1887

Abstract

MADS-box transcription factors (TFs) regulate functionally diverse gene targets in eukaryotes. In select ascomycetes, MADS-box TFs have been shown to play a role in virulence, and vegetative and sexual development. Here, we characterized MADS-box TFs, Mads1 and Mads2, in terms of their roles in secondary metabolism and sexual mating. Sequence analyses showed that and encode TFs with a SRF-type dimerization domain and a MEF2-type dimerization domain, respectively. The and knockout mutants (Fmt1 and Fmt2 strains, respectively) exhibited decreased vegetative growth and FB1 production when compared to the wild-type. Fmt1 showed reduced expression of 14 polyketide synthase (PKS) genes present in the organism, whereas Fmt2 did not display a change in PKS gene expression. Significantly, the deletion of and in the genotype (Fmt4 and Fmt5 strains, respectively) led to strains that failed to produce perithecia and ascospores when crossed with the wild-type strain. Notably, deletion of either gene did not have an effect on the ability of the fungus to colonize maize stalk or kernels. FB1 production and PKS expression data suggest that Mads1 is a broad regulator of secondary metabolism in , and may target regulons upstream of Mads2 to influence FB1 production. In addition, MADS-box TFs in play a critical role in the perithecia development.

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2013-11-01
2020-09-26
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References

  1. Alvarez-Buylla E. R., Pelaz S., Liljegren S. J., Gold S. E., Burgeff C., Ditta G. S., Ribas de Pouplana L., Martínez-Castilla L., Yanofsky M. F..( 2000;). An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci U S A97:5328–5333 [CrossRef][PubMed]
    [Google Scholar]
  2. Barrera L. O., Ren B..( 2006;). The transcriptional regulatory code of eukaryotic cells–insights from genome-wide analysis of chromatin organization and transcription factor binding. Curr Opin Cell Biol18:291–298 [CrossRef][PubMed]
    [Google Scholar]
  3. Bloemendal S., Bernhards Y., Bartho K., Dettmann A., Voigt O., Teichert I., Seiler S., Wolters D. A., Pöggeler S., Kück U..( 2012;). A homologue of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol84:310–323 [CrossRef][PubMed]
    [Google Scholar]
  4. Brown D. W., Yu J. H., Kelkar H. S., Fernandes M., Nesbitt T. C., Keller N. P., Adams T. H., Leonard T. J..( 1996;). Twenty-five coregulated transcripts define a sterigmatocystin gene cluster in Aspergillus nidulans.. Proc Natl Acad Sci U S A93:1418–1422 [CrossRef][PubMed]
    [Google Scholar]
  5. Calvo A. M., Wilson R. A., Bok J. W., Keller N. P..( 2002;). Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev66:447–459 [CrossRef][PubMed]
    [Google Scholar]
  6. Damveld R. A., Arentshorst M., Franken A., vanKuyk P. A., Klis F. M., van den Hondel C. A., Ram A. F. J..( 2005;). The Aspergillus niger MADS-box transcription factor RlmA is required for cell wall reinforcement in response to cell wall stress. Mol Microbiol58:305–319 [CrossRef][PubMed]
    [Google Scholar]
  7. De Bodt S., Raes J., Van de Peer Y., Theissen G..( 2003;). And then there were many: MADS goes genomic. Trends Plant Sci8:475–483 [CrossRef][PubMed]
    [Google Scholar]
  8. De Jong J. C., McCormack B. J., Smirnoff N., Talbot N. J..( 1997;). Glycerol generates turgor in rice blast. Nature389:244–245 [CrossRef]
