Trehalose 6-phosphate phosphatase is required for development, virulence and mycotoxin biosynthesis apart from trehalose biosynthesis in Fusarium graminearum

Fungal Genetics and Biology

Volumn 63, Issue , 2014, Pages 24-41

  Song, Xiu Shi ^a   Li, He Ping ^a   Zhang, Jing Bo ^a   Song, Bo ^a   Huang, Tao ^a   Du, Xiao Min ^a   Gong, An Dong ^a   Liu, Yi Ke ^a   Feng, Yan Ni ^a   Agboola, Rebecca S ^a   Liao, Yu Cai ^a,b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b National Center of Plant Gene Research Wuhan   (China)

Author keywords

Cell polarity; Development; Fusarium graminearum; Mycotoxin; Trehalose 6 phosphate phosphatase; Virulence

Indexed keywords

CHITIN SYNTHASE; ERGOSTEROL; GUANINE NUCLEOTIDE BINDING PROTEIN; HEXOKINASE; MYCOTOXIN; PHOSPHATASE; TREHALOSE 6 PHOSPHATE PHOSPHATASE; TREHALOSE 6 PHOSPHATE SYNTHETASE; UNCLASSIFIED DRUG; VOMITOXIN;

ARTICLE; BIOSYNTHESIS; CELL POLARITY; CELL STRUCTURE; CELL WALL; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL DEVELOPMENT; FUNGAL GENE; FUNGAL VIRULENCE; FUSARIUM GRAMINEARUM; GENE DELETION; GENE EXPRESSION; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPRODUCTION; SPOROGENESIS; TPS1 GENE; TPS2 GENE; WILD TYPE;

FUNGI; GIBBERELLA ZEAE; SOLANUM TUBEROSUM; TRITICUM AESTIVUM;

CELL POLARITY; DEVELOPMENT; FUSARIUM GRAMINEARUM; MYCOTOXIN; TREHALOSE 6-PHOSPHATE PHOSPHATASE; VIRULENCE;

CELL WALL; FUNGAL PROTEINS; FUSARIUM; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSYLTRANSFERASES; HYPHAE; MUTATION; MYCOTOXINS; PHOSPHORIC MONOESTER HYDROLASES; SPORES, FUNGAL; TREHALOSE; TRITICUM;

EID: 84892483473     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.11.005     Document Type: Article

References (119)

