2013.
Go to original source... - Zeier J., Pink B., Mueller M.J., Berger S.: Light conditions influence specific defence responses in incompatible plant-pathogen interactions: Uncoupling systemic resistance from salicylic acid and PR-1 accumulation. - Planta 219: 673-683, 2004.
Go to original source... - Zeisler-Diehl V., Müller Y., Schreiber L.: Epicuticular wax on leaf cuticles does not establish the transpiration barrier, which is essentially formed by intracuticular wax. - J. Plant Physiol. 227: 66-74, 2018.
Go to original source... - Zeisler V., Schreiber L.: Epicuticular wax on cherry laurel (Prunus laurocerasus) leaves does not constitute the cuticular transpiration barrier. - Planta 243: 65-81, 2016.
Go to original source... - Zhao H., Kosma D.K., Lü S.: Functional role of long-chain acyl-CoA synthetases in plant development and stress responses. - Front. Plant Sci. 12: 640996, 2021.
Go to original source... - Zhao L., Haslam T.M., Sonntag A. et al.: Functional overlap of long-chain acyl-CoA synthetases in Arabidopsis. - Plant Cell Physiol. 60: 1041-1054, 2019.
Go to original source... - Zimmermann P., Hirsch-Hoffmann M., Hennig L., Gruissem W.: GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. - Plant Physiol. 136: 2621-2632, 2004.
Go to original source... - Ziv C., Zhao Z., Gao Y.G., Xia Y.: Multifunctional roles of plant cuticle during plant-pathogen interactions. - Front. Plant Sci. 9: 1088, 2018.
Go to original source...



