The DNA damage response signaling cascade regulates proliferation of the phytopathogenic fungus Ustilago maydis in plantaw

Plant Cell

Volumn 23, Issue 4, 2011, Pages 1654-1665

  de Sena Tomas, Carmen ^a   Fernandez Alvarez, Alfonso ^b   Holloman, William K ^c   Perez Marti ́n, Jose ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; USTILAGO MAYDIS;

EID: 79957684787     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.082552     Document Type: Article

References (40)

1. Banuett, F., and Herskowitz, I. (1996). Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122: 2965-2976.
2. Bonilla, C.Y., Melo, J.A., and Toczyski, D.P. (2008). Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell 30: 267-276.
3. Bosotti, R., Isacchi, A., and Sonnhammer, E.L. (2000). FAT: A novel domain in PIK-related kinases. Trends Biochem. Sci. 25: 225-227.
4. Brachmann, A., Konig, J., Julius, C., and Feldbrugge, M. (2004). A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics 272: 216-226.
5. Brachmann, A., Weinzierl, G., Kamper, J., and Kahmann, R. (2001). Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42: 1047-1063.
6. Brauchle, M., Baumer, K., and Gonczy, P. (2003). Differential activation of the DNA replication checkpoint contributes to asynchrony of cell division in C. elegans embryos. Curr. Biol. 13: 819-827.
7. Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei, A., and Kahmann, R. (2009). Ustilago maydis as a pathogen. Annu. Rev. Phytopathol. 47: 423-445.
8. Brown, A.J., and Casselton, L.A. (2001). Mating in mushrooms: Increasing the chances but prolonging the affair. Trends Genet. 17: 393-400.
9. Casselton, L.A. (2002). Mate recognition in fungi. Heredity 88: 142-147.
10. Casselton, L.A., and Olesnicky, N.S. (1998). Molecular genetics of mating recognition in basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62: 55-70.
11. Castillo-Lluva, S., and Perez-Martin, J. (2005). The induction of the mating program in the phytopathogen Ustilago maydis is controlled by a G1 cyclin. Plant Cell 17: 3544-3560.
12. Chen, E.H., Grote, E., Mohler, W., and Vignery, A. (2007). Cell-cell fusion. FEBS Lett. 581: 2181-2193.
13. Chen, Y., and Sanchez, Y. (2004). Chk1 in the DNA damage response: Conserved roles from yeasts to mammals. DNA Repair (Amst.) 3: 1025-1032.
14. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., and Kahmann, R. (2009). Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog. 5: e1000290.
15. Feldbrugge, M., Kamper, J., Steinberg, G., and Kahmann, R. (2004). Regulation of mating and pathogenic development in Ustilago maydis. Curr. Opin. Microbiol. 7: 666-672.
16. Flor-Parra, I., Castillo-Lluva, S., and Perez-Martin, J. (2007). Polar growth in the infectious hyphae of the phytopathogen Ustilago maydis depends on a virulence-specific cyclin. Plant Cell 19: 3280-3296.
17. Flor-Parra, I., Vranes, M., Kamper, J., and Perez-Martin, J. (2006). Biz1, a zinc finger protein required for plant invasion by Ustilago maydis, regulates the levels of a mitotic cyclin. Plant Cell 18: 2369-2387.
18. Garcia-Muse, T., Steinberg, G., and Perez-Martin, J. (2004). Characterization of B-type cyclins in the smut fungus Ustilago maydis: Roles in morphogenesis and pathogenicity. J. Cell Sci. 117: 487-506.
19. Gladfelter, A., and Berman, J. (2009). Dancing genomes: Fungal nuclear positioning. Nat. Rev. Microbiol. 7: 875-886.
20. Ikeda, K., Nakamura, H., and Matsumoto, N. (2003). Mycelial incompatibility operative in pairings between single basidiospore isolates of Helicobasidium mompa. Mycol. Res. 107: 847-853.
21. Kojic, M., Kostrub, C.F., Buchman, A.R., and Holloman, W.K. (2002). BRCA2 homolog required for proficiency in DNA repair, recombination, and genome stability in Ustilago maydis. Mol. Cell 10: 683-691.
22. Kruger, J., Loubradou, G., Wanner, G., Regenfelder, E., Feldbrugge, M., and Kahmann, R. (2000). Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. Mol. Plant Microbe Interact. 13: 1034-1040.
23. Kues, U. (2000). Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64: 316-353.
24. Kumar, S., Tamura, K., Jakobsen, I.B., and Nei, M. (2001). MEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 17: 1244-1245.
25. Lee, S.C., Ni, M., Li, W., Shertz, C, and Heitman, J. (2010). The evolution of sex: A perspective from the fungal kingdom. Microbiol. Mol. Biol. Rev. 74: 298-340.
26. Mielnichuk, N., and Perez-Martin, J. (2008). 14-3-3 regulates the G2/ M transition in the basidiomycete Ustilago maydis. Fungal Genet. Biol. 45: 1206-1215.
27. Mielnichuk, N., Sgarlata, C, and Perez-Martin, J. (2009). A role for the DNA-damage checkpoint kinase Chk1 in the virulence program of the fungus Ustilago maydis. J. Cell Sci. 122: 4130-4140.
28. Nyberg, K.A., Michelson, R.J., Putnam, C.W., and Weinert, T.A. (2002). Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36: 617-656.
29. Perez-Martin, J. (2009). DNA-damage response in the basidiomycete fungus Ustilago maydis relies in a sole Chk1 -like kinase. DNA Repair (Amst.) 8: 720-731.
30. Ramadan, K., Shevelev, I., and Hubscher, U. (2004). The DNA-polymerase-X family: Controllers of DNA quality? Nat. Rev. Mol. Cell Biol. 5: 1038-1043.
31. Scherer, M., Heimel, K., Starke, V., and Kamper, J. (2006). The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18: 2388-2401.
32. Sgarlata, C., and Perez-Martin, J. (2005). Inhibitory phosphorylation of a mitotic cyclin-dependent kinase regulates the morphogenesis, cell size and virulence of the smut fungus Ustilago maydis. J. Cell Sci. 118: 3607-3622.
33. Sherman, M.H., Kuraishy, A.I., Deshpande, C., Hong, J.S., Cacalano, N.A., Gatti, R.A., Manis, J.P., Damore, M.A., Pellegrini, M., and Teitell, M.A. (2010). AID-induced genotoxic stress promotes B cell differentiation in the germinal center via ATM and LKB1 signaling. Mol. Cell 39: 873-885.
34. Sibon, O.C., Stevenson, V.A., and Theurkauf, W.E. (1997). DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388: 93-97.
35. Soutoglou, E., and Misteli, T. (2008). Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320: 1507- 1510.
36. Straube, A., Weber, I., and Steinberg, G. (2005). A novel mechanism of nuclear envelope break-down in a fungus: Nuclear migration strips off the envelope. EMBO J. 24: 1674-1685.
37. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
38. Toettcher, J.E., Loewer, A., Ostheimer, G.J., Yaffe, M.B., Tidor, B., and Lahav, G. (2009). Distinct mechanisms act in concert to mediate cell cycle arrest. Proc. Natl. Acad. Sci. USA 106: 785-790.
39. Wahl, R., Zahiri, A., and Kamper, J. (2010). The Ustilago maydis b mating type locus controls hyphal proliferation and expression of secreted virulence factors in planta. Mol. Microbiol. 75: 208-220.
40. Zhou, B.B., and Elledge, S.J. (2000). The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.