Fight Hard or Die Trying: Current Status of Lipid Signaling during Plant-Pathogen Interaction
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article, Review
PubMed
34070722
PubMed Central
PMC8228701
DOI
10.3390/plants10061098
PII: plants10061098
Knihovny.cz E-resources
- Keywords
- lipids, microbes, oxylipins, pathogens, phosphatidic acid, plants,
- Publication type
- Journal Article MeSH
- Review MeSH
Plant diseases pose a substantial threat to food availability, accessibility, and security as they account for economic losses of nearly $300 billion on a global scale. Although various strategies exist to reduce the impact of diseases, they can introduce harmful chemicals to the food chain and have an impact on the environment. Therefore, it is necessary to understand and exploit the plants' immune systems to control the spread of pathogens and enable sustainable agriculture. Recently, growing pieces of evidence suggest a functional myriad of lipids to be involved in providing structural integrity, intracellular and extracellular signal transduction mediators to substantial cross-kingdom cell signaling at the host-pathogen interface. Furthermore, some pathogens recognize or exchange plant lipid-derived signals to identify an appropriate host or development, whereas others activate defense-related gene expression. Typically, the membrane serves as a reservoir of lipids. The set of lipids involved in plant-pathogen interaction includes fatty acids, oxylipins, phospholipids, glycolipids, glycerolipids, sphingolipids, and sterols. Overall, lipid signals influence plant-pathogen interactions at various levels ranging from the communication of virulence factors to the activation and implementation of host plant immune defenses. The current review aims to summarize the progress made in recent years regarding the involvement of lipids in plant-pathogen interaction and their crucial role in signal transduction.
See more in PubMed
Mehta S., James D., Reddy M.K. Recent Approaches in Omics for Plant Resilience to Climate Change. Springer; Berlin/Heidelberg, Germany: 2019. Omics technologies for abiotic stress tolerance in plants: Current status and prospects; pp. 1–34.
Sharma P., Sharma M.M.M., Patra A., Vashisth M., Mehta S., Singh B., Tiwari M., Pandey V. Transcription Factors for Abiotic Stress Tolerance in Plants. Elsevier; Amsterdam, The Netherlands: 2020. The role of key transcription factors for cold tolerance in plants; pp. 123–152.
Mehta S., Gogna M., Singh B., Patra A., Singh I.K., Singh A. Plant Stress Biology. Springer; Berlin/Heidelberg, Germany: 2020. Silicon: A plant nutritional “non-entity” for mitigating abiotic stresses; pp. 17–49.
Lal S.K., Kumar S., Sheri V., Mehta S., Varakumar P., Ram B., Borphukan B., James D., Fartyal D., Reddy M.K. Advances in Seed Priming. Springer; Berlin/Heidelberg, Germany: 2018. Seed priming: An emerging technology to impart abiotic stress tolerance in crop plants; pp. 41–50.
Mehta S., Singh B., Dhakate P., Rahman M., Islam M.A. Disease Resistance in Crop Plants. Springer; Berlin/Heidelberg, Germany: 2019. Rice, marker-assisted breeding, and disease resistance; pp. 83–111.
Mohammadi H., Hazrati S., Ghorbanpour M. Plant Life under Changing Environment. Elsevier; Amsterdam, The Netherlands: 2020. Tolerance mechanisms of medicinal plants to abiotic stresses; pp. 663–679.
Mohsin A., Ayesha J., Sajid H.N., Anicet B., Waqas K.K., Aamir L., Imtiaz A.S., Joy O.N. Biotic Stress Triggered Small RNA and RNAi Defense Response in Plants. Mol. Biol. Rep. 2020;47:5511–5522. PubMed
Xu Y. Envirotyping for deciphering environmental impacts on crop plants. Appl. Genet. 2016;129:653–673. doi: 10.1007/s00122-016-2691-5. PubMed DOI PMC
Surówka E., Rapacz M., Janowiak F. Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives I. Springer; Berlin/Heidelberg, Germany: 2020. Climate change influences the interactive effects of simultaneous impact of abiotic and biotic stresses on plants; pp. 1–50.
Pecinka A., Mittelsten Scheid O. Stress-induced chromatin changes: A critical view on their heritability. Plant. Cell Physiol. 2012;53:801–808. doi: 10.1093/pcp/pcs044. PubMed DOI PMC
Goswami K., Mittal D., Gautam B., Sopory S.K., Sanan-Mishra N. Mapping the salt stress-induced changes in the root miRNome in Pokkali rice. Biomolecules. 2020;10:498. doi: 10.3390/biom10040498. PubMed DOI PMC
Madhusudhan P., Sinha P., Rajput L.S., Bhattacharya M., Sharma T., Bhuvaneshwari V., Gaikwad K., Krishnan S.G., Singh A.K. Effect of temperature on Pi54-mediated leaf blast resistance in rice. World J. Microbiol. Biotechnol. 2019;35:148. doi: 10.1007/s11274-019-2724-8. PubMed DOI
Rajput L.S., Sharma T., Madhusudhan P., Sinha P. Effect of temperature on rice blast infection process with emphasis on appressoria formation by Magnaporthe oryzae. Int. J. Curr. Microbiol. Appl. Sci. 2017;6:1931–1939.
