Membrane component ergosterol builds a platform for promoting effector secretion and virulence in Magnaporthe oryzae.
Magnaporthe oryzae
SNARE
effector secretion
ergosterol
lipid raft
pathogenicity
plasma membrane integrity
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2023
02 2023
Historique:
received:
02
06
2022
accepted:
14
10
2022
pubmed:
28
10
2022
medline:
7
1
2023
entrez:
27
10
2022
Statut:
ppublish
Résumé
The plasma membrane (PM) functions as a physical border between the extracellular and cytoplasmic environments that contribute to the interaction between host plants and pathogenic fungi. As a specific sterol constituent in the cell membrane, ergosterol plays a significant role in fungal development. However, the role of ergosterol in the infection of the rice blast fungus Magnaporthe oryzae remains unclear. In this study, we found that a sterol reductase, MoErg4, is involved in ergosterol biosynthesis and the regulation of plasma membrane integrity in M. oryzae. We found that defects in ergosterol biosynthesis disrupt lipid raft formation in the PM and cause an abnormal distribution of the t-soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) protein MoSso1, inhibiting its interaction with the v-SNARE protein MoSnc1. In addition, we found that MoSso1-MoSnc1 interaction is important for biotrophic interface complex development and cytoplasmic effector protein secretion. Our findings suggested that ergosterol-enriched lipid rafts constitute a platform for interactions among various SNARE proteins that are required for the development and pathogenicity of M. oryzae.
Substances chimiques
Fungal Proteins
0
SNARE Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
930-943Subventions
Organisme : NIAID NIH HHS
ID : R21 AI168867
Pays : United States
Organisme : NIAID NIH HHS
ID : R03 AI156254
Pays : United States
Informations de copyright
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.
Références
Affentranger S, Martinelli S, Hahn J, Rossy J, Niggli V. 2011. Dynamic reorganization of flotillins in chemokine-stimulated human T-lymphocytes. BMC Cell Biology 12: 28.
Ahmad A, Khan A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N. 2011. Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. European Journal of Clinical Microbiology & Infectious Diseases 30: 41-50.
Ammendolia DA, Bement WM, Brumell JH. 2021. Plasma membrane integrity: implications for health and disease. BMC Biology 19: 71.
Bodin S, Planchon D, Rios Morris E, Comunale F, Gauthier-Rouvière C. 2014. Flotillins in intercellular adhesion - from cellular physiology to human diseases. Journal of Cell Science 127: 5139-5147.
Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116: 153-166.
Borner GH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, Macaskill A, Napier JA, Beale MH, Lilley KS, Dupree P. 2005. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiology 137: 104-116.
Cai H, Reinisch K, Ferro-Novick S. 2007. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Developmental Cell 12: 671-682.
Chen XL, Shi T, Yang J, Shi W, Gao X, Chen D, Xu X, Xu JR, Talbot NJ, Peng YL. 2014. N-glycosylation of effector proteins by an α-1,3-mannosyltransferase is required for the rice blast fungus to evade host innate immunity. Plant Cell 26: 1360-1376.
Chumley FG, Valent B. 1990. Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea. Molecular Plant-Microbe Interactions 3: 135.
Crowley LC, Scott AP, Marfell BJ, Boughaba JA, Chojnowski G, Waterhouse NJ. 2016. Measuring cell death by propidium iodide uptake and flow cytometry. Cold Spring Harbor Protocols 2016: 87-163.
Douglas LM, Konopka JB. 2014. Fungal membrane organization: the eisosome concept. Annual Review of Microbiology 68: 377-393.
Esquivel BD, White TC. 2017. Accumulation of azole drugs in the fungal plant pathogen Magnaporthe oryzae is the result of facilitated diffusion influx. Frontiers in Microbiology 8: 1320.
Fisher MC, Hawkins NJ, Sanglard D, Gurr SJ. 2018. Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science 360: 739-742.
Gajate C, Mollinedo F. 2021. Lipid raft isolation by sucrose gradient centrifugation and visualization of raft-located proteins by fluorescence microscopy: the use of combined techniques to assess Fas/CD95 location in rafts during apoptosis triggering. Methods in Molecular Biology 2187: 147-186.
