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Lipid-Mediated Signaling Between Fungi and Plants

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Biocommunication of Fungi

Abstract

Lipid-mediated inter-kingdom signaling in plant-fungal interactions is the exchange of molecules between plants and fungal pathogens and symbiotes. Recently these interactions were implicated in determining whether inter-organismal interactions result in parasitism, symbiosis or commencialism. Lipids constitute a very large group of structurally diverse molecules that have diverse functions in cell metabolism. One group of lipids, oxygenated lipids (oxylipins), is gaining increased interest as molecular signals that orchestrate a myriad of metabolic processes in both plants and fungi. Growing momentum implicates these metabolites as key players during the signal exchange between different interacting organisms. Recent studies have revealed oxylipins as key regulators of sporulation and secondary metabolite production while others have discovered their roles in manipulating plant metabolism and defense responses for the advantage of fungal and other pathogens. The focus of this chapter is to describe recent advances in our understanding of oxylipin-mediated signal communication between fungi and plants, highlighting pathogenic systems.

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References

  • Acosta IF, Laparra H, Romero SP, Schmelz E, Hamberg M, Mottinger JP, Moreno MA, Dellaporta SL (2009) tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323:262–265

    Article  PubMed  CAS  Google Scholar 

  • Agrios GN (2005) Plant pathology. Elsevier Academic, Burlington

    Google Scholar 

  • Andreou A, Brodhun F, Feussner I (2009) Biosynthesis of oxylipins in non-mammals. Prog Lipid Res 48:148–170

    Article  PubMed  CAS  Google Scholar 

  • Bos CL, Richel DJ, Ritsema T, Peppelenbosch MP, Versteeg HH (2004) Prostanoids and prostanoid receptors in signal transduction. Int J Biochem Cell Biol 36:1187–1205

    Article  PubMed  CAS  Google Scholar 

  • Boue SM, Shih BY, Carter-Wientjes CH, Cleveland TE (2005) Effect of soybean lipoxygenase on volatile generation and inhibition of Aspergillus flavus mycelial growth. J Agric Food Chem 53:4778–4783

    Article  PubMed  CAS  Google Scholar 

  • Briscoe CP, Tadayyon M, Andrews JL, Benson WG, Chambers JK, Eilert MM, Ellis C, Elshourbagy NA, Goetz AS, Minnick DT, Murdock PR, Sauls HR Jr, Shabon U, Spinage LD, Strum JC, Szekeres PG, Tan KB, Way JM, Ignar DM, Wilson S, Muir AI (2003) The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J Biol Chem 278:11303–11311

    Article  PubMed  CAS  Google Scholar 

  • Brodhagen M, and Keller NP (2006) Signalling pathways connecting mycotoxin production and sporulation. Mol Plant Pathol 7:285–301

    Article  PubMed  CAS  Google Scholar 

  • Brodhagen M, Tsitsigiannis DI, Hornung E, Goebel C, Feussner I, Keller NP (2008) Reciprocal oxylipin-mediated cross-talk in the Aspergillus-seed pathosystem. Mol Microbiol 67:378–391

    Article  PubMed  CAS  Google Scholar 

  • Brodhun F, Feussner I (2011) Oxylipins in fungi. FEBS J 278:1047–1063

    Article  PubMed  CAS  Google Scholar 

  • Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol Plant Pathol 6:629–639

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Scott JB, Bhaheetharan J, Sharpee WC, Milde L, Wilson RA, Keller NP (2009) Oxygenase coordination is required for morphological transition and the host-fungus interaction of Aspergillus flavus. Mol Plant Microbe Interact 22:882–894

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Zarnowski R, Sharpee WC, Keller NP (2008) Morphological transitions governed by density dependence and lipoxygenase activity in Aspergillus flavus. Appl Environ Microbiol 74:5674–5685

    Article  CAS  Google Scholar 

  • Burow GB, Nesbitt TC, Dunlap J, Keller NP (1997) Seed lipoxygenase products modulate Aspergillus mycotoxin biosynthesis. Mol Plant Microbe Interact 10:380–387

    Article  CAS  Google Scholar 

  • Calvo AM, Hinze LL, Gardner HW, Keller NP (1999) Sporogenic effect of polyunsaturated fatty acids on development of Aspergillus spp. Appl Environ Microbiol 65:3668–3673

