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Mycology
An International Journal on Fungal Biology
Volume 12, 2021 - Issue 1: model fungi
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Research Article

Current views on endocytosis in filamentous fungi

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Pages 1-9 | Received 17 Jan 2020, Accepted 05 Mar 2020, Published online: 24 Mar 2020

References

  • Abe K, Gomi K, Hasegawa F, Machida M. Impact of Aspergillus oryzae genomics on industrial production of metabolites. Mycopathologia. 2006;162(3):143–153. doi:10.1007/s11046-006-0049-2.
  • Araujo-Bazan L, Peñalva MA, Espeso EA. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol Microbiol. 2008;67(4):891–905. doi:10.1111/mmi.2008.67.issue-4.
  • Atkinson HA, Daniels A, Read ND. Live-cell imaging of endocytosis during conidial germination in the rice blast fungus Magnaporthe grisea. Fungal Genet Biol. 2002;37(3):233–244. doi:10.1016/S1087-1845(02)00535-2.
  • Baker SE. Aspergillus niger genomics: past, present and into the future. Medical Mycology. 2006;44:S17–S21. doi:10.1080/13693780600921037.
  • Bartnicki-Garcia S, Bartnicki DD, Gierz G, Lopez-Franco R, Bracker CE. Evidence that Spitzenkörper behavior determines the shape of a fungal hypha: a test of the hyphoid model. Exp Mycol. 1995;19(2):153–159. doi:10.1006/emyc.1995.1017.
  • Bartnicki-Garcia S, Garduno-Rosales M, Delgado-Alvarez DL, Mourino-Perez RR. Experimental measurement of endocytosis in fungal hyphae. Fungal Genet Biol. 2018;118:32–36. doi:10.1016/j.fgb.2018.07.001.
  • Bartnicki-Garcia S, Hergert F, Gierz G. Computer simulation of fungal morphogenesis and the mathematical basis for hyphal (tip) growth. Protoplasma. 1989;153:46–57. doi:10.1007/BF01322464.
  • Cairns TC, Nai C, Meyer V. How a fungus shapes biotechnology: 100 years of Aspergillus niger research. Fungal Biol Biotechnol. 2018;5(13):14. doi:10.1186/s40694-018-0054-5.
  • Cairns TC, Zheng X, Zheng P, Sun J, Meyer V. Moulding the mould: understanding and reprogramming filamentous fungal growth and morphogenesis for next generation cell factories. Biotechnol Biofuels. 2019;12:77. doi:10.1186/s13068-019-1400-4.
  • Costa R, Warren DT, Ayscough KR. Lsb5p interacts with actin regulators Sla1p and Las17p, ubiquitin and Arf3p to couple actin dynamics to membrane trafficking processes. Biochem J. 2005;387:649–658. doi:10.1042/BJ20041729.
  • De Souza CP, Hashmi SB, Osmani AH, Andrews P, Ringelberg CS, Dunlap JC, Osmani SA. Functional analysis of the Aspergillus nidulans kinome. PLoS One. 2013;8(3):e58008–e58008. doi:10.1371/journal.pone.0058008.
  • Delgado-Alvarez DL, Callejas-Negrete OA, Gomez N, Freitag M, Roberson RW, Smith LG, Mourino-Perez RR. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet Biol. 2010;47(7):573–586. doi:10.1016/j.fgb.2010.03.004.
  • Fischer-Parton S, Parton RM, Hickey PC, Dijksterhuis J, Atkinson HA, Read ND. Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J Microsc. 2000;198(3):246–259. doi:10.1046/j.1365-2818.2000.00708.x.
  • Fuchs U, Hause G, Schuchardt I, Steinberg G. Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell. 2006;18(8):2066–2081. doi:10.1105/tpc.105.039388.
  • Gachet Y, Hyams JS. Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis. J Cell Sci. 2005;118(18):4231–4242. doi:10.1242/jcs.02530.
  • Gierz G, Bartnicki-Garcia S. A three-dimensional model of fungal morphogenesis based on the vesicle supply center concept. J Theor Biol. 2001;208(2):151–164. doi:10.1006/jtbi.2000.2209.
