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. 2004 Jan;166(1):113–124. doi: 10.1534/genetics.166.1.113

REN1 is required for development of microconidia and macroconidia, but not of chlamydospores, in the plant pathogenic fungus Fusarium oxysporum.

Toshiaki Ohara 1, Iori Inoue 1, Fumio Namiki 1, Hitoshi Kunoh 1, Takashi Tsuge 1
PMCID: PMC1470687  PMID: 15020411

Abstract

The filamentous fungus Fusarium oxysporum is a soil-borne facultative parasite that causes economically important losses in a wide variety of crops. F. oxysporum exhibits filamentous growth on agar media and undergoes asexual development producing three kinds of spores: microconidia, macroconidia, and chlamydospores. Ellipsoidal microconidia and falcate macroconidia are formed from phialides by basipetal division; globose chlamydospores with thick walls are formed acrogenously from hyphae or by the modification of hyphal cells. Here we describe rensa, a conidiation mutant of F. oxysporum, obtained by restriction-enzyme-mediated integration mutagenesis. Molecular analysis of rensa identified the affected gene, REN1, which encodes a protein with similarity to MedA of Aspergillus nidulans and Acr1 of Magnaporthe grisea. MedA and Acr1 are presumed transcription regulators involved in conidiogenesis in these fungi. The rensa mutant and REN1-targeted strains lack normal conidiophores and phialides and form rod-shaped, conidium-like cells directly from hyphae by acropetal division. These mutants, however, exhibit normal vegetative growth and chlamydospore formation. Nuclear localization of Ren1 was verified using strains expressing the Ren1-green fluorescent protein fusions. These data strongly suggest that REN1 encodes a transcription regulator required for the correct differentiation of conidiogenesis cells for development of microconidia and macroconidia in F. oxysporum.

