Septation of infectious hyphae is critical for appressoria formation and virulence in the smut fungus Ustilago maydis

PLoS Pathogens

Volumn 7, Issue 5, 2011, Pages

  Freitag, Johannes ^a   Lanver, Daniel ^b   Böhmer, Christian ^a   Schink, Kay Oliver ^a,c   Bölker, Michael ^a   Sandrock, Björn ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

DRF1 PROTEIN; FUNGAL PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR DON1; INITIATION FACTOR; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN CDC42; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; CYTOKINESIS; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; GENE DELETION; HOST; MUTANT; PLANT TISSUE; USTILAGO MAYDIS; BIOSYNTHESIS; CYTOLOGY; GENE INACTIVATION; GENETICS; MAIZE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; USTILAGO;

FUNGI; USTILAGO MAYDIS;

ACTOMYOSIN; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CDC42 GTP-BINDING PROTEIN; FUNGAL PROTEINS; GENE KNOCKOUT TECHNIQUES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HYPHAE; PLANT DISEASES; PLANT LEAVES; POLYMERASE CHAIN REACTION; SEQUENCE DELETION; SIGNAL TRANSDUCTION; USTILAGO; ZEA MAYS;

EID: 79958046640     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002044     Document Type: Article

References (68)

1. Emmett RW, Parbery DG, (1975) Appressoria. Annu Rev Phytopathol pp. 147-165.
2. Tucker SL, Talbot NJ, (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39: 385-417.
3. Bechinger C, Giebel KF, Schnell M, Leiderer P, Deising HB, et al. (1999) Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285: 1896-1899.
4. Dixon KP, Xu JR, Smirnoff N, Talbot NJ, (1999) Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11: 2045-2058.
5. Kumamoto CA, (2008) Molecular mechanisms of mechanosensing and their roles in fungal contact sensing. Nat Rev Microbiol 6: 667-673.
6. Wilson RA, Talbot NJ, (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7: 185-195.
7. Lanver D, Mendoza-Mendoza A, Brachmann A, Kahmann R, (2010) Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22: 2085-2101.
8. Banuett F, (1992) Ustilago maydis, the delightful blight. Trends Genet 8: 174-180.
9. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
10. Garcia-Muse T, Steinberg G, Pérez-Martin J, (2003) Pheromone-induced G2 arrest in the phytopathogenic fungus Ustilago maydis. Eukaryot Cell 2: 494-500.
11. Steinberg G, Schliwa M, Lehmler C, Bölker M, Kahmann, R, et al. (1998) Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J Cell Sci 111: 2235-2246.
12. Mendoza-Mendoza A, Berndt P, Djamei A, Weise C, Linne U, et al. (2009) Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol Microbiol 71: 895-911.
13. Schirawski J, Böhnert HU, Steinberg G, Snetselaar K, Adamikowa L, et al. (2005) Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17: 3532-3543.
14. Banuett F, Herskowitz I, (1994) Morphological transitions in the life cycle of Ustilago maydis and their genetic control by the a and b loci. Exp Mycol 18: 247-266.
15. Bölker M, Urban M, Kahmann R, (1992) The a mating type locus of U. maydis specifies cell signaling components. Cell 68: 441-450.
16. Kahmann R, Bölker M, (1996) Self/nonself recognition in fungi: old mysteries and simple solutions. Cell 85: 145-148.
17. Kämper J, Reichmann M, Romeis T, Bölker M, Kahmann R, (1995) Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81: 73-83.
18. Heimel K, Scherer M, Schuler D, Kämper J, (2010) The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell 22: 2908-2922.
19. Mahlert M, Leveleki L, Hlubek A, Sandrock B, Bölker M, (2006) Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol Microbiol 59: 567-578.
20. Hlubek A, Schink KO, Mahlert M, Sandrock B, Bölker M, (2008) Selective activation by the guanine nucleotide exchange factor Don1 is a main determinant of Cdc42 signaling specificity in Ustilago maydis. Mol Microbiol 68: 615-623.
21. Sandrock B, Böhmer C, Bölker M, (2006) Dual function of the germinal centre kinase Don3 during mitosis and cytokinesis in Ustilago maydis. Mol Microbiol 62: 655-666.
22. Weinzierl G, Leveleki L, Hassel A, Kost G, Wanner G, et al. (2002) Regulation of cell separation in the dimorphic fungus Ustilago maydis. Mol Microbiol 45: 219-231.
23. Higgs HN, (2005) Formin proteins: a domain-based approach. Trends Biochem Sci 30: 342-353.
24. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD, (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124: 423-435.
25. Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S, et al. (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297: 612-615.
26. Liu W, Sato A, Khadka D, Bharti R, Diaz H, et al. (2008) Mechanism of activation of the Formin protein Daam1. Proc Natl Acad Sci U S A 105: 210-215.
27. Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D, (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4: 626-631.
28. Castrillon DH, Wasserman SA, (1994) Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120: 3367-3377.
29. Chalkia D, Nikolaidis N, Makalowski W, Klein J, Nei M, (2008) Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol Biol Evol 25: 2717-2733.
30. Evangelista M, Zigmond S, Boone C, (2003) Formins: signaling effectors for assembly and polarization of actin filaments. J Cell Sci 116: 2603-2611.
