The Fungal Cell Wall pp 113-129 | Cite as
Control of Actin and Calcium for Chitin Synthase Delivery to the Hyphal Tip of Aspergillus
- 1 Mentions
- 261 Downloads
Abstract
Filamentous fungi are covered by a cell wall consisting mainly of chitin and glucan. The synthesis of chitin, a β-1,4-linked homopolymer of N-acetylglucosamine, is essential for hyphal morphogenesis. Fungal chitin synthases are integral membrane proteins that have been classified into seven classes. ChsB, a class III chitin synthase, is known to play a key role in hyphal tip growth and has been used here as a model to understand the cell biology of cell wall biosynthesis in Aspergillus nidulans. Chitin synthases are transported on secretory vesicles to the plasma membrane for new cell wall synthesis. Super-resolution localization imaging as a powerful biophysical approach indicated dynamics of the Spitzenkörper where spatiotemporally regulated exocytosis and cell extension, whereas high-speed pulse-chase imaging has revealed ChsB transport mechanism mediated by kinesin-1 and myosin-5. In addition, live imaging analysis showed correlations among intracellular Ca2+ levels, actin assembly, and exocytosis in growing hyphal tips. This suggests that pulsed Ca2+ influxes coordinate the temporal control of actin assembly and exocytosis, which results in stepwise cell extension. It is getting clear that turgor pressure and cell wall pressure are involved in the activation of Ca2+ channels for Ca2+ oscillation and cell extension. Here the cell wall synthesis and tip growth meet again.
References
- Abenza JF, Galindo A, Pantazopoulou A, Gil C, de los Rios V, Penalva MA (2010) Aspergillus RabB Rab5 integrates acquisition of degradative identity with the long distance movement of early endosomes. Mol Biol Cell 21:2756–69Google Scholar
- Abenza JF, Pantazopoulou A, Rodriguez JM, Galindo A, Penalva MA (2009) Long-distance movement of Aspergillus nidulans early endosomes on microtubule tracks. Traffic 10:57–75PubMedGoogle Scholar
- Araujo-Bazan L, Penalva MA, Espeso EA (2008) Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol Microbiol 67:891–905PubMedGoogle Scholar
- Berepiki A, Lichius A, Read ND (2011) Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9:876–887PubMedGoogle Scholar
- Bergs A, Ishitsuka Y, Evangelinos M, Nienhaus GU, Takeshita N (2016) Dynamics of actin cables in polarized growth of the filamentous fungus Aspergillus nidulans. Front Microbiol 7:682PubMedPubMedCentralGoogle Scholar
- Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S et al (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–1645PubMedGoogle Scholar
- Blumenthal HJ, Roseman S (1957) Quantitative estimation of chitin in fungi. J Bacteriol 74:222–224PubMedPubMedCentralGoogle Scholar
- Borgia PT, Iartchouk N, Riggle PJ, Winter KR, Koltin Y, Bulawa CE (1996) The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet Biol 20:193–203PubMedGoogle Scholar
- Brand A, Shanks S, Duncan VM, Yang M, Mackenzie K, Gow NA (2007) Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 17:347–352PubMedPubMedCentralGoogle Scholar
- Brand AC, Morrison E, Milne S, Gonia S, Gale CA, Gow NA (2014) Cdc42 GTPase dynamics control directional growth responses. Proc Natl Acad Sci USA 111:811–816PubMedGoogle Scholar
- de Groot PW, Brandt BW, Horiuchi H, Ram AF, de Koster CG, Klis FM (2009) Comprehensive genomic analysis of cell wall genes in Aspergillus nidulans. Fungal Genet Biol 46:S72–S81PubMedGoogle Scholar
- Egan MJ, Tan K, Reck-Peterson SL (2012) Lis1 is an initiation factor for dynein-driven organelle transport. J Cell Biol 197:971–982PubMedPubMedCentralGoogle Scholar
- Fischer R, Zekert N, Takeshita N (2008) Polarized growth in fungi—interplay between the cytoskeleton, positional markers and membrane domains. Mol Microbiol 68:813–826PubMedGoogle Scholar
