Distinct roles for different autophagy-associated genes in the virulence of the fungal wheat pathogen Zymoseptoria tritici

Fungal Genetics and Biology - Tập 163 - Trang 103748 - 2022
Harry T. Child1, Michael J. Deeks1, Ken Haynes1, Jason J. Rudd2, Steven Bates1
1University of Exeter, College of Life and Environmental Sciences, Geoffrey Pope Building, Stocker Road, Exeter EX4 4QD, UK
2Dept of Bio-Interactions and Crop Protection, Rothamsted Research, Harpenden AL5 2JQ, UK

Tài liệu tham khảo

Asakura, 2009, Atg26-Mediated Pexophagy Is Required for Host Invasion by the Plant Pathogenic Fungus Colletotrichum orbiculare, Plant Cell, 21, 1291, 10.1105/tpc.108.060996 Cheong, 2008, The Atg1 Kinase Complex Is Involved in the Regulation of Protein Recruitment to Initiate Sequestering Vesicle Formation for Nonspecific Autophagy in Saccharomyces cerevisiae, Mol. Biol. Cell, 19, 668, 10.1091/mbc.e07-08-0826 Child Corral-Ramos, 2015, Autophagy contributes to regulation of nuclear dynamics during vegetative growth and hyphal fusion in Fusarium oxysporum, Autophagy, 11, 131, 10.4161/15548627.2014.994413 Deng, 2013, The role of Snx41-based pexophagy in Magnaporthe development, PLoS ONE, 8, e79128, 10.1371/journal.pone.0079128 Di Tommaso, 2011, T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension, Nucleic Acids Res, 39, W13, 10.1093/nar/gkr245 Duan, 2013, Linkage of autophagy to fungal development, lipid storage and virulence in Metarhizium robertsii, Autophagy, 9, 538, 10.4161/auto.23575 Duncan, 2000, Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola, Mycol. Res., 104, 1074, 10.1017/S0953756299002294 Feng, 2014, The machinery of macroautophagy, Cell Res., 24, 24, 10.1038/cr.2013.168 Filomeni, 2015, Oxidative stress and autophagy: the clash between damage and metabolic needs, Cell Death Differ., 22, 377, 10.1038/cdd.2014.150 Fones, 2015, The impact of Septoria tritici Blotch disease on wheat: An EU perspective, Fungal Genet. Biol., 79, 3, 10.1016/j.fgb.2015.04.004 Fones, 2017, A role for random, humidity-dependent epiphytic growth prior to invasion of wheat by Zymoseptoria tritici, Fungal Genet. Biol., 106, 51, 10.1016/j.fgb.2017.07.002 Francisco, 2019, Morphological changes in response to environmental stresses in the fungal plant pathogen Zymoseptoria tritici, Sci. Rep., 9, 9642, 10.1038/s41598-019-45994-3 Ichimura, 2000, A ubiquitin-like system mediates protein lipidation, Nature, 408, 488, 10.1038/35044114 Josefsen, 2012, Autophagy provides nutrients for nonassimilating fungal structures and is necessary for plant colonization but not for infection in the necrotrophic plant pathogen Fusarium graminearum, Autophagy, 8, 326, 10.4161/auto.18705 Kabeya, 2009, Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae, Biochem. Biophys. Res. Commun., 389, 612, 10.1016/j.bbrc.2009.09.034 Kema, 2018, Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance, Nat Genet, 50, 375, 10.1038/s41588-018-0052-9 Kema, 1996, Histology of the pathogenesis of Mycosphaerella graminicola in wheat, Phytopathology, 86, 777, 10.1094/Phyto-86-777 Keon, 2007, Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host, Mol. Plant Microbe Interact., 20, 178, 10.1094/MPMI-20-2-0178 Kershaw, 2009, Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease, PNAS, 106, 15967, 10.1073/pnas.0901477106 Khan, 2012, Multifunction of autophagy-related genes in filamentous fungi, Microbiol. Res., 167, 339, 10.1016/j.micres.2012.01.004 Kilaru, 2015, A codon-optimized green fluorescent protein for live cell imaging in Zymoseptoria tritici, Fungal Genet. Biol., 79, 125, 10.1016/j.fgb.2015.03.022 King, 2017, A conserved fungal