31. Li F, Higgs HN, (2003) The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 13: 1335-1340.
32. Brachmann A, Weinzierl G, Kämper J, Kahmann R, (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42: 1047-1063.
33. Day PR, Anagnostakis SL, (1971) Corn smut dikaryon in culture. Nat New Biol 231: 19-20.
34. Snetselaar KM, Mims CW, (1992) Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84: 193-203.
35. Schmitz HP, Kaufmann A, Köhli M, Laissue PP, Philippsen P, (2006) From function to shape: a novel role of a formin in morphogenesis of the fungus Ashbya gossypii. Mol Biol Cell 17: 130-145.
36. Böhmer C, Böhmer M, Bölker M, Sandrock B, (2008) Cdc42 and the Ste20-like kinase Don3 act independently in triggering cytokinesis in Ustilago maydis. J Cell Sci 121: 143-148.
37. Evangelista M, Blundell K, Longtine MS, Chow CJ, Adames N, et al. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276: 118-122.
38. Böhmer C, Ripp C, Bölker M, (2009) The germinal centre kinase Don3 triggers the dynamic rearrangement of higher-order septin structures during cytokinesis in Ustilago maydis. Mol Microbiol 74: 1484-1496.
39. Alvarez-Tabares I, Perez-Martin J, (2010) Septins from the phyotpathogenic fungus Ustilago maydis are required for proper morphogenesis but dispensable for virulence. PLoS One 5: e12933.
40. Spellig T, Bottin A, Kahmann R, (1996) Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol Gen Genet 252: 503-509.
41. Scherer M, Heimel K, Starke V, Kämper J, (2006) The Clp1 protein is required for clamp formation and pathogenic development of Ustilago maydis. Plant Cell 18: 2388-2401.
42. Evangelista M, Pruyne D, Amberg DC, Boone C, Bretscher A, (2002) Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 4: 260-269.
43. Kikyo M, Tanaka K, Kamei T, Ozaki K, Fujiwara T, et al. (1999) An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 18: 7046-7054.
44. Pruyne D, Bretscher A, (2000) Polarization of cell growth in yeast. The role of the cortical actin cytoskeleton. J Cell Sci 113: 571-585.
45. Imamura H, Tanaka K, Hihara T, Umikawa M, Kamei T, et al. (1997) Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J 16: 2745-2755.
46. Kamei T, Tanaka K, Hihara T, Umikawa M, Imamura H, et al. (1998) Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J Biol Chem 273: 28341-28345.
47. Bathe M, Chang F, (2010) Cytokinesis and the contractile ring in fission yeast: towards a systems-level understanding. Trends Microbiol 18: 38-45.
48. Chang F, Woollard A, Nurse P, (1996) Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J Cell Sci 109: 131-142.
49. Chang F, Drubin D, Nurse P, (1997) cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profiling. J Cell Biol 137: 169-182.
50. Yonetani A, Chang F, (2010) Regulation of Cytokinesis by the forming Cdc12p. Curr Biol 20: 561-566.
51. Olson MF, (2003) Dispatch. GTPase signaling: new functions for Diaphanous-related formins. Curr Biol 13: R360-362.
52. Schirenbeck A, Bretschneider T, Arasada R, Schleicher M, Faix J, (2005) The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat Cell Biol 7: 619-625.
53. Robinow CF, (1963) Observations on cell growth, mitosis, and division in the fungus Basidiobolus ranarum. J Cell Biol 17: 123-152.
54. Ingold CT, (1982) Retraction-septa in various fungi. Trans Br Mycol Soc 79: 373-38.
55. de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ, (1997) Glycerol generates turgor in rice blast. Nature 389: 244-245.
56. Choi W, Dean RA, (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9: 1973-1983.
57. Döhlemann G, Wahl R, Vranes M, de Vries RP, Kämper J, et al. (2008) Establishment of compatibility in the Ustilago maydis/maize pathosystem. J Plant Physiol 165, 29-40.
58. Veneault-Fourrey C, Barooah M, Egan M, Wakley G, Talbot NJ, (2006) Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312: 580-583.
59. Kershaw MJ, Talbot NJ, (2009) Genome-wide functional analysis reveals that infection-assciated fungal autophagy is essential for rice blast disease. Proc Natl Acad Sci U S A 106: 15967-15972.
60. Saunders DG, Dagdas YF, Talbot NJ, (2010) Spatial uncoupling of mitosis and cytokinesis during appressorium-mediated plant infection by the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2417-2428.
61. Christensen JJ, (1963) Corn smut caused by Ustilago maydis. Am. Phytopathol. Soc. Monogr. No 2.
62. Wadsworth P, (2005) Cytokinesis: rho marks the spot. Curr Biol 15: R871-874.
63. Oliferenko S, Chew TG, Balasubramanian MK, (2009) Positioning cytokinesis. Genes Dev 23: 660-674.
64. Schulz B, Banuett F, Dahl M, Schlesinger R, Schäfer W, et al. (1990) The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60: 295-306.
65. Loubradou G, Brachmann A, Feldbrügge M, Kahmann R, (2001) A homologue of the transcriptional repressor Ssn6p antagonizes cAMP signaling in Ustilago maydis. Mol Microbiol 40: 719-730.
66. Brachmann A, König J, Julius C, Feldbrügge M, (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272: 216-226.
67. Bottin A, Kämper J, Kahmann R, (1996) Isolation of a carbon source-regulated gene from Ustilago maydis. Mol Gen Genet 253: 342-352.
68. Böhmer M, Colby T, Böhmer C, Bräutigam A, Schmidt J, et al. (2007) Proteomic analysis of dimorphic transition in the phytopathogenic fungus Ustilago maydis. Proteomics 7: 675-685.