Gessner MO, Schmitt AL. 1996. Use of solid-phase extraction to determine ergosterol concentrations in plant tissue colonized by fungi. Applied and Environmental Microbiology 62: 415-419.
Gimpl G, Fahrenholz F. 2002. Cholesterol as stabilizer of the oxytocin receptor. Biochimica et Biophysica Acta 1564: 384-392.
Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, Martinez-Rocha AL, Saitoh H, Terauchi R, Talbot NJ, Valent B. 2013. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nature Communications 4: 1996.
Holthuis JC, Nichols BJ, Dhruvakumar S, Pelham HR. 1998. Two syntaxin homologues in the TGN/endosomal system of yeast. EMBO Journal 17: 113-126.
Horn A, Jaiswal JK. 2019. Structural and signaling role of lipids in plasma membrane repair. Current Topics in Membranes 84: 67-98.
Ji H, Zhang W, Zhou Y, Zhang M, Zhu J, Song Y, Lü J. 2000. A three-dimensional model of lanosterol 14α-demethylase of Candida albicans and its interaction with azole antifungals. Journal of Medicinal Chemistry 43: 2493-2505.
Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology 44: 41-60.
Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K, Kang S, Valent B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22: 1388-1403.
Lass-Flörl C. 2011. Triazole antifungal agents in invasive fungal infections: a comparative review. Drugs 71: 2405-2419.
Lees ND, Skaggs B, Kirsch DR, Bard M. 1995. Cloning of the late genes in the ergosterol biosynthetic pathway of Saccharomyces cerevisiae - a review. Lipids 30: 221-226.
Li X, Gao C, Li L, Liu M, Yin Z, Zhang H, Zheng X, Wang P, Zhang Z. 2017. MoEnd3 regulates appressorium formation and virulence through mediating endocytosis in rice blast fungus Magnaporthe oryzae. PLoS Pathogens 13: e1006449.
Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
Liu M, Hu J, Zhang A, Dai Y, Chen W, He Y, Zhang H, Zheng X, Zhang Z. 2021. Auxilin-like protein MoSwa2 promotes effector secretion and virulence as a clathrin uncoating factor in the rice blast fungus Magnaporthe oryzae. New Phytologist 230: 720-736.
Liu M, Zhang S, Hu J, Sun W, Padilla J, He Y, Li Y, Yin Z, Liu X, Wang W et al. 2019. Phosphorylation-guarded light-harvesting complex II contributes to broad-spectrum blast resistance in rice. Proceedings of the National Academy of Sciences, USA 116: 17572-17577.
Liu W, Liu J, Triplett L, Leach JE, Wang GL. 2014. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annual Review of Phytopathology 52: 213-241.
Liu X, Fu J, Yun Y, Yin Y, Ma Z. 2011. A sterol C-14 reductase encoded by FgERG24B is responsible for the intrinsic resistance of Fusarium graminearum to amine fungicides. Microbiology 157: 1665-1675.
Liu X, Qian B, Gao C, Huang S, Cai Y, Zhang H, Zheng X, Wang P, Zhang Z. 2016. The putative protein phosphatase MoYvh1 functions upstream of MoPdeH to regulate the development and pathogenicity in Magnaporthe oryzae. Molecular Plant-Microbe Interactions 29: 496-507.
Liu X, Zhou Q, Guo Z, Liu P, Shen L, Chai N, Qian B, Cai Y, Wang W, Yin Z et al. 2020. A self-balancing circuit centered on MoOsm1 kinase governs adaptive responses to host-derived ROS in Magnaporthe oryzae. eLife 9: e61605.
London E, Brown DA. 2000. Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochimica et Biophysica Acta 1508: 182-195.
Mamode Cassim A, Gouguet P, Gronnier J, Laurent N, Germain V, Grison M, Boutté Y, Gerbeau-Pissot P, Simon-Plas F, Mongrand S. 2019. Plant lipids: key players of plasma membrane organization and function. Progress in Lipid Research 73: 1-27.
Mayor S, Sabharanjak S, Maxfield FR. 1998. Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO Journal 17: 4626-4638.
van Meer G, Voelker DR, Feigenson GW. 2008. Membrane lipids: where they are and how they behave. Nature Reviews. Molecular Cell Biology 9: 112-124.
Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BP et al. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24: 322-335.