1. Al-Bader N., Vanier G., Liu H., Gravelat F.N., Urb M., Hoareau C.M., Campoli P., Chabot J., Filler S.G., Sheppard D.C. Role of trehalose biosynthesis in Aspergillus fumigatus development, stress response, and virulence. Infect. Immun. 2010, 78:3007-3018.
2. Arellano M., Coll P.M., Yang W., Duran A., Tamanoi F., Perez P. Characterization of the geranylgeranyl transferase type I from Schizosaccharomyces pombe. Mol. Microbiol. 1998, 29:1357-1367.
3. Arisan-Atac I., Wolschek M.F., Kubicek C.P. Trehalose-6-phosphate synthase A affects citrate accumulation by Aspergillus niger under conditions of high glycolytic flux. FEMS Microbiol. Lett. 1996, 140:77-83.
4. Avonce N., Mendoza-Vargas A., Morett E., Iturriaga G. Insights on the evolution of trehalose biosynthesis. BMC Evol. Biol. 2006, 6:109.
5. Babour A., Kabani M., Boisrame A., Beckerich J.M. Characterization of Ire1 in the yeast Yarrowia lipolytica reveals an important role for the Sls1 nucleotide exchange factor in unfolded protein response regulation. Curr. Genet. 2008, 53:337-346.
6. Basu U., Si K., Warner J.R., Maitra U. The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 2001, 21:1453-1462.
7. Bell W., Klaassen P., Ohnacker M., Boller T., Herweijer M., Schoppink P., Van der Zee P., Wiemken A. Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. Eur. J. Biochem. 1992, 209:951-959.
8. Borgia P.T., Miao Y., Dodge C.L. The orlA gene from Aspergillus nidulans encodes a trehalose-6-phosphate phosphatase necessary for normal growth and chitin synthesis at elevated temperatures. Mol. Microbiol. 1996, 20:1287-1296.
9. Boudreau B.A., Larson T.M., Brown D.W., Busman M., Roberts E.S., Kendra D.F., McQuade K.L. Impact of temperature stress and validamycin A on compatible solutes and fumonisin production in F. verticillioides: Role of trehalose-6-phosphate synthase. Fungal Genet. Biol. 2013, 57:1-10.
10. Bowman S.M., Free S.J. The structure and synthesis of the fungal cell wall. BioEssays 2006, 28:799-808.
11. Bugeja H.E., Hynes M.J., Andrianopoulos A. HgrA is necessary and sufficient to drive hyphal growth in the dimorphic pathogen Penicillium marneffei. Mol. Microbiol. 2013, 88:998-1014.
12. Cao Y., Wang Y., Dai B., Wang B., Zhang H., Zhu Z., Xu Y., Jiang Y., Zhang G. Trehalose is an important mediator of Cap1p oxidative stress response in Candida albicans. Biol. Pharm. Bull. 2008, 31:421-425.
13. Chen F., Zhang J., Song X., Yang J., Li H., Tang H., Liao Y.C. Combined metabonomic and quantitative real-time PCR analyses reveal systems metabolic changes of Fusarium graminearum induced by Tri5 gene deletion. J. Proteome Res. 2011, 10:2273-2285.
14. Chen G.S., Wu K.H., Chang J.L. A survey report of food poisons caused by fusarium head blight in wheat. Henan J. Prevent. Med. 2003, 14:366.
15. Chen, L.F., Bai, G.H., Desjardins A.E., 2000. Recent advances in wheat head scab research in China. National Agricultural Library Internet Publication, USDA, <>. http://www.nal.usda.gov/pgdic/WHS/whsindex.html.
16. De Assis L.J., Zingali R.B., Masuda C.A., Rodrigues S.P., Montero-Lomeli M. Pyruvate decarboxylase activity is regulated by the Ser/Thr protein phosphatase Sit4p in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 2013, 13:518-528.
17. Deshaies R.J., Schekman R. SEC62 encodes a putative membrane protein required for protein translocation into the yeast endoplasmic reticulum. J. Cell Biol. 1989, 109:2653-2664.
18. De Silva-Udawatta M.N., Cannon J.F. Roles of trehalose phosphate synthase in yeast glycogen metabolism and sporulation. Mol. Microbiol. 2001, 40:1345-1356.
19. D'Mello J.P.F., Placinta C.M., Macdonald A.M.C. Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Anim. Feed Sci. Technol. 1999, 80:183-205.
