Breakpoint: Cell Wall and Glycoproteins and their Crucial Role in the Phytopathogenic Fungi Infection

Author(s): Verónica Plaza, Evelyn Silva-Moreno, Luis Castillo*.

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


The cell wall that surrounds fungal cells is essential for their survival, provides protection against physical and chemical stresses, and plays relevant roles during infection. In general, the fungal cell wall is composed of an outer layer of glycoprotein and an inner skeletal layer of β-glucans or α- glucans and chitin. Chitin synthase genes have been shown to be important for septum formation, cell division and virulence. In the same way, chitin can act as a potent elicitor to activate defense response in several plant species; however, the fungi can convert chitin to chitosan during plant infection to evade plant defense mechanisms. Moreover, α-1,3-Glucan, a non-degradable polysaccharide in plants, represents a key feature in fungal cell walls formed in plants and plays a protective role for this fungus against plant lytic enzymes. A similar case is with β-1,3- and β-1,6-glucan which are essential for infection, structure rigidity and pathogenicity during fungal infection. Cell wall glycoproteins are also vital to fungi. They have been associated with conidial separation, the increase of chitin in conidial cell walls, germination, appressorium formation, as well as osmotic and cell wall stress and virulence; however, the specific roles of glycoproteins in filamentous fungi remain unknown. Fungi that can respond to environmental stimuli distinguish these signals and relay them through intracellular signaling pathways to change the cell wall composition. They play a crucial role in appressorium formation and penetration, and release cell wall degrading enzymes, which determine the outcome of the interaction with the host. In this review, we highlight the interaction of phypatophogen cell wall and signaling pathways with its host and their contribution to fungal pathogenesis.

Keywords: Phytopathogen, fungi cell wall, glycoproteins, virulence factor, cell wall-degrading enzymes, signaling pathways.

Ruiz-Herrera, J.; Elorza, M.V.; Valentín, E.; Sentandreu, R. Molecular organization of the cell wall of Candida albicans and its relation to pathogenicity. FEMS Yeast Res., 2006, 6(1), 14-29.
[] [PMID: 16423067]
Adams, D.J. Fungal cell wall chitinases and glucanases. Microbiology, 2004, 150(Pt 7), 2029-2035.
[] [PMID: 15256547]
De Las Peñas, A.; Pan, S.J.; Castaño, I.; Alder, J.; Cregg, R.; Cormack, B.P. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev., 2003, 17(18), 2245-2258.
[] [PMID: 12952896]
Hoyer, L.L.; Green, C.B.; Oh, S.H.; Zhao, X. Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family--a sticky pursuit. Med. Mycol., 2008, 46(1), 1-15.
[] [PMID: 17852717]
de Boer, A.D.; de Groot, P.W.J.; Weindl, G.; Schaller, M.; Riedel, D.; Diez-Orejas, R.; Klis, F.M.; de Koster, C.G.; Dekker, H.L.; Gross, U.; Bader, O.; Weig, M. The Candida albicans cell wall protein Rhd3/Pga29 is abundant in the yeast form and contributes to virulence. Yeast, 2010, 27(8), 611-624.
[] [PMID: 20533408]
Laforet, L.; Moreno, I.; Sánchez-Fresneda, R.; Martínez-Esparza, M.; Martínez, J.P.; Argüelles, J.C.; de Groot, P.W.J.; Valentín-Gomez, E. Pga26 mediates filamentation and biofilm formation and is required for virulence in Candida albicans. FEMS Yeast Res., 2011, 11(5), 389-397.
[] [PMID: 21439008]
Gelis, S.; de Groot, P.W.J.; Castillo, L.; Moragues, M.D.; Sentandreu, R.; Gómez, M.M.; Valentín, E. Pga13 in Candida albicans is localized in the cell wall and influences cell surface properties, morphogenesis and virulence. Fungal Genet. Biol., 2012, 49(4), 322-331.
[] [PMID: 22343036]
Fujikawa, T.; Kuga, Y.; Yano, S.; Yoshimi, A.; Tachiki, T.; Abe, K.; Nishimura, M. Dynamics of cell wall components of Magnaporthe grisea during infectious structure development. Mol. Microbiol., 2009, 73(4), 553-570.
[] [PMID: 19602150]
Fujikawa, T.; Sakaguchi, A.; Nishizawa, Y.; Kouzai, Y.; Minami, E.; Yano, S.; Koga, H.; Meshi, T.; Nishimura, M. Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog., 2012, 8(8)e1002882
[] [PMID: 22927818]
Shahinian, S.; Bussey, H. beta-1,6-Glucan synthesis in Saccharomyces cerevisiae. Mol. Microbiol., 2000, 35(3), 477-489.
[] [PMID: 10672173]
Ruiz-Herrera, J.; Ortiz-Castellanos, L.; Martínez, A.I.; León-Ramírez, C.; Sentandreu, R. Analysis of the proteins involved in the structure and synthesis of the cell wall of Ustilago maydis. Fungal Genet. Biol., 2008, 45(Suppl. 1), S71-S76.
[] [PMID: 18508396]
Ruiz-Herrera, J.; Ortiz-Castellanos, L. Analysis of the phylogenetic relationships and evolution of the cell walls from yeasts and fungi. FEMS Yeast Res., 2010, 10(3), 225-243.
[] [PMID: 19891730]
Robledo-Briones, M.; Ruiz-Herrera, J. Regulation of genes involved in cell wall synthesis and structure during Ustilago maydis dimorphism. FEMS Yeast Res., 2013, 13(1), 74-84.
[] [PMID: 23167842]
De Groot, P.W.; Martinez, A.I.; Castillo, L. A Genomic Inventory of Cell Wall Biosynthesis in the Ubiquitous Plant Pathogen Botrytis cinerea.; The Fungal Cell Wall; Mora-Montes, H.M., Ed.; Nova Biomedical: Hauppauge, NY, 2013.
Ruiz-Herrera, j.Fungal Cell Wall: Structure, Synthesis, and Assembly, Second Edition; 2nd Edition ed.; October 19, 2016, p. 203.
Liu, J.; Wang, H.; McCollum, D.; Balasubramanian, M.K. Drc1p/Cps1p, a 1,3-beta-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe. Genetics, 1999, 153(3), 1193-1203.
[PMID: 10545452]
Cortés, J.C.G.; Ishiguro, J.; Durán, A.; Ribas, J.C. Localization of the (1,3)beta-D-glucan synthase catalytic subunit homologue Bgs1p/Cps1p from fission yeast suggests that it is involved in septation, polarized growth, mating, spore wall formation and spore germination. J. Cell Sci., 2002, 115(Pt 21), 4081-4096.
[] [PMID: 12356913]
Tentler, S.; Palas, J.; Enderlin, C.; Campbell, J.; Taft, C.; Miller, T.K.; Wood, R.L.; Selitrennikoff, C.P. Inhibition of Neurospora crassa growth by a glucan synthase-1 antisense construct. Curr. Microbiol., 1997, 34(5), 303-308.