Morrow IC, Rea S, Martin S, Prior IA, Prohaska R, Hancock JF, James DE, Parton RG. 2002. Flotillin-1/reggie-2 traffics to surface raft domains via a novel Golgi-independent pathway. Identification of a novel membrane targeting domain and a role for palmitoylation. The Journal of Biological Chemistry 277: 48834-48841.
Naglik JR, Challacombe SJ, Hube B. 2003. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiology and Molecular Biology Reviews 67: 400-428.
Nishimura T, Mochizuki S, Ishii-Minami N, Fujisawa Y, Kawahara Y, Yoshida Y, Okada K, Ando S, Matsumura H, Terauchi R et al. 2016. Magnaporthe oryzae glycine-rich secretion protein, Rbf1 critically participates in pathogenicity through the focal formation of the biotrophic interfacial complex. PLoS Pathogens 12: e1005921.
Otto GP, Nichols BJ. 2011. The roles of flotillin microdomains - endocytosis and beyond. Journal of Cell Science 124: 3933-3940.
Parks LW, Casey WM. 1995. Physiological implications of sterol biosynthesis in yeast. Annual Review of Microbiology 49: 95-116.
Pike LJ. 2006. Rafts defined: a report on the keystone symposium on lipid rafts and cell function. Journal of Lipid Research 47: 1597-1598.
Qi Z, Liu M, Dong Y, Zhu Q, Li L, Li B, Yang J, Li Y, Ru Y, Zhang H et al. 2016. The syntaxin protein (MoSyn8) mediates intracellular trafficking to regulate conidiogenesis and pathogenicity of rice blast fungus. New Phytologist 209: 1655-1667.
Qi Z, Wang Q, Dou X, Wang W, Zhao Q, Lv R, Zhang H, Zheng X, Wang P, Zhang Z. 2012. MoSwi6, an APSES family transcription factor, interacts with MoMps1 and is required for hyphal and conidial morphogenesis, appressorial function and pathogenicity of Magnaporthe oryzae. Molecular Plant Pathology 13: 677-689.
Qian B, Su X, Ye Z, Liu X, Liu M, Shen D, Chen H, Zhang H, Wang P, Zhang Z. 2022. MoErv29 promotes apoplastic effector secretion contributing to virulence of the rice blast fungus Magnaporthe oryzae. New Phytologist 233: 1289-1302.
Roche Y, Gerbeau-Pissot P, Buhot B, Thomas D, Bonneau L, Gresti J, Mongrand S, Perrier-Cornet JM, Simon-Plas F. 2008. Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts. The FASEB Journal 22: 3980-3991.
Rossi G, Salminen A, Rice LM, Brünger AT, Brennwald P. 1997. Analysis of a yeast SNARE complex reveals remarkable similarity to the neuronal SNARE complex and a novel function for the C terminus of the SNAP-25 homolog, Sec9. The Journal of Biological Chemistry 272: 16610-16617.
Ruckenstuhl C, Lang S, Poschenel A, Eidenberger A, Baral PK, Kohút P, Hapala I, Gruber K, Turnowsky F. 2007. Characterization of squalene epoxidase of Saccharomyces cerevisiae by applying terbinafine-sensitive variants. Antimicrobial Agents and Chemotherapy 51: 275-284.
Ruge E, Korting HC, Borelli C. 2005. Current state of three-dimensional characterisation of antifungal targets and its use for molecular modelling in drug design. International Journal of Antimicrobial Agents 26: 427-441.
Ryder LS, Talbot NJ. 2015. Regulation of appressorium development in pathogenic fungi. Current Opinion in Plant Biology 26: 8-13.
Salaün C, Gould GW, Chamberlain LH. 2005. Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells. The Journal of Biological Chemistry 280: 19449-19453.
Shoji JY, Kikuma T, Kitamoto K. 2014. Vesicle trafficking, organelle functions, and unconventional secretion in fungal physiology and pathogenicity. Current Opinion in Microbiology 20: 1-9.
Singer SJ, Nicolson GL. 1972. The fluid mosaic model of the structure of cell membranes. Science 175: 720-731.
Sokolov SS, Trushina NI, Severin FF, Knorre DA. 2019. Ergosterol turnover in yeast: an interplay between biosynthesis and transport. Biochemistry 84: 346-357.