Feussner I., Wasternack C. The lipoxygenase pathway. Annu. Rev. Plant Biol. 2002;53:275–297. doi: 10.1146/annurev.arplant.53.100301.135248. PubMed DOI
Blée E. Impact of phyto-oxylipins in plant defense. Trends Plant Sci. 2002;7:315–322. doi: 10.1016/S1360-1385(02)02290-2. PubMed DOI
Upchurch R.G. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol. Lett. 2008;30:967–977. doi: 10.1007/s10529-008-9639-z. PubMed DOI
Somerville C. Plant lipids: Metabolism, mutants, and membranes. Science. 1991;252:80–87. doi: 10.1126/science.252.5002.80. PubMed DOI
Nakamura Y., Li-Beisson Y. Lipids in Plant and Algae Development. Volume 86 Springer; Berlin/Heidelberg, Germany: 2016.
Kobayashi K., Endo K., Wada H. Lipids in Plant and Algae Development. Springer; Cham, Switzerland: 2016. Roles of lipids in photosynthesis; pp. 21–49. PubMed
Belin B.J., Busset N., Giraud E., Molinaro A., Silipo A., Newman D.K. Hopanoid lipids: From membranes to plant–bacteria interactions. Nat. Rev. Microbiol. 2018;16:304. doi: 10.1038/nrmicro.2017.173. PubMed DOI PMC
Cassim A.M., Gouguet P., Gronnier J., Laurent N., Germain V., Grison M., Boutté Y., Gerbeau-Pissot P., Simon-Plas F., Mongrand S. Plant lipids: Key players of plasma membrane organization and function. Prog. Lipid Res. 2019;73:1–27. doi: 10.1016/j.plipres.2018.11.002. PubMed DOI
Harwood J. Lipids in Plants and Microbes. Springer Science & Business Media; Berlin/Heidelberg, Germany: 2012.
Okazaki Y., Saito K. Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J. 2014;79:584–596. doi: 10.1111/tpj.12556. PubMed DOI
Mumtaz F., Zubair M., Khan F., Niaz K. Recent Advances in Natural Products Analysis. Elsevier; Amsterdam, The Netherlands: 2020. Analysis of plants lipids; pp. 677–705.
Brügger B. Lipidomics: Analysis of the lipid composition of cells and subcellular organelles by electrospray ionization mass spectrometry. Annu. Rev. Biochem. 2014;83:79–98. doi: 10.1146/annurev-biochem-060713-035324. PubMed DOI
Dlouhý O., Kurasová I., Karlický V., Javornik U., Šket P., Petrova N.Z., Krumova S.B., Plavec J., Ughy B., Špunda V. Modulation of non-bilayer lipid phases and the structure and functions of thylakoid membranes: Effects on the water-soluble enzyme violaxanthin de-epoxidase. Sci. Rep. 2020;10:11959. doi: 10.1038/s41598-020-68854-x. PubMed DOI PMC
Datta R., Heaster T.M., Sharick J.T., Gillette A.A., Skala M.C. Fluorescence lifetime imaging microscopy: Fundamentals and advances in instrumentation, analysis, and applications. J. Biomed. Opt. 2020;25:071203. doi: 10.1117/1.JBO.25.7.071203. PubMed DOI PMC
Xu T., Hu C., Xuan Q., Xu G. Recent advances in analytical strategies for mass spectrometry-based lipidomics. Anal. Chim. Acta. 2020;1137:156–169. doi: 10.1016/j.aca.2020.09.060. PubMed DOI PMC
Sun T., Wang X., Cong P., Xu J., Xue C. Mass spectrometry-based lipidomics in food science and nutritional health: A comprehensive review. Compr. Rev. Food Sci. Food Saf. 2020;19:2530–2558. doi: 10.1111/1541-4337.12603. PubMed DOI
Canonne J., Froidure-Nicolas S., Rivas S. Phospholipases in action during plant defense signaling. Plant Signal. Behav. 2011;6:13–18. doi: 10.4161/psb.6.1.14037. PubMed DOI PMC
Bessire M., Chassot C., Jacquat A.C., Humphry M., Borel S., Petétot J.M.C., Métraux J.P., Nawrath C. A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 2007;26:2158–2168. doi: 10.1038/sj.emboj.7601658. PubMed DOI PMC
Sylvain R., Amandine L., Dominique R. Very long chain fatty acid and lipid signaling in the response of plants to pathogens. Plant Signal. Behav. 2009;4:94–99. PubMed PMC
Rafał O., Katarzyna P., Agata P., Magdalena C., Agnieszka L., Krzysztof M. Plant–fungal interactions: A case study of Epicoccoum nigrum link. Plants. 2020;9:1691. PubMed PMC
Reszczyńska E., Hanaka A. Lipids composition in plant membranes. Cell Biochem. Biophys. 2020;78:401–414. doi: 10.1007/s12013-020-00947-w. PubMed DOI PMC
