1,059
Views
5
CrossRef citations to date
0
Altmetric
Review Article

Role of cell membrane homeostasis in the pathogenicity of pathogenic filamentous fungi

&
Article: 2299183 | Received 27 Aug 2023, Accepted 20 Dec 2023, Published online: 29 Dec 2023

References

  • Yadav DK, Kumar S, Choi EH, et al. Molecular dynamic simulations of oxidized skin lipid bilayer and permeability of reactive oxygen species. Sci Rep. 2019;9(1):4496. doi: 10.1038/s41598-019-40913-y
  • Mychack A, Janakiraman A, Brun YV. Defects in the first step of lipoprotein maturation underlie the synthetic lethality of Escherichia coli lacking the inner membrane proteins YciB and DcrB. J Bacteriol. 2021;203(6). doi: 10.1128/JB.00640-20
  • van Meer G, Voelker DR, Feigenson GW. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol. 2008;9(2):112–11. doi: 10.1038/nrm2330
  • Nicolson GL. The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim Biophys Acta. 2014;1838:1451–1466. doi: 10.1016/j.bbamem.2013.10.019
  • Sonnino S, Prinetti A. Membrane domains and the “lipid raft” concept. Curr Med Chem. 2013;20:4–21. doi: 10.2174/0929867311320010003
  • Horn A, Jaiswal JK. Structural and signaling role of lipids in plasma membrane repair. Curr Top Membr. 2019;84:67–98.
  • Baltussen T, Zoll J, Verweij PE, et al. Molecular mechanisms of conidial germination in aspergillus spp. Microbiol Mol Biol Rev. 2020;84(1). doi: 10.1128/MMBR.00049-19
  • Fortwendel JR. Orchestration of morphogenesis in filamentous fungi: conserved roles for ras signaling networks. Fungal Biol Rev. 2015;29(2):54–62. doi: 10.1016/j.fbr.2015.04.003
  • Cerioni L, Volentini SI, Prado FE, et al. Cellular damage induced by a sequential oxidative treatment on penicillium digitatum. J Appl Microbiol. 2010;109(4):1441–1449. doi: 10.1111/j.1365-2672.2010.04775.x
  • Malinsky J, Opekarova M. New insight into the roles of membrane microdomains in physiological activities of fungal cells. Int Rev Cell Mol Biol. 2016;325:119–180.
  • Ziolkowska NE, Christiano R, Walther TC. Organized living: formation mechanisms and functions of plasma membrane domains in yeast. Trends Cell Biol. 2012;22(3):151–158. doi: 10.1016/j.tcb.2011.12.002
  • Harayama T, Riezman H. Understanding the diversity of membrane lipid composition. Nat Rev Mol Cell Biol. 2018;19(5):281–296. doi: 10.1038/nrm.2017.138
  • Epand RM. Introduction to membrane lipids. Methods Mol Biol. 2015;1232:1–6.
  • Escriba PV, Busquets X, Inokuchi J, et al. Membrane lipid therapy: modulation of the cell membrane composition and structure as a molecular base for drug discovery and new disease treatment. Prog Lipid Res. 2015;59:38–53. doi: 10.1016/j.plipres.2015.04.003
  • Thomas FB, Omnus DJ, Bader JM, et al. Tricalbin proteins regulate plasma membrane phospholipid homeostasis. Life Sci Alliance. 2022;5(8):e202201430. doi: 10.26508/lsa.202201430
  • Akhberdi O, Zhang Q, Wang H, et al. Roles of phospholipid methyltransferases in pycnidia development, stress tolerance and secondary metabolism in the taxol-producing fungus pestalotiopsis microspore. Microbiol Res. 2018;210:33–42. doi: 10.1016/j.micres.2018.03.001
  • Beauvais A, Latge JP. Membrane and cell wall targets in aspergillus fumigatus. Drug Resist Updat. 2001;4(1):38–49. doi: 10.1054/drup.2001.0185
  • Fernandes CM, de Castro PA, Singh A, et al. Functional characterization of the Aspergillus nidulans glucosylceramide pathway reveals that LCB Delta8-desaturation and C9-methylation are relevant to filamentous growth, lipid raft localization and Psd1 defensin activity. Mol Microbiol. 2016;102:488–505. doi: 10.1111/mmi.13474