    PubMed  CAS  Google Scholar 

  • Champe SP, el-Zayat AA (1989) Isolation of a sexual sporulation hormone from Aspergillus nidulans. J Bacteriol 171:3982–3988

    PubMed  CAS  Google Scholar 

  • Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494

    Article  PubMed  CAS  Google Scholar 

  • Christensen SA, Kolomiets MV (2011) The lipid language of plant-fungal interactions. Fungal Genet Biol 48:4–14

    Article  PubMed  CAS  Google Scholar 

  • De Lucca AJ, Carter-Wientjes CH, Boué S, Bhatnagar D (2011) Volatile trans-2-hexenal, a soybean aldehyde, inhibits Aspergillus flavus growth and aflatoxin production in corn. J Food Sci 76:M381–M386

    Article  PubMed  Google Scholar 

  • Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889

    Article  PubMed  CAS  Google Scholar 

  • Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297

    Article  PubMed  CAS  Google Scholar 

  • Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350

    Article  PubMed  CAS  Google Scholar 

  • Gao XQ, Kolomiets MV (2009) Host-derived lipids and oxylipins are crucial signals in modulating mycotoxin production by fungi. Toxin Rev 28:79–88

    Article  CAS  Google Scholar 

  • Gao X, Shim WB, Gobel C, Kunze S, Feussner I, Meeley R, Balint-Kurti P, Kolomiets M (2007) Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin. Mol Plant Microbe Interact 20:922–933

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Brodhagen M, Isakeit T, Brown SH, Gobel C, Betran J, Feussner I, Keller NP, Kolomiets MV (2009) Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Mol Plant Microbe Interact 22:222–231

    Article  PubMed  Google Scholar 

  • Gerwick WH, Moghaddam M, Hamberg M (1991) Oxylipin metabolism in the red alga Gracilariopsis lemaneiformis: mechanism of formation of vicinal dihydroxy fatty acids. Arch Biochem Biophys 290:436–444

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Goodrich-Tanrikulu M, Mahoney NE, Rodriguez SB (1995) The plant growth regulator methyl jasmonate inhibits aflatoxin production by Aspergillus flavus. Microbiology 141(Pt 11):2831–2837

    Article  PubMed  CAS  Google Scholar 

  • Hamberg M, Ponce de Leon I, Rodriguez MJ, Castresana C (2005) Alpha-dioxygenases. Biochem Biophys Res Commun 338:169–174

    Article  PubMed  CAS  Google Scholar 

  • Horn BW, Moore GG, Carbone I (2009a) Sexual reproduction in Aspergillus flavus. Mycologia 101:423–429

    Article  PubMed  Google Scholar 

  • Horn BW, Ramirez-Prado JH, Carbone I (2009b) The sexual state of Aspergillus parasiticus. Mycologia 101:275–280

    Article  PubMed  Google Scholar 

  • Horn BW, Moore GG, Carbone I (2011) Sexual reproduction in aflatoxin-producing Aspergillus nomius. Mycologia 103:174–183

    Article  PubMed  Google Scholar 

  • Hosoi T, Koguchi Y, Sugikawa E, Chikada A, Ogawa K, Tsuda N, Suto N, Tsunoda S, Taniguchi T, Ohnuki T (2002) Identification of a novel human eicosanoid receptor coupled to G(i/o). J Biol Chem 277:31459–31465

    Article  PubMed  CAS  Google Scholar 

  • Hwang IS, Hwang BK (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol 152:948–967

    Article  PubMed  CAS  Google Scholar 

  • Isakeit T, Gao X, Kolomiets M (2007) Increased resistance of a maize mutant lacking the 9-lipoxygenase gene, ZmLOX3, to root rot caused by Exserohilum pedicellatum. J Phytopathol 155:758–760

    Article  CAS  Google Scholar 

  • Jambois A, Lapeyrie F (2005) Jasmonates, together with zeatin, induce hypaphorine accumulation by the ectomycorrhizal fungus Pisolithus microcarpus. Symbiosis 39:137–141

    CAS  Google Scholar 

  • La Camera S, Geoffroy P, Samaha H, Ndiaye A, Rahim G, Legrand M, Heitz T (2005) A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 44:810–825