[] [PMID: 9099631]
Thompson, J.R.; Douglas, C.M.; Li, W.; Jue, C.K.; Pramanik, B.; Yuan, X.; Rude, T.H.; Toffaletti, D.L.; Perfect, J.R.; Kurtz, M. A glucan synthase FKS1 homolog in cryptococcus neoformans is single copy and encodes an essential function. J. Bacteriol., 1999, 181(2), 444-453.
[PMID: 9882657]
Lesage, G.; Bussey, H. Cell wall assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 2006, 70(2), 317-343.
[] [PMID: 16760306]
Choquer, M.; Boccara, M.; Gonçalves, I.R.; Soulié, M.C.; Vidal-Cros, A. Survey of the Botrytis cinerea chitin synthase multigenic family through the analysis of six euascomycetes genomes. Eur. J. Biochem., 2004, 271(11), 2153-2164.
[] [PMID: 15153106]
Ruiz-Herrera, J.; González-Prieto, J.M.; Ruiz-Medrano, R. Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res., 2002, 1(4), 247-256.
[] [PMID: 12702327]
Zhou, H.; Hu, H.; Zhang, L.; Li, R.; Ouyang, H.; Ming, J.; Jin, C. O-Mannosyltransferase 1 in Aspergillus fumigatus (AfPmt1p) is crucial for cell wall integrity and conidium morphology, especially at an elevated temperature. Eukaryot. Cell, 2007, 6(12), 2260-2268.
[] [PMID: 17905922]
Fernández-Alvarez, A.; Elías-Villalobos, A.; Ibeas, J.I. The O-mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell, 2009, 21(10), 3397-3412.
[] [PMID: 19880800]
Kriangkripipat, T.; Momany, M. Aspergillus nidulans protein O-mannosyltransferases play roles in cell wall integrity and developmental patterning. Eukaryot. Cell, 2009, 8(10), 1475-1485.
[] [PMID: 19666781]
Plaza, V.; Lagües, Y.; Carvajal, M.; Pérez-García, L.A.; Mora-Montes, H.M.; Canessa, P.; Larrondo, L.F.; Castillo, L. bcpmr1 encodes a P-type Ca(2+)/Mn(2+)-ATPase mediating cell-wall integrity and virulence in the phytopathogen Botrytis cinerea. Fungal Genet. Biol., 2015, 76, 36-46.
[] [PMID: 25677379]
Lussier, M.; Sdicu, A.M.; Bussey, H. The KTR and MNN1 mannosyltransferase families of Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1999, 1426(2), 323-334.
[] [PMID: 9878809]
Wagener, J.; Echtenacher, B.; Rohde, M.; Kotz, A.; Krappmann, S.; Heesemann, J.; Ebel, F. The putative alpha-1,2-mannosyltransferase AfMnt1 of the opportunistic fungal pathogen Aspergillus fumigatus is required for cell wall stability and full virulence. Eukaryot. Cell, 2008, 7(10), 1661-1673.
[] [PMID: 18708564]
Schäfer, W. MOLECULAR MECHANISMS OF FUNGAL PATHOGENICITY TO PLANTS. Annu. Rev. Phytopathol., 1994, 32(1), 461-477.
Oliver, R.; Osbourn, A. Molecular dissection of fungal phytopathogenicity. Microbiology, 1995, 141(Pt 1), 1-9.
[] [PMID: 7894700]
Hamer, J.E.; Holden, D.W. Linking approaches in the study of fungal pathogenesis: A commentary. Fungal Genet. Biol., 1997, 21(1), 11-16.
Kahmann, R.; Basse, C.; Feldbrügge, M. Fungal-plant signalling in the Ustilago maydis-maize pathosystem. Curr. Opin. Microbiol., 1999, 2(6), 647-650.
[] [PMID: 10607627]
Knogge, W. Fungal pathogenicity. Curr. Opin. Plant Biol., 1998, 1(4), 324-328.
[] [PMID: 10066600]
Maier, F.J.; Schäfer, W. Mutagenesis via insertional- or restriction enzyme-mediated-integration (REMI) as a tool to tag pathogenicity related genes in plant pathogenic fungi. Biol. Chem., 1999, 380(7-8), 855-864.
[] [PMID: 10494834]
Sweigard, J.A.; Carroll, A.M.; Farrall, L.; Chumley, F.G.; Valent, B. Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol. Plant Microbe Interact., 1998, 11(5), 404-412.
[] [PMID: 9574508]
Mendgen, K.; Hahn, M.; Deising, H. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu. Rev. Phytopathol., 1996, 34, 367-386.
[] [PMID: 15012548]
Gonçalves, I.R.; Brouillet, S.; Soulié, M.C.; Gribaldo, S.; Sirven, C.; Charron, N.; Boccara, M.; Choquer, M. Genome-wide analyses of chitin synthases identify horizontal gene transfers towards bacteria and allow a robust and unifying classification into fungi. BMC Evol. Biol., 2016, 16(1), 252.
[] [PMID: 27881071]
Yarden, O.; Yanofsky, C. Chitin synthase 1 plays a major role in cell wall biogenesis in Neurospora crassa. Genes Dev., 1991, 5(12B), 2420-2430.
[] [PMID: 1836444]
Munro, C.A.; Gow, N.A.R. Chitin synthesis in human pathogenic fungi. Med. Mycol., 2001, 39(Suppl. 1), 41-53.
[] [PMID: 11800268]
Roncero, C. The genetic complexity of chitin synthesis in fungi. Curr. Genet., 2002, 41(6), 367-378.
[] [PMID: 12228806]
Niño-Vega, G.A.; Carrero, L.; San-Blas, G. Isolation of the CHS4 gene of Paracoccidioides brasiliensis and its accommodation in a new class of chitin synthases. Med. Mycol., 2004, 42(1), 51-57.
[] [PMID: 14982114]
Zhang, Y.Z.; Chen, Q.; Liu, C.H.; Liu, Y.B.; Yi, P.; Niu, K.X.; Wang, Y.Q.; Wang, A.Q.; Yu, H.Y.; Pu, Z.E.; Jiang, Q.T.; Wei, Y.M.; Qi, P.F.; Zheng, Y.L. Chitin synthase gene FgCHS8 affects virulence and fungal cell wall sensitivity to environmental stress in Fusarium graminearum. Fungal Biol., 2016, 120(5), 764-774.
[] [PMID: 27109372]
Bowen, A.R.; Chen-Wu, J.L.; Momany, M.; Young, R.; Szaniszlo, P.J.; Robbins, P.W. Classification of fungal chitin synthases. Proc. Natl. Acad. Sci. USA, 1992, 89(2), 519-523.