  • Goode BL, Eskin JA, Wendland B. Actin and endocytosis in budding yeast. Genetics. 2015;199(2):315–358. doi:10.1534/genetics.112.145540.
  • Harris SD. Cell polarity in filamentous fungi: shaping the mold. Int Rev Cytol Elsevier Inc. 2006;251:41–77.
  • Harris SD. Hyphal morphogenesis: an evolutionary perspective. Fungal Biol. 2011;115(6):475–484. doi:10.1016/j.funbio.2011.02.002.
  • Harris SD, Turner G, Meyer V, Espeso EA, Specht T, Takeshita N, Helmstedt K. Morphology and development in Aspergillus nidulans: A complex puzzle. Fungal Genet Biol. 2009;46(1):S82–S92. doi:10.1016/j.fgb.2008.07.023.
  • Hernandez-Gonzalez M, Bravo-Plaza I, Pinar M, de Los Rios V, Arst HN Jr., Peñalva MA. Endocytic recycling via the TGN underlies the polarized hyphal mode of life. PLoS Genet. 2018;14(4):e1007291. doi:10.1371/journal.pgen.1007291.
  • Hoffmann J, Mendgen K. Endocytosis and membrane turnover in the germ tube of Uromyces fabae. Fungal Genet Biol. 1998;24(1–2):77–85. doi:10.1006/fgbi.1998.1059.
  • Howard JP, Hutton JL, Olson JM, Payne GS. Sla1p serves as the targeting signal recognition factor for NPFX(1,2)D-mediated endocytosis. J Cell Biol. 2002;157(2):315–326. doi:10.1083/jcb.200110027.
  • Jorgensen TR, Goosen T, Hondel CA, Ram AF, Iversen JJ. Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway. BMC Genomics. 2009;10:44. doi:10.1186/1471-2164-10-44.
  • Jorgensen TR, Nitsche BM, Lamers GE, Arentshorst M, van den Hondel CA, Ram AF. Transcriptomic insights into the physiology of Aspergillus niger approaching a specific growth rate of zero. Appl Environ Microbiol. 2010;76(16):5344–5355. doi:10.1128/AEM.00450-10.
  • Kiss E, Hegedüs B, Virágh M, Varga T, Merényi Z, Kószó T, Bálint B, Prasanna AN, Krizsán K, Kocsubé S, et al. Comparative genomics reveals the origin of fungal hyphae and multicellularity. Nat Commun. 2019;10(1):4080. doi:10.1038/s41467-019-12085-w.
  • Köhler JR, Casadevall A, Perfect J. The spectrum of fungi that infects humans. Cold Spring Harb Perspect Med. 2014;5(1):a019273. doi:10.1101/cshperspect.a019273.
  • Konzack S, Rischitor PE, Enke C, Fischer R. The role of the kinesin motor KipA in microtubule organization and polarized growth of Aspergillus nidulans. Mol Biol Cell. 2005;16(2):497–506. doi:10.1091/mbc.e04-02-0083.
  • Li L, Chen X, Zhang S, Yang J, Chen D, Liu M, Zhang H, Zheng X, Wang P, Peng Y, et al. MoCAP proteins regulated by MoArk1-mediated phosphorylation coordinate endocytosis and actin dynamics to govern development and virulence of Magnaporthe oryzae. PLoS Genet. 2017a;13(5):e1006814. doi:10.1371/journal.pgen.1006814.
  • Li L, Zhang S, Liu X, Yu R, Li X, Liu M, Zhang H, Zheng X, Wang P, Zhang Z. Magnaporthe oryzae Abp1, a MoArk1 kinase-interacting actin binding protein, links actin cytoskeleton regulation to growth, endocytosis, and pathogenesis. Molecular Plant-Microbe Interactions. 2019;32(4):437–451. doi:10.1094/MPMI-10-18-0281-R.
  • Li X, Gao C, Li L, Liu M, Yin Z, Zhang H, Zheng X, Wang P, Zhang Z. MoEnd3 regulates appressorium formation and virulence through mediating endocytosis in rice blast fungus Magnaporthe oryzae. PLoS Pathog. 2017b;13(6):e1006449. doi:10.1371/journal.ppat.1006449.