Xiang T.N., Junrey A., Martin B., David E., Jacqueline B. Understanding host–pathogen interactions in Brassica napus in the omics era. Plants. 2020;9:1336. PubMed PMC
Bayer P.E., Golicz A.A., Tirnaz S., Chan C.K.K., Edwards D., Batley J. Variation in abundance of predicted resistance genes in the Brassica oleracea pangenome. Plant Biotechnol. J. 2019;17:789–800. doi: 10.1111/pbi.13015. PubMed DOI PMC
Viehweger K., Dordschbal B., Roos W. Elicitor-activated phospholipase A2 generates lysophosphatidylcholines that mobilize the vacuolar H+ pool for pH signaling via the activation of Na+-dependent proton fluxes. Plant Cell. 2002;14:1509–1525. doi: 10.1105/tpc.002329. PubMed DOI PMC
Munnik T., Laxalt A.M. Plant Lipid Signaling Protocols. Springer; Berlin/Heidelberg, Germany: 2013. Measuring PLD activity in vivo; pp. 219–231. PubMed
Abd-El-Haliem A.M., Joosten M.H. Plant phosphatidylinositol-specific phospholipase C at the center of plant innate immunity. J. Integr. Plant Biol. 2017;59:164–179. doi: 10.1111/jipb.12520. PubMed DOI
Ruelland E., Kravets V., Derevyanchuk M., Martinec J., Zachowski A., Pokotylo I. Role of phospholipid signalling in plant environmental responses. Environ. Exp. Bot. 2015;114:129–143. doi: 10.1016/j.envexpbot.2014.08.009. DOI
Kocourkova D., Krčková Z., Pejchar P., Veselková Š., Valentova O., Wimalasekera R., Scherer G.F., Martinec J. The phosphatidylcholine-hydrolysing phospholipase C NPC4 plays a role in response of Arabidopsis roots to salt stress. J. Exp. Bot. 2011;62:3753–3763. doi: 10.1093/jxb/err039. PubMed DOI PMC
Arisz S.A., Testerink C., Munnik T. Plant PA signaling via diacylglycerol kinase. BBA Mol. Cell Biol. Lipid. 2009;1791:869–875. doi: 10.1016/j.bbalip.2009.04.006. PubMed DOI
Gai Z., Wang Y., Ding Y., Qian W., Qiu C., Xie H., Sun L., Jiang Z., Ma Q., Wang L. Exogenous abscisic acid induces the lipid and flavonoid metabolism of tea plants under drought stress. Sci. Rep. 2020;10:12275. doi: 10.1038/s41598-020-69080-1. PubMed DOI PMC
Zalejski C., Zhang Z., Quettier A.L., Maldiney R., Bonnet M., Brault M., Demandre C., Miginiac E., Rona J.P., Sotta B. Diacylglycerol pyrophosphate is a second messenger of abscisic acid signaling in Arabidopsis thaliana suspension cells. Plant J. 2005;42:145–152. doi: 10.1111/j.1365-313X.2005.02373.x. PubMed DOI
Delage E., Ruelland E., Guillas I., Zachowski A., Puyaubert J. Arabidopsis type-III phosphatidylinositol 4-kinases β1 and β2 are upstream of the phospholipase C pathway triggered by cold exposure. Plant Cell Physiol. 2012;53:565–576. doi: 10.1093/pcp/pcs011. PubMed DOI
Kilaru A., Blancaflor E.B., Venables B.J., Tripathy S., Mysore K.S., Chapman K.D. The N-acylethanolamine-mediated regulatory pathway in plants. Chem. Biodiver. 2007;4:1933–1955. doi: 10.1002/cbdv.200790161. PubMed DOI
Lynch D.V., Dunn T.M. An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytol. 2004;161:677–702. doi: 10.1111/j.1469-8137.2004.00992.x. PubMed DOI
Li C., Liu G., Xu C., Lee G.I., Bauer P., Ling H.-Q., Ganal M.W., Howe G.A. The tomato suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell. 2003;15:1646–1661. doi: 10.1105/tpc.012237. PubMed DOI PMC
Wasternack C. Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 2007;100:681–697. doi: 10.1093/aob/mcm079. PubMed DOI PMC
Nakashita H., Yasuda M., Nitta T., Asami T., Fujioka S., Arai Y., Sekimata K., Takatsuto S., Yamaguchi I., Yoshida S. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 2003;33:887–898. doi: 10.1046/j.1365-313X.2003.01675.x. PubMed DOI
Truman W., Bennett M.H., Kubigsteltig I., Turnbull C., Grant M. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. USA. 2007;104:1075–1080. doi: 10.1073/pnas.0605423104. PubMed DOI PMC
Howe G.A. Plant hormones: Metabolic end run to jasmonate. Nat. Chem. Biol. 2018;14:109–110. doi: 10.1038/nchembio.2553. PubMed DOI