[] [PMID: 1731323]
Kong, L.A.; Yang, J.; Li, G.T.; Qi, L.L.; Zhang, Y.J.; Wang, C.F.; Zhao, W.S.; Xu, J.R.; Peng, Y.L. Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog., 2012, 8(2) e1002526
[] [PMID: 22346755]
Lenardon, M.D.; Munro, C.A.; Gow, N.A. Chitin synthesis and fungal pathogenesis. Curr. Opin. Microbiol., 2010, 13(4), 416-423.
[] [PMID: 20561815]
Beth-Din, A.; Yarden, O. The Neurospora crassa chs3 gene encodes an essential class I chitin synthase. Mycologia, 2000, 92(1), 65-73.
Fajardo-Somera, R.A.; Jöhnk, B.; Bayram, Ö.; Valerius, O.; Braus, G.H.; Riquelme, M. Dissecting the function of the different chitin synthases in vegetative growth and sexual development in Neurospora crassa. Fungal Genet. Biol., 2015, 75, 30-45.
[] [PMID: 25596036]
Horiuchi, H. Functional diversity of chitin synthases of Aspergillus nidulans in hyphal growth, conidiophore development and septum formation. Med. Mycol., 2009, 47(Suppl. 1), S47-S52.
[] [PMID: 18651309]
Sánchez-León, E.; Verdín, J.; Freitag, M.; Roberson, R.W.; Bartnicki-Garcia, S.; Riquelme, M. Traffic of chitin synthase 1 (CHS-1) to the Spitzenkörper and developing septa in hyphae of Neurospora crassa: actin dependence and evidence of distinct microvesicle populations. Eukaryot. Cell, 2011, 10(5), 683-695.
[] [PMID: 21296914]
Horiuchi, H.; Fujiwara, M.; Yamashita, S.; Ohta, A.; Takagi, M. Proliferation of intrahyphal hyphae caused by disruption of csmA, which encodes a class V chitin synthase with a myosin motor-like domain in Aspergillus nidulans. J. Bacteriol., 1999, 181(12), 3721-3729.
[PMID: 10368147]
Takeshita, N.; Yamashita, S.; Ohta, A.; Horiuchi, H. 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., 2006, 59(5), 1380-1394.
[] [PMID: 16468983]
Motoyama, T.; Fujiwara, M.; Kojima, N.; Horiuchi, H.; Ohta, A.; Takagi, M. The Aspergillus nidulans genes chsA and chsD encode chitin synthases which have redundant functions in conidia formation. [corrected and republished article originally appeared in Mol Gen Genet 1996 Jun; 251(4):442-50]. Mol. Gen. Genet., 1997, 253(4), 520-528.
[] [PMID: 9037115]
Weber, I.; Assmann, D.; Thines, E.; Steinberg, G. Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell, 2006, 18(1), 225-242.
[] [PMID: 16314447]
XoconostleCazares. B.; LeonRamirez, C.; RuizHerrera, J., Two chitin synthase genes from Ustilago maydis. Microbiol-Uk, 1996, 142, 377-387.
Cui, Z.; Ding, Z.; Yang, X.; Wang, K.; Zhu, T. Gene disruption and characterization of a class V chitin synthase in Botrytis cinerea. Can. J. Microbiol., 2009, 55(11), 1267-1274.
[] [PMID: 19940935]
Arbelet, D.; Malfatti, P.; Simond-Côte, E.; Fontaine, T.; Desquilbet, L.; Expert, D.; Kunz, C.; Soulié, M.C. Disruption of the Bcchs3a chitin synthase gene in Botrytis cinerea is responsible for altered adhesion and overstimulation of host plant immunity. Mol. Plant Microbe Interact., 2010, 23(10), 1324-1334.
[] [PMID: 20672878]
Morcx, S.; Kunz, C.; Choquer, M.; Assie, S.; Blondet, E.; Simond-Côte, E.; Gajek, K.; Chapeland-Leclerc, F.; Expert, D.; Soulie, M.C. Disruption of Bcchs4, Bcchs6 or Bcchs7 chitin synthase genes in Botrytis cinerea and the essential role of class VI chitin synthase (Bcchs6). Fungal Genet. Biol., 2013, 52, 1-8.
[] [PMID: 23268147]
Hayafune, M.; Berisio, R.; Marchetti, R.; Silipo, A.; Kayama, M.; Desaki, Y.; Arima, S.; Squeglia, F.; Ruggiero, A.; Tokuyasu, K.; Molinaro, A.; Kaku, H.; Shibuya, N. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl. Acad. Sci. USA, 2014, 111(3), E404-E413.
[] [PMID: 24395781]
Geoghegan, I.A.; Gurr, S.J. Chitosan Mediates Germling Adhesion in Magnaporthe oryzae and Is Required for Surface Sensing and Germling Morphogenesis. PLoS Pathog., 2016, 12(6) e1005703
[] [PMID: 27315248]
El Gueddari, N.E.; Rauchhaus, U.; Moerschbacher, B.M.; Deising, H.B. Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol., 2002, 156(1), 103-112.
Liu, Z.L.; Gay, L.M.; Tuveng, T.R.; Agger, J.W.; Westereng, B.; Mathiesen, G.; Horn, S.J.; Vaaje-Kolstad, G.; van Aalten, D.M.F.; Eijsink, V.G.H. Structure and function of a broadspecificity chitin deacetylase from Aspergillus nidulans FGSC A4; Sci Rep-Uk, 2017, p. 7.
Blair, D.E.; Hekmat, O.; Schüttelkopf, A.W.; Shrestha, B.; Tokuyasu, K.; Withers, S.G.; van Aalten, D.M.F. Structure and mechanism of chitin deacetylase from the fungal pathogen Colletotrichum lindemuthianum. Biochemistry, 2006, 45(31), 9416-9426.
[] [PMID: 16878976]
Christodoulidou, A.; Bouriotis, V.; Thireos, G. Two sporulation-specific chitin deacetylase-encoding genes are required for the ascospore wall rigidity of Saccharomyces cerevisiae. J. Biol. Chem., 1996, 271(49), 31420-31425.
[] [PMID: 8940152]
Christodoulidou, A.; Briza, P.; Ellinger, A.; Bouriotis, V. Yeast ascospore wall assembly requires two chitin deacetylase isozymes. FEBS Lett., 1999, 460(2), 275-279.
[] [PMID: 10544249]
Upadhya, R.; Baker, L.G.; Lam, W.C.; Specht, C.A.; Donlin, M.J.; Lodge, J.K. Cryptococcus neoformans Cda1 and its chitin deacetylase activity are required for fungal pathogenesis. MBio, 2018, 9(6), e02087-e18.
[] [PMID: 30459196]
Vos, A.; Dekker, N.; Distel, B.; Leunissen, J.A.; Hochstenbach, F. Role of the synthase domain of Ags1p in cell wall alpha-glucan biosynthesis in fission yeast. J. Biol. Chem., 2007, 282(26), 18969-18979.