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Selected References

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  1. Adams T. H., Wieser J. K., Yu J. H. Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev. 1998 Mar;62(1):35–54. doi: 10.1128/mmbr.62.1.35-54.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. An Z., Farman M. L., Budde A., Taura S., Leong S. A. New cosmid vectors for library construction, chromosome walking and restriction mapping in filamentous fungi. Gene. 1996 Oct 17;176(1-2):93–96. doi: 10.1016/0378-1119(96)00225-9. [DOI] [PubMed] [Google Scholar]
  3. Andrianopoulos A., Timberlake W. E. The Aspergillus nidulans abaA gene encodes a transcriptional activator that acts as a genetic switch to control development. Mol Cell Biol. 1994 Apr;14(4):2503–2515. doi: 10.1128/mcb.14.4.2503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aramayo R., Timberlake W. E. The Aspergillus nidulans yA gene is regulated by abaA. EMBO J. 1993 May;12(5):2039–2048. doi: 10.1002/j.1460-2075.1993.tb05853.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Borneman A. R., Hynes M. J., Andrianopoulos A. The abaA homologue of Penicillium marneffei participates in two developmental programmes: conidiation and dimorphic growth. Mol Microbiol. 2000 Dec;38(5):1034–1047. doi: 10.1046/j.1365-2958.2000.02202.x. [DOI] [PubMed] [Google Scholar]
  6. Boylan M. T., Mirabito P. M., Willett C. E., Zimmerman C. R., Timberlake W. E. Isolation and physical characterization of three essential conidiation genes from Aspergillus nidulans. Mol Cell Biol. 1987 Sep;7(9):3113–3118. doi: 10.1128/mcb.7.9.3113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Busby T. M., Miller K. Y., Miller B. L. Suppression and enhancement of the Aspergillus nidulans medusa mutation by altered dosage of the bristle and stunted genes. Genetics. 1996 May;143(1):155–163. doi: 10.1093/genetics/143.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Caelles C., Delseny M., Puigdomènech P. The hydroxyproline-rich glycoprotein gene from Oryza sativa. Plant Mol Biol. 1992 Feb;18(3):617–619. doi: 10.1007/BF00040682. [DOI] [PubMed] [Google Scholar]
  9. Chang Y. C., Timberlake W. E. Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics. 1993 Jan;133(1):29–38. doi: 10.1093/genetics/133.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cole G. T. Models of cell differentiation in conidial fungi. Microbiol Rev. 1986 Jun;50(2):95–132. doi: 10.1128/mr.50.2.95-132.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Couteaudier Y., Alabouvette C. Survival and inoculum potential of conidia and chlamydospores of Fusarium oxysporum f.sp. lini in soil. Can J Microbiol. 1990 Aug;36(8):551–556. doi: 10.1139/m90-096. [DOI] [PubMed] [Google Scholar]
  12. Galagan James E., Calvo Sarah E., Borkovich Katherine A., Selker Eric U., Read Nick D., Jaffe David, FitzHugh William, Ma Li-Jun, Smirnov Serge, Purcell Seth. The genome sequence of the filamentous fungus Neurospora crassa. Nature. 2003 Apr 24;422(6934):859–868. doi: 10.1038/nature01554. [DOI] [PubMed] [Google Scholar]
  13. Gems D. H., Clutterbuck A. J. Enhancers of conidiation mutants in Aspergillus nidulans. Genetics. 1994 May;137(1):79–85. doi: 10.1093/genetics/137.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gritz L., Davies J. Plasmid-encoded hygromycin B resistance: the sequence of hygromycin B phosphotransferase gene and its expression in Escherichia coli and Saccharomyces cerevisiae. Gene. 1983 Nov;25(2-3):179–188. doi: 10.1016/0378-1119(83)90223-8. [DOI] [PubMed] [Google Scholar]
  15. Hamer J. E., Valent B., Chumley F. G. Mutations at the smo genetic locus affect the shape of diverse cell types in the rice blast fungus. Genetics. 1989 Jun;122(2):351–361. doi: 10.1093/genetics/122.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Han S., Navarro J., Greve R. A., Adams T. H. Translational repression of brlA expression prevents premature development in Aspergillus. EMBO J. 1993 Jun;12(6):2449–2457. doi: 10.1002/j.1460-2075.1993.tb05899.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Inoue Iori, Namiki Fumio, Tsuge Takashi. Plant colonization by the vascular wilt fungus Fusarium oxysporum requires FOW1, a gene encoding a mitochondrial protein. Plant Cell. 2002 Aug;14(8):1869–1883. doi: 10.1105/tpc.002576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kimura A., Takano Y., Furusawa I., Okuno T. Peroxisomal metabolic function is required for appressorium-mediated plant infection by Colletotrichum lagenarium. Plant Cell. 2001 Aug;13(8):1945–1957. doi: 10.1105/TPC.010084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kimura N., Tsuge T. Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol. 1993 Jul;175(14):4427–4435. doi: 10.1128/jb.175.14.4427-4435.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kuspa A., Loomis W. F. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8803–8807. doi: 10.1073/pnas.89.18.8803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lau G. W., Hamer J. E. Acropetal: a genetic locus required for conidiophore architecture and pathogenicity in the rice blast fungus. Fungal Genet Biol. 1998 Jun-Jul;24(1-2):228–239. doi: 10.1006/fgbi.1998.1053. [DOI] [PubMed] [Google Scholar]