  • Li Y, Li B, Liu L, Chen H, Zhang H, Zheng X, Zhang Z. FgMon1, a guanine nucleotide exchange factor of FgRab7, is important for vacuole fusion, autophagy and plant infection in Fusarium graminearum. Sci Rep. 2015;5:18101. doi:10.1038/srep18101.
  • Liu K, Hua Z, Nepute JA, Graham TR. Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol Biol Cell. 2007;18(2):487–500. doi:10.1091/mbc.e06-07-0592.
  • Lu R, Drubin DG, Sun Y. Clathrin-mediated endocytosis in budding yeast at a glance. J Cell Sci. 2016;129(8):1531–1536. doi:10.1242/jcs.182303.
  • Meyer V, Arentshorst M, Flitter SJ, Nitsche BM, Kwon MJ, Reynaga-Pena CG, Bartnicki-Garcia S, van den Hondel CA, Ram AF. Reconstruction of signaling networks regulating fungal morphogenesis by transcriptomics. Eukaryot Cell. 2009;8(11):1677–1691. doi:10.1128/EC.00050-09.
  • Muñoz JF, McEwen JG, Clay OK, Cuomo CA. Genome analysis reveals evolutionary mechanisms of adaptation in systemic dimorphic fungi. Sci Rep. 2018;8(1):4473. doi:10.1038/s41598-018-22816-6.
  • Newpher TM, Smith RP, Lemmon V, Lemmon SK. In vivo dynamics of clathrin and Its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast. Dev Cell. 2005;9(1):87–98. doi:10.1016/j.devcel.2005.04.014.
  • Peñalva MA. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal Genet Biol. 2005;42(12):963–975. doi:10.1016/j.fgb.2005.09.004.
  • Peñalva MA. Endocytosis in filamentous fungi: cinderella gets her reward. Curr Opin Microbiol. 2010;13(6):684–692. doi:10.1016/j.mib.2010.09.005.
  • Piao HL, Machado IMP, Payne GS. NPFXD-mediated endocytosis is required for polarity and function of a yeast cell wall stress sensor. Mol Biol Cell. 2007;18(1):57–65. doi:10.1091/mbc.e06-08-0721.
  • Ramsubramaniam N, Harris SD, Marten MR. The phosphoproteome of Aspergillus nidulans reveals functional association with cellular processes involved in morphology and secretion. Proteomics. 2014;14(21–22):2454–2459. doi:10.1002/pmic.v14.21-22.
  • Reynaga-Peña CG, Gierz G, Bartnicki-Garcia S. Analysis of the role of the Spitzenkörper in fungal morphogenesis by computer simulation of apical branching in Aspergillus niger. Proc Natl Acad Sci USA. 1997;94(17):9096–9101. doi:10.1073/pnas.94.17.9096.
  • Riquelme M, Aguirre J, Bartnicki-Garcia S, Braus GH, Feldbrugge M, Fleig U, Hansberg W, Herrera-Estrella A, Kamper J, Kuck U, et al. Fungal morphogenesis, from the polarized growth of hyphae to complex reproduction and infection structures. Microbiol Mol Biol Rev. 2018;82:2.
  • Schultzhaus Z, Johnson TB, Shaw BD. Clathrin localization and dynamics in Aspergillus nidulans. Mol Microbiol. 2017;103(2):299–318. doi:10.1111/mmi.2017.103.issue-2.
  • Schultzhaus Z, Quintanilla L, Hilton A, Shaw BD. Live cell imaging of actin dynamics in the filamentous fungus Aspergillus nidulans. Microsc Microanal. 2016;22(2):264–274. doi:10.1017/S1431927616000131.
  • Schultzhaus Z, Yan H, Shaw BD. Aspergillus nidulans flippase DnfA is cargo of the endocytic collar and plays complementary roles in growth and phosphatidylserine asymmetry with another flippase, DnfB. Mol Microbiol. 2015;97(1):18–32. doi:10.1111/mmi.13019.
  • Shaw BD, Chung DW, Wang CL, Quintanilla LA, Upadhyay S. A role for endocytic recycling in hyphal growth. Fungal Biol. 2011;115(6):541–546. doi:10.1016/j.funbio.2011.02.010.
  • Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS, Kissinger JC, Li W, Nayak V, Pinney DF, et al. FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res. 2012;40(Database issue):D675–D681. doi:10.1093/nar/gkr918.
  • Steinberg G. Endocytosis and early endosome motility in filamentous fungi. Curr Opin Microbiol. 2014;20:10–18. doi:10.1016/j.mib.2014.04.001.
  • Steinberg G, Peñalva MA, Riquelme M, Wosten HA, Harris SD. Cell biology of hyphal growth. Microbiol Spectr. 2017;5(2):34.
  • Sudbery P. Fluorescent proteins illuminate the structure and function of the hyphal tip apparatus. Fungal Genet Biol. 2011;48(9):849–857. doi:10.1016/j.fgb.2011.02.004.
  • Taheri-Talesh N, Horio T, Araujo-Bazan L, Dou X, Espeso EA, Peñalva MA, Osmani SA, Oakley BR. The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell. 2008;19(4):1439–1449. doi:10.1091/mbc.e07-05-0464.
  • Takeshita N. Coordinated process of polarized growth in filamentous fungi. Biosci Biotechnol Biochem. 2016;80(9):1693–1699. doi:10.1080/09168451.2016.1179092.
  • Takeshita N, Mania D, Herrero S, Ishitsuka Y, Nienhaus GU, Podolski M, Howard J, Fischer R. The cell-end marker TeaA and the microtubule polymerase AlpA contribute to microtubule guidance at the hyphal tip cortex of Aspergillus nidulans to provide polarity maintenance. J Cell Sci. 2013;126:5400–5411. doi:10.1242/jcs.129841.
  • Tan PK, Howard JP, Payne GS. The sequence NPFXD defines a new class of endocytosis signal in Saccharomyces cerevisiae. J Cell Biol. 1996;135(6):1789–1800. doi:10.1083/jcb.135.6.1789.
  • Thilo L. Quantification of endocytosis-derived membrane traffic. BBA-Biomembranes. 1985;822(2):243–266. doi:10.1016/0304-4157(85)90010-3.
  • Upadhyay S, Shaw BD. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol Microbiol. 2008;68(3):690–705. doi:10.1111/j.1365-2958.2008.06178.x.
  • Veiter L, Rajamanickam V, Herwig C. The filamentous fungal pellet-relationship between morphology and productivity. Appl Microbiol Biotechnol. 2018;102(7):2997–3006. doi:10.1007/s00253-018-8818-7.
  • Verdín J, Sánchez-León E, Rico-Ramírez AM, Martínez-Núñez L, Fajardo-Somera RA, Riquelme M. Off the wall: the rhyme and reason of Neurospora crassa hyphal morphogenesis. Cell Surf. 2019;5(1):100020. doi:10.1016/j.tcsw.2019.100020.
  • Vida TA, Emr SD. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol. 1995;128(5):779–792. doi:10.1083/jcb.128.5.779.
  • Virag A, Harris SD. The Spitzenkörper: a molecular perspective. Mycol Res. 2006;110:4–13. doi:10.1016/j.mycres.2005.09.005.
  • Yang CD, Dang X, Zheng HW, Chen XF, Lin XL, Zhang DM, Abubakar YS, Chen X, Lu G, Wang Z, et al. Two Rab5 homologs are essential for the development and pathogenicity of the rice blast fungus Magnaporthe oryzae. Front Plant Sci. 2017;8:620. doi:10.3389/fpls.2017.00620.
  • Zeilinger S, Gupta VK, Dahms TES, Silva RN, Singh HB, Upadhyay RS, Gomes EV, Tsui CK-M, Nayak SC. Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev. 2016;40(2):182–207. doi:10.1093/femsre/fuv045.
  • Zheng W, Lin Y, Fang W, Zhao X, Lou Y, Wang G, Zheng H, Liang Q, Abubakar YS, Olsson S, et al. The endosomal recycling of FgSnc1 by FgSnx41-FgSnx4 heterodimer is essential for polarized growth and pathogenicity in Fusarium graminearum. New Phytologist. 2018;219(2):654–671. doi:10.1111/nph.2018.219.issue-2.