[] [PMID: 17472966]
Douglas, C.M. Fungal beta(1,3)-D-glucan synthesis. Med. Mycol., 2001, 39(Suppl. 1), 55-66.
[] [PMID: 11800269]
Sánchez-León, E.; Riquelme, M. Live imaging of β-1,3-glucan synthase FKS-1 in Neurospora crassa hyphae. Fungal Genet. Biol., 2015, 82, 104-107.
[] [PMID: 26150287]
Douglas, C.M. DIppolito, J. A.; Shei, G. J.; Meinz, M.; Onishi, J.; Marrinan, J. A.; Li, W.; Abruzzo, G. K.; Flattery, A.; Bartizal, K.; Mitchell, A.; Kurtz, M. B., Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob. Agents Ch., 1997, 41(11), 2471-2479.
Ha, Y.S.; Covert, S.F.; Momany, M. FsFKS1, the 1,3-beta-glucan synthase from the caspofungin-resistant fungus Fusarium solani. Eukaryot. Cell, 2006, 5(7), 1036-1042.
[] [PMID: 16835448]
Etienne-Manneville, S.; Hall, A. Rho GTPases in cell biology. Nature, 2002, 420(6916), 629-635.
[] [PMID: 12478284]
Sit, S.T.; Manser, E. Rho GTPases and their role in organizing the actin cytoskeleton. J. Cell Sci., 2011, 124(Pt 5), 679-683.
[] [PMID: 21321325]
Richthammer, C.; Enseleit, M.; Sanchez-Leon, E.; März, S.; Heilig, Y.; Riquelme, M.; Seiler, S. RHO1 and RHO2 share partially overlapping functions in the regulation of cell wall integrity and hyphal polarity in Neurospora crassa. Mol. Microbiol., 2012, 85(4), 716-733.
[] [PMID: 22703449]
Kwon, M.J.; Arentshorst, M.; Roos, E.D.; van den Hondel, C.A.M.J.J.; Meyer, V.; Ram, A.F.J. Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol. Microbiol., 2011, 79(5), 1151-1167.
[] [PMID: 21205013]
Vasara, T.; Saloheimo, M.; Keränen, S.; Penttilä, M. Trichoderma reesei rho3 a homologue of yeast RH03 suppresses the growth defect of yeast sec15-1 mutation. Curr. Genet., 2001, 40(2), 119-127.
[] [PMID: 11680821]
Vasara, T.; Salusjärvi, L.; Raudaskoski, M.; Keränen, S.; Penttilä, M.; Saloheimo, M. Interactions of the Trichoderma reesei rho3 with the secretory pathway in yeast and T. reesei. Mol. Microbiol., 2001, 42(5), 1349-1361.
[] [PMID: 11886564]
Rasmussen, C.G.; Glass, N.L. A Rho-type GTPase, rho-4, is required for septation in Neurospora crassa. Eukaryot. Cell, 2005, 4(11), 1913-1925.
[] [PMID: 16278458]
Dünkler, A.; Wendland, J. Candida albicans Rho-type GTPase-encoding genes required for polarized cell growth and cell separation. Eukaryot. Cell, 2007, 6(5), 844-854.
[] [PMID: 17351079]
Si, H.; Justa-Schuch, D.; Seiler, S.; Harris, S.D. Regulation of septum formation by the Bud3-Rho4 GTPase module in Aspergillus nidulans. Genetics, 2010, 185(1), 165-176.
[] [PMID: 20176976]
Kim, J.M.; Zeng, C.J.T.; Nayak, T.; Shao, R.; Huang, A.C.; Oakley, B.R.; Liu, B. Timely septation requires SNAD-dependent spindle pole body localization of the septation initiation network components in the filamentous fungus Aspergillus nidulans. Mol. Biol. Cell, 2009, 20(12), 2874-2884.
[] [PMID: 19386763]
Maerz, S.; Dettmann, A.; Ziv, C.; Liu, Y.; Valerius, O.; Yarden, O.; Seiler, S. Two NDR kinase-MOB complexes function as distinct modules during septum formation and tip extension in Neurospora crassa. Mol. Microbiol., 2009, 74(3), 707-723.
[] [PMID: 19788544]
Justa-Schuch, D.; Heilig, Y.; Richthammer, C.; Seiler, S. Septum formation is regulated by the RHO4-specific exchange factors BUD3 and RGF3 and by the landmark protein BUD4 in Neurospora crassa. Mol. Microbiol., 2010, 76(1), 220-235.
[] [PMID: 20199606]
Herrero, A.B.; Magnelli, P.; Mansour, M.K.; Levitz, S.M.; Bussey, H.; Abeijon, C. KRE5 gene null mutant strains of Candida albicans are avirulent and have altered cell wall composition and hypha formation properties. Eukaryot. Cell, 2004, 3(6), 1423-1432.
[] [PMID: 15590817]
Aimanianda, V.; Clavaud, C.; Simenel, C.; Fontaine, T.; Delepierre, M.; Latgé, J.P. Cell wall beta-(1,6)-glucan of Saccharomyces cerevisiae: structural characterization and in situ synthesis. J. Biol. Chem., 2009, 284(20), 13401-13412.
[] [PMID: 19279004]
Mio, T.; Yamada-Okabe, T.; Yabe, T.; Nakajima, T.; Arisawa, M.; Yamada-Okabe, H. Isolation of the Candida albicans homologs of Saccharomyces cerevisiae KRE6 and SKN1: expression and physiological function. J. Bacteriol., 1997, 179(7), 2363-2372.
[] [PMID: 9079924]
Staab, J.F.; Bradway, S.D.; Fidel, P.L.; Sundstrom, P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science, 1999, 283(5407), 1535-1538.
[] [PMID: 10066176]
Han, Q.; Wang, N.; Yao, G.; Mu, C.; Wang, Y.; Sang, J. Blocking β-1,6-glucan synthesis by deleting KRE6 and SKN1 attenuates the virulence of Candida albicans. Mol. Microbiol., 2019, 111(3), 604-620.
[] [PMID: 30507002]
Oliveira-Garcia, E.; Deising, H.B. Attenuation of PAMP-triggered immunity in maize requires down-regulation of the key β-1,6-glucan synthesis genes KRE5 and KRE6 in biotrophic hyphae of Colletotrichum graminicola. Plant J., 2016, 87(4), 355-375.
[] [PMID: 27144995]
Oliveira-Garcia, E.; Valent, B. How eukaryotic filamentous pathogens evade plant recognition. Curr. Opin. Microbiol., 2015, 26, 92-101.
[] [PMID: 26162502]
Loibl, M.; Strahl, S. Protein O-mannosylation: what we have learned from baker’s yeast. Biochim. Biophys. Acta, 2013, 1833(11), 2438-2446.