    [Google Scholar]
  9. Desjardins A. E..( 2003;). Gibberella from A (venaceae) to Z (eae). Annu Rev Phytopathol41:177–198 [CrossRef][PubMed]
    [Google Scholar]
  10. Dodou E., Treisman R..( 1997;). The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol Cell Biol17:1848–1859[PubMed]
    [Google Scholar]
  11. Duncan K. E., Howard R. J..( 2010;). Biology of maize kernel infection by Fusarium verticillioides.. Mol Plant Microbe Interact23:6–16 [CrossRef][PubMed]
    [Google Scholar]
  12. Flaherty J. E., Woloshuk C. P..( 2004;). Regulation of fumonisin biosynthesis in Fusarium verticillioides by a zinc binuclear cluster-type gene, ZFR1. Appl Environ Microbiol70:2653–2659 [CrossRef][PubMed]
    [Google Scholar]
  13. Flaherty J. E., Pirttilä A. M., Bluhm B. H., Woloshuk C. P..( 2003;). PAC1, a pH-regulatory gene from Fusarium verticillioides.. Appl Environ Microbiol69:5222–5227 [CrossRef][PubMed]
    [Google Scholar]
  14. Fraser J. A., Heitman J..( 2004;). Evolution of fungal sex chromosomes. Mol Microbiol51:299–306 [CrossRef][PubMed]
    [Google Scholar]
  15. Fraser J. A., Heitman J..( 2005;). Chromosomal sex-determining regions in animals, plants and fungi. Curr Opin Genet Dev15:645–651 [CrossRef][PubMed]
    [Google Scholar]
  16. Fu J., Hettler E., Wickes B. L..( 2006;). Split marker transformation increases homologous integration frequency in Cryptococcus neoformans.. Fungal Genet Biol43:200–212 [CrossRef][PubMed]
    [Google Scholar]
  17. Gelderblom W. C. A., Jaskiewicz K., Marasas W. F. O., Thiel P. G., Horak R. M., Vleggaar R., Kriek N. P. J..( 1988;). Fumonisins–novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme.. Appl Environ Microbiol54:1806–1811[PubMed]
    [Google Scholar]
  18. Heintzman N. D., Ren B..( 2007;). The gateway to transcription: identifying, characterizing and understanding promoters in the eukaryotic genome. Cell Mol Life Sci64:386–400 [CrossRef][PubMed]
    [Google Scholar]
  19. Hopwood D. A., Sherman D. H..( 1990;). Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu Rev Genet24:37–66 [CrossRef][PubMed]
    [Google Scholar]
  20. Howard R. J., Ferrari M. A., Roach D. H., Money N. P..( 1991;). Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci U S A88:11281–11284 [CrossRef][PubMed]
    [Google Scholar]
  21. Johnson A. D..( 1995;). Molecular mechanisms of cell-type determination in budding yeast. Curr Opin Genet Dev5:552–558 [CrossRef][PubMed]
    [Google Scholar]
  22. Johnson P. F., McKnight S. L..( 1989;). Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem58:799–839 [CrossRef][PubMed]
    [Google Scholar]
  23. Kim H., Smith J. E., Ridenour J. B., Woloshuk C. P., Bluhm B. H..( 2011;). HXK1 regulates carbon catabolism, sporulation, fumonisin B1 production and pathogenesis in Fusarium verticillioides. Microbiology157:2658–2669 [CrossRef][PubMed]
    [Google Scholar]
  24. Kroken S., Glass N. L., Taylor J. W., Yoder O. C., Turgeon B. G..( 2003;). Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci U S A100:15670–15675 [CrossRef][PubMed]
    [Google Scholar]
  25. Krüger J., Aichinger C., Kahmann R., Bölker M..( 1997;). A MADS-box homologue in Ustilago maydis regulates the expression of pheromone-inducible genes but is nonessential. Genetics147:1643–1652[PubMed]
    [Google Scholar]
  26. Lemon B., Tjian R..( 2000;). Orchestrated response: a symphony of transcription factors for gene control. Genes Dev14:2551–2569 [CrossRef][PubMed]
