Glycosylphosphatidylinositol-anchored proteins in Fusarium graminearum: Inventory, variability, and virulence

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Rittenour, William R ^a,b   Harris, Steven D ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b Chestnut Brew Works LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETHANOLAMINE PHOSPHOTRANSFERASE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; FUNGAL PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL;

ARTICLE; BIOINFORMATICS; CELL ADHESION; CONIDIUM; CONTROLLED STUDY; FUNGAL CELL WALL; FUNGAL STRAIN; FUNGAL VIRULENCE; FUSARIUM GRAMINEARUM; GENE; GENE DELETION; GENETIC VARIABILITY; GPI7 GENE; GROWTH RATE; MACROCONIDIUM; NONHUMAN; TRANSMISSION ELECTRON MICROSCOPY; WHEAT; AMINO ACID SEQUENCE; BIOLOGY; CHEMISTRY; FUSARIUM; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; SPECIES DIFFERENCE; VIRULENCE;

COMPUTATIONAL BIOLOGY; FUNGAL PROTEINS; FUSARIUM; GLYCOSYLPHOSPHATIDYLINOSITOLS; MUTATION; REPETITIVE SEQUENCES, AMINO ACID; SPECIES SPECIFICITY; TRITICUM; VIRULENCE;

EID: 84896725588     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081603     Document Type: Article

References (51)