  • Li S, Du L, Yuen G, et al. Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans. Mol Biol Cell. 2006;17(3):1218–1227. doi: 10.1091/mbc.e05-06-0533
  • Head BP, Patel HH, Insel PA. Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim Biophys Acta. 2014;1838(2):532–545. doi: 10.1016/j.bbamem.2013.07.018
  • Markham P, Robson GD, Bainbridge BW, et al. Choline: its role in the growth of filamentous fungi and the regulation of mycelial morphology. FEMS Microbiol Rev. 1993;10:287–300. doi: 10.1111/j.1574-6968.1993.tb05872.x
  • Cotado-Sampayo M, Ramos PO, Perez RO, et al. Specificity of commercial anti-spectrin antibody in the study of fungal and oomycete spectrin: cross-reaction with proteins other than spectrin. Fungal Genet Biol. 2008;45(6):1008–1015. doi: 10.1016/j.fgb.2008.02.003
  • Fontaine T. Sphingolipids from the human fungal pathogen Aspergillus fumigatus. Biochimie. 2017;141:9–15. doi: 10.1016/j.biochi.2017.06.012
  • Hassing B, Candy A, Eaton CJ, et al. Localisation of phosphoinositides in the grass endophyte epichloë festucae and genetic and functional analysis of key components of their biosynthetic pathway in E. festucae symbiosis and Fusarium oxysporum pathogenesis. Fungal Genet Biol. 2022;159:103669. doi: 10.1016/j.fgb.2022.103669
  • Redkar A, Di Pietro A. Adapt your shuttling proteins for virulence: a lesson from the corn smut fungusUstilago maydis. New Phytol. 2018;220(2):353–356. doi: 10.1111/nph.15429
  • Zhu X, Li L, Wang J, et al. Vacuolar protein-sorting receptor MoVps13 regulates conidiation and pathogenicity in rice blast fungus magnaporthe oryzae. J Fungi (Basel). 2021;7(12):1084. doi: 10.3390/jof7121084
  • Phillips R, Ursell T, Wiggins P, et al. Emerging roles for lipids in shaping membrane-protein function. Nature. 2009;459(7245):379–385. doi: 10.1038/nature08147
  • Fabri J, Rocha MC, Malavazi I. Overview of the interplay between cell wall integrity signaling pathways and membrane lipid biosynthesis in fungi: perspectives for Aspergillus fumigatus. Curr Protein Pept Sci. 2020;21:265–283. doi: 10.2174/1389203720666190705164203
  • Turk M, Abramovic Z, Plemenitas A, et al. Salt stress and plasma-membrane fluidity in selected extremophilic yeasts and yeast-like fungi. FEMS Yeast Res. 2007;7:550–557. doi: 10.1111/j.1567-1364.2007.00209.x
  • Sangappillai V, Nadarajah K. Fatty acid synthase beta dehydratase in the lipid biosynthesis pathway is required for conidiogenesis, pigmentation and appressorium formation in magnaporthe oryzae S6. Int J Mol Sci. 2020;21(19):7224. doi: 10.3390/ijms21197224
  • Wang ZY, Soanes DM, Kershaw MJ, et al. Functional analysis of lipid metabolism in magnaporthe grisea reveals a requirement for peroxisomal fatty acid beta-oxidation during appressorium-mediated plant infection. Mol Plant Microbe Interact. 2007;20:475–491. doi: 10.1094/MPMI-20-5-0475
  • Goodrich-Tanrikulu M, Howe K, Stafford A, et al. Changes in fatty acid composition of Neurospora crassa accompany sexual development and ascospore germination. Microbiology (Reading). 1998;144(Pt 7):1713–1720. doi: 10.1099/00221287-144-7-1713
  • Khunyoshyeng S, Cheevadhanarak S, Rachdawong S, et al. Differential expression of desaturases and changes in fatty acid composition during sporangiospore germination and development in mucor rouxii. Fungal Genet Biol. 2002;37(1):13–21. doi: 10.1016/S1087-1845(02)00028-2
  • 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. doi: 10.1105/tpc.12.9.1703