glycosyltransferase facilitates pathogenesis of plants by enabling hyphal growth on solid surfaces, PLoS Pathog., 13, e1006672, 10.1371/journal.ppat.1006672 Kiššová, 2007, Selective and Non-Selective Autophagic Degradation of Mitochondria in Yeast ND ES RIB, Autophagy, 4, 329, 10.4161/auto.4034 Klionsky, 2011, A comprehensive glossary of autophagy-related molecules and processes (2 nd edition), Autophagy, 7, 1273, 10.4161/auto.7.11.17661 Liu, 2018, Lipidation-independent vacuolar functions of Atg8 rely on its noncanonical interaction with a vacuole membrane protein, eLife, 7, e41237, 10.7554/eLife.41237 Liu, 2017, Autophagy-related protein MoAtg14 is involved in differentiation, development and pathogenicity in the rice blast fungus Magnaporthe oryzae, Sci. Rep., 7 Liu, 2007, Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in Appressorium turgor and pathogenesis, Eukaryot. Cell, 6, 997, 10.1128/EC.00011-07 Lv, 2017, Genome-wide functional analysis reveals that autophagy is necessary for growth, sporulation, deoxynivalenol production and virulence in Fusarium graminearum, Sci. Rep., 7, 11062, 10.1038/s41598-017-11640-z Lv, 2020, The sorting nexin FgAtg20 is involved in the Cvt pathway, non-selective macroautophagy, pexophagy and pathogenesis in Fusarium graminearum, Cell. Microbiol., 22, e13208, 10.1111/cmi.13208 Lynch-Day, 2010, The Cvt pathway as a model for selective autophagy, FEBS Lett., 584, 1359, 10.1016/j.febslet.2010.02.013 Maeda, 2017, Autophagy-independent function of Atg8 in lipid droplet dynamics in yeast, J. Biochem., 161, 339 Maeda, 2015, A defect of the vacuolar putative lipase Atg15 accelerates degradation of lipid droplets through lipolysis A defect of the vacuolar putative lipase Atg15 accelerates degradation of lipid droplets through lipolysis, Autophagy, 11, 1247, 10.1080/15548627.2015.1056969 Meiling-Wesse, 2002, Ccz1p/Aut11p/Cvt16p is essential for autophagy and the cvt pathway, FEBS Lett., 526, 71, 10.1016/S0014-5793(02)03119-8 Meng, 2020, UvAtg8-Mediated Autophagy Regulates Fungal Growth, Stress Responses, Conidiation, and Pathogenesis in Ustilaginoidea virens, Rice, 13, 10.1186/s12284-020-00418-z Mikawa, 2010, Fission yeast Vps1 and Atg8 contribute to oxidative stress resistance, Genes Cells, 15, 229, 10.1111/j.1365-2443.2009.01376.x Minina, 2014, Autophagy as initiator or executioner of cell death, Trends Plant Sci., 19, 692, 10.1016/j.tplants.2014.07.007 Mizushima, 2010, The role of the Atg1/ULK1 complex in autophagy regulation, Curr. Opin. Cell Biol., 22, 132, 10.1016/j.ceb.2009.12.004 Mizushima, 2011, Autophagy: Renovation of cells and tissues, Cell, 147, 728, 10.1016/j.cell.2011.10.026 Mizushima, 2010, Autophagy in mammalian development and differentiation, Nat. Cell Biol., 12, 823, 10.1038/ncb0910-823 Motteram, 2009, Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola, Mol. Plant Microbe Interact., 22, 790, 10.1094/MPMI-22-7-0790 Nadal, 2010, The autophagy genes atg8 and atg1 affect morphogenesis and pathogenicity in Ustilago maydis, Mol. Plant Pathol, 11, 463, 10.1111/j.1364-3703.2010.00620.x Nakatogawa, 2007, Atg8, a Ubiquitin-like Protein Required for Autophagosome Formation, Mediates Membrane Tethering and Hemifusion, Cell, 130, 165, 10.1016/j.cell.2007.05.021 Nakatogawa, 2012, The Autophagy-related Protein Kinase Atg1 Interacts with the Ubiquitin-like Protein Atg8 via the Atg8 Family Interacting Motif to Facilitate Autophagosome Formation, J. Biol. Chem., 287, 28503, 10.1074/jbc.C112.387514 Nguyen, 2011, Autophagy-related lipase FgATG15 of Fusarium graminearum is important for lipid turnover and plant infection, Fungal Genet. Biol., 48, 217, 