20. Dong Y., Steffenson B.J., Mirocha C.J. Analysis of ergosterol in single kernel and ground grain by gas chromatography-mass spectrometry. J. Agric. Food Chem. 2006, 54:4121-4125.
21. Duvick J.P., Rood T., Rao A.G., Marshak D.R. Purification and characterization of a novel antimicrobial peptide from maize (Zea mays L.) kernels. J. Biol. Chem. 1992, 267:18814-18820.
22. Elbein A.D., Pan Y.T., Pastuszak I., Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology 2003, 13:17R-27R.
23. Elliott B., Haltiwanger R.S., Futcher B. Synergy between trehalose and Hsp104 for thermotolerance in Saccharomyces cerevisiae. Genetics 1996, 144:923-933.
24. Fernandez J., Wilson R.A. The sugar sensor, trehalose-6-phosphate synthase (Tps1), regulates primary and secondary metabolism during infection by the rice blast fungus: will Magnaporthe oryzae's ''sweet tooth'' become Its ''Achilles' heel''α. Mycology 2011, 2:46-53.
25. Fernandez J., Wright J.D., Hartline D., Quispe C.F., Madayiputhiya N., Wilson R.A. Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genet. 2012, 8:e1002673.
26. Fiehn O., Kopka J., Trethewey R.N., Willmitzer L. Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Anal. Chem. 2000, 72:3573-3580.
27. Flores C.L., Gancedo C., Petit T. Disruption of Yarrowia lipolytica TPS1 gene encoding trehalose-6-P synthase does not affect growth in glucose but impairs growth at high temperature. PLoS ONE 2011, 6:e23695.
28. Forment J., Mulet J.M., Vicente O., Serrano R. The yeast SR protein kinase Sky1p modulates salt tolerance, membrane potential and the Trk1,2 potassium transporter. Biochim. Biophys. Acta 2002, 1565:36-40.
29. Foster A.J., Jenkinson J.M., Talbot N.J. Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J. 2003, 22:225-235.
30. Fuentes J.L., Datta K., Sullivan S.M., Walker A., Maddock J.R. In vivo functional characterization of the Saccharomyces cerevisiae 60S biogenesis GTPase Nog1. Mol. Genet. Genomics 2007, 278:105-123.
31. +, which affects viability after entry into the stationary phase in Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 2007, 71:3041-3047.
32. Gancedo C., Flores C.L. The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res. 2004, 4:351-359.
33. Goswami R.S., Kistler H.C. Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 2005, 95:1397-1404.
34. Graia F., Berteaux-Lecellier V., Zickler D., Picard M. Ami1, an orthologue of the Aspergillus nidulans apsA gene, is involved in nuclear migration events throughout the life cycle of Podospora anserina. Genetics 2000, 155:633-646.
35. Grauslund M., Lopes J.M., Ronnow B. Expression of GUT1, which encodes glycerol kinase in Saccharomyces cerevisiae, is controlled by the positive regulators Adr1p, Ino2p and Ino4p and the negative regulator Opi1p in a carbon source-dependent fashion. Nucleic Acids Res. 1999, 27:4391-4398.
36. 2 production in Phanerochaete chrysosporium mycelia. Biochem. Biophys. Res. Commun. 1984, 118:437-443.
37. Gurvitz A., Rottensteiner H., Kilpelainen S.H., Hartig A., Hiltunen J.K., Binder M., Dawes I.W., Hamilton B. The Saccharomyces cerevisiae peroxisomal 2,4-dienoyl-CoA reductase is encoded by the oleate-inducible gene SPS19. J. Biol. Chem. 1997, 272:22140-22147.
38. Harris S.D. Morphogenesis in germinating Fusarium graminearum macroconidia. Mycologia 2005, 97:880-887.
39. Hartl L., Gastebois A., Aimanianda V., Latge J.P. Characterization of the GPI-anchored endo beta-1,3-glucanase Eng2 of Aspergillus fumigatus. Fungal Genet. Biol. 2011, 48:185-191.
40. Homan K.T., Glukhova A., Tesmer J.J.G. Regulation of G protein-coupled receptor kinases by phospholipids. Curr. Med. Chem. 2013, 20:39-46.
41. Ichinose H., Kotake T., Tsumuraya Y., Kaneko S. Characterization of an exo-beta-1,3-D-galactanase from Streptomyces avermitilis NBRC14893 acting on arabinogalactan-proteins. Biosci. Biotechnol. Biochem. 2006, 70:2745-2750.