  • Zhang L, Cao X, Wang Z, et al. Brassinolide alleviated chilling injury of banana fruit by regulating unsaturated fatty acids and phenolic compounds. Sci Hortic. 2022;297:110922. doi: 10.1016/j.scienta.2022.110922
  • Resnick MA, Mortimer RK. Unsaturated fatty acid mutants of Saccharomyces cerevisiae. J Bacteriol. 1966;92(3):597–600. doi: 10.1128/jb.92.3.597-600.1966
  • Wisnieski BJ, Kiyomoto RK. Fatty acid desaturase mutants of yeast: growth requirements and electron spin resonance spin-label distribution. J Bacteriol. 1972;109(1):186–195. doi: 10.1128/jb.109.1.186-195.1972
  • Reich M, Gobel C, Kohler A, et al. Fatty acid metabolism in the ectomycorrhizal fungus Laccaria bicolor. New Phytol. 2009;182(4):950–964. doi: 10.1111/j.1469-8137.2009.02819.x
  • Ballweg S, Ernst R. Control of membrane fluidity: the OLE pathway in focus. Biol Chem. 2017;398(2):215–228. doi: 10.1515/hsz-2016-0277
  • Micoogullari Y, Basu SS, Ang J, et al. Dysregulation of very-long-chain fatty acid metabolism causes membrane saturation and induction of the unfolded protein response. Mol Biol Cell. 2020;31(1):7–17. doi: 10.1091/mbc.E19-07-0392
  • Covino R, Ballweg S, Stordeur C, et al. A eukaryotic sensor for membrane lipid saturation. Mol Cell. 2016Jul 7;63(1):49–59. doi: 10.1016/j.molcel.2016.05.015
  • Ogasawara Y, Kira S, Mukai Y, et al. Ole1, fatty acid desaturase, is required for Atg9 delivery and isolation membrane expansion during autophagy in Saccharomyces cerevisiae. Biol Open. 2017 Jan 15;6(1):35–40. doi: 10.1242/bio.022053.
  • Peng YJ, Wang JJ, Lin HY, et al. HapX, an indispensable bZIP Transcription factor for iron acquisition, regulates infection initiation by orchestrating conidial oleic acid homeostasis and cytomembrane functionality in Mycopathogen Beauveria bassiana. mSystems. 2020;5(5). doi: 10.1128/mSystems.00695-20
  • Luo X, Affeldt KJ, Keller NP. Characterization of the far transcription factor family in Aspergillus flavus. G3. 2016;6(6):3269–3281. doi: 10.1534/g3.116.032466
  • Surma MA, Klose C, Peng D, et al. A lipid E-MAP identifies Ubx2 as a critical regulator of lipid saturation and lipid bilayer stress. Mol Cell. 2013;51(4):519–530. doi: 10.1016/j.molcel.2013.06.014
  • Paege N, Warnecke D, Zauner S, et al. Species-Specific Differences in the Susceptibility of Fungi to the Antifungal Protein AFP Depend on C-3 Saturation of Glycosylceramides. mSphere. 2019;4(6). doi: 10.1128/mSphere.00741-19
  • Peng YJ, Zhang H, Feng MG, et al. SterylAcetyl hydrolase 1 (BbSay1) links lipid homeostasis to conidiogenesis and virulence in the entomopathogenic fungus beauveria bassiana. J Fungi (Basel). 2022;8(3):292. doi: 10.3390/jof8030292
  • Douglas LM, Konopka JB. Fungal membrane organization: the eisosome concept. Annu Rev Microbiol. 2014;68(1):377–393. doi: 10.1146/annurev-micro-091313-103507
  • Guna A, Hegde RS. Transmembrane Domain Recognition during Membrane Protein Biogenesis and Quality Control. Curr Biol. 2018;28(8):R498–R511. doi: 10.1016/j.cub.2018.02.004
  • DeZwaan TM, Carroll AM, Valent B, et al. Magnaporthe grisea pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell. 1999;11(10):2013–2030. doi: 10.1105/tpc.11.10.2013
  • Shang J, Tang G, Yang J, et al. Sensing of a spore surface protein by a drosophila chemosensory protein induces behavioral defense against fungal parasitic infections. Curr Biol. 2023;33:276–286. doi: 10.1016/j.cub.2022.11.004
  • Ota K, Butala M, Viero G, et al. Fungal MACPF-like proteins and aegerolysins: bi-component pore-forming proteins? Subcell Biochem. 2014;80:271–291.
