1,327
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Activation of microlipophagy during early infection of insect hosts by Metarhizium robertsii

, , , & ORCID Icon
Pages 608-623 | Received 31 Jan 2021, Accepted 10 Jun 2021, Published online: 21 Jun 2021

References

  • Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8:931–937.
  • Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition). Autophagy. 2021;17:1–382.
  • Ohsumi Y. Historical landmarks of autophagy research. Cell Res. 2014;24:9–23.
  • Galluzzi L, Baehrecke EH, Ballabio A, et al. Molecular definitions of autophagy and related processes. EMBO J. 2017;36:1811–1836.
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol. 2011;27:107–132.
  • Schuck S. Microautophagy - distinct molecular mechanisms handle cargoes of many sizes. J Cell Sci. 2020;133:jcs246322.
  • Sieńko K, Poormassalehgoo A, Yamada K, et al. Microautophagy in plants: consideration of its molecular mechanism. Cells. 2020;9:887.
  • van Zutphen T, Todde V, De Boer R, et al. Lipid droplet autophagy in the yeast Saccharomyces cerevisiae. Mol Biol Cell. 2014;25:290–301.
  • Wang CW, Miao YH, Chang YS. A sterol-enriched vacuolar microdomain mediates stationary phase lipophagy in budding yeast. J Cell Biol. 2014;206:357–366.
  • Garcia EJ, Liao PC, Tan G, et al. Membrane dynamics and protein targets of lipid droplet microautophagy during ER stress-induced proteostasis in the budding yeast, Saccharomyces cerevisiae. Autophagy. 2020;1–21. doi: 10.1080/15548627.2020.1826691
  • Vevea JD, Garcia EJ, Chan RB, et al. Role for lipid droplet biogenesis and microlipophagy in adaptation to lipid imbalance in yeast. Dev Cell. 2015;35:584–599.
  • Hashemi HF, Goodman JM. The life cycle of lipid droplets. Curr Opin Cell Biol. 2015;33:119–124.
  • Goodman JM. The importance of microlipophagy in liver. Proc Natl Acad Sci USA. 2021;118:e2024058118.
  • Farré JC, Subramani S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Biol. 2016;17:537–552.
  • Wen X, Klionsky DJ. An overview of macroautophagy in yeast. J Mol Biol. 2016;428:1681–1699.
  • Hofius D, Li L, Hafrén A, et al. Autophagy as an emerging arena for plant-pathogen interactions. Curr Opin Plant Biol. 2017;38:117–123.
  • Palmer GE, Askew DS, Williamson PR. The diverse roles of autophagy in medically important fungi. Autophagy. 2008;4:982–988.
  • Ying SH, Feng MG. Insight into vital role of autophagy in sustaining biological control potential of fungal pathogens against pest insects and nematodes. Virulence. 2019;10:429–437.
  • Veneault-Fourrey C, Barooah M, Egan M, et al. Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science. 2006;312:580–583.
  • Kershaw MJ, Talbot NJ. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci USA. 2009;106:15967–15972.
  • Lv W, Wang C, Yang N, et al. Genome-wide functional analysis reveals that autophagy is necessary for growth, sporulation, deoxynivalenol production and virulence in Fusarium graminearum. Sci Rep. 2017;7:11062.
  • Zhao X, Feng W, Zhu X, et al. Conserved autophagy pathway contributes to stress tolerance and virulence and differentially controls autophagic flux upon nutrient starvation in Cryptococcus neoformans. Front Microbiol. 2019;10:2690.
  • Jiang ST, Chang AN, Han LT, et al. Autophagy regulates fungal virulence and sexual reproduction in Cryptococcus neoformans. Front Cell Dev Biol. 2020;8:374.
  • Wang CS, Wang SB. Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol. 2017;62:73–90.
  • Wang CS, Feng MG. Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biol Control. 2014;68:129–135.
  • Duan ZB, Chen YX, Huang W, et al. Linkage of autophagy to fungal development, lipid storage and virulence in Metarhizium robertsii. Autophagy. 2013;9:538–549.
  • Liu XH, Gao HM, Xu F, et al. Autophagy vitalizes the pathogenicity of pathogenic fungi. Autophagy. 2012;8:1415–1425.
  • Hu X, Xiao G, Zheng P, et al. Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proc Natl Acad Sci USA. 2014;111:16796–16801.
  • Wilson RA, Talbot NJ. Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol. 2009;7:185–195.
  • Thines E, Weber RW, Talbot NJ. MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell. 2000;12:1703–1718.
  • Gao Q, Lu Y, Yao H, et al. Phospholipid homeostasis maintains cell polarity, development and virulence in Metarhizium robertsii. Environ Microbiol. 2016;18:3976–3990.
  • Chen YX, Li B, Cen K, et al. Diverse effect of phosphatidylcholine biosynthetic genes on phospholipid homeostasis, cell autophagy and fungal developments in Metarhizium robertsii. Environ Microbiol. 2018;20:293–304.
  • Wang CS, St Leger RJ. The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. J Biol Chem. 2007;282:21110–21115.
  • Gaspar ML, Hofbauer HF, Kohlwein SD, et al. Coordination of storage lipid synthesis and membrane biogenesis: evidence for cross-talk between triacylglycerol metabolism and phosphatidylinositol synthesis. J Biol Chem. 2011;286:1696–1708.