- Fleissner A, Leeder AC, Roca MG, Read ND, Glass NL (2009) Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci USA 106:19387–19392PubMedGoogle Scholar
- Fukuda K, Yamada K, Deoka K, Yamashita S, Ohta A, Horiuchi H (2009) Class III chitin synthase ChsB of Aspergillus nidulans localizes at the sites of polarized cell wall synthesis and is required for conidial development. Eukaryot Cell 8:945–956PubMedPubMedCentralGoogle Scholar
- Fujiwara M, Horiuchi H, Ohta A, Takagi M (1997) A novel fungal gene encoding chitin synthase with a myosin motor-like domain. Biochem Biophys Res Commun 236:75–78PubMedGoogle Scholar
- Fujiwara M, Ichinomiya M, Motoyama T, Horiuchi H, Ohta A, Takagi M (2000) Evidence that the Aspergillus nidulans class I and class II chitin synthase genes, chsC and chsA, share critical roles in hyphal wall integrity and conidiophore development. J Biochem 127:359–366PubMedGoogle Scholar
- Gibeaux R, Hoepfner D, Schlatter I, Antony C, Philippsen P (2013) Organization of organelles within hyphae of Ashbya gossypii revealed by electron tomography. Eukaryot Cell 12:1423–1432PubMedPubMedCentralGoogle Scholar
- Goldbeter A (2002) Computational approaches to cellular rhythms. Nature 420:238–245PubMedGoogle Scholar
- Gonçalves I, Brouillet S, Soulie MC, Gribaldo S, Sirven C, Charron N, Boccara M, Choquer M (2016) Genome-wide analyses of chitin synthases identify horizontal gene transfers towards bacteria and allow a robust and unifying classification into fungi. BMC Evol Biol 16:252PubMedPubMedCentralGoogle Scholar
- Goryachev AB, Lichius A, Wright GD, Read ND (2012) Excitable behavior can explain the “ping-pong” mode of communication between cells using the same chemoattractant. BioEssays 34:259–266PubMedGoogle Scholar
- Hammond JW, Cai D, Blasius TL, Li Z, Jiang Y et al (2009) Mammalian Kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol 7:e72PubMedGoogle Scholar
- Harris SD (2009) The Spitzenkörper: a signalling hub for the control of fungal development? Mol Microbiol 73:733–736PubMedGoogle Scholar
- Herzog S, Schumann MR, Fleissner A (2015) Cell fusion in Neurospora crassa. Curr Opin Microbiol 28:53–59PubMedGoogle Scholar
- Hess ST, Girirajan TP, Mason MD (2006) Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91:4258–4272PubMedPubMedCentralGoogle Scholar
- Higashitsuji Y, Herrero S, Takeshita N, Fischer R (2009) The cell end marker protein TeaC is involved in growth directionality and septation in Aspergillus nidulans. Eukaryot Cell 8:957–967PubMedPubMedCentralGoogle Scholar
- Horio T, Oakley BR (2005) The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Mol Biol Cell 16:918–926PubMedPubMedCentralGoogle Scholar
- Horiuchi H (2009) Functional diversity of chitin synthases of Aspergillus nidulans in hyphal growth, conidiophore development and septum formation. Med Mycol 47(Suppl 1):S47–S52PubMedGoogle Scholar
- Ichinomiya M, Yamada E, Yamashita S, Ohta A, Horiuchi H (2005) Class I and class II chitin synthases are involved in septum formation in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 4:1125–1136PubMedPubMedCentralGoogle Scholar
- Iida H, Nakamura H, Ono T, Okumura MS, Anraku Y (1994) MID1, a novel Saccharomyces cerevisiae gene encoding a plasma membrane protein, is required for Ca2+ influx and mating. Mol Cell Biol 14:8259–8271PubMedPubMedCentralGoogle Scholar
- Ishitsuka Y, Savage N, Li Y, Bergs A, Grun N, Kohler D, Donnelly R, Nienhaus GU, Fischer R, Takeshita N (2015) Superresolution microscopy reveals a dynamic picture of cell polarity maintenance during directional growth. Sci Adv 1:e1500947PubMedPubMedCentralGoogle Scholar
- Janmey PA (1994) Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu Rev Physiol 56:169–191PubMedGoogle Scholar