[] [PMID: 23434682]
Juchimiuk, M.; Kruszewska, J.; Palamarczyk, G. Dolichol phosphate mannose synthase from the pathogenic yeast Candida albicans is a multimeric enzyme. Biochim. Biophys. Acta, 2015, 1850(11), 2265-2275.
[] [PMID: 26299246]
Orłowski, J.; Machula, K.; Janik, A.; Zdebska, E.; Palamarczyk, G. Dissecting the role of dolichol in cell wall assembly in the yeast mutants impaired in early glycosylation reactions. Yeast, 2007, 24(4), 239-252.
[] [PMID: 17397129]
Prill, S.K.H.; Klinkert, B.; Timpel, C.; Gale, C.A.; Schröppel, K.; Ernst, J.F. PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol. Microbiol., 2005, 55(2), 546-560.
[] [PMID: 15659169]
Gentzsch, M.; Tanner, W. The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J., 1996, 15(21), 5752-5759.
[] [PMID: 8918452]
González, M.; Brito, N.; Frías, M.; González, C. Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLoS One, 2013, 8(6) e65924
[] [PMID: 23762450]
Willer, T.; Brandl, M.; Sipiczki, M.; Strahl, S. Protein O-mannosylation is crucial for cell wall integrity, septation and viability in fission yeast. Mol. Microbiol., 2005, 57(1), 156-170.
[] [PMID: 15948957]
Le, T.H.T.; Oki, A.; Goto, M.; Shimizu, K. Protein O-mannosyltransferases are required for sterigmatocystin production and developmental processes in Aspergillus nidulans. Curr. Genet., 2018, 64(5), 1043-1056.
[] [PMID: 29492587]
Dürr, G.; Strayle, J.; Plemper, R.; Elbs, S.; Klee, S.K.; Catty, P.; Wolf, D.H.; Rudolph, H.K. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol. Biol. Cell, 1998, 9(5), 1149-1162.
[] [PMID: 9571246]
Bates, S.; Hughes, H.B.; Munro, C.A.; Thomas, W.P.H.; MacCallum, D.M.; Bertram, G.; Atrih, A.; Ferguson, M.A.J.; Brown, A.J.P.; Odds, F.C.; Gow, N.A.R. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J. Biol. Chem., 2006, 281(1), 90-98.
[] [PMID: 16263704]
Pinchai, N.; Juvvadi, P.R.; Fortwendel, J.R.; Perfect, B.Z.; Rogg, L.E.; Asfaw, Y.G.; Steinbach, W.J. The Aspergillus fumigatus P-type Golgi apparatus Ca2+/Mn2+ ATPase PmrA is involved in cation homeostasis and cell wall integrity but is not essential for pathogenesis. Eukaryot. Cell, 2010, 9(3), 472-476.
[] [PMID: 20097742]
Wang, J.; Zhou, G.; Ying, S.H.; Feng, M.G. 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.
[] [PMID: 23206243]
De Groot, P.W.; Hellingwerf, K.J.; Klis, F.M. Genome-wide identification of fungal GPI proteins. Yeast, 2003, 20(9), 781-796.
[] [PMID: 12845604]
Eisenhaber, B.; Schneider, G.; Wildpaner, M.; Eisenhaber, F. A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J. Mol. Biol., 2004, 337(2), 243-253.
[] [PMID: 15003443]
Klis, F.M.; Mol, P.; Hellingwerf, K.; Brul, S. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev., 2002, 26(3), 239-256.
[] [PMID: 12165426]
de Groot, P.W.J.; de Boer, A.D.; Cunningham, J.; Dekker, H.L.; de Jong, L.; Hellingwerf, K.J.; de Koster, C.; Klis, F.M. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell, 2004, 3(4), 955-965.
[] [PMID: 15302828]
Yin, Q.Y.; de Groot, P.W.J.; Dekker, H.L.; de Jong, L.; Klis, F.M.; de Koster, C.G. Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages. J. Biol. Chem., 2005, 280(21), 20894-20901.
[] [PMID: 15781460]
Castillo, L.; Calvo, E.; Martínez, A.I.; Ruiz-Herrera, J.; Valentín, E.; Lopez, J.A.; Sentandreu, R. A study of the Candida albicans cell wall proteome. Proteomics, 2008, 8(18), 3871-3881.
[] [PMID: 18712765]
de Groot, P.W.J.; Brandt, B.W.; Horiuchi, H.; Ram, A.F.J.; de Koster, C.G.; Klis, F.M. Comprehensive genomic analysis of cell wall genes in Aspergillus nidulans. Fungal Genet. Biol., 2009, 46(Suppl. 1), S72-S81.
[] [PMID: 19585695]
Maddi, A.; Bowman, S.M.; Free, S.J. Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet. Biol., 2009, 46(10), 768-781.
[] [PMID: 19555771]
Backhaus, K.; Heilmann, C.J.; Sorgo, A.G.; Purschke, G.; de Koster, C.G.; Klis, F.M.; Heinisch, J.J. A systematic study of the cell wall composition of Kluyveromyces lactis. Yeast, 2010, 27(8), 647-660.
[] [PMID: 20641021]
de Groot, P.W.J.; Yin, Q.Y.; Weig, M.; Sosinska, G.J.; Klis, F.M.; de Koster, C.G. Mass spectrometric identification of covalently bound cell wall proteins from the fission yeast Schizosaccharomyces pombe. Yeast, 2007, 24(4), 267-278.
[] [PMID: 17230583]
de Groot, P.W.J.; Kraneveld, E.A.; Yin, Q.Y.; Dekker, H.L.; Gross, U.; Crielaard, W.; de Koster, C.G.; Bader, O.; Klis, F.M.; Weig, M. The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot. Cell, 2008, 7(11), 1951-1964.
[] [PMID: 18806209]
Romano, J.; Nimrod, G.; Ben-Tal, N.; Shadkchan, Y.; Baruch, K.; Sharon, H.; Osherov, N. Disruption of the Aspergillus fumigatus ECM33 homologue results in rapid conidial germination, antifungal resistance and hypervirulence. Microbiology, 2006, 152(Pt 7), 1919-1928.
[] [PMID: 16804168]
Chang, P.K.; Zhang, Q.; Scharfenstein, L.; Mack, B.; Yoshimi, A.; Miyazawa, K.; Abe, K. Aspergillus flavus GPI-anchored protein-encoding ecm33 has a role in growth, development, aflatoxin biosynthesis, and maize infection. Appl. Microbiol. Biotechnol., 2018, 102(12), 5209-5220.
[] [PMID: 29696338]
Zhu, W.; Wei, W.; Wu, Y.; Zhou, Y.; Peng, F.; Zhang, S.; Chen, P.; Xu, X. BcCFEM1, a CFEM domain-containing protein with putative GPI-anchored site, is Involved in pathogenicity, conidial production, and stress tolerance in Botrytis cinerea. Front. Microbiol., 2017, 8, 1807.