42. Igarashi K., Tani T., Rie K., Masahiro S. Family 3 beta-glucosidase from cellulose-degrading culture of the white-rot fungus Phanerochaete chrysosporium is a glucan 1,3-beta-glucosidase. J. Biosci. Bioeng. 2003, 95:572-576.
43. Jaques A.K., Fukamizo T., Hall D., Barton R.C., Escott G.M., Parkinson T., Hitchcock C.A., Adams D.J. Disruption of the gene encoding the ChiB1 chitinase of Aspergillus fumigatus and characterization of a recombinant gene product. Microbiology 2003, 149:2931-2939.
44. Jazwinski S.M. Rtg2 protein: at the nexus of yeast longevity and aging. FEMS Yeast Res. 2005, 5:1253-1259.
45. Kandror O., DeLeon A., Goldberg A.L. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc. Natl. Acad. Sci. USA 2002, 99:9727-9732.
46. Kim J.E., Lee H.J., Lee J., Kim K.W., Yun S.H., Shim W.B., Lee Y.W. Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Curr. Genet. 2009, 55:449-459.
47. Kitagaki H., Cowart L.A., Matmati N., Vaena de Avalos S., Novgorodov S.A., Zeidan Y.H., Bielawski J., Obeid L.M., Hannun Y.A. Isc1 regulates sphingolipid metabolism in yeast mitochondria. Biochim. Biophys. Acta 2007, 1768:2849-2861.
48. Kulkarni K., Yang J., Zhang Z., Barford D. Multiple factors confer specific Cdc42 and Rac protein activation by dedicator of cytokinesis (DOCK) nucleotide exchange factors. J. Biol. Chem. 2011, 286:25341-25351.
49. Kwon H.B., Yeo E.T., Hahn S.E., Bae S.C., Kim D.Y., Byun M.O. Cloning and characterization of genes encoding trehalose-6-phosphate synthase (TPS1) and trehalose-6-phosphate phosphatase (TPS2) from Zygosaccharomyces rouxii. FEMS Yeast Res. 2003, 3:433-440.
50. Lambrechts M.G., Bauer F.F., Marmur J., Pretorius I.S. Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc. Natl. Acad. Sci. USA 1996, 93:8419-8424.
51. Li F., Palecek S.P. Identification of Candida albicans genes that induce Saccharomyces cerevisiae cell adhesion and morphogenesis. Biotechnol. Prog. 2005, 21:1601-1609.
52. Li L., Chang S.S., Liu Y. RNA interference in filamentous fungi. Cell. Mol. Life Sci. 2010, 67:3849-3863.
53. Li L., Wright S.J., Krystofova S., Park G., Borkovich K.A. Heterotrimeric G protein signaling in filamentous fungi. Annu. Rev. Microbiol. 2007, 61:423-452.
54. Li S., Myung K., Guse D., Donkin B., Proctor R.H., Grayburn W.S., Calvo A.M. FvVE1 regulates filamentous growth, the ratio of microconidia to macroconidia and cell wall formation in Fusarium verticillioides. Mol. Microbiol. 2006, 62:1418-1432.
55. Li X., Zhang J.B., Song B., Li H.P., Xu H.Q., Qu B., Dang F.J., Liao Y.C. Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome p450 gene. Phytopathology 2010, 100:183-191.
56. Liu, D.J., 2001. Breeding wheat for scab resistance-a worldwide hard nut to crack. In: Proceedings of International Conference on Wheat Genetics and Breeding-Perspectives of the 21st Century for Wheat Genetics and Breeding. Agriculture Publisher, Beijing, China, pp. 4-7.
57. Lowe R.G., Lord M., Rybak K., Trengove R.D., Oliver R.P., Solomon P.S. Trehalose biosynthesis is involved in sporulation of Stagonospora nodorum. Fungal Genet. Biol. 2009, 46:381-389.
58. Lu W.Z., Chen S.H., Wang Y.Z. Research on Wheat Scab 2001, Science Publisher, Beijing, China.
59. Maddi A., Fu C., Free S.J. The Neurospora crassa dfg5 and dcw1 genes encode alpha-1,6-mannanases that function in the incorporation of glycoproteins into the cell wall. PLoS ONE 2012, 7:e38872.
60. Maidan M.M., De Rop L., Relloso M., Diez-Orejas R., Thevelein J.M., Van Dijck P. Combined inactivation of the Candida albicans GPR1 and TPS2 genes results in avirulence in a mouse model for systemic infection. Infect. Immun. 2008, 76:1686-1694.