Lee H.-J., Park O.K. Lipases associated with plant defense against pathogens. Plant Sci. 2019;279:51–58. doi: 10.1016/j.plantsci.2018.07.003. PubMed DOI
Jose J., Reina P., Alexander Y. Surface lipids and plant defences. Plant Physiol. Biochem. 2009;47:540–549. PubMed
Jyoti S. Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annu. Rev. Phytopathol. 2005;43:229–260. PubMed
Raffaele S., Vailleau F., Léger A., Joubès J., Miersch O., Huard C., Blée E., Mongrand S., Domergue F., Roby D. A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008;20:752–767. doi: 10.1105/tpc.107.054858. PubMed DOI PMC
Xiao F., Mark G.S., Xiao Y., Sun Z., Baker D., Tang X., Jenks M.A., Zhou J.M. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 2004;23:2903–2913. doi: 10.1038/sj.emboj.7600290. PubMed DOI PMC
Zabka V., Stangl M., Bringmann G., Vogg G., Riederer M., Hildebrandt U. Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol. 2008;177:251–263. doi: 10.1111/j.1469-8137.2007.02233.x. PubMed DOI
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. 2007;144:1093–1103. doi: 10.1104/pp.106.094318. PubMed DOI PMC
Pontes J.G.M., Fernandes L.S., dos Santos R.V., Tasic L., Fill T. Virulence factors in the phytopathogen-host interactions: An overview. J. Agric. Food Chem. 2020;68:7555–7570. doi: 10.1021/acs.jafc.0c02389. PubMed DOI
Singh A., Bhatnagar N., Pandey A., Pandey G.K. Plant phospholipase C family: Regulation and functional role in lipid signaling. Cell Calcium. 2015;58:139–146. doi: 10.1016/j.ceca.2015.04.003. PubMed DOI
Vossen J.H., Abd-El-Haliem A., Fradin E.F., Van Den Berg G.C., Ekengren S.K., Meijer H.J., Seifi A., Bai Y., Ten Have A., Munnik T., et al. Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J. 2010;62:224–239. doi: 10.1111/j.1365-313X.2010.04136.x. PubMed DOI
Sawada K., Hasegawa M., Tokuda L., Kameyama J., Kodama O., Kohchi T., Yoshida K., Shinmyo A. Enhanced resistance to blast fungus and bacterial blight in transgenic rice constitutively expressing OsSBP, a rice homologue of mammalian selenium-binding proteins. Biosci. Biotechnol. Biochem. 2004;68:873–880. doi: 10.1271/bbb.68.873. PubMed DOI
Kousik C., Ritchie D. Development of bacterial spot on near-isogenic lines of bell pepper carrying gene pyramids composed of defeated major resistance genes. Phytopathology. 1999;89:1066–1072. doi: 10.1094/PHYTO.1999.89.11.1066. PubMed DOI
Graham N.S., Hammond J.P., Lysenko A., Mayes S., Lochlainn S.Ó., Blasco B., Bowen H.C., Rawlings C.J., Rios J.J., Welham S. Genetical and comparative genomics of Brassica under altered Ca2+ supply identifies Arabidopsis Ca-transporter orthologs. Plant Cell. 2014;26:2818–2830. doi: 10.1105/tpc.114.128603. PubMed DOI PMC
Catanzariti A.-M., Dodds P.N., Lawrence G.J., Ayliffe M.A., Ellis J.G. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell. 2006;18:243–256. doi: 10.1105/tpc.105.035980. PubMed DOI PMC
Shan W., Cao M., Leung D., Tyler B.M. The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps 1b. Mol. Plant Microbe Interact. 2004;17:394–403. doi: 10.1094/MPMI.2004.17.4.394. PubMed DOI
Heyer M., Reichelt M., Mithöfer A. A holistic approach to analyze systemic jasmonate accumulation in individual leaves of Arabidopsis Rosettes upon wounding. Front. Plant Sci. 2018;9:1569. doi: 10.3389/fpls.2018.01569. PubMed DOI PMC
Chapman S., Stevens L.J., Boevink P.C., Engelhardt S., Alexander C.J., Harrower B., Champouret N., McGeachy K., Van Weymers P.S., Chen X. Detection of the virulent form of AVR3a from Phytophthora infestans following artificial evolution of potato resistance gene R3a. PLoS ONE. 2014;9:e110158. doi: 10.1371/journal.pone.0110158. PubMed DOI PMC
USDA Petitions for Determination of Nonregulated Status 2000. [(accessed on 25 March 2021)]; Available online: https://www.aphis.usda.gov/aphis/ourfocus/biotechnology/permits-notifications-petitions/petitions/petition-status.