    [Google Scholar]
  27. Lengeler K. B., Davidson R. C., D’souza C., Harashima T., Shen W. C., Wang P., Pan X. W., Waugh M., Heitman J..( 2000;). Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev64:746–785 [CrossRef][PubMed]
    [Google Scholar]
  28. Leslie J. F., Summerell B. A..( 2006;). The Fusarium Laboratory Manual Ames, IA: Blackwell Publishing; [CrossRef]
    [Google Scholar]
  29. Levin D. E..( 2005;). Cell wall integrity signaling in Saccharomyces cerevisiae.. Microbiol Mol Biol Rev69:262–291 [CrossRef][PubMed]
    [Google Scholar]
  30. Ma L. J., van der Does H. C., Borkovich K. A., Coleman J. J., Daboussi M. J., Di Pietro A., Dufresne M., Freitag M., Grabherr M. et al.( 2010;). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium.. Nature464:367–373 [CrossRef][PubMed]
    [Google Scholar]
  31. Marasas W. F. O., Miller J. D., Riley R. T., Visconti A..( 2001;). Fumonisins – occurrence, toxicology, metabolism and risk assessment. Fusarium: Paul E. Nelson Memorial Symposium332–359 St Paul, MN: American Phytopathological Society;
    [Google Scholar]
  32. Mead J., Bruning A. R., Gill M. K., Steiner A. M., Acton T. B., Vershon A. K..( 2002;). Interactions of the Mcm1 MADS box protein with cofactors that regulate mating in yeast. Mol Cell Biol22:4607–4621 [CrossRef][PubMed]
    [Google Scholar]
  33. Mehrabi R., Ding S., Xu J. R..( 2008;). MADS-box transcription factor mig1 is required for infectious growth in Magnaporthe grisea.. Eukaryot Cell7:791–799 [CrossRef][PubMed]
    [Google Scholar]
  34. Messenguy F., Dubois E..( 2003;). Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene316:1–21 [CrossRef][PubMed]
    [Google Scholar]
  35. Munkvold G. P., Desjardins A. E..( 1997;). Fumonisins in maize - can we reduce their occurrence?. Plant Disease81:556–565 [CrossRef]
    [Google Scholar]
  36. Nelson P. E., Desjardins A. E., Plattner R. D..( 1993;). Fumonisins, mycotoxins produced by fusarium species: biology, chemistry, and significance. Annu Rev Phytopathol31:233–252 [CrossRef][PubMed]
    [Google Scholar]
  37. Nolting N., Pöggeler S..( 2006a;). A STE12 homologue of the homothallic ascomycete Sordaria macrospora interacts with the MADS box protein MCM1 and is required for ascosporogenesis. Mol Microbiol62:853–868 [CrossRef][PubMed]
    [Google Scholar]
  38. Nolting N., Pöggeler S..( 2006b;). A MADS box protein interacts with a mating-type protein and is required for fruiting body development in the homothallic ascomycete Sordaria macrospora.. Eukaryot Cell5:1043–1056 [CrossRef][PubMed]
    [Google Scholar]
  39. Norman C., Runswick M., Pollock R., Treisman R..( 1988;). Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell55:989–1003 [CrossRef][PubMed]
    [Google Scholar]
  40. Passmore S., Elble R., Tye B. K..( 1989;). A protein involved in minichromosome maintenance in yeast binds a transcriptional enhancer conserved in eukaryotes. Genes Dev3:921–935 [CrossRef][PubMed]
    [Google Scholar]
  41. Proctor R. H., Desjardins A. E., Plattner R. D., Hohn T. M..( 1999;). A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet Biol27:100–112 [CrossRef][PubMed]
    [Google Scholar]
  42. Sagaram U. S., Shim W. B..( 2007;). Fusarium verticillioides GBB1, a gene encoding heterotrimeric G protein β subunit, is associated with fumonisin B1 biosynthesis and hyphal development but not with fungal virulence. Mol Plant Pathol8:375–384 [CrossRef][PubMed]