61. Maier F.J., Malz S., Losch A.P., Lacour T., Schafer W. Development of a highly efficient gene targeting system for Fusarium graminearum using the disruption of a polyketide synthase gene as a visible marker. FEMS Yeast Res. 2005, 5:653-662.
62. Mamarabadi M., Jensen B., Lubeck M. Three endochitinase-encoding genes identified in the biocontrol fungus Clonostachys rosea are differentially expressed. Curr. Genet. 2008, 54:57-70.
63. Martin S.G. Microtubule-dependent cell morphogenesis in the fission yeast. Trends Cell Biol. 2009, 19:447-454.
64. Martin-Cuadrado A.B., Encinar del Dedo J., de Medina-Redondo M., Fontaine T., del Rey F., Latge J.P., Vazquez de Aldana C.R. The Schizosaccharomyces pombe endo-1,3-beta-glucanase Eng1 contains a novel carbohydrate binding module required for septum localization. Mol. Microbiol. 2008, 69:188-200.
65. Martinez-Esparza M., Tapia-Abellan A., Vitse-Standaert A., Garcia-Penarrubia P., Arguelles J.C., Poulain D., Jouault T. Glycoconjugate expression on the cell wall of tps1/tps1 trehalose-deficient Candida albicans strain and implications for its interaction with macrophages. Glycobiology 2011, 21:796-805.
66. Marvin M.E., Williams P.H., Cashmore A.M. The Candida albicans CTR1 gene encodes a functional copper transporter. Microbiology 2003, 149:1461-1474.
67. 6 zinc finger gene pro1 involved in fungal sexual development. Fungal Genet. Biol. 2002, 36:107-116.
68. Mitsuda N., Ohme-Takagi M. NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. Plant J. 2008, 56:768-788.
69. Mösch H.U., Fink G.R. Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. Genetics 1997, 145:671-684.
70. Munn A.L., Thanabalu T. Verprolin: a cool set of actin-binding sites and some very HOT prolines. IUBMB Life 2009, 61:707-712.
71. Nasmith C.G., Walkowiak S., Wang L., Leung W.W., Gong Y., Johnston A., Harris L.J., Guttman D.S., Subramaniam R. Tri6 is a global transcription regulator in the phytopathogen Fusarium graminearum. PLoS Pathog. 2011, 7:e1002266.
72. Neiman A.M., Mhaiskar V., Manus V., Galibert F., Dean N. Saccharomyces cerevisiae HOC1, a suppressor of pkc1, encodes a putative glycosyltransferase. Genetics 1997, 145:637-645.
73. Neklesa T.K., Davis R.W. Superoxide anions regulate TORC1 and its ability to bind Fpr1:rapamycin complex. Proc. Natl. Acad. Sci. USA 2008, 105:15166-15171.
74. Ngamskulrungroj P., Himmelreich U., Breger J.A., Wilson C., Chayakulkeeree M., Krockenberger M.B., Malik R., Daniel H.M., Toffaletti D., Djordjevic J.T., Mylonakis E., Meyer W., Perfect J.R. The trehalose synthesis pathway is an integral part of the virulence composite for Cryptococcus gattii. Infect. Immun. 2009, 77:4584-4596.
75. Nicholson P., Rezanoor H.N., Simpson D.R., Joyce D. Differentiation and quantification of the cereal eyespot fungi Tapesia yallundae and Tapesia acuformis using a PCR assay. Plant. Pathol. 1997, 46:842-856.
76. Ono Y., Sorimachi H. Calpains-an elaborate proteolytic system. Biochim. Biophys. Acta 2012, 1824:224-236.
77. Parry D.W., Jenkinson P., McLeod L. Fusarium ear blight (scab) in small grain cereals-a review. Plant. Pathol. 1995, 44:207-238.
78. Petzold E.W., Himmelreich U., Mylonakis E., Rude T., Toffaletti D., Cox G.M., Miller J.L., Perfect J.R. Characterization and regulation of the trehalose synthesis pathway and its importance in the pathogenicity of Cryptococcus neoformans. Infect. Immun. 2006, 74:5877-5887.
79. Proctor R.H., Hohn T.M., McCormick S.P. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant Microbe Interact. 1995, 8:593-601.
80. Proctor R.H., Hohn T.M., McCormick S.P., Desjardins A.E. Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl. Environ. Microbiol. 1995, 61:1923-1930.
81. Purvis J.E., Yomano L.P., Ingram L.O. Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl. Environ. Microbiol. 2005, 71:3761-3769.