Song W.-Y., Wang G.-L., Chen L.-L., Kim H.-S., Pi L.-Y., Holsten T., Gardner J., Wang B., Zhai W.-X., Zhu L.-H. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995;270:1804–1806. doi: 10.1126/science.270.5243.1804. PubMed DOI
Itoh Y., Takahashi K., Takizawa H., Nikaidou N., Tanaka H., Nishihashi H., Watanabe T., Nishizawa Y. Family 19 chitinase of Streptomyces griseus HUT6037 increases plant resistance to the fungal disease. Biosci. Biotechnol. Biochem. 2003;67:847–855. doi: 10.1271/bbb.67.847. PubMed DOI
Ghanem M.E., Ghars M.A., Frettinger P., Pérez-Alfocea F., Lutts S., Wathelet J.-P., du Jardin P., Fauconnier M.-L. Organ-dependent oxylipin signature in leaves and roots of salinized tomato plants (Solanum lycopersicum) J. Plant Physiol. 2012;169:1090–1101. doi: 10.1016/j.jplph.2012.03.015. PubMed DOI
Wasternack C., Feussner I. The oxylipin pathways: Biochemistry and function. Annu. Rev. Plant Biol. 2018;69:363–386. doi: 10.1146/annurev-arplant-042817-040440. PubMed DOI
Hamberg M., Sanz A., Rodriguez M.J., Calvo A.P., Castresana C. Activation of the fatty acid α-dioxygenase pathway during bacterial infection of tobacco leaves: Formation of oxylipins protecting against cell death. J. Biol. Chem. 2003;278:51796–51805. doi: 10.1074/jbc.M310514200. PubMed DOI
Mariutto M., Fauconnier M.-L., Ongena M., Laloux M., Wathelet J.-P., Du Jardin P., Thonart P., Dommes J. Reprogramming of fatty acid and oxylipin synthesis in rhizobacteria-induced systemic resistance in tomato. Plant Mol. Biol. 2014;84:455–467. doi: 10.1007/s11103-013-0144-y. PubMed DOI
Christensen S.A., Huffaker A., Kaplan F., Sims J., Ziemann S., Doehlemann G., Ji L., Schmitz R.J., Kolomiets M.V., Alborn H.T. Maize death acids, 9-lipoxygenase–derived cyclopente (a) nones, display activity as cytotoxic phytoalexins and transcriptional mediators. Proc. Natl. Acad. Sci. USA. 2015;112:11407–11412. doi: 10.1073/pnas.1511131112. PubMed DOI PMC
Scalschi L., Llorens E., García-Agustín P., Vicedo B. Role of Jasmonic acid pathway in tomato plant-Pseudomonas syringae interaction. Plants. 2020;9:136. doi: 10.3390/plants9020136. PubMed DOI PMC
Hu J., Huang J., Xu H., Wang Y., Li C., Wen P., You X., Zhang X., Pan G., Li Q. Rice stripe virus suppresses jasmonic acid-mediated resistance by hijacking brassinosteroid signaling pathway in rice. PLoS Pathog. 2020;16:e1008801. doi: 10.1371/journal.ppat.1008801. PubMed DOI PMC
Fonseca S., Chini A., Hamberg M., Adie B., Porzel A., Kramell R., Miersch O., Wasternack C., Solano R. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 2009;5:344–350. doi: 10.1038/nchembio.161. PubMed DOI
Choi W.-G., Hilleary R., Swanson S.J., Kim S.-H., Gilroy S. Rapid, long-distance electrical and calcium signaling in plants. Annu. Rev. Plant Biol. 2016;67:287–307. doi: 10.1146/annurev-arplant-043015-112130. PubMed DOI
Choi W.G., Miller G., Wallace I., Harper J., Mittler R., Gilroy S. Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J. 2017;90:698–707. doi: 10.1111/tpj.13492. PubMed DOI PMC
Mousavi S.A., Chauvin A., Pascaud F., Kellenberger S., Farmer E.E. Glutamate Receptor-like genes mediate leaf-to-leaf wound signalling. Nature. 2013;500:422–426. doi: 10.1038/nature12478. PubMed DOI
Toyota M., Spencer D., Sawai-Toyota S., Jiaqi W., Zhang T., Koo A.J., Howe G.A., Gilroy S. Glutamate triggers long-distance, calcium-based plant defense signaling. Science. 2018;361:1112–1115. doi: 10.1126/science.aat7744. PubMed DOI
Wang J., Song L., Gong X., Xu J., Li M. Functions of jasmonic acid in plant regulation and response to abiotic stress. Int. J. Mol. Sci. 2020;21:1446. doi: 10.3390/ijms21041446. PubMed DOI PMC
Hong Y., Zhao J., Guo L., Kim S.-C., Deng X., Wang G., Zhang G., Li M., Wang X. Plant phospholipases D and C and their diverse functions in stress responses. Prog. Lipid Res. 2016;62:55–74. doi: 10.1016/j.plipres.2016.01.002. PubMed DOI