  22. Lu S., Lyngholm L., Yang G., Bronson C., Yoder O. C., Turgeon B. G. Tagged mutations at the Tox1 locus of Cochliobolus heterostrophus by restriction enzyme-mediated integration. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12649–12653. doi: 10.1073/pnas.91.26.12649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marshall M. A., Timberlake W. E. Aspergillus nidulans wetA activates spore-specific gene expression. Mol Cell Biol. 1991 Jan;11(1):55–62. doi: 10.1128/mcb.11.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Miller K. Y., Wu J., Miller B. L. StuA is required for cell pattern formation in Aspergillus. Genes Dev. 1992 Sep;6(9):1770–1782. doi: 10.1101/gad.6.9.1770. [DOI] [PubMed] [Google Scholar]
  25. Mirabito P. M., Adams T. H., Timberlake W. E. Interactions of three sequentially expressed genes control temporal and spatial specificity in Aspergillus development. Cell. 1989 Jun 2;57(5):859–868. doi: 10.1016/0092-8674(89)90800-3. [DOI] [PubMed] [Google Scholar]
  26. Mullaney E. J., Hamer J. E., Roberti K. A., Yelton M. M., Timberlake W. E. Primary structure of the trpC gene from Aspergillus nidulans. Mol Gen Genet. 1985;199(1):37–45. doi: 10.1007/BF00327506. [DOI] [PubMed] [Google Scholar]
  27. Namiki F., Matsunaga M., Okuda M., Inoue I., Nishi K., Fujita Y., Tsuge T. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol Plant Microbe Interact. 2001 Apr;14(4):580–584. doi: 10.1094/MPMI.2001.14.4.580. [DOI] [PubMed] [Google Scholar]
  28. Namiki F., Shiomi T., Kayamura T., Tsuge T. Characterization of the formae speciales of Fusarium oxysporum causing wilts of cucurbits by DNA fingerprinting with nuclear repetitive DNA sequences. Appl Environ Microbiol. 1994 Aug;60(8):2684–2691. doi: 10.1128/aem.60.8.2684-2691.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nishimura M., Hayashi N., Jwa N. S., Lau G. W., Hamer J. E., Hasebe A. Insertion of the LINE retrotransposon MGL causes a conidiophore pattern mutation in Magnaporthe grisea. Mol Plant Microbe Interact. 2000 Aug;13(8):892–894. doi: 10.1094/MPMI.2000.13.8.892. [DOI] [PubMed] [Google Scholar]
  30. Okuda M., Ikeda K., Namiki F., Nishi K., Tsuge T. Tfo1: an Ac-like transposon from the plant pathogenic fungus Fusarium oxysporum. Mol Gen Genet. 1998 Jun;258(6):599–607. doi: 10.1007/s004380050773. [DOI] [PubMed] [Google Scholar]
  31. Prade R. A., Timberlake W. E. The Aspergillus nidulans brlA regulatory locus consists of overlapping transcription units that are individually required for conidiophore development. EMBO J. 1993 Jun;12(6):2439–2447. doi: 10.1002/j.1460-2075.1993.tb05898.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. SANDERSON K. E., SRB A. M. HETEROKARYOSIS AND PARASEXUALITY IN THE FUNGUS ASCOCHYTA IMPERFECTA. Am J Bot. 1965 Jan;52:72–81. [PubMed] [Google Scholar]
  33. Sewall T. C., Mims C. W., Timberlake W. E. abaA controls phialide differentiation in Aspergillus nidulans. Plant Cell. 1990 Aug;2(8):731–739. doi: 10.1105/tpc.2.8.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shi Z., Christian D., Leung H. Interactions between spore morphogenetic mutations affect cell types, sporulation, and pathogenesis in Magnaporthe grisea. Mol Plant Microbe Interact. 1998 Mar;11(3):199–207. doi: 10.1094/MPMI.1998.11.3.199. [DOI] [PubMed] [Google Scholar]
  35. Springer M. L. Genetic control of fungal differentiation: the three sporulation pathways of Neurospora crassa. Bioessays. 1993 Jun;15(6):365–374. doi: 10.1002/bies.950150602. [DOI] [PubMed] [Google Scholar]
  36. Talbot N. J. Having a blast: exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol. 1995 Jan;3(1):9–16. doi: 10.1016/s0966-842x(00)88862-9. [DOI] [PubMed] [Google Scholar]
  37. Timberlake W. E. Molecular genetics of Aspergillus development. Annu Rev Genet. 1990;24:5–36. doi: 10.1146/annurev.ge.24.120190.000253. [DOI] [PubMed] [Google Scholar]
  38. Wang H., Clark I., Nicholson P. R., Herskowitz I., Stillman D. J. The Saccharomyces cerevisiae SIN3 gene, a negative regulator of HO, contains four paired amphipathic helix motifs. Mol Cell Biol. 1990 Nov;10(11):5927–5936. doi: 10.1128/mcb.10.11.5927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wu J., Miller B. L. Aspergillus asexual reproduction and sexual reproduction are differentially affected by transcriptional and translational mechanisms regulating stunted gene expression. Mol Cell Biol. 1997 Oct;17(10):6191–6201. doi: 10.1128/mcb.17.10.6191. [DOI] [PMC free article] [PubMed] [Google Scholar]

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