1. Barbosa IP, Kemmelmeier C (1993) Chemical composition of the hyphal wall from Fusarium graminearum. Exp Mycol 17: 274-283. doi:10.1006/emyc.1993.1026. (Pubitemid 2029238)
2. de Groot PWJ, Ram AFJ, Klis FM (2005) Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet Biol 42: 657-675. doi:10.1016/j.fgb.2005.04.002. PubMed: 15896991.
3. Schoffelmeer EAM, Klis FM, Sietsma JH, Cornelissen BJ (1999) The cell wall of Fusarium oxysporum. Fungal Genet Biol 27: 275-282. doi:10.1006/fgbi. 1999.1153. PubMed: 10441453. (Pubitemid 29412849)
4. Guo B, Styles CA, Feng Q, Fink GR (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci U S A 97: 12158-12163. doi:10.1073/pnas.220420397. PubMed: 11027318.
5. Mouyna I, Fontaine T, Vai M, Monod M, Fonzi WA et al. (2000) Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 275: 14882-14889. doi:10.1074/jbc.275.20.14882. PubMed: 10809732. (Pubitemid 30337202)
6. Kapteyn JC, Montijn RC, Vink E, de la Cruz J, Llobell A et al. (1996) Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. Glycobiology 6: 337-345. doi:10.1093/glycob/6.3.337. PubMed: 8724141.
7. Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F (2004) 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 337: 243-253. doi:10.1016/j.jmb.2004.01.025. PubMed: 15003443. (Pubitemid 38293395)
8. de Groot PWJ, Brandt BW, Horiuchi H, Ram AFJ, de Koster CG et al. (2009) Comprehensive genomic analysis of cell wall genes in Aspergillus nidulans. Fungal Genet Biol 46: S72-S81. doi:10.1016/j.fgb.2008.07.022. PubMed: 19585695.
9. de Groot PWJ, de Boer W, Cunningham J, Dekker HL, de Jong L et al. (2004) Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot Cell 3: 955-965. doi:10.1128/EC.3.4.955-965.2004. PubMed: 15302828. (Pubitemid 39098871)
10. de Groot PWJ, Hellingwerf KJ, Klis FM (2003) Genome-wide identification of fungal GPI proteins. Yeast 20: 781-796. doi:10.1002/yea.1007. PubMed: 12845604. (Pubitemid 36850044)
11. Levdansky E, Romano J, Shadkchan Y, Sharon H, Verstrepen KJ et al. (2007) Coding tandem repeats generate diversity in Aspergillus fumigatus genes. Eukaryot Cell 6: 1380-1391. doi:10.1128/EC.00229-06. PubMed: 17557878. (Pubitemid 47257707)
12. Linder T, Gustafsson CM (2008) Molecular phylogenetics of ascomycotal adhesins - a novel family of putative cell-surface adhesive proteins in fission yeasts. Fungal Genet Biol 45: 485-497. doi:10.1016/j.fgb.2007.08.002. PubMed: 17870620. (Pubitemid 351308111)
13. Verstrepen KJ, Jansen A, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990. doi:10.1038/ng1618. PubMed: 16086015. (Pubitemid 43086157)
14. Ecker M, Deutzmann R, Lehle L, Mrsa V, Tanner W (2006) Pir proteins of Saccharomyces cerevisiae are attached to β-1,3glucan by a new protein-carbohydrate linkage. J Biol Chem 281: 11523-11529. doi:10.1074/jbc. M600314200. PubMed: 16495216. (Pubitemid 43855408)
15. Vishwakarma RA, Menon AK (2005) Flip-flop of glycosylphosphatidylinositols (GPIs) across the endoplasmic reticulum. Chem Commun 4: 453-455. (Pubitemid 40187658)
16. Vishwakarma RA, Vehring S, Mehta A, Sinha A, Pomorski T et al. (2005) New fluorescent probes reveal that flippase-mediated flip-flop of phosphatidylinositol across the endoplasmic reticulum membrane does not depend on the stereochemistry of the lipid. Org Biomol Chem 3: 1275-1283. doi:10.1039/b500300h. PubMed: 15785818. (Pubitemid 40538248)
17. Zacks MA, Garg N (2006) Recent developments in the molecular, biochemical and functional characterization of GPI8 and the GPI-anchoring mechanism. Mol Membr Biol 23: 209-225. doi:10.1080/09687860600601494. PubMed: 16785205. (Pubitemid 43922333)
18. Bowman SM, Piwowar A, Dabbous MA, Vierula J (2006) Mutational analysis of the glycosylphosphatidylinositol (GPI) anchor pathway demonstrates that GPI-anchored proteins are required for cell wall biogenesis and normal hyphal growth in Neurospora crassa. Eukaryot Cell 5: 587-600. doi:10.1128/EC.5.3.587- 600.2006. PubMed: 16524913.
19. Richard M, de Groot PWJ, Courtin O, Poulain D, Klis FM et al. (2002) GPI7 affects cell-wall protein anchorage in Saccharomyces cerevisiae and Candida albicans. Microbiology 148: 2125-2133. PubMed: 12101300. (Pubitemid 34785296)
20. Li H, Zhou H, Luo Y, Ouyang H, Hu H et al. (2007) Glycosylphosphatidylinositol (GPI) anchor is required in Aspergillus fumigatus for morphogenesis and virulence. Mol Microbiol 64: 1014-1027. doi:10.1111/j.1365-2958.2007.05709.x. PubMed: 17501924. (Pubitemid 46743963)
21. Cox GM, McDade HC, Chen SCA, Tucker SC, Gottfredsson M et al. (2001) Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol Microbiol 39: 166-175. doi:10.1046/j.1365-2958.2001.02236.x. PubMed: 11123698. (Pubitemid 32057686)
22. Ghannoum MA (2000) Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev 13: 122-143. doi:10.1128/CMR.13.1.122- 143.2000. PubMed: 10627494. (Pubitemid 30039346)
23. Ghannoum MA, Spellberg B, Saporito-Irwin SM, Fonzi WA (1995) Reduced virulence of Candida albicans PHR1 mutants. Infect Immun 63: 4528-4530. PubMed: 7591097.
24. Kaur J, Ma B, Cormack BP (2007) A family of glycosylphosphatidylinositol- linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S A 104: 7628-7633. doi:10.1073/pnas.0611195104. PubMed: 17456602. (Pubitemid 47185957)
25. Narasimhan ML, Lee H, Damsz B, Singh NK, Ibeas JI et al. (2003) Overexpression of a cell wall glycoprotein in Fusarium oxysporum increases virulence and resistance to a plant PR-5 protein. Plant J 36: 390-400. doi:10.1046/j.1365-313X.2003.01886.x. PubMed: 14617095. (Pubitemid 37436061)
26. Ahn N, Kim S, Choi W, Im K-H, Lee Y-H (2004) Extracellular matrix protein gene, EMP1, is required for appressorium formation and pathogenicity of the rice blast fungus, Magnaporthe grisea. Mol Cells 17: 166-173. PubMed: 15055545. (Pubitemid 39137062)