Bargmann B.O., Munnik T. The role of phospholipase D in plant stress responses. Curr. Opin. Plant Biol. 2006;9:515–522. doi: 10.1016/j.pbi.2006.07.011. PubMed DOI
Chen G., Greer M.S., Weselake R.J. Plant phospholipase A: Advances in molecular biology, biochemistry, and cellular function. Biomol. Concepts. 2013;4:527–532. doi: 10.1515/bmc-2013-0011. PubMed DOI
Chen G., Snyder C.L., Greer M.S., Weselake R.J. Biology and biochemistry of plant phospholipases. Crit. Rev. Plant Sci. 2011;30:239–258. doi: 10.1080/07352689.2011.572033. DOI
Pokotylo I., Pejchar P., Potocký M., Kocourková D., Krčková Z., Ruelland E., Kravets V., Martinec J. The plant non-specific phospholipase C gene family. Novel competitors in lipid signalling. Prog. Lipid Res. 2013;52:62–79. doi: 10.1016/j.plipres.2012.09.001. PubMed DOI
Tang Y., Zhao C.-Y., Tan S.-T., Xue H.-W. Arabidopsis type II phosphatidylinositol 4-kinase PI4Kγ5 regulates auxin biosynthesis and leaf margin development through interacting with membrane-bound transcription factor ANAC078. PLoS Genet. 2016;12:e1006252. doi: 10.1371/journal.pgen.1006252. PubMed DOI PMC
Kobayashi K., Kondo M., Fukuda H., Nishimura M., Ohta H. Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc. Natl. Acad. Sci. USA. 2007;104:17216–17221. doi: 10.1073/pnas.0704680104. PubMed DOI PMC
Chen Q., Yang G. Signal function studies of ROS, especially RBOH-dependent ROS, in plant growth, development and environmental stress. J. Plant Growth Regul. 2020;39:157–171. doi: 10.1007/s00344-019-09971-4. DOI
Zhang W., Qin C., Zhao J., Wang X. Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc. Natl. Acad. Sci. USA. 2004;101:9508–9513. doi: 10.1073/pnas.0402112101. PubMed DOI PMC
Yao H.Y., Xue H.W. Phosphatidic acid plays key roles regulating plant development and stress responses. J. Integr. Plant Biol. 2018;60:851–863. doi: 10.1111/jipb.12655. PubMed DOI
Hou Q., Ufer G., Bartels D. Lipid signaling in plant responses to abiotic stress. Plant Cell Environ. 2016;5:1029–1048. doi: 10.1111/pce.12666. PubMed DOI
Zheng S.Z., Liu Y.L., Li B., Shang Z.l., Zhou R.G., Sun D.Y. Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J. 2012;69:689–700. doi: 10.1111/j.1365-313X.2011.04823.x. PubMed DOI
Rodas-Junco B.A., Nic-Can G.I., Muñoz-Sánchez A., Hernández-Sotomayor S. Phospholipid signaling is a component of the salicylic acid response in plant cell suspension cultures. Int. J. Mol. Sci. 2020;21:5285. doi: 10.3390/ijms21155285. PubMed DOI PMC
Sheng X., Yung Y.C., Chen A., Chun J. Lysophosphatidic acid signalling in development. Development. 2015;142:1390–1395. doi: 10.1242/dev.121723. PubMed DOI PMC
Mortimer J.C., Scheller H.V. Synthesis and Function of Complex Sphingolipid Glycosylation. Trends Plant Sci. 2020;25:522–524. doi: 10.1016/j.tplants.2020.03.007. PubMed DOI
Alsiyabi A., Solis A.G., Cahoon E.B., Saha R. Dissecting the regulatory roles of ORM proteins in the sphingolipid pathway of plants. Plos Comput. Biol. 2021;17:e1008284. doi: 10.1371/journal.pcbi.1008284. PubMed DOI PMC
Michaelson L.V., Napier J.A., Molino D., Faure J.-D. Plant sphingolipids: Their importance in cellular organization and adaption. BBA Mol. Cell Biol. Lipid. 2016;1861:1329–1335. doi: 10.1016/j.bbalip.2016.04.003. PubMed DOI PMC
Abbas H.K., Tanaka T., Shier W.T. Biological activities of synthetic analogues of Alternaria alternata toxin (AAL-toxin) and fumonisin in plant and mammalian cell cultures. Phytochemistry. 1995;40:1681–1689. doi: 10.1016/0031-9422(95)00470-R. PubMed DOI
Spassieva S.D., Markham J.E., Hille J. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J. 2002;32:561–572. doi: 10.1046/j.1365-313X.2002.01444.x. PubMed DOI
Sychta K., Słomka A., Kuta E. Insights into plant programmed cell death induced by heavy metals—discovering a Terra incognita. Cells. 2021;10:65. doi: 10.3390/cells10010065. PubMed DOI PMC