- Johnston IR (1965) The composition of the cell wall of Aspergillus niger. Biochem J 96:651–658PubMedPubMedCentralGoogle Scholar
- Kanzaki M, Nagasawa M, Kojima I, Sato C, Naruse K et al (1999) Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285:882–886PubMedGoogle Scholar
- Kholodenko BN (2006) Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 7:165–176PubMedPubMedCentralGoogle Scholar
- Kim HS, Czymmek KJ, Patel A, Modla S, Nohe A et al (2012) Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca(2+) signatures associated with polarized growth, development, and pathogenesis. Fungal Geneti Biol 49:589–601Google Scholar
- Kobayashi T, Abe K, Asai K, Gomi K, Juvvadi PR et al (2007) Genomics of Aspergillus oryzae. Biosci Biotechnol Biochem 71:646–670PubMedGoogle Scholar
- Latgé JP, Beauvais A, Chamilos G (2017) The cell wall of the human fungal pathogen Aspergillus fumigatus: biosynthesis, organization, immune response, and virulence. Annu Rev Microbiol 71:99–116PubMedGoogle Scholar
- Lenardon MD, Munro CA, Gow NAR (2010a) Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 13:416–423PubMedPubMedCentralGoogle Scholar
- Lenardon MD, Milne SA, Mora-Montes HM, Kaffarnik FA, Peck SC, Brown AJ, Munro CA, Gow NA (2010b) Phosphorylation regulates polarisation of chitin synthesis in Candida albicans. J Cell Sci 123:2199–2206PubMedPubMedCentralGoogle Scholar
- Lenz JH, Schuchardt I, Straube A, Steinberg G (2006) A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J 25:2275–2286PubMedPubMedCentralGoogle Scholar
- Lin C, Schuster M, Guimaraes SC, Ashwin P, Schrader M et al (2016) Active diffusion and microtubule-based transport oppose myosin forces to position organelles in cells. Nat Commun 7:11814PubMedPubMedCentralGoogle Scholar
- Locke EG, Bonilla M, Liang L, Takita Y, Cunningham KW (2000) A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol Cell Biol 20:6686–6694PubMedPubMedCentralGoogle Scholar
- Lopez-Franco R, Bartnicki-Garcia S, Bracker CE (1994) Pulsed growth of fungal hyphal tips. Proc Natl Acad Sci USA 91:12228–12232PubMedGoogle Scholar
- Motoyama T, Kojima N, Horiuchi H, Ohta A, Takagi M (1994) Isolation of a chitin synthase gene (chsC) of Aspergillus nidulans. Biosci Biotechnol Biochem 58:2254–2257PubMedGoogle Scholar
- Muszkieta L, Aimanianda V, Mellado E, Gribaldo S, Alcàzar-Fuoli L, Szewczyk E, Prevost MC, Latgé JP (2014) Deciphering the role of the chitin synthase families 1 and 2 in the in vivo and in vitro growth of Aspergillus fumigatus by multiple gene targeting deletion. Cell Microbiol 16:1784–1805PubMedGoogle Scholar
- Nienhaus GU, Nienhaus K, Holzle A, Ivanchenko S, Renzi F et al (2006) Photoconvertible fluorescent protein EosFP: biophysical properties and cell biology applications. Photochem Photobiol 82:351–358PubMedGoogle Scholar
- Nienhaus K, Nienhaus GU, Wiedenmann J, Nar H (2005) Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP. Proc Natl Acad Sci USA 102:9156–9159PubMedGoogle Scholar
- Paidhungat M, Garrett S (1997) A homolog of mammalian, voltage-gated calcium channels mediates yeast pheromone-stimulated Ca2+ uptake and exacerbates the cdc1(Ts) growth defect. Mol Cell Biol 17:6339–6347PubMedPubMedCentralGoogle Scholar
- Pantazopoulou A, Pinar M, Xiang X, Penalva MA (2014) Maturation of late Golgi cisternae into RabE(RAB11) exocytic post-Golgi carriers visualized in vivo. Mol Biol Cell 25:2428–2443PubMedPubMedCentralGoogle Scholar
- Penalva MA, Zhang J, Xiang X, Pantazopoulou A (2017) Transport of fungal RAB11 secretory vesicles involves myosin-5, dynein/dynactin/p25 and kinesin-1 and is independent of kinesin-3. Mol Biol Cell 28:947–961PubMedPubMedCentralGoogle Scholar