  • Wang F, Wang Y, Zhang X, et al. Recent progress of cell-penetrating peptides as new carriers for intracellular cargo delivery. J Control Release. 2014;174:126–136. doi: 10.1016/j.jconrel.2013.11.020
  • Eichel K, von Zastrow M. Subcellular Organization of GPCR Signaling. Trends Pharmacol Sci. 2018;39(2):200–208. doi: 10.1016/j.tips.2017.11.009
  • Lebreton S, Zurzolo C, Paladino S. Organization of GPI-anchored proteins at the cell surface and its physiopathological relevance. Crit Rev Biochem Mol Biol. 2018;53(4):403–419. doi: 10.1080/10409238.2018.1485627
  • Yun Y, Guo P, Zhang J, et al. Flippases play specific but distinct roles in the development, pathogenicity, and secondary metabolism ofFusarium graminearum. Mol Plant Pathol. 2020;21(10):1307–1321. doi: 10.1111/mpp.12985
  • Mazheika I, Voronko O, Kamzolkina O. Early endocytosis as a key to understanding mechanisms of plasma membrane tension regulation in filamentous fungi. Biol Cell. 2020;112(12):409–426. doi: 10.1111/boc.202000066
  • Blanchoin L, Boujemaa-Paterski R, Sykes C, et al. Actin dynamics, architecture, and mechanics in cell motility. Physiol Rev. 2014;94(1):235–263. doi: 10.1152/physrev.00018.2013
  • Juvvadi PR, Fortwendel JR, Rogg LE, et al. Differential localization patterns of septins during growth of the human fungal pathogen Aspergillus fumigatus reveal novel functions. Biochem Biophys Res Commun. 2011;405(2):238–243. doi: 10.1016/j.bbrc.2011.01.017
  • Vargas-Muniz JM, Renshaw H, Richards AD, et al. The Aspergillus fumigatus septins play pleiotropic roles in septation, conidiation, and cell wall stress, but are dispensable for virulence. Fungal Genet Biol. 2015;81:41–51. doi: 10.1016/j.fgb.2015.05.014
  • Badrane H, Nguyen MH, Clancy CJ. Highly dynamic and specific phosphatidylinositol 4,5-bisphosphate, septin, and cell wall integrity pathway responses correlate with caspofungin activity against Candida albicans. Antimicrob Agents Chemother. 2016;60(6):3591–3600. doi: 10.1128/AAC.02711-15
  • Badrane H, Nguyen MH, Blankenship JR, et al. Rapid redistribution of phosphatidylinositol-(4,5)-bisphosphate and septins during the Candida albicans response to caspofungin. Antimicrob Agents Chemother. 2012;56(9):4614–4624. doi: 10.1128/AAC.00112-12
  • Mela A, Momany M. Septins coordinate cell wall integrity and lipid metabolism in a sphingolipid-dependent process. J Cell Sci. 2022;135(5). doi: 10.1242/jcs.258336
  • Roelants FM, Su BM, von Wulffen J, et al. Protein kinase Gin4 negatively regulates flippase function and controls plasma membrane asymmetry. J Cell Bio. 2015;208(3):299–311. doi: 10.1083/jcb.201410076
  • Takeshita N. Control of actin and calcium for chitin synthase delivery to the hyphal tip of Aspergillus. Curr Top Microbiol Immunol. 2020;425:113–129.
  • Seidl-Seiboth V, Zach S, Frischmann A, et al. Spore germination of Trichoderma atroviride is inhibited by its LysM protein TAL6. FEBS J. 2013;280(5):1226–1236. doi: 10.1111/febs.12113
  • Zhang LB, Tang L, Guan Y, et al. Subcellular localization of Sur7 and its pleiotropic effect on cell wall integrity, multiple stress responses, and virulence of Beauveria bassiana. Appl Microbiol Biotechnol. 2020;104(15):6669–6678. doi: 10.1007/s00253-020-10736-3
  • McMahon HT, Gallop JL. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 2005;438(7068):590–596. doi: 10.1038/nature04396
  • Kunding AH, Mortensen MW, Christensen SM, et al. Intermembrane docking reactions are regulated by membrane curvature. Biophys J. 2011;101(11):2693–2703. doi: 10.1016/j.bpj.2011.09.059
  • Roux A, Koster G, Lenz M, et al. Membrane curvature controls dynamin polymerization. Proc Natl Acad Sci, USA. 2010;107:4141–4146. doi: 10.1073/pnas.0913734107
  • Mim C, Unger VM. Membrane curvature and its generation by BAR proteins. Trends Biochem Sci. 2012;37(12):526–533. doi: 10.1016/j.tibs.2012.09.001