Suzuki K., Yano A., Nishiuchi T., Nakano T., Kodama H., Yamaguchi K., Shinshi H. Comprehensive analysis of early response genes to two different microbial elicitors in tobacco cells. Plant Sci. 2007;173:291–301. doi: 10.1016/j.plantsci.2007.06.002. DOI
Zhang Y., Zhu H., Zhang Q., Li M., Yan M., Wang R., Wang L., Welti R., Zhang W., Wang X. Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell. 2009;21:2357–2377. doi: 10.1105/tpc.108.062992. PubMed DOI PMC
Zhang Q., Xiao S. Lipids in salicylic acid-mediated defense in plants: Focusing on the roles of phosphatidic acid and phosphatidylinositol 4-phosphate. Front. Plant Sci. 2015;6:387. doi: 10.3389/fpls.2015.00387. PubMed DOI PMC
Kirik A., Mudgett M.B. SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT. Proc. Natl. Acad. Sci. USA. 2009;106:20532–20537. doi: 10.1073/pnas.0903859106. PubMed DOI PMC
De Jong C.F., Laxalt A.M., Bargmann B.O., De Wit P.J., Joosten M.H., Munnik T. Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J. 2004;39:1–12. doi: 10.1111/j.1365-313X.2004.02110.x. PubMed DOI
Johansson O.N., Fahlberg P., Karimi E., Nilsson A.K., Ellerström M., Andersson M.X. Redundancy among phospholipase D isoforms in resistance triggered by recognition of the Pseudomonas syringae effector AvrRpm1 in Arabidopsis thaliana. Front. Plant Sci. 2014;5:639. doi: 10.3389/fpls.2014.00639. PubMed DOI PMC
Zhao J., Devaiah S.P., Wang C., Li M., Welti R., Wang X. Arabidopsis phospholipase Dβ1 modulates defense responses to bacterial and fungal pathogens. New Phytol. 2013;199:228–240. doi: 10.1111/nph.12256. PubMed DOI PMC
Zhang Z., Shrestha J., Tateda C., Greenberg J.T. Salicylic acid signaling controls the maturation and localization of the Arabidopsis defense protein accelerated cell Death6. Mol. Plant. 2014;7:1365–1383. doi: 10.1093/mp/ssu072. PubMed DOI PMC
Klose J., De Sá M.M., Kronstad J.W. Lipid-induced filamentous growth in Ustilago maydis. Mol. Microbiol. 2004;52:823–835. doi: 10.1111/j.1365-2958.2004.04019.x. PubMed DOI
Devescovi G., Bigirimana J., Degrassi G., Cabrio L., LiPuma J.J., Kim J., Hwang I., Venturi V. Involvement of a quorum-sensing-regulated lipase secreted by a clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl. Environ. Microbiol. 2007;73:4950–4958. doi: 10.1128/AEM.00105-07. PubMed DOI PMC
Subramoni S., Suárez-Moreno Z., Venturi V. Handbook of Hydrocarbon and Lipid Microbiology. Springer; Berlin, Germany: 2010. Lipases as pathogenicity factors of plant pathogens.
Viswanath K.K., Varakumar P., Pamuru R.R., Basha S.J., Mehta S., Rao A.D. Plant lipoxygenases and their role in plant physiology. J. Plant Biol. 2020;63:83–95. doi: 10.1007/s12374-020-09241-x. DOI
Walley J.W., Kliebenstein D.J., Bostock R.M., Dehesh K. Fatty acids and early detection of pathogens. Curr. Opin. Plant Biol. 2013;16:520–526. doi: 10.1016/j.pbi.2013.06.011. PubMed DOI
Gorman Z., Christensen S.A., Yan Y., He Y., Borrego E., Kolomiets M.V. Green leaf volatiles and jasmonic acid enhance susceptibility to anthracnose diseases caused by Colletotrichum graminicola in maize. Mol. Plant Pathol. 2020;21:702–715. doi: 10.1111/mpp.12924. PubMed DOI PMC
Oliw E.H., Hamberg M. Biosynthesis of jasmonates from linoleic acid by the fungus Fusarium oxysporum. Evidence for a novel allene oxide cyclase. Lipids. 2019;54:543–556. doi: 10.1002/lipd.12180. PubMed DOI
Fyans J.K., Altowairish M.S., Li Y., Bignell D.R. Characterization of the coronatine-like phytotoxins produced by the common scab pathogen Streptomyces scabies. Mol. Plant Microbe Interact. 2015;28:443–454. doi: 10.1094/MPMI-09-14-0255-R. PubMed DOI
Sakata N., Ishiga T., Masuo S., Hashimoto Y., Ishiga Y. Coronatine contributes Pseudomonas cannabina pv. alisalensis virulence by overcoming both stomatal and apoplastic defenses in dicot and monocot plants. bioRxiv. 2020 doi: 10.1101/2020.08.19.256685. PubMed DOI