    Article  PubMed  Google Scholar 

  • Lopez-Raez JA, Verhage A, Fernandez I, Garcia JM, Azcon-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601

    Article  PubMed  CAS  Google Scholar 

  • Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr Opin Plant Biol 9:274–280

    Article  PubMed  CAS  Google Scholar 

  • Miersch O, Bohlmann H, Wasternack C (1999) Jasmonates and related compounds from Fusarium oxysporum. Phytochemistry 50:517–523

    Article  CAS  Google Scholar 

  • Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21:1273–1290

    Article  PubMed  CAS  Google Scholar 

  • Mueller MJ (2004) Archetype signals in plants: the phytoprostanes. Curr Opin Plant Biol 7:441–448

    Article  PubMed  CAS  Google Scholar 

  • Obinata H, Hattori T, Nakane S, Tatei K, Izumi T (2005) Identification of 9-hydroxyoctadecadienoic acid and other oxidized free fatty acids as ligands of the G protein-coupled receptor G2A. J Biol Chem 280:40676–40683

    Article  PubMed  CAS  Google Scholar 

  • Pare PW, Alborn HT, Tumlinson JH (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95:13971–13975

    Article  PubMed  CAS  Google Scholar 

  • Reboutier D, Bianchi M, Brault M, Roux C, Dauphin A, Rona JP, Legue V, Lapeyrie F, Bouteau F (2002) The indolic compound hypaphorine produced by ectomycorrhizal fungus interferes with auxin action and evokes early responses in nonhost Arabidopsis thaliana. Mol Plant Microbe Interact 15:932–938

    Article  PubMed  CAS  Google Scholar 

  • Ren A, Qin L, Shi L, Dong X, da Mu S, Li YX, Zhao MW (2010) Methyl jasmonate induces ganoderic acid biosynthesis in the basidiomycetous fungus Ganoderma lucidum. Bioresour Technol 101:6785–6790

    Article  PubMed  CAS  Google Scholar 

  • Shi L, Ren A, Mu D, Zhao M (2010) Current progress in the study on biosynthesis and regulation of ganoderic acids. Appl Microbiol Biotechnol 88:1243–1251

    Article  PubMed  CAS  Google Scholar 

  • Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J 58:927–939

    Article  PubMed  CAS  Google Scholar 

  • Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  PubMed  CAS  Google Scholar 

  • Tsitsigiannis DI, Keller NP (2006) Oxylipins act as determinants of natural product biosynthesis and seed colonization in Aspergillus nidulans. Mol Microbiol 59:882–892

    Article  PubMed  CAS  Google Scholar 

  • Tsitsigiannis DI, Keller NP (2007) Oxylipins as developmental and host-fungal communication signals. Trends Microbiol 15:109–118

    Article  PubMed  CAS  Google Scholar 

  • Vergopoulou S, Galanopoulou D, Markaki P (2001) Methyl jasmonate stimulates aflatoxin B-1 biosynthesis by Aspergillus parasiticus. J Agric Food Chem 49:3494–3498

    Article  PubMed  CAS  Google Scholar 

  • Voigt CA, Schafer W, Salomon S (2005) A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J 42:364–375

    Article  PubMed  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed  CAS  Google Scholar 

  • Wright MS, Greene-McDowelle DM, Zeringue HJ, Bhatnagar D, Cleveland TE (2000) Effects of volatile aldehydes from Aspergillus-resistant varieties of corn on Aspergillus parasiticus growth and aflatoxin biosynthesis. Toxicon 38:1215–1223

    Article  PubMed  CAS  Google Scholar 

  • Yan Y, Christensen S, Isakeit T, Engelberth J, Meeley R, Hayward A, Neil Emery RJ, Kolomiets M (2012) Disruption of OPR7 and OPR8 Reveals the Versatile Functions of JA in Maize Development and Defense. Plant Cell (in print)

    Google Scholar 

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Acknowledgements

This work was supported by the NSF grant IOS-0951272 to Dr. Michael Kolomiets.

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Correspondence to Michael V. Kolomiets .

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Borrego, E.J., Kolomiets, M.V. (2012). Lipid-Mediated Signaling Between Fungi and Plants. In: Witzany, G. (eds) Biocommunication of Fungi. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4264-2_16

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