  • Celio GJ, Mims CW, Richardson EA. Ultrastructure and immunocytochemistry of the host–pathogen interface in poinsettia leaves infected with powdery mildew. Can J Bot. 2004;82:421–429. doi: 10.1139/b04-019
  • Bridges AA, Jentzsch MS, Oakes PW, et al. Micron-scale plasma membrane curvature is recognized by the septin cytoskeleton. J Cell Bio. 2016;213(1):23–32. doi: 10.1083/jcb.201512029
  • Cannon KS, Woods BL, Crutchley JM, et al. An amphipathic helix enables septins to sense micrometer-scale membrane curvature. J Cell Bio. 2019;218(4):1128–1137. doi: 10.1083/jcb.201807211
  • Momany M, Talbot NJ. Septins focus cellular growth for host infection by pathogenic fungi. Front Cell Dev Biol. 2017;5:33. doi: 10.3389/fcell.2017.00033
  • Dagdas YF, Yoshino K, Dagdas G, et al. Septin-mediated plant cell invasion by the rice blast fungus, magnaporthe oryzae. Science. 2012;336(6088):1590–1595. doi: 10.1126/science.1222934
  • Nath S, Dancourt J, Shteyn V, et al. Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nat Cell Biol. 2014;16(5):415–424. doi: 10.1038/ncb2940
  • Lin HY, Ding JL, Peng YJ, et al. Proteomic and phosphoryproteomic investigations reveal that autophagy-related protein 1, a protein kinase for autophagy initiation, synchronously deploys phosphoregulation on the ubiquitin-like conjugation system in the mycopathogen beauveria bassiana. mSystems. 2022;7(1):e146321. doi: 10.1128/msystems.01463-21
  • McMahon HT, Boucrot E. Membrane curvature at a glance. J Cell Sci. 2015;128(6):1065–1070. doi: 10.1242/jcs.114454
  • Rojas ER, Huang KC, Theriot JA. Homeostatic cell growth is accomplished mechanically through membrane tension inhibition of cell-wall synthesis. Cell Syst. 2017;5:578–590. doi: 10.1016/j.cels.2017.11.005
  • Radeck J, Lautenschlager N, Mascher T. The essential UPP phosphatase pair BcrC and UppP connects cell wall homeostasis during growth and sporulation with cell envelope stress response in Bacillus subtilis. Front Microbiol. 2017;8:2403. doi: 10.3389/fmicb.2017.02403
  • Athanasopoulos A, Andre B, Sophianopoulou V, et al. Fungal plasma membrane domains. FEMS Microbiol Rev. 2019;43(6):642–673. doi: 10.1093/femsre/fuz022
  • Commer B, Shaw BD. Current views on endocytosis in filamentous fungi. Mycology. 2020;12:1–9. doi: 10.1080/21501203.2020.1741471
  • Peng YJ, Ding JL, Lin HY, et al. A virulence-related lectin traffics into eisosome and contributes to functionality of cytomembrane and cell-wall in the insect-pathogenic fungus Beauveria bassiana. Fungal Biol. 2021;125(11):914–922. doi: 10.1016/j.funbio.2021.06.005
  • Zhao X, Yang X, Lu Z, et al. MADS-box transcription factor Mcm1 controls cell cycle, fungal development, cell integrity and virulence in the filamentous insect pathogenic fungus beauveria bassiana. Environ Microbiol. 2019;21(9):3392–3416. doi: 10.1111/1462-2920.14629
  • Vangalis V, Papaioannou IA, Markakis EA, et al. Hex1, the major component of woronin bodies, is required for normal development, pathogenicity, and stress response in the plant pathogenic fungus verticillium dahliae. J Fungi (Basel). 2020Dec 7;6(4):344. doi: 10.3390/jof6040344
  • Palma-Guerrero J, Huang IC, Jansson HB, et al. Chitosan permeabilizes the plasma membrane and kills cells of neurospora crassa in an energy dependent manner. Fungal Genet Biol. 2009;46(8):585–594. doi: 10.1016/j.fgb.2009.02.010
  • Stepien L, Lalak-Kanczugowska J. Signaling pathways involved in virulence and stress response of plant-pathogenic fusarium species. Fungal Biol Rev. 2021;35:27–39. doi: 10.1016/j.fbr.2020.12.001
  • Wen Z, Tian H, Xia Y, et al. MaPmt1, a protein O-mannosyltransferase, contributes to virulence through governing the appressorium turgor pressure in metarhizium acridum. Fungal Genet Biol. 2020;145:103480. doi: 10.1016/j.fgb.2020.103480
  • Klein DA, Paschke MW. Filamentous fungi: the indeterminate lifestyle and microbial ecology. Microb Ecol. 2004;47(3):224–235. doi: 10.1007/s00248-003-1037-4