Thatcher L.F., Powell J.J., Aitken E.A., Kazan K., Manners J.M. The lateral organ boundaries domain transcription factor LBD20 functions in Fusarium wilt susceptibility and jasmonate signaling in Arabidopsis. Plant Physiol. 2012;160:407–418. doi: 10.1104/pp.112.199067. PubMed DOI PMC
Caillaud M.C., Asai S., Rallapalli G., Piquerez S., Fabro G., Jones J.D. A downy mildew effector attenuates salicylic acid–triggered immunity in Arabidopsis by interacting with the host mediator complex. PLoS Biol. 2013;11:e1001732. doi: 10.1371/journal.pbio.1001732. PubMed DOI PMC
Zhu W., Wei W., Fu Y., Cheng J., Xie J., Li G., Yi X., Kang Z., Dickman M.B., Jiang D. A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS ONE. 2013;8:e53901. doi: 10.1371/journal.pone.0053901. PubMed DOI PMC
Plett J.M., Kemppainen M., Kale S.D., Kohler A., Legué V., Brun A., Tyler B.M., Pardo A.G., Martin F. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 2011;21:1197–1203. doi: 10.1016/j.cub.2011.05.033. PubMed DOI
Kloppholz S., Kuhn H., Requena N. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 2011;21:1204–1209. doi: 10.1016/j.cub.2011.06.044. PubMed DOI
Du M., Zhai Q., Deng L., Li S., Li H., Yan L., Huang Z., Wang B., Jiang H., Huang T., et al. Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell. 2014;26:3167–3184. doi: 10.1105/tpc.114.128272. PubMed DOI PMC
Scala A., Mirabella R., Mugo C., Matsui K., Haring M.A., Schuurink R.C. E-2-hexenal promotes susceptibility to Pseudomonas syringae by activating jasmonic acid pathways in Arabidopsis. Front. Plant Sci. 2013;4:74. doi: 10.3389/fpls.2013.00074. PubMed DOI PMC
Rangaswamy V., Mitchell R., Ullrich M., Bender C. Analysis of genes involved in biosynthesis of coronafacic acid, the polyketide component of the phytotoxin coronatine. J. Bacteriol. 1998;180:3330–3338. doi: 10.1128/JB.180.13.3330-3338.1998. PubMed DOI PMC
Yinggen K., Yuanrong K., Mengxiao W., Hongbo L., Shugang H., Qinglu Z., Xianghua L., Jinghua X., Shiping W. Jasmonic acid-involved OsEDS1 signaling in rice-bacteria interactions. Rice. 2019;12:25. PubMed PMC
Jha G., Rajeshwari R., Sonti R.V. Functional interplay between two Xanthomonas oryzae pv. oryzae secretion systems in modulating virulence on rice. Mol. Plant Microbe Interact. 2007;20:31–40. doi: 10.1094/MPMI-20-0031. PubMed DOI
Smolka M.B., Martins D., Winck F.V., Santoro C.E., Castellari R.R., Ferrari F., Brum I.J., Galembeck E., Della Coletta Filho H., Machado M.A. Proteome analysis of the plant pathogen Xylella fastidiosa reveals major cellular and extracellular proteins and a peculiar codon bias distribution. Proteomics. 2003;3:224–237. doi: 10.1002/pmic.200390031. PubMed DOI
Reis H., Pfiffi S., Hahn M. Molecular and functional characterization of a secreted lipase from Botrytis cinerea. Mol. Plant Pathol. 2005;6:257–267. doi: 10.1111/j.1364-3703.2005.00280.x. PubMed DOI
Berto P., Comménil P., Belingheri L., Dehorter B. Occurrence of a lipase in spores of Alternaria brassicicola with a crucial role in the infection of cauliflower leaves. FEMS Microbiol. Lett. 1999;180:183–189. doi: 10.1111/j.1574-6968.1999.tb08794.x. PubMed DOI
Feng J., Liu G., Selvaraj G., Hughes G.R., Wei Y. A secreted lipase encoded by LIP1 is necessary for efficient use of saturated triglyceride lipids in Fusarium graminearum. Microbiology. 2005;151:3911–3921. doi: 10.1099/mic.0.28261-0. PubMed DOI
Eddine A.N., Hannemann F., Schäfer W. Cloning and expression analysis of NhL1, a gene encoding an extracellular lipase from the fungal pea pathogen Nectria haematococca MP VI (Fusarium solani f. sp. pisi) that is expressed in planta. Mol. Genet. Genom. 2001;265:215–224. doi: 10.1007/s004380000410. PubMed DOI
Wang Z.-Y., Soanes D.M., Kershaw M.J., Talbot N.J. Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid β-oxidation during appressorium-mediated plant infection. Mol. Plant Microbe Interact. 2007;20:475–491. doi: 10.1094/MPMI-20-5-0475. PubMed DOI