10.1016/j.fgb.2010.11.004 Nitsche, 2013, Autophagy promotes survival in aging submerged cultures of the filamentous fungus Aspergillus niger, Appl. Microbiol. Biotechnol., 97, 8205, 10.1007/s00253-013-4971-1 Orvedahl, 2009, Eating the enemy within: Autophagy in infectious diseases, Cell Death Differ., 16, 57, 10.1038/cdd.2008.130 Palma-Guerrero, 2016, Comparative transcriptomic analyses of Zymoseptoria tritici strains show complex lifestyle transitions and intraspecific variability in transcription profiles, Mol. Plant Pathol, 17, 845, 10.1111/mpp.12333 Parzych, 2018, A newly characterized vacuolar serine carboxypeptidase, Atg42/Ybr139w, is required for normal vacuole function and the terminal steps of autophagy in the yeast Saccharomyces cerevisiae, Mol. Biol. Cell, 29, 1089, 10.1091/mbc.E17-08-0516 Pinan-Lucarré, 2005, Accelerated cell death in Podospora autophagy mutants, Eukaryot. Cell, 4, 1765, 10.1128/EC.4.11.1765-1774.2005 Pinar, 2013, Live-cell imaging of Aspergillus nidulans autophagy, Autophagy, 9, 1024, 10.4161/auto.24483 Pollack, 2009, Autophagy in filamentous fungi, Fungal Genet. Biol., 46, 1, 10.1016/j.fgb.2008.10.010 Rambold, 2015, Fatty Acid Trafficking in Starved Cells: Regulation by Lipid Droplet Lipolysis, Autophagy, and Article Fatty Acid Trafficking in Starved Cells: Regulation by Lipid Droplet Lipolysis, Autophagy, and Mitochondrial Fusion Dynamics, Dev. Cell, 32, 678, 10.1016/j.devcel.2015.01.029 Reggiori, 2013, Autophagic processes in yeast: Mechanism, machinery and regulation, Genetics, 194, 341, 10.1534/genetics.112.149013 Ren, 2017, The autophagy-related gene BcATG1 is involved in fungal development and pathogenesis in Botrytis cinerea, Mol. Plant Pathol, 18, 238, 10.1111/mpp.12396 Richie, 2007, Unexpected link between metal ion deficiency and autophagy in Aspergillus fumigatus, Eukaryot. Cell, 6, 2437, 10.1128/EC.00224-07 Rudd, 2015, Transcriptome and Metabolite Profiling of the Infection Cycle of Zymoseptoria tritici on Wheat Reveals a Biphasic Interaction with Plant Immunity Involving Differential Pathogen Chromosomal Contributions and a Variation on the Hemibiotrophic Lifest, Plant Physiol., 167, 1158, 10.1104/pp.114.255927 Sánchez-Vallet, 2015, Is Zymoseptoria tritici a hemibiotroph?, Fungal Genet. Biol., 79, 29, 10.1016/j.fgb.2015.04.001 Shi, 2019, CpATG8, a homolog of yeast autophagy protein ATG8, is required for pathogenesis and hypovirus accumulation in the chest blight fungus, Front. Cell. Infect. Microbiol., 9, 1, 10.3389/fcimb.2019.00222 Shimamura, 2019, Autophagy-Inducing Factor Atg1 Is Required for Virulence in the Pathogenic Fungus Candida glabrata, Front. Microbiol., 10, 10.3389/fmicb.2019.00027 Shimizu, 2004, Role of Bcl-2 family proteins in a non-apoptopic programmed cell death dependent on autophagy genes, Nat. Cell Biol., 6, 1221, 10.1038/ncb1192 Shoji, 2006, Vacuolar membrane dynamics in the filamentous fungus Aspergillus oryzae, Eukaryot. Cell, 5, 411, 10.1128/EC.5.2.411-421.2006 Shoji, 2011, Autophagy in basal hyphal compartments: A green strategy of great recyclers, Fungal Biol. Rev., 25, 79, 10.1016/j.fbr.2011.04.001 Shoji, 2010, Macroautophagy-mediated degradation of whole nuclei in the filamentous fungus Aspergillus oryzae, PLoS ONE, 5, e15650, 10.1371/journal.pone.0015650 Sidhu, 2015 Sidhu, 2015, Exploitation of sulfonylurea resistance marker and non-homologous end joining mutants for functional analysis in Zymoseptoria tritici, Fungal Genet. Biol., 79, 102, 10.1016/j.fgb.2015.04.015 Singh, 2009, Autophagy regulates lipid metabolism, Nature, 458, 1131, 10.1038/nature07976 Suffert, 2019, Sexual Reproduction in the Fungal Foliar