    [Google Scholar]
  43. Sagaram U. S., Butchko R. A. E., Shim W. B..( 2006;). The putative monomeric G-protein GBP1 is negatively associated with fumonisin B1 production in Fusarium verticillioides. Mol Plant Pathol7:381–389 [CrossRef][PubMed]
    [Google Scholar]
  44. Sagaram U. S., Shaw B. D., Shim W. B..( 2007;). Fusarium verticillioides GAP1, a gene encoding a putative glycolipid-anchored surface protein, participates in conidiation and cell wall structure but not virulence. Microbiology153:2850–2861 [CrossRef][PubMed]
    [Google Scholar]
  45. Schwarz-Sommer Z., Huijser P., Nacken W., Saedler H., Sommer H..( 1990;). Genetic control of flower development by homeotic genes in Antirrhinum majus.. Science250:931–936 [CrossRef][PubMed]
    [Google Scholar]
  46. Shim W. B., Woloshuk C. P..( 1999;). Nitrogen repression of fumonisin B1 biosynthesis in Gibberella fujikuroi.. FEMS Microbiol Lett177:109–116 [CrossRef][PubMed]
    [Google Scholar]
  47. Shim W. B., Woloshuk C. P..( 2001;). Regulation of fumonisin B(1) biosynthesis and conidiation in Fusarium verticillioides by a cyclin-like (C-type) gene, FCC1. Appl Environ Microbiol67:1607–1612 [CrossRef][PubMed]
    [Google Scholar]
  48. Shin J. H., Kim J. E., Malapi-Wight M., Choi Y. E., Shaw B. D., Shim W. B..( 2013;). Protein phosphatase 2A regulatory subunits perform distinct functional roles in the maize pathogen Fusarium verticillioides.. Mol Plant Pathol14:518–529 [CrossRef][PubMed]
    [Google Scholar]
  49. Shore P., Sharrocks A. D..( 1995;). The MADS-box family of transcription factors. Eur J Biochem229:1–13 [CrossRef][PubMed]
    [Google Scholar]
  50. Sommer H., Beltrán J. P., Huijser P., Pape H., Lönnig W. E., Saedler H., Schwarz-Sommer Z..( 1990;). Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J9:605–613[PubMed]
    [Google Scholar]
  51. Staunton J., Weissman K. J..( 2001;). Polyketide biosynthesis: a millennium review. Nat Prod Rep18:380–416 [CrossRef][PubMed]
    [Google Scholar]
  52. Stevens R. B..( 1974;). Mycology Guidebook – Mycological Society of America Seattle, WA: University of Washington Press;
    [Google Scholar]
  53. Wang E., Norred W. P., Bacon C. W., Riley R. T., Merrill A. H. Jr.( 1991;). Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme.. J Biol Chem266:14486–14490[PubMed]
    [Google Scholar]
  54. Woloshuk C. P., Shim W.-B..( 2013;). Aflatoxins, fumonisins, and trichothecenes: a convergence of knowledge. FEMS Microbiol Rev37:94–109 [CrossRef][PubMed]
    [Google Scholar]
  55. Wu W., Huang X., Cheng J., Li Z., de Folter S., Huang Z., Jiang X., Pang H., Tao S..( 2011;). Conservation and evolution in and among SRF- and MEF2-type MADS domains and their binding sites. Mol Biol Evol28:501–511 [CrossRef][PubMed]
    [Google Scholar]
  56. Yanofsky M. F., Ma H., Bowman J. L., Drews G. N., Feldmann K. A., Meyerowitz E. M..( 1990;). The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature346:35–39 [CrossRef][PubMed]
    [Google Scholar]
  57. Zhou X. Y., Liu W. D., Wang C. F., Xu Q. J., Wang Y., Ding S. L., Xu J. R..( 2011;). A MADS-box transcription factor MoMcm1 is required for male fertility, microconidium production and virulence in Magnaporthe oryzae.. Mol Microbiol80:33–53 [CrossRef][PubMed]
    [Google Scholar]
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