[] [PMID: 28979251]
Epstein, L.; Nicholson, R.L. Adhesion of Spores and Hyphae to Plant Surfaces.Plant Relationships; Part, A.; Carroll, G.C.; Tudzynski, P., Eds.; Springer Berlin Heidelberg: Berlin, Heidelberg, 1997, pp. 11-25.
Howard, R.J. Breaching the Outer Barriers — Cuticle and Cell Wall Penetration.Plant Relationships; Part, A.; Carroll, G.C.; Tudzynski, P., Eds.; Springer Berlin Heidelberg: Berlin, Heidelberg,, 1997, pp. 43-60.
Schoffelmeer, E.A.M.; Vossen, J.H.; van Doorn, A.A.; Cornelissen, B.J.C.; Haring, M.A. FEM1, a Fusarium oxysporum glycoprotein that is covalently linked to the cell wall matrix and is conserved in filamentous fungi. Mol. Genet. Genomics, 2001, 265(1), 143-152.
[] [PMID: 11370861]
Ahn, N.; Kim, S.; Choi, W.; Im, K.H.; Lee, Y.H. Extracellular matrix protein gene, EMP1, is required for appressorium formation and pathogenicity of the rice blast fungus, Magnaporthe grisea. Mol. Cells, 2004, 17(1), 166-173.
[PMID: 15055545]
DeZwaan, T.M.; Carroll, A.M.; Valent, B.; Sweigard, J.A. 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.
[] [PMID: 10521529]
Kulkarni, R.D.; Thon, M.R.; Pan, H.; Dean, R.A. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol., 2005, 6(3), R24.
[] [PMID: 15774025]
Brown, N.A.; Schrevens, S.; van Dijck, P.; Goldman, G.H. Fungal G-protein-coupled receptors: mediators of pathogenesis and targets for disease control. Nat. Microbiol., 2018, 3(4), 402-414.
[] [PMID: 29588541]
Dilks, T.; Halsey, K.; De Vos, R.P.; Hammond-Kosack, K.E.; Brown, N.A. Non-canonical fungal G-protein coupled receptors promote Fusarium head blight on wheat. PLoS Pathog., 2019, 15(4) e1007666
[] [PMID: 30934025]
Dean, R.A.; Talbot, N.J.; Ebbole, D.J.; Farman, M.L.; Mitchell, T.K.; Orbach, M.J.; Thon, M.; Kulkarni, R.; Xu, J.R.; Pan, H.; Read, N.D.; Lee, Y.H.; Carbone, I.; Brown, D.; Oh, Y.Y.; Donofrio, N.; Jeong, J.S.; Soanes, D.M.; Djonovic, S.; Kolomiets, E.; Rehmeyer, C.; Li, W.; Harding, M.; Kim, S.; Lebrun, M.H.; Bohnert, H.; Coughlan, S.; Butler, J.; Calvo, S.; Ma, L.J.; Nicol, R.; Purcell, S.; Nusbaum, C.; Galagan, J.E.; Birren, B.W. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature, 2005, 434(7036), 980-986.
[] [PMID: 15846337]
Xu, X.; Li, G.; Li, L.; Su, Z.; Chen, C. Genome-wide comparative analysis of putative Pth11-related G protein-coupled receptors in fungi belonging to Pezizomycotina. BMC Microbiol., 2017, 17(1), 166.
[] [PMID: 28743231]
Gronover, C.S.; Schumacher, J.; Hantsch, P.; Tudzynski, B. A novel seven-helix transmembrane protein BTP1 of Botrytis cinerea controls the expression of GST-encoding genes, but is not essential for pathogenicity. Mol. Plant Pathol., 2005, 6(3), 243-256.
[] [PMID: 20565654]
Catlett, N.L.; Yoder, O.C.; Turgeon, B.G. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell, 2003, 2(6), 1151-1161.
[] [PMID: 14665450]
Wolanin, P.M.; Thomason, P.A.; Stock, J.B. Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol., 2002, 3(10), S3013.
[] [PMID: 12372152]
Viaud, M.; Fillinger, S.; Liu, W.; Polepalli, J.S.; Le Pêcheur, P.; Kunduru, A.R.; Leroux, P.; Legendre, L. A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol. Plant Microbe Interact., 2006, 19(9), 1042-1050.
[] [PMID: 16941908]
Liu, W.; Soulié, M.C.; Perrino, C.; Fillinger, S. The osmosensing signal transduction pathway from Botrytis cinerea regulates cell wall integrity and MAP kinase pathways control melanin biosynthesis with influence of light. Fungal Genet. Biol., 2011, 48(4), 377-387.
[] [PMID: 21176789]
Kilani, J.; Davanture, M.; Zivy, M.; Fillinger, S. Comparative proteomics of osmotic signal transduction mutants in Botrytis cinerea explain loss of pathogenicity phenotypes and highlight interaction with cAMP and Ca2+ signalling pathways. bioRxiv, 2019.
Buck, V.; Quinn, J.; Soto Pino, T.; Martin, H.; Saldanha, J.; Makino, K.; Morgan, B.A.; Millar, J.B.A. Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol. Biol. Cell, 2001, 12(2), 407-419.
[] [PMID: 11179424]
Morigasaki, S.; Shiozaki, K. Two-Component Signaling to the Stress Map Kinase Cascade in Fission Yeast. Methods in Enzymology, Vol 471: Two-Component Signaling Systems. Part C, 2010, 471, 279-289.
Temme, N.; Oeser, B.; Massaroli, M.; Heller, J.; Simon, A.; Collado, I.G.; Viaud, M.; Tudzynski, P. BcAtf1, a global regulator, controls various differentiation processes and phytotoxin production in Botrytis cinerea. Mol. Plant Pathol., 2012, 13(7), 704-718.
[] [PMID: 22293085]
Deising, H.B.; Werner, S.; Wernitz, M. The role of fungal appressoria in plant infection. Microbes Infect., 2000, 2(13), 1631-1641.
[] [PMID: 11113382]
Howard, R.J.; Ferrari, M.A.; Roach, D.H.; Money, N.P. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. USA, 1991, 88(24), 11281-11284.
[] [PMID: 1837147]
Bechinger, C.; Giebel, K.F.; Schnell, M.; Leiderer, P.; Deising, H.B.; Bastmeyer, M. Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science, 1999, 285(5435), 1896-1899.
[] [PMID: 10489364]
deJong, J.C. MCCormack, B. J.; Smirnoff, N.; Talbot, N. J., Glycerol generates turgor in rice blast. Nature, 1997, 389(6648), 244-245.
Chumley, F.G.; Valent, B. Genetic-analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe-Grisea. Mol. Plant Microbe Interact., 1990, 3(3), 135-143.
Liu, C.; Li, Z.; Xing, J.; Yang, J.; Wang, Z.; Zhang, H.; Chen, D.; Peng, Y.L.; Chen, X.L. Global analysis of sumoylation function reveals novel insights into development and appressorium-mediated infection of the rice blast fungus. New Phytol., 2018, 219(3), 1031-1047.