27. Rittenour WR, Harris SD (2008) Characterization of Fusarium graminearum Mes1 reveals a role in cell-surface organization and virulence. Fungal Genet Biol 45: 933-946. doi:10.1016/j.fgb.2008.01.007. PubMed: 18339563.
28. Cappellini RA, Peterson JL (1965) Macroconidium formation in submerged cultures by a non-sporulating strain of Gibberella zeae. Mycologia 57: 962-966. doi:10.2307/3756895.
29. Bowden RL, Leslie JF (1999) Sexual recombination in Gibberella zeae. Phytopathology 89: 182-188. doi:10.1094/PHYTO.1999.89.2.182. PubMed: 18944794. (Pubitemid 29068812)
30. Ram AFJ, Klis FM (2006) Identification of fungal cell wall using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1: 2253-2256. doi:10.1038/nprot.2006.397. PubMed: 17406464.
31. Orlean P, Menon AK (2007) GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids. J Lipid Res 48: 993-1011. doi:10.1194/jlr.R700002-JLR200. PubMed: 17361015. (Pubitemid 46708667)
32. Benachour A, Sipos G, Flury I, Reggiori F, Canivenc-Gansel E et al. (1999) Deletion of GPI7, a yeast gene required for addition of a side chain to the glycosylphosphatidylionsitol (GPI) core structure, affects GPI protein transport, remodeling, and cell wall integrity. J Biol Chem 274: 15251-15261. doi:10.1074/jbc.274.21.15251. PubMed: 10329735.
33. Jansen C, von Wettstein D, Schäfer W, Kogel KH, Felk A et al. (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci U S A 102: 16892-16897. doi:10.1073/pnas.0508467102. PubMed: 16263921. (Pubitemid 41688873)
34. Pritsch C, Muehlbauer GJ, Bushness WR, Somers DA, Vance CP (2000) Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Mol Plant-Microbe Interact 13: 159-169. doi:10.1094/MPMI.2000.13.2.159. PubMed: 10659706. (Pubitemid 30061599)
35. Kulkarni RD, Kelkar HS, Dean RA (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28: 118-121. doi:10.1016/S0968-0004(03)00025-2. PubMed: 12633989. (Pubitemid 36293846)
36. Zhang N, Harrex AL, Holland BR, Fenton LE, Cannon RD et al. (2003) Sixty alleles of the ALS7 open reading frame in Candida albicans: ALS7 is a hypermutable contingency locus. Genome Res 13: 2005-2017. doi:10.1101/gr. 1024903. PubMed: 12952872. (Pubitemid 37161758)
37. Fujita M, Yoko-o T, Okamoto M, Jigami Y (2004) GPI7 involved in glycosylphosphatidylinositol biosynthesis in essential for yeast cell separation. J Biol Chem 279: 51869-51879. doi:10.1074/jbc.M405232200. PubMed: 15452134. (Pubitemid 39656554)
38. Richard M, Ibata-Ombetta S, Dromer F, Bordon-Pallier F, Jouault T et al. (2002) Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol Microbiol 44: 841-853. doi:10.1046/j.1365-2958.2002.02926.x. PubMed: 11994163. (Pubitemid 34526593)
39. Kuranda MJ, Robbins PW (1991) Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem 266: 19758-19767. PubMed: 1918080. (Pubitemid 21908292)
40. Mouassite M, Camougrand N, Schwob E, Demaison G, Laclau M et al. (2000) The 'SUN' family: yeast SUN4/SCW3 is involved in cell septation. Yeast 16: 905-919. doi:10.1002/1097-0061(200007)16:10. PubMed: 10870102. (Pubitemid 30466097)
41. Leidich SD, Ibrahim AS, Fu Y, Koul A, Jessup C et al. (1998) Cloning and disruption of caPLB1, a phospholipase B gene involved in the pathogenicity of Candida albicans. J Biol Chem 273: 26078-26086. doi:10.1074/jbc.273.40.26078. PubMed: 9748287. (Pubitemid 28475842)
42. Stintzi A, Heitz T, Prasad V, Wiedemann-Merdinoglu S, Kauffmann S et al. (1993) Plant 'pathogenesis-related' proteins and their role in defense against pathogens. Biochimie 75: 687-706. doi:10.1016/0300-9084(93)90100-7. PubMed: 8286442. (Pubitemid 23305236)
43. Singh NK, Bracker CA, Hasegawa PM, Handa AK, Buckel S et al. (1987) Characterization of osmotin: a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiol 85: 529-536. doi:10.1104/pp.85.2.529. PubMed: 16665731.
44. Verstrepen KJ, Reynolds TB, Fink GR (2004) Origins of variation in the fungal cell surface. Nat Rev Microbiol 2: 533-540. doi:10.1038/nrmicro927. PubMed: 15197389. (Pubitemid 39200029)
45. Apoga D, Jansson H-B, Tunlid A (2001) Adhesion of conidia and germlings of the plant pathogenic fungus Bipolaris sorokiniana to solid surfaces. Mycol Res 103: 1251-1260. (Pubitemid 33119166)
46. Doss RP, Potter SW, Chastagner GA, Christian JK (1993) Adhesion of nongerminated Botrytis cinerea conidia to several substrata. Appl Environ Microbiol 59: 1786-1791. PubMed: 16348954. (Pubitemid 23171551)
47. Hughes HB, Carzaniga R, Rawlings SL, Green JR, O'Connell RJ (1999) Spore surface glycoproteins of Colletotrichum lindemuthianum are recognized by a monoclonal antibody which inhibits adhesion to polystyrene. Microbiol 145: 1927-1936. doi:10.1099/13500872-145-8-1927. PubMed: 10463159. (Pubitemid 29396923)
48. Schumacher CFA, Steiner U, Dehne H-W, Oerke E-C (2008) Localized adhesion of nongerminated Venturia inaequalis conidia to leaves and artificial surfaces. Phytopathol 98: 760-768. doi:10.1094/PHYTO-98-7-0760. PubMed: 18943251. (Pubitemid 352018208)
49. Zelinger E, Hawes CR, Gurr SJ, Dewey FM (2006) Attachment and adhesion of conidia of Stagonospora nodorum to natural and artificial surfaces. Physiol Mol Plant Pathol 68: 209-215. doi:10.1016/j.pmpp.2006.11.002. (Pubitemid 46274152)
50. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29: 877-896. doi:10.1016/j.femsre.2005.01.004. PubMed: 16219510. (Pubitemid 41416842)
51. Goodman CS, Davis GW, Zito K (1997) The many faces of fasciclin II: Genetic analysis reveals multiple roles for a cell adhesion molecule during the generation of neuronal specificity. Cold Spring Harb Symp Quant Biol 62: 479-491. doi:10.1101/SQB.1997.062.01.055. PubMed: 9598382. (Pubitemid 28198567)