Haplo-insufficiency for different genes differentially reduces pathogenicity and virulence in a fungal phytopathogen

Fungal Genetics and Biology

Volumn 49, Issue 1, 2012, Pages 21-29

  Pham, Cau D ^a,b   Yu, Zhanyang ^a,c   Ben Lovely, C ^a   Agarwal, Charu ^a   Myers, David A ^a   Paul, Jinny A ^a   Cooper, Michael ^a   Barati, Michelle ^a   Perlin, Michael H ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Appressorium; Haplo insufficiency; Pathogenicity; Signaling; Ustilago maydis

Indexed keywords

ARTICLE; CELL GROWTH; CELL SEPARATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DIPLOIDY; FUNGAL GENE; FUNGAL PLANT DISEASE; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE EXPRESSION; GENE FUNCTION; GENETIC REGULATION; HAPLOIDY; HAPLOINSUFFICIENCY; HSL7 GENE; NONHUMAN; PDC1 GENE; PDE1 GENE; PHENOTYPE; PRIORITY JOURNAL; RHO1 GENE;

FUNGAL PROTEINS; HYPHAE; PLANT DISEASES; PLOIDIES; USTILAGO; VIRULENCE; VIRULENCE FACTORS; ZEA MAYS;

USTILAGO MAYDIS; ZEA MAYS;

EID: 84856468200     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.11.007     Document Type: Article

References (49)