[PMID: 30156025]
Kubo, Y.; Suzuki, K.; Furusawa, I.; Ishida, N.; Yamamoto, M. Relation of Appressorium Pigmentation and Penetration of Nitrocellulose Membranes by Colletotrichum-Lagenarium. Phytopathology, 1982, 72(5), 498-501.
Rasmussen, J.B.; Hanau, R.M. Exogenous Scytalone Restores Appressorial Melanization and Pathogenicity in Albino Mutants of Colletotrichum-Graminicola. Can. J. Plant Pathol., 1989, 11(4), 349-352.
Talbot, N.J.; Ebbole, D.J.; Hamer, J.E. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell, 1993, 5(11), 1575-1590.
[PMID: 8312740]
Lau, G.; Hamer, J.E. Regulatory genes controlling MPG1 expression and pathogenicity in the rice blast fungus Magnaporthe grisea. Plant Cell, 1996, 8(5), 771-781.
[] [PMID: 12239399]
Pham, C.L.L.; Rey, A.; Lo, V.; Soules, M.; Ren, Q.; Meisl, G.; Knowles, T.P.J.; Kwan, A.H.; Sunde, M. Self-assembly of MPG1, a hydrophobin protein from the rice blast fungus that forms functional amyloid coatings, occurs by a surface-driven mechanism. Sci. Rep., 2016, 25288.
Lau, G.W.; Hamer, J.E. Acropetal: a genetic locus required for conidiophore architecture and pathogenicity in the rice blast fungus. Fungal Genet. Biol., 1998, 24(1-2), 228-239.
[] [PMID: 9742203]
Villalba, F.; Lebrun, M.H.; Hua-Van, A.; Daboussi, M.J.; Grosjean-Cournoyer, M.C. Transposon impala, a novel tool for gene tagging in the rice blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact., 2001, 14(3), 308-315.
[] [PMID: 11277428]
Balhadere, P.V.; Foster, A.J.; Talbot, N.J. Identification of pathogenicity mutants of the rice blast fungus Magnaporthe grisea by insertional mutagenesis. Mol. Plant Microbe Interact., 1999, 12(2), 129-142.
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., 2017, 13(6) e1006449
[] [PMID: 28628655]
Lebeda, A.; Luhova, L.; Sedlarova, M.; Jancova, D. The role of enzymes in plant-fungal pathogens interactions - Review. Z Pflanzenk Pflanzen, 2001, 108(1), 89-111.
Williamson, B.; Tudzynski, B.; Tudzynski, P.; van Kan, J.A.L. Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol., 2007, 8(5), 561-580.
[] [PMID: 20507522]
Choquer, M.; Fournier, E.; Kunz, C.; Levis, C.; Pradier, J.M.; Simon, A.; Viaud, M. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol. Lett., 2007, 277(1), 1-10.
[] [PMID: 17986079]
Fillinger, S. Botrytis - the fungus, the pathogen and its management in agricultural systems; Springer Berlin Heidelberg: New York, NY, 2015.
Stahl, D.J.; Schäfer, W. Cutinase is not required for fungal pathogenicity on pea. Plant Cell, 1992, 4(6), 621-629.
[PMID: 1392588]
Rogers, L.M.; Kim, Y.K.; Guo, W.; González-Candelas, L.; Li, D.; Kolattukudy, P.E. Requirement for either a host- or pectin-induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proc. Natl. Acad. Sci. USA, 2000, 97(17), 9813-9818.
[] [PMID: 10931947]
van der Vlugt-Bergmans, C.J.; Wagemakers, C.A.; van Kan, J.A. Cloning and expression of the cutinase A gene of Botrytis cinerea. Mol. Plant Microbe Interact., 1997, 10(1), 21-29.
[] [PMID: 9002269]
Yakoby, N.; Beno-Moualem, D.; Keen, N.T.; Dinoor, A.; Pines, O.; Prusky, D. Colletotrichum gloeosporioides pelB is an important virulence factor in avocado fruit-fungus interaction. Mol. Plant Microbe Interact., 2001, 14(8), 988-995.
[] [PMID: 11497471]
Bowen, J.K.; Templeton, M.D.; Sharrock, K.R.; Crowhurst, R.N.; Rikkerink, E.H.A. Gene inactivation in the plant pathogen Glomerella cingulata: three strategies for the disruption of the pectin lyase gene pnlA. Mol. Gen. Genet., 1995, 246(2), 196-205.
[] [PMID: 7862090]
Shieh, M.T.; Brown, R.L.; Whitehead, M.P.; Cary, J.W.; Cotty, P.J.; Cleveland, T.E.; Dean, R.A. Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Appl. Environ. Microbiol., 1997, 63(9), 3548-3552.
[PMID: 9293005]
ten Have, A.; Mulder, W.; Visser, J.; van Kan, J.A.L. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol. Plant Microbe Interact., 1998, 11(10), 1009-1016.
[] [PMID: 9768518]
Gao, S.; Nuss, D.L. Distinct roles for two G protein alpha subunits in fungal virulence, morphology, and reproduction revealed by targeted gene disruption. Proc. Natl. Acad. Sci. USA, 1996, 93(24), 14122-14127.
[] [PMID: 11038529]
Isshiki, A.; Akimitsu, K.; Yamamoto, M.; Yamamoto, H. Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol. Plant Microbe Interact., 2001, 14(6), 749-757.
[] [PMID: 11386370]
Scott-Craig, J.S.; Cheng, Y.Q.; Cervone, F.; De Lorenzo, G.; Pitkin, J.W.; Walton, J.D. Targeted mutants of Cochliobolus carbonum lacking the two major extracellular polygalacturonases. Appl. Environ. Microbiol., 1998, 64(4), 1497-1503.
[PMID: 9546185]
Tonukari, N.J.; Scott-Craig, J.S.; Walton, J.D. The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell, 2000, 12(2), 237-248.
[PMID: 10662860]
Hardie, D.G.; Carling, D.; Carlson, M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem., 1998, 67, 821-855.
[] [PMID: 9759505]
Kronstad, J.; De Maria, A.D.; Funnell, D.; Laidlaw, R.D.; Lee, N.; de Sá, M.M.; Ramesh, M. Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Arch. Microbiol., 1998, 170(6), 395-404.
[] [PMID: 9799282]
Gronover, C.S.; Kasulke, D.; Tudzynski, P.; Tudzynski, B. The role of G protein alpha subunits in the infection process of the gray mold fungus Botrytis cinerea. Mol. Plant Microbe Interact., 2001, 14(11), 1293-1302.
[] [PMID: 11763127]
Klimpel, A.; Gronover, C.S.; Williamson, B.; Stewart, J.A.; Tudzynski, B. The adenylate cyclase (BAC) in Botrytis cinerea is required for full pathogenicity. Mol. Plant Pathol., 2002, 3(6), 439-450.