- Perez-Nadales E, Nogueira MF, Baldin C, Castanheira S, El Ghalid M et al (2014) Fungal model systems and the elucidation of pathogenicity determinants. Fungal Genet Biol 70:42–67PubMedPubMedCentralGoogle Scholar
- Pinar M, Arst HN, Jr., Pantazopoulou A, Tagua VG, de los Rios V et al (2015) TRAPPII regulates exocytic Golgi exit by mediating nucleotide exchange on the Ypt31 ortholog RabERAB11. Proc Natl Acad Sci USA 112:4346–51Google Scholar
- Punt PJ, van Biezen N, Conesa A, Albers A, Mangnus J, van den Hondel C (2002) Filamentous fungi as cell factories for heterologous protein production. Trends Biotechnol 20:200–206PubMedGoogle Scholar
- Riquelme M, Aguirre J, Bartnicki-García S, Braus GH, Feldbrügge M, Fleig U, Hansberg W, Herrera-Estrella A, Kämper J, Kück U, Mouriño-Pérez RR, Takeshita N, Fischer R (2018) Fungal morphogenesis, from the polarized growth of hyphae to complex reproduction and infection structures. Microbiol Mol Biol Rev 82:e00068–17PubMedPubMedCentralGoogle Scholar
- Renshaw H, Vargas-Muñiz JM, Richards AD, Asfaw YG, Juvvadi PR, Steinbach WJ (2016) Distinct roles of myosins in Aspergillus fumigatus hyphal growth and pathogenesis. Infect Immun 84:1556–1564PubMedPubMedCentralGoogle Scholar
- Requena N, Alberti-Segui C, Winzenburg E, Horn C, Schliwa M et al (2001) Genetic evidence for a microtubule-destabilizing effect of conventional kinesin and analysis of its consequences for the control of nuclear distribution in Aspergillus nidulans. Mol Microbiol 42:121–132PubMedGoogle Scholar
- Riquelme M, Bredeweg EL, Callejas-Negrete O, Roberson RW, Ludwig S et al (2014) The Neurospora crassa exocyst complex tethers Spitzenkörper vesicles to the apical plasma membrane during polarized growth. Mol Biol Cell 25:1312–1326PubMedPubMedCentralGoogle Scholar
- Riquelme M, Reynaga-Pena CG, Gierz G, Bartnicki-Garcia S (1998) What determines growth direction in fungal hyphae? Fungal gGenet Biol 24:101–109Google Scholar
- Riquelme M, Sanchez-Leon E (2014) The Spitzenkörper: a choreographer of fungal growth and morphogenesis. Curr Opin Microbiol 20:27–33PubMedGoogle Scholar
- Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B, Castro-Longoria E et al (2011) Architecture and development of the Neurospora crassa hypha—a model cell for polarized growth. Fungal Biol 115:446–474PubMedGoogle Scholar
- Rittenour WR, Si H, Harris SD (2009) Hyphal morphogenesis in Aspergillus nidulans. Fungal Biol Rev 23:20–29Google Scholar
- Rogg LE, Fortwendel JR, Juvvadi PR, Steinbach WJ (2012) Regulation of expression, activity and localization of fungal chitin synthases. Med Mycol 50:2–17PubMedGoogle Scholar
- Sacristan C, Reyes A, Roncero C (2012) Neck compartmentalization as the molecular basis for the different endocytic behaviour of Chs3 during budding or hyperpolarized growth in yeast cells. Mol Microbiol 83:1124–1135PubMedGoogle Scholar
- Sahl SJ, Moerner WE (2013) Super-resolution fluorescence imaging with single molecules. Curr Opin Struct Biol 23:778–787PubMedPubMedCentralGoogle Scholar
- Schneggenburger R, Neher E (2005) Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15:266–274PubMedGoogle Scholar
- Schuster M, Kilaru S, Fink G, Collemare J, Roger Y, Steinberg G (2011) Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array. Mol Biol Cell 22:3645–3657PubMedPubMedCentralGoogle Scholar
- Schuster M, Martin-Urdiroz M, Higuchi Y, Hacker C, Kilaru S, Gurr SJ, Steinberg G (2016) Co-delivery of cell-wall-forming enzymes in the same vesicle for coordinated fungal cell wall formation. Nat Microbiol 1:16149PubMedGoogle Scholar
- Seiler S, Nargang FE, Steinberg G, Schliwa M (1997) Kinesin is essential for cell morphogenesis and polarized secretion in Neurospora crassa. EMBO J 16:3025–3034PubMedPubMedCentralGoogle Scholar