Souza CM, Pichler H. 2007. Lipid requirements for endocytosis in yeast. Biochimica et Biophysica Acta 1771: 442-454.
Talbot NJ, Ebbole DJ, Hamer JE. 1993. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5: 1575-1590.
Tang W, Ru Y, Hong L, Zhu Q, Zuo R, Guo X, Wang J, Zhang H, Zheng X, Wang P et al. 2015. System-wide characterization of bZIP transcription factor proteins involved in infection-related morphogenesis of Magnaporthe oryzae. Environmental Microbiology 17: 1377-1396.
Umebayashi K, Nakano A. 2003. Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. The Journal of Cell Biology 161: 1117-1131.
Valkonen M, Kalkman ER, Saloheimo M, Penttilä M, Read ND, Duncan RR. 2007. Spatially segregated SNARE protein interactions in living fungal cells. The Journal of Biological Chemistry 282: 22775-22785.
Vanden Bossche H. 1985. Biochemical targets for antifungal azole derivatives: hypothesis on the mode of action. Current Topics in Medical Mycology 1: 313-351.
Vemanna RS, Babitha KC, Solanki JK, Amarnatha Reddy V, Sarangi SK, Udayakumar M. 2017. Aldo-keto reductase-1 (AKR1) protect cellular enzymes from salt stress by detoxifying reactive cytotoxic compounds. Plant Physiology and Biochemistry 113: 177-186.
Vijayaraghavareddy P, Adhinarayanreddy V, Vemanna RS, Sreeman S, Makarla U. 2017. Quantification of membrane damage/cell death using Evan's blue staining technique. Bio-Protocol 7: e2519.
Wachtler V, Rajagopalan S, Balasubramanian MK. 2003. Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. Journal of Cell Science 116: 867-874.
Wang J, Du Y, Zhang H, Zhou C, Qi Z, Zheng X, Wang P, Zhang Z. 2013. The actin-regulating kinase homologue MoArk1 plays a pleiotropic function in Magnaporthe oryzae. Molecular Plant Pathology 14: 470-482.
Wang T, Li L, Hong W. 2017. SNARE proteins in membrane trafficking. Traffic 18: 767-775.
Weete JD, Abril M, Blackwell M. 2010. Phylogenetic distribution of fungal sterols. PLoS ONE 5: e10899.
White TC, Marr KA, Bowden RA. 1998. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clinical Microbiology Reviews 11: 382-402.
Wilson RA, Talbot NJ. 2009. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nature Reviews. Microbiology 7: 185-195.
Xu X, Bittman R, Duportail G, Heissler D, Vilcheze C, London E. 2001. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. The Journal of Biological Chemistry 276: 33540-33546.
Yan X, Ma WB, Li Y, Wang H, Que YW, Ma ZH, Talbot NJ, Wang ZY. 2011. A sterol 14α-demethylase is required for conidiation, virulence and for mediating sensitivity to sterol demethylation inhibitors by the rice blast fungus Magnaporthe oryzae. Fungal Genetics and Biology 48: 144-153.
Yang S, Yan D, Li M, Li D, Zhang S, Fan G, Peng L, Pan S. 2022. Ergosterol depletion under bifonazole treatment induces cell membrane damage and triggers a ROS-mediated mitochondrial apoptosis in Penicillium expansum. Fungal Biology 126: 1-10.
Yin Z, Feng W, Chen C, Xu J, Li Y, Yang L, Wang J, Liu X, Wang W, Gao C et al. 2020. Shedding light on autophagy coordinating with cell wall integrity signaling to govern pathogenicity of Magnaporthe oryzae. Autophagy 16: 900-916.
Zhong Z, Norvienyeku J, Yu J, Chen M, Cai R, Hong Y, Chen L, Zhang D, Wang B, Zhou J et al. 2015. Two different subcellular-localized acetoacetyl-CoA acetyltransferases differentiate diverse functions in Magnaporthe oryzae. Fungal Genetics and Biology 83: 58-67.
Zweytick D, Hrastnik C, Kohlwein SD, Daum G. 2000. Biochemical characterization and subcellular localization of the sterol C-24(28) reductase, Erg4p, from the yeast Saccharomyces cerevisiae. FEBS Letters 470: 83-87.