  • Kurat CF, Natter K, Petschnigg J, et al. Obese yeast: triglyceride lipolysis is functionally conserved from mammals to yeast. J Biol Chem. 2006;281:491–500.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
  • Ryder LS, Talbot NJ. Regulation of appressorium development in pathogenic fungi. Curr Opin Plant Biol. 2015;26:8–13.
  • Ortiz-Urquiza A, Keyhani NO. Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects. 2013;4:357–374.
  • Yan X, Talbot NJ. Investigating the cell biology of plant infection by the rice blast fungus Magnaporthe oryzae. Curr Opin Microbiol. 2016;34:147–153.
  • Zhu XM, Li L, Wu M, et al. Current opinions on autophagy in pathogenicity of fungi. Virulence. 2019;10:481–489.
  • Reggiori F, Tucker KA, Stromhaug PE, et al. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell. 2004;6:79–90.
  • Yin Z, Chen C, Yang J, et al. Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in Magnaporthe oryzae. Autophagy. 2019;15:1234–1257.
  • Foster AJ, Ryder LS, Kershaw MJ, et al. The role of glycerol in the pathogenic lifestyle of the rice blast fungus Magnaporthe oryzae. Environ Microbiol. 2017;19:1008–1016.
  • Xie Z, Nair U, Klionsky DJ. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008;19:3290–3298.
  • Yu ZQ, Ni T, Hong B, et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy. 2012;8:883–892.
  • Kraft C, Martens S. Mechanisms and regulation of autophagosome formation. Curr Opin Cell Biol. 2012;24:496–501.
  • Schulze RJ, Krueger EW, Weller SG, et al. Direct lysosome-based autophagy of lipid droplets in hepatocytes. Proc Natl Acad Sci USA. 2020;117:32443–32452.
  • Yin Z, Feng W, Chen C, et al. Shedding light on autophagy coordinating with cell wall integrity signaling to govern pathogenicity of Magnaporthe oryzae. Autophagy. 2020;16:900–916.
  • Ward C, Martinez-Lopez N, Otten EG, et al. Autophagy, lipophagy and lysosomal lipid storage disorders. Biochim Biophys Acta. 2016;1864:269–284.
  • Maeda Y, Oku M, Sakai Y. A defect of the vacuolar putative lipase Atg15 accelerates degradation of lipid droplets through lipolysis. Autophagy. 2015;11:1247–1258.
  • Wang CW, Miao YH, Chang YS. Control of lipid droplet size in budding yeast requires the collaboration between Fld1 and Ldb16. J Cell Sci. 2014;127:1214–1228.
  • Schmidt C, Ploier B, Koch B, et al. Analysis of yeast lipid droplet proteome and lipidome. Methods Cell Biol. 2013;116:15–37.
  • Krahmer N, Mann M. Catching lipid droplet contacts by proteomics. Contact. 2019;2:2515256419859186.
  • Chen YX, Cen K, Lu Y, et al. Nitrogen-starvation triggers cellular accumulation of triacylglycerol in Metarhizium robertsii. Fungal Biol. 2018;122:410–419.
  • Huang W, Hong S, Tang G, et al. Unveiling the function and regulation control of the DUF3129 family proteins in fungal infection of hosts. Philos Trans R Soc Lond B Biol Sci. 2019;374:20180321.
  • Sánchez-Wandelmer J, Kriegenburg F, Rohringer S, et al. Atg4 proteolytic activity can be inhibited by Atg1 phosphorylation. Nat Commun. 2017;8:295.
  • Noda NN, Ohsumi Y, Inagaki F. Atg8-family interacting motif crucial for selective autophagy. FEBS Lett. 2010;584:1379–1385.
  • Yamaguchi M, Noda NN, Nakatogawa H, et al. Autophagy-related protein 8 (Atg8) family interacting motif in Atg3 mediates the Atg3-Atg8 interaction and is crucial for the cytoplasm-to-vacuole targeting pathway. J Biol Chem. 2010;285:29599–29607.
  • Nakatogawa H, Ohbayashi S, Sakoh-Nakatogawa M, et al. 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. 2012;287:28503–28507.
  • Gao Q, Shang YF, Huang W, et al. Glycerol-3-phosphate acyltransferase contributes to triacylglycerol biosynthesis, lipid droplet formation, and host invasion in Metarhizium robertsii. Appl Environ Microbiol. 2013;79:7646–7653.
  • Luo FF, Hong S, Chen B, et al. Unveiling of swainsonine biosynthesis via a multi-branched pathway in fungi. ACS Chem Biol. 2020;15:2476–2484.
  • Huang W, Shang Y, Chen P, et al. Basic leucine zipper (bZIP) domain transcription factor MBZ1 regulates cell wall integrity, spore adherence, and virulence in Metarhizium robertsii. J Biol Chem. 2015;290:8218–8231.
  • Huang A, Lu M, Ling E, et al. A M35 family metalloprotease is required for fungal virulence against insects by inactivating host prophenoloxidases and beyond. Virulence. 2020;11:222–237.
  • Tang GR, Shang YF, Li SQ, et al. MrHex1 is required for Woronin body formation, fungal development and virulence in Metarhizium robertsii. J Fungi. 2020;6:172.
  • Cen K, Li B, Lu YZ, et al. Divergent LysM effectors contribute to the virulence of Beauveria bassiana by evasion of insect immune defenses. PLoS Pathog. 2017;13:e1006604.
  • Wang CS, St Leger RJ. Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryot Cell. 2005;4:937–947.
  • Shang JM, Shang YF, Tang GR, et al. Identification of a key G-protein coupled receptor in mediating appressorium formation and fungal virulence against insects. Sci China Life Sci. 2021;64:466–477.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.