Pathogen Zymoseptoria tritici Is Driven by Antagonistic Density Dependence Mechanisms, Microb. Ecol., 77, 110, 10.1007/s00248-018-1211-3 Sumita, 2017, Characterization of the autophagy-related gene BmATG8 in Bipolaris maydis, Fungal Biology, 121, 785, 10.1016/j.funbio.2017.05.008 Suzuki, 2001, The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation, EMBO J., 20, 5971, 10.1093/emboj/20.21.5971 Suzuki, 2007, Hierarchy of Atg proteins in pre-autophagosomal structure organization, Genes Cells, 12, 209, 10.1111/j.1365-2443.2007.01050.x Tamura, 2010, Atg8 regulates vacuolar membrane dynamics in a lipidation-independent manner in Pichia pastoris, J. Cell Sci., 123, 4107, 10.1242/jcs.070045 Torggler, 2017, Assays to Monitor Autophagy in Saccharomyces cerevisiae, Cells, 6, 23, 10.3390/cells6030023 Torriani, 2015, Zymoseptoria tritici: A major threat to wheat production, integrated approaches to control, Fungal Genet. Biol., 79, 8, 10.1016/j.fgb.2015.04.010 Veneault-Fourrey, 2006, Autophagic Fungal Cell Death Is Necessary for Infection by the Rice Rice Blast Fungus, Science, 312, 580, 10.1126/science.1124550 Voigt, 2013, Autophagy genes Smatg8 and Smatg4 are required for fruiting-body development, vegetative growth and ascospore germination in the filamentous ascomycete Sordaria macrospora, Autophagy, 9, 33, 10.4161/auto.22398 Wang, 2019, Independent losses and duplications of autophagy-related genes in fungal tree of life, Environ. Microbiol., 21, 226, 10.1111/1462-2920.14451 Xie, 2007, Autophagosome formation: Core machinery and adaptations, Nat. Cell Biol., 9, 1102, 10.1038/ncb1007-1102 Yanagisawa, 2013, Functional analysis of Aoatg1 and detection of the Cvt pathway in Aspergillus oryzae, FEMS Microbiol. Lett., 338, 168, 10.1111/1574-6968.12047 Yemelin, 2017, Identification of factors involved in dimorphism and pathogenicity of Zymoseptoria tritici, PLoS ONE, 12, e0183065, 10.1371/journal.pone.0183065 Ying, S.H., Liu, J., Chu, X.L., Xie, X.Q. & Feng, M.G. (2016) The autophagy-related genes BbATG1 and BbATG8 have different functions in differentiation, stress resistance and virulence of mycopathogen Beauveria bassiana. Scientific Reports, 6, 1–12. https://doi.org/10.1038/srep26376. Zhan, 2017, Genome-Wide Identification and Analysis of MAPK and MAPKK Gene Families in Bread Wheat (Triticum aestivum L.), Genes, 8, 284, 10.3390/genes8100284 Zhang, 2007, The role of autophagy in mitochondria maintenance: Characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains, Autophagy, 3, 337, 10.4161/auto.4127 van Zutphen, 2014, Lipid droplet autophagy in the yeast Saccharomyces cerevisiae, Mol. Biol. Cell, 25, 290, 10.1091/mbc.e13-08-0448 Zwiers, 2001, Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola, Curr. Genet., 39, 388, 10.1007/s002940100216 Goodwin, S. B., B. M'Barek S, B. Dhillon, A. H. Wittenberg, C. F. Crane, J. K. Hane, A. J. Foster, T. A. Van der Lee, J. Grimwood, A. Aerts, J. Antoniw, A. Bailey, B. Bluhm, J. Bowler, J. Bristow, A. van der Burgt, B. Canto-Canché, A. C. Churchill, L. Conde-Ferràez, H. J. Cools, P. M. Coutinho, M. Csukai, P. Dehal, P. De Wit, B. Donzelli, H. C. van de Geest, R. C. van Ham, K. E. Hammond-Kosack, B. Henrissat, A. Kilian, A. K. Kobayashi, E. Koopmann, Y. Kourmpetis, A. Kuzniar, E. Lindquist, V. Lombard, C. Maliepaard, N. Martins, R. Mehrabi, J. P. Nap, A. Ponomarenko, J. J. Rudd, A. Salamov, J. Schmutz, H. J. Schouten, H. Shapiro, I. Stergiopoulos, S. F. Torriani, H. Tu, R. P. de Vries, C. Waalwijk, S. B. Ware, A. Wiebenga, L. H. Zwiers, R. P. Oliver, I. V. Grigoriev and G. H. Kema 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7, e1002070.