[] [PMID: 20569351]
Schumacher, J.; Kokkelink, L.; Huesmann, C.; Jimenez-Teja, D.; Collado, I.G.; Barakat, R.; Tudzynski, P.; Tudzynski, B. The cAMP-dependent signaling pathway and its role in conidial germination, growth, and virulence of the gray mold Botrytis cinerea. Mol. Plant Microbe Interact., 2008, 21(11), 1443-1459.
[] [PMID: 18842094]
Doehlemann, G.; Berndt, P.; Hahn, M. Different signalling pathways involving a Galpha protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol. Microbiol., 2006, 59(3), 821-835.
[] [PMID: 16420354]
Xu, J.R.; Hamer, J.E. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev., 1996, 10(21), 2696-2706.
[] [PMID: 8946911]
Xu, J.R. Map kinases in fungal pathogens. Fungal Genet. Biol., 2000, 31(3), 137-152.
[] [PMID: 11273677]
Mey, G.; Held, K.; Scheffer, J.; Tenberge, K.B.; Tudzynski, P. CPMK2, an SLT2-homologous mitogen-activated protein (MAP) kinase, is essential for pathogenesis of Claviceps purpurea on rye: evidence for a second conserved pathogenesis-related MAP kinase cascade in phytopathogenic fungi. Mol. Microbiol., 2002, 46(2), 305-318.
[] [PMID: 12406210]
Jenczmionka, N.J.; Schäfer, W. The Gpmk1 MAP kinase of Fusarium graminearum regulates the induction of specific secreted enzymes. Curr. Genet., 2005, 47(1), 29-36.
[] [PMID: 15549317]
Solomon, P.S.; Waters, O.D.C.; Simmonds, J.; Cooper, R.M.; Oliver, R.P. The Mak2 MAP kinase signal transduction pathway is required for pathogenicity in Stagonospora nodorum. Curr. Genet., 2005, 48(1), 60-68.
[] [PMID: 16028107]
Segmüller, N.; Ellendorf, U.; Tudzynski, B.; Tudzynski, P. BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot. Cell, 2007, 6(2), 211-221.
[] [PMID: 17189492]
Dixon, K.P.; Xu, J.R.; Smirnoff, N.; Talbot, N.J. Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell, 1999, 11(10), 2045-2058.
[] [PMID: 10521531]
Kojima, K.; Bahn, Y.S.; Heitman, J. Calcineurin, Mpk1 and Hog1 MAPK pathways independently control fludioxonil antifungal sensitivity in Cryptococcus neoformans. Microbiology, 2006, 152(Pt 3), 591-604.
[] [PMID: 16514140]
Park, S.M.; Choi, E.S.; Kim, M.J.; Cha, B.J.; Yang, M.S.; Kim, D.H. Characterization of HOG1 homologue, CpMK1, from Cryphonectria parasitica and evidence for hypovirus-mediated perturbation of its phosphorylation in response to hypertonic stress. Mol. Microbiol., 2004, 51(5), 1267-1277.
[] [PMID: 14982623]
Rui, O.; Hahn, M. The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol. Plant Pathol., 2007, 8(2), 173-184.
[] [PMID: 20507489]
González-Rubio, G.; Fernández-Acero, T.; Martín, H.; Molina, M. Mitogen-activated protein kinase phosphatases (MKPs) in fungal signaling: Conservation, function, and regulation. Int. J. Mol. Sci., 2019, 20(7) E1709
[] [PMID: 30959830]
Viaud, M.; Brunet-Simon, A.; Brygoo, Y.; Pradier, J.M.; Levis, C. Cyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporin A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea. Mol. Microbiol., 2003, 50(5), 1451-1465.
[] [PMID: 14651630]
Liu, S.; Hou, Y.; Liu, W.; Lu, C.; Wang, W.; Sun, S. Components of the calcium-calcineurin signaling pathway in fungal cells and their potential as antifungal targets. Eukaryot. Cell, 2015, 14(4), 324-334.
[] [PMID: 25636321]
Gioti, A.; Simon, A.; LePecheur, P.; Giraud, C.; Pradier, J.M.; Viaud, M.; Levis, C. Expression profiling of Botrytis cinerea genes identifies three patterns of up-regulation in Planta and an FKBP12 protein affecting pathogenicity (vol 358, pg 372, 2006). J. Mol. Biol., 2006, 364(3), 550-550.
Harren, K.; Schumacher, J.; Tudzynski, B. The Ca2+/calcineurin-dependent signaling pathway in the gray mold Botrytis cinerea: the role of calcipressin in modulating calcineurin activity. PLoS One, 2012, 7(7) e41761
[] [PMID: 22844520]
Vanetten, H.D.; Sandrock, R.W.; Wasmann, C.C.; Soby, S.D.; Mccluskey, K.; Wang, P. Detoxification of Phytoanticipins and Phytoalexins by Phytopathogenic Fungi. Can. J. Bot., 1995, 73, S518-S525.
Morrissey, J.P.; Osbourn, A.E. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol. Mol. Biol. Rev., 1999, 63(3), 708-724.
[PMID: 10477313]
Thakur, M.; Sohal, B.S. Role of elicitors in inducing resistance in plants against pathogen infection: A review. ISRN Biochem., 2013, 2013 762412
[] [PMID: 25969762]
Diaz, I. Plant defense genes against biotic stresses. Int. J. Mol. Sci., 2018, 19(8)E2446
[] [PMID: 30126226]
Podolak, I.; Galanty, A.; Sobolewska, D. Saponins as cytotoxic agents: a review. Phytochem. Rev., 2010, 9(3), 425-474.
[] [PMID: 20835386]
Bowyer, P.; Clarke, B.R.; Lunness, P.; Daniels, M.J.; Osbourn, A.E. Host range of a plant pathogenic fungus determined by a saponin detoxifying enzyme. Science, 1995, 267(5196), 371-374.
[] [PMID: 7824933]
Martin-Hernandez, A.M.; Dufresne, M.; Hugouvieux, V.; Melton, R.; Osbourn, A. Effects of targeted replacement of the tomatinase gene on the interaction of Septoria lycopersici with tomato plants. Mol. Plant Microbe Interact., 2000, 13(12), 1301-1311.
[] [PMID: 11106022]
Wasmann, C.C.; VanEtten, H.D. Transformation-mediated chromosome loss and disruption of a gene for pisatin demethylase decrease the virulence of Nectria haematococca on pea. Mol. Plant Microbe Interact., 1996, 9(9), 793-803.
Han, Y.; Liu, X.; Benny, U.; Kistler, H.C.; VanEtten, H.D. Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J., 2001, 25(3), 305-314.
[] [PMID: 11208022]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Page: [227 - 244]
Pages: 18
DOI: 10.2174/1389203720666190906165111
Price: $65

Article Metrics

PDF: 14