82. Puttikamonkul S., Willger S.D., Grahl N., Perfect J.R., Movahed N., Bothner B., Park S., Paderu P., Perlin D.S., Cramer R.A. Trehalose 6-phosphate phosphatase is required for cell wall integrity and fungal virulence but not trehalose biosynthesis in the human fungal pathogen Aspergillus fumigatus. Mol. Microbiol. 2010, 77:891-911.
83. Qu B., Li H.P., Zhang J.B., Huang T., Carter J., Liao Y.C., Nicholson P. Comparison of genetic diversity and pathogenicity of fusarium head blight pathogens from China and Europe by SSCP and seedling assays on wheat. Plant. Pathol. 2008, 57:642-651.
84. Rønnow B., Kielland-Brandt M.C. GUT2, a gene for mitochondrial glycerol 3-phosphate dehydrogenase of Saccharomyces cerevisiae. Yeast 1993, 9:1121-1130.
85. Roy A., Lu C.F., Marykwas D.L., Lipke P.N., Kurjan J. The AGA1 product is involved in cell surface attachment of the Saccharomyces cerevisiae cell adhesion glycoprotein a-Agglutinin. Mol. Cell. Biol. 1991, 11:4196-4206.
86. Ruepp A., Zollner A., Maier D., Albermann K., Hani J., Mokrejs M., Tetko I., Guldener U., Mannhaupt G., Munsterkotter M., Mewes H.W. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004, 32:5539-5545.
87. Sasano Y., Haitani Y., Hashida K., Ohtsu I., Shima J., Takagi H. Simultaneous accumulation of proline and trehalose in industrial baker's yeast enhances fermentation ability in frozen dough. J. Biosci. Bioeng. 2012, 113:592-595.
88. Schaber M., Lindgren A., Schindler K., Bungard D., Kaldis P., Winter E. CAK1 promotes meiosis and spore formation in Saccharomyces cerevisiae in a CDC28-independent fashion. Mol. Cell. Biol. 2002, 22:57-68.
89. Schrempf H. Characteristics of chitin-binding proteins from Streptomycetes. EXS 1999, 87:99-108.
90. Seong K.Y., Pasquali M., Zhou X., Song J., Hilburn K., McCormick S., Dong Y., Xu J.R., Kistler H.C. Global gene regulation by Fusarium transcription factors Tri6 and Tri10 reveals adaptations for toxin biosynthesis. Mol. Microbiol. 2009, 72:354-367.
91. Singer M.A., Lindquist S. Multiple effects of trehalose on protein folding in vitro and in vivo. Mol. Cell 1998, 1:639-648.
92. Snaith H.A., Thompson J., Yates J.R., Sawin K.E. Characterization of Mug33 reveals complementary roles for actin cable-dependent transport and exocyst regulators in fission yeast exocytosis. J. Cell Sci. 2011, 124:2187-2199.
93. Son H., Seo Y.S., Min K., Park A.R., Lee J., Jin J.M., Lin Y., Cao P., Hong S.Y., Kim E.K., Lee S.H., Cho A., Lee S., Kim M.G., Kim Y., Kim J.E., Kim J.C., Choi G.J., Yun S.H., Lim J.Y., Kim M., Lee Y.H., Choi Y.D., Lee Y.W. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog. 2011, 7:e1002310.
94. Song B., Li H.P., Zhang J.B., Wang J.H., Gong A.D., Song X.S., Chen T., Liao Y.C. Type II myosin gene in Fusarium graminearum is required for septation, development, mycotoxin biosynthesis and pathogenicity. Fungal Genet. Biol. 2013, 54:60-70.
95. Strom A.R., Kaasen I. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Mol. Microbiol. 1993, 8:205-210.
96. Su S.S., Mitchell A.P. Identification of functionally related genes that stimulate early meiotic gene expression in yeast. Genetics 1993, 133:67-77.
97. Swinnen E., Wanke V., Roosen J., Smets B., Dubouloz F., Pedruzzi I., Cameroni E., De Virgilio C., Winderickx J. Rim15 and the crossroads of nutrient signalling pathways in Saccharomyces cerevisiae. Cell Div. 2006, 1:3.
98. Thevelein J.M. Regulation of trehalose mobilization in fungi. Microbiol. Rev. 1984, 48:42-59.
99. Thevelein J.M., Hohmann S. Trehalose synthase: guard to the gate of glycolysis in yeastα. Trends Biochem. Sci. 1995, 20:3-10.
100. Tinoco M.L.P., Dias B.B.A., Astta R.C.D., Pamphile J.A., Aragão F.J.L. In vivo trans-specific gene silencing in fungal cells by in planta expression of a double-stranded RNA. BMC Biol. 2010, 8:27.
101. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 2001, 98:5116-5121.