  • Richie DL, Hartl L, Aimanianda V, et al. A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLOS Pathog. 2009;5(1):e1000258. doi: 10.1371/journal.ppat.1000258
  • Garcia-Rubio R, de Oliveira HC, Rivera J, et al. The fungal cell wall: Candida, Cryptococcus, and Aspergillus species. Front Microbiol. 2019;10:2993. doi: 10.3389/fmicb.2019.02993
  • Wang J, Zhou G, Ying SH, et al. P-type calcium ATPase functions as a core regulator of beauveria bassiana growth, conidiation and responses to multiple stressful stimuli through cross-talk with signalling networks. Environ Microbiol. 2013;15(3):967–979. doi: 10.1111/1462-2920.12044
  • Liu J, Wang C, Kong L, et al. Rho2 involved in development, stress response and pathogenicity of Fusarium oxysporum. World J Microbiol Biotechnol. 2023;39(10):272. doi: 10.1007/s11274-023-03720-2
  • Ruiz-Roldan C, Pareja-Jaime Y, Gonzalez-Reyes JA, et al. The transcription factor Con7-1 is a master regulator of morphogenesis and virulence in Fusarium oxysporum. Mol Plant Microbe Interact. 2015;28(1):55–68. doi: 10.1094/MPMI-07-14-0205-R
  • Yang JY, Fang YL, Wang P, et al. Pleiotropic roles of ChSat4 in asexual development, cell wall integrity maintenance, and pathogenicity in Colletotrichum higginsianum. Front Microbiol. 2018;9:2311. doi: 10.3389/fmicb.2018.02311
  • Lebiedzinska M, Szabadkai G, Jones AW, et al. Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other subcellular organelles. Int J Biochem Cell Biol. 2009;41:1805–1816. doi: 10.1016/j.biocel.2009.02.017
  • Christianson JC, Ye Y. Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat Struct Mol Biol. 2014;21(4):325–335. doi: 10.1038/nsmb.2793
  • Christianson JC, Carvalho P. Order through destruction: how ER-associated protein degradation contributes to organelle homeostasis. EMBO J. 2022;41(6):e109845. doi: 10.15252/embj.2021109845
  • Galluzzi L, Kepp O, Trojel-Hansen C, et al. Mitochondrial control of cellular life, stress, and death. Circ Res. 2012;111(9):1198–1207. doi: 10.1161/CIRCRESAHA.112.268946
  • Nakatogawa H. Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol. 2020;21(8):439–458. doi: 10.1038/s41580-020-0241-0
  • Hu Y, Wang J, Ying S, et al. Five vacuolar Ca2+ exchangers play different roles in calcineurin-dependent Ca2+/Mn2+ tolerance, multistress responses and virulence of a filamentous entomopathogen. Fungal Genet Biol. 2014;73:12–19. doi: 10.1016/j.fgb.2014.09.005
  • Liu Q, Li D, Jiang K, et al. AoPEX1 and AoPEX6 are required for mycelial growth, conidiation, stress response, fatty acid utilization, and trap formation in arthrobotrys oligospora. Microbiol Spectr. 2022;10(2):e27522. doi: 10.1128/spectrum.00275-22
  • Ding JL, Li XH, Lei JH, et al. Succinate dehydrogenase subunit C contributes to mycelial growth and development, stress response, and virulence in the insect parasitic fungus beauveria bassiana. Microbiol Spectr. 2022;10(5):e289122. doi: 10.1128/spectrum.02891-22
  • Larsen JB, Jensen MB, Bhatia VK, et al. Membrane curvature enables N-Ras lipid anchor sorting to liquid-ordered membrane phases. Nat Chem Biol. 2015;11(3):192–194. doi: 10.1038/nchembio.1733
  • Martin SW, Douglas LM, Konopka JB. Cell cycle dynamics and quorum sensing in Candida albicans chlamydospores are distinct from budding and hyphal growth. Eukaryot Cell. 2005;4(7):1191–1202. doi: 10.1128/EC.4.7.1191-1202.2005
  • Pedersen R, Drubin DG. Type I myosins anchor actin assembly to the plasma membrane during clathrin-mediated endocytosis. J Cell Bio. 2019;218(4):1138–1147. doi: 10.1083/jcb.201810005
  • Peng YJ, Hou J, Zhang H, et al. Systematic contributions of CFEM domain-containing proteins to iron acquisition are essential for interspecies interaction of the filamentous pathogenic fungus beauveria bassiana. Environ Microbiol. 2022;24(8):3693–3704. doi: 10.1111/1462-2920.16032