1. Agarwal C., Schultz D.J., Perlin M.H. Two phosphodiesterases from Ustilago maydis share structural and biochemical properties with non-fungal phosphodiesterases. Front. Mycol. 2010, 1. 10.3389/fmicb.2010.00127.
2. Agarwal, C., Schultz, D.J., Perlin, M.H. Ustilago maydis phosphodiesterases play a role in dimorphic switch and in pathogenicity, in preparation.
3. Arellano M., Coll P.M., Pérez P. RHO GTPases in the control of cell morphology, cell polarity, and actin localization in fission yeast. Microsc. Res. Tech. 1999, 47:51-60.
4. Baek S.T., Han S., Nam M., Kim Y.D., Kim L., Lee H.J., Heo K.S., Lee H., Lee M., Park S.K., Maeng P.J., Park Y., Lee S., Kim D.U., Kim D., Hoe K.L. Genome-wide identification of haploinsufficiency in fission yeast. J. Microbiol. Biotechnol. 2008, 18:1059-1063.
5. Banuett F. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev. Genet. 1995, 29:179-208.
6. Banuett F., Herskowitz I. Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl. Acad. Sci. USA 1989, 86:5878-5882.
7. Bassilana M., Arkowitz R.A. Rac1 and Cdc42 have different roles in Candida albicans development. Eukaryot. Cell 2006, 5:321-329.
8. Bölker M. Ustilago maydis - a valuable model system for the study of fungal dimorphism and virulence. Microbiology 2001, 147:1395-1401.
9. Bölker M., Genin S., Lehmler C., Kahmann R. Genetic regulation of mating and dimorphism in Ustilago maydis. Can. J. Bot. 1995, 73:320-325.
10. Boyce K.J., Kretschmer M., Kronstad J.W. The vtc4 gene influences polyphosphate storage, morphogenesis, and virulence in the maize pathogen Ustilago maydis. Eukaryot. Cell 2006, 5:1399-1409.
11. Brachmann A., Schirawski J., Müller P., Kahmann R. An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J. 2003, 22:2199-2210.
12. Brachmann A., König J., Julius C., Feldbrügge M. A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics 2004, 272:216-226. (Epub 2004 Erratum in: Mol. Genet. Genomics 2004, 272, 488).
13. Castillo-Lluva S., Alvarez-Tabarés I., Weber I., Steinberg G., Pérez-Martín J. Sustained cell polarity and virulence in the phytopathogenic fungus Ustilago maydis depends on an essential cyclin-dependent kinase from the Cdk5/Pho85 family. J. Cell Sci. 2007, 120:1584-1595.
14. Chae H.-D., Lee K., Williams D.A., Gu Y. Cross-talk between RhoH and Rac1 in regulation of actin cytoskeleton and chemotaxis of hematopoietic progenitor cells. Blood 2008, 111:2597-2605.
15. Chiabrando D., Tolosano E. Diamond Blackfan Anemia at the Crossroad between ribosome biogenesis and heme metabolism. Adv. Hematol. 2010, 2010:790632. (Epub 2010 May 5).
16. Deutschbauer A.M., Jaramillo D.F., Proctor M., Kumm J., Hillenmeyer M.E., Davis R.W., Nislow C., Giaever G. Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 2005, 169:1915-1925.
17. Flor-Parra I., Vranes M., Kämper J., Pérez-Martín J. Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin. Plant Cell 2006, 18:2369-2387.
18. Gold S.E., Brogdon S.M., Mayorga M.E., Kronstad J.W. The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 1997, 9:1585-1594.
19. Hillenmeyer M.E., Fung E., Wildenhain J., Pierce S.E., Hoon S., Lee W., Proctor M., St. Onge R.P., Tyers M., Koller D., Altman R.B., Davis R.W., Nislow C., Giaever G. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 2008, 320:362-365.
20. Hirota K., Tanaka K., Ohta K., Yamamoto M. Gef1p and Scd1p, the two GDP-GTP exchange factors for Cdc42p, form a ring structure that shrinks during cytokinesis in Schizosaccharomyces pombe. Mol. Biol. Cell 2003, 14:3617-3627.
21. Holliday R. Ustilago maydis. Handbook of Genetics 1974, 575-595. Plenum, New York. R.C. King (Ed.).
22. Huang N., Lee I., Marcotte E.M., Hurles M.E. Characterising and predicting haploinsufficiency in the human genome. PLoS Genet. 2010, 6(10):e1001154.
23. Ingram D.A., Yang F.C., Travers J.B., Wenning M.J., Hiatt K., New S., Hood A., Shannon K., Williams D.A., Clapp D.W. Genetic and biochemical evidence that haploinsufficiency of the Nf1 tumor suppressor gene modulates melanocyte and mast cell fates in vivo. J. Exp. Med. 2000, 191:181-188.
24. Johnson D.I., Pringle J.R. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 1990, 111:143-152.
25. Kahmann R., Kämper J. Ustilago maydis: how its biology relates to pathogenic development. New Phytologist. 2004, 164:31-42.
26. Köhler J.R., Fink G.R. Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc. Natl. Acad. Sci. USA 1996, 93:13223-13228.
27. Kronstad J.W., Leong S.A. Isolation of two alleles of the b locus of Ustilago maydis. Proc. Natl. Acad. Sci. USA 1989, 86:978-982.
28. Leveleki L., Mahlert M., Sandrock B., Bölker M. The PAK family kinase Cla4 is required for budding and morphogenesis in Ustilago maydis. Mol. Microbiol. 2004, 54:396-406.
29. Lovely C.B., Aulakh K.B., Perlin M.H. Role of Hsl7 in morphology and pathogenicity and its interaction with other signaling components in the plant pathogen Ustilago maydis. Eukaryot. Cell 2011, 10.
30. Mahlert M., Leveleki K., Hlubek A., Sandrock B., Bölker M. Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol. Microbiol. 2006, 59:567-578.
31. Menotta M., Amicucci A., Basili G., Rivero F., Polidori E., Sisti D., Stocchi V. Molecular characterization of the small GTPase CDC42 in the ectomycorrhizal fungus Tuber borchii Vittad. Protoplasma 2007, 231:227-237.
32. Mielnichuk N., Pérez-Martín J. 14-3-3 Regulates the G2/M transition in the basidiomycete Ustilago maydis. Fungal Genet. Biol. 2008, 45:1206-1215.
33. 2 detoxification is required for virulence. Plant Cell 2007, 19:2293-2309.
34. Müller P., Weinzierl G., Brachmann A., Feldbrügge M., Kahmann R. Mating and pathogenic development of the smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot. Cell 2003, 2:1187-1199.
35. Nasim M.T., Ghouri A., Patel B., James V., Rudarakanchana N., Morrell N.W., Trembath R.C. Stoichiometric imbalance in the receptor complex contributes to dysfunctional BMPR-II mediated signaling in pulmonary arterial hypertension. Hum. Mol. Genet. 2008, 17:1683-1694.
36. Pham C.D., Yu Z., Sandrock B., Bölker M., Gold S.E., Perlin M.H. Ustilago maydis Rho1 and 14-3-3 homologues participate in pathways controlling cell separation and cell polarity. Eukaryot. Cell 2009, 8:977-989.
37. Scherer M., Heimel K., Starke V., Kämper J. The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 2006, 18:2388-2401.
38. Schirawski J., Böhnert H.U., Steinberg G., Snetselaar K., Adamikowa L., Kahmann R. Endoplasmic Reticulum Glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 2005, 17:3532-3543.
39. Skibbe D.S., Doehlemann G., Fernandes J., Walbot V. Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 2010, 328:89-92. 10.1126/science.1185775.
40. Smith D.G., Garcia-Pedrajas M.D., Hong W., Yu Z., Gold S.E., Perlin M.H. An ste20 homologue in Ustilago maydis plays a role in mating and pathogenicity. Eukaryot. Cell 2004, 3:180-189.
41. Spellig T.M., Bölker M., Lottspeich F., Frank R.W., Kahmann R. Pheromones trigger filamentous growth in Ustilago maydis. EMBO J. 1994, 13:1620-1627.
42. Uhl M.A., Biery M., Craig N., Johnson A.D. Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J. 2003, 22:2668-2678.
43. Urban M., Kahmann R., Bölker M. Identification of the pheromone response element in Ustilago maydis. Mol. Gen. Genet. 1996, 251:31-37.
44. Ushinsky S.C., Harcus D., Ash J., Dignard D., Marcil A., Morchhauser J., Thomas D.Y., Whiteway M., Leberer E. CDC42 is required for polarized growth in human pathogen Candida albicans. Eukaryot. Cell 2002, 1:95-104.
45. Veitia R.A. Exploring the etiology of haploinsufficiency. BioEssays 2002, 24:175-184.
46. 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, 18:225-242.
47. Yamochi W., Tanaka K., Nonaka H., Maeda A., Musha T., Takai Y. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J. Cell Biol. 1994, 125:1077-1093.
48. Yon J., Fried M. Precise gene fusion by PCR. Nucl. Acids Res. 1989, 17:4895.
49. Zheng W., Zhao Z., Chen J., Liu W., Ke H., Zhou J., Lu G., Darvill A.G., Albersheim P., Wu S., Wang Z. A Cdc42 ortholog is required for penetration and virulence of Magnaporthe grisea. Fungal Genet. Biol. 2009, 46:450-560.