- Serrano A, Hammadeh HH, Herzog S, Illgen J, Schumann MR et al (2017) The dynamics of signal complex formation mediating germling fusion in Neurospora crassa. Fungal Genet Biol 101:31–33PubMedGoogle Scholar
- Smedler E, Uhlen P (2014) Frequency decoding of calcium oscillations. Biochim Biophys Acta 1840:964–969PubMedGoogle Scholar
- Steinberg G (2011) Motors in fungal morphogenesis: cooperation versus competition. Current Opin Microbiol 14:660–667Google Scholar
- Sudvery PE (2008) Regulation of polarized growth in fungi. Fungal Biol Rev 22:44–55Google Scholar
- Taheri-Talesh N, Horio T, Araujo-Bazan L, Dou X, Espeso EA et al (2008) The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 19:1439–1449PubMedPubMedCentralGoogle Scholar
- Taheri-Talesh N, Xiong Y, Oakley BR (2012) the Functions of myosin II and myosin V homologs in tip growth and septation in Aspergillus nidulans. PLoS ONE 7:e31218PubMedPubMedCentralGoogle Scholar
- Takeshita N (2016) Coordinated process of polarized growth in filamentous fungi. Biosci Biotech Biochem 80:1693–1699Google Scholar
- Takeshita N (2018) Oscillatory fungal cell growth. Fungal Genet Biol 110:10–14PubMedGoogle Scholar
- Takeshita N, Evangelinos M, Zhou L, Serizawa T, Somera-Fajardo RA et al (2017) Pulses of Ca2+ coordinate actin assembly and exocytosis for stepwise cell extension. Proc Natl Acad Sci USA 114:5701–5706PubMedGoogle Scholar
- Takeshita N, Higashitsuji Y, Konzack S, Fischer R (2008) Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 19:339–351PubMedPubMedCentralGoogle Scholar
- Takeshita N, Manck R, Grun N, de Vega SH, Fischer R (2014) Interdependence of the actin and the microtubule cytoskeleton during fungal growth. Curr Opin Microbiol 20:34–41PubMedGoogle Scholar
- Takeshita N, Ohta A, Horiuchi H (2005) CsmA, a class V chitin synthase with a myosin motor-like domain, is localized through direct interaction with the actin cytoskeleton in Aspergillus nidulans. Mol Biol Cell 16:1961–1970PubMedPubMedCentralGoogle Scholar
- Takeshita N, Yamashita S, Ohta A, Horiuchi H (2006) Aspergillus nidulans class V and VI chitin synthases CsmA and CsmB, each with a myosin motor-like domain, perform compensatory functions that are essential for hyphal tip growth. Mol Microbiol 59:1380–1394PubMedGoogle Scholar
- Takeshita N, Wernet V, Tsuizaki M, Grun N, Hoshi HO et al (2015) Transportation of Aspergillus nidulans class III and V chitin synthases to the hyphal tips depends on conventional kinesin. PLoS ONE 10:e0125937PubMedPubMedCentralGoogle Scholar
- Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS, Vale RD (2014) A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159:635–646PubMedPubMedCentralGoogle Scholar
- Wang S, Cao J, Liu X, Hu H, Shi J et al (2012) Putative calcium channels CchA and MidA play the important roles in conidiation, hyphal polarity and cell wall components in Aspergillus nidulans. PLoS ONE 7:e46564PubMedPubMedCentralGoogle Scholar
- Wiedenmann J, Gayda S, Adam V, Oswald F, Nienhaus K et al (2011) From EosFP to mIrisFP: structure-based development of advanced photoactivatable marker proteins of the GFP-family. J Biophotn 4:377–390Google Scholar
- Yanai K, Kojima N, Takaya N, Horiuchi H, Ohta A, Takagi M (1994) Isolation and characterization of two chitin synthase genes from Aspergillus nidulans. Biosci Biotechnol Biochem 58:1828–1835PubMedGoogle Scholar
- Zelter A, Bencina M, Bowman BJ, Yarden O, Read ND (2004) A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genet Biol 41:827–841PubMedGoogle Scholar
- Zhou L, Evangelinos M, Wernet V, Eckert AF, Ishitsuka Y, Fischer R, Nienhaus GU, Takeshita N (2018) Superresolution and pulse-chase imaging reveal the role of vesicle transport in polar growth of fungal cells. Sci Adv 4:e1701798PubMedPubMedCentralGoogle Scholar