102. Van Dijck P., De Rop L., Szlufcik K., Van Ael E., Thevelein J.M. Disruption of the Candida albicans TPS2 gene encoding trehalose-6-phosphate phosphatase decreases infectivity without affecting hypha formation. Infect. Immun. 2002, 70:1772-1782.
103. Vuorio O.E., Kalkkinen N., Londesborough J. Cloning of two related genes encoding the 56-kDa and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 1993, 216:849-861.
104. Waterman S.R., Park Y.D., Raja M., Qiu J., Hammoud D.A., O'Halloran T.V., Williamson P.R. Role of CTR4 in the Virulence of Cryptococcus neoformans. MBio. 2012, 3. e00285-12.
105. Wendland J., Philippsen P. Cell polarity and hyphal morphogenesis are controlled by multiple rho-protein modules in the filamentous ascomycete Ashbya gossypii. Genetics 2001, 157:601-610.
106. Wilson R.A., Jenkinson J.M., Gibson R.P., Littlechild J.A., Wang Z.Y., Talbot N.J. Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J. 2007, 26:3673-3685.
107. Wilson R.A., Gibson R.P., Quispe C.F., Littlechild J.A., Talbot N.J. An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. Proc. Natl. Acad. Sci. 2010, 107:21902-21907.
108. Windels C.E. Economic and social impacts of fusarium head blight: changing farms and rural communities in the northern great plains. Phytopathology 2000, 90:17-21.
109. Woloshuk C.P., Shim W.B. Aflatoxins, fumonisins, and trichothecenes: a convergence of knowledge. FEMS Microbiol. Rev. 2013, 37:94-109.
110. Wolschek M.F., Kubicek C.P. The filamentous fungus Aspergillus niger contains two "differentially regulated" trehalose-6-phosphate synthase-encoding genes, tpsA and tpsB. J. Biol. Chem. 1997, 272:2729-2735.
111. Wu A.B., Li H.P., Zhao C.S., Liao Y.C. Comparative pathogenicity of Fusarium graminearum isolates from China revealed by wheat coleoptile and floret inoculations. Mycopathologia 2005, 160:75-83.
112. Xu Y.B., Li H.P., Zhang J.B., Song B., Chen F.F., Duan X.J., Xu H.Q., Liao Y.C. Disruption of the chitin synthase gene CHS1 from Fusarium asiaticum results in an altered structure of cell walls and reduced virulence. Fungal Genet. Biol. 2010, 47:205-215.
113. Yuan S.J., Liang P., Wu W.H., Xu D.H., Yang C.Y., Han J.L., Li Z.H. Feature analysis on the evolvement of meteorologic elements during wheat Gibberella pathogen formation period in Hebei, Beijing and Tianjing. Acta Agricul. Boreali-Sinica 2007, 2:220-224.
114. Zakharova K., Tesei D., Marzban G., Dijksterhuis J., Wyatt T., Sterflinger K. Microcolonial fungi on rocks: a life in constant droughtα. Mycopathologia 2012, 10.1007/s11046-012-9592-1.
115. Zaragoza O., Blazquez M.A., Gancedo C. Disruption of the Candida albicans TPS1 gene encoding trehalose-6-phosphate synthase impairs formation of hyphae and decreases infectivity. J. Bacteriol. 1998, 180:3809-3815.
116. Zaragoza O., de Virgilio C., Ponton J., Gancedo C. Disruption in Candida albicans of the TPS2 gene encoding trehalose-6-phosphate phosphatase affects cell integrity and decreases infectivity. Microbiology 2002, 148:1281-1290.
117. Zhan X.L., Hong Y., Zhu T., Mitchell A.P., Deschenes R.J., Guan K.L. Essential functions of protein tyrosine phosphatases PTP2 and PTP3 and RIM11 tyrosine phosphorylation in Saccharomyces cerevisiae meiosis and sporulation. Mol. Biol. Cell 2000, 11:663-676.
118. Zhang J.B., Wang J.H., Gong A.D., Chen F.F., Song B., Li X., Li H.P., Peng C.H., Liao Y.C. Natural occurrence of fusarium head blight, mycotoxins and mycotoxin-producing isolates of Fusarium in commercial fields of wheat in Hubei. Plant. Pathol. 2013, 62:92-102.
119. Zhou X., Zhang H., Li G., Shaw B., Xu J.R. The Cyclase-associated protein Cap1 is important for proper regulation of infection-related morphogenesis in Magnaporthe oryzae. PLoS Pathog. 2012, 8:e1002911.