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Transcription Factor Amr1 Induces Melanin Biosynthesis and Suppresses Virulence in Alternaria brassicicola

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Cho, Yangrae, Srivastava, Akhil, Ohm, Robin A., Lawrence, Christopher B., Wang, Koon-Hui, Grigoriev, Igor V., Marahatta, Sharadchandra P.·2012·PLoS Pathogens
DOI 10.1371/journal.ppat.1002974PMC PMC3486909
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Abstract

Alternaria brassicicola is a successful saprophyte and necrotrophic plant pathogen. Several A. brassicicola genes have been characterized as affecting pathogenesis of Brassica species. To study regulatory mechanisms of pathogenesis, we mined 421 genes in silico encoding putative transcription factors in a machine-annotated, draft genome sequence of A. brassicicola. In this study, targeted gene disruption mutants for 117 of the transcription factor genes were produced and screened. Three of these genes were associated with pathogenesis. Disruption mutants of one gene (AbPacC) were nonpathogenic and another gene (AbVf8) caused lesions less than half the diameter of wild-type lesions. Unexpectedly, mutants of the third gene, Amr1, caused lesions with a two-fold larger diameter than the wild type and complementation mutants. Amr1 is a homolog of Cmr1, a transcription factor that regulates melanin biosynthesis in several fungi. We created gene deletion mutants of Δamr1 and characterized their phenotypes. The Δamr1 mutants used pectin as a carbon source more efficiently than the wild type, were melanin-deficient, and more sensitive to UV light and glucanase digestion. The AMR1 protein was localized in the nuclei of hyphae and in highly melanized conidia during the late stage of plant pathogenesis. RNA-seq analysis revealed that three genes in the melanin biosynthesis pathway, along with the deleted Amr1 gene, were expressed at low levels in the mutants. In contrast, many hydrolytic enzyme-coding genes were expressed at higher levels in the mutants than in the wild type during pathogenesis. The results of this study suggested that a gene important for survival in nature negatively affected virulence, probably by a less efficient use of plant cell-wall materials. We speculate that the functions of the Amr1 gene are important to the success of A. brassicicola as a competitive saprophyte and plant parasite.

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  1. [2]Ciuffetti L, Tuori R, Gaventa J (1997) A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9: 135– 144. 9061946 PMC156906
  2. [3]Del Sorbo G, Scala F, Parrella G, Lorito M, Comparini C, et al (2000) Functional expression of the gene cu, encoding the phytotoxic hydrophobin cerato-ulmin, enables Ophiostoma quercus, a nonpathogen on elm, to cause symptoms of Dutch elm disease. Mol Plant Microbe Interact 13: 43– 53. 10656584
  3. [5]Ito K, Tanaka T, Hatta R, Yamamoto M, Akimitsu K, et al (2004) Dissection of the host range of the fungal plant pathogen Alternaria alternata by modification of secondary metabolism. Mol Microbiol 52: 399– 411. 15066029
  4. [6]Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, et al (2000) Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact 13: 742– 753. 10875335
  5. [7]Spassieva SD, Markham JE, Hille J (2002) The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J 32: 561– 572. 12445127
  6. [8]Tanaka A, Shiotani H, Yamamoto M, Tsuge T (1999) Insertional mutagenesis and cloning of the genes required for biosynthesis of the host-specific AK-toxin in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 12: 691– 702. 10432635
  7. [9]Pedras MS, Chumala PB, Jin W, Islam MS, Hauck DW (2009) The phytopathogenic fungus Alternaria brassicicola: phytotoxin production and phytoalexin elicitation. Phytochemistry 70: 394– 402. 19223049
  8. [10]Hashimoto M, Higuchi Y, Takahashi S, Osada H, Sakaki T, et al (2009) Functional analyses of cytochrome P450 genes responsible for the early steps of brassicicene C biosynthesis. Bioorg Med Chem Lett 19: 5640– 5643. 19700326
  9. [11]Wight WD, Kim KH, Lawrence CB, Walton JD (2009) Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. Mol Plant Microbe Interact 22: 1258– 1267. 19737099
  10. [14]Cho Y, Cramer RA Jr, Kim KH, Davis J, Mitchell TK, et al (2007) The Fus3/Kss1 MAP kinase homolog Amk1 regulates the expression of genes encoding hydrolytic enzymes in Alternaria brassicicola. Fungal Genet Biol 44: 543– 553. 17280842
  11. [15]Cho Y, Kim K-H, La Rota M, Scott D, Santopietro G, et al (2009) Identification of virulence factors by high throughput targeted gene deletion of regulatory genes in Alternaria brassicicola. Mol Microbiol 72: 1316– 1333. 19460100
  12. [16]Craven KD, Velez H, Cho Y, Lawrence CB, Mitchell TK (2008) Anastomosis is required for virulence of the fungal necrotroph Alternaria brassicicola. Eukaryot Cell 7: 675– 683. 18310356 PMC2292617
  13. [17]Kim KH, Willger SD, Park SW, Puttikamonkul S, Grahl N, et al (2009) TmpL, a transmembrane protein required for intracellular redox homeostasis and virulence in a plant and an animal fungal pathogen. PLoS Pathog 5: e1000653. 19893627 PMC2766074
  14. [18]Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, et al (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18: 2836– 2853. 17056706 PMC1626607
  15. [19]Kim K-H, Cho Y, La Rota M, Cramer R, Lawrence C (2007) Functional analysis of the Alternaria brassicicola nonribosomal peptide synthetase gene AbNPS2 reveals a role in conidial cell wall construction. Mol Plant Pathol 8: 23– 39. 20507476
  16. [20]Srivastava A, Ohm RA, Oxiles L, Brooks F, Lawrence CB, et al (2012) A Zinc-Finger-Family Transcription Factor, AbVf19, Is Required for the Induction of a Gene Subset Important for Virulence in Alternaria brassicicola. Mol Plant Microbe Interact 25: 443– 452. 22185468
  17. [21]Eliahu N, Igbaria A, Rose MS, Horwitz BA, Lev S (2007) Melanin biosynthesis in the maize pathogen Cochliobolus heterostrophus depends on two mitogen-activated protein kinases, Chk1 and Mps1, and the transcription factor Cmr1. Eukaryot Cell 6: 421– 429. 17237364 PMC1828933
  18. [22]Tsuji G, Kenmochi Y, Takano Y, Sweigard J, Farrall L, et al (2000) Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and Pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 38: 940– 954. 11123670
  19. [23]Kimura N, Tsuge T (1993) Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol 175: 4427– 4435. 8392512 PMC204883
  20. [24]Thomma BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4: 225– 236. 20569383
  21. [25]Kawamura C, Tsujimoto T, Tsuge T (1999) Targeted disruption of a melanin biosynthesis gene affects conidial development and UV tolerance in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 12: 59– 63. 9885194
  22. [27]Wang Y, Casadevall A (1994) Decreased susceptibility of melanized Cryptococcus neoformans to UV light. Appl Environ Microbiol 60: 3864– 3866. 7986054 PMC201897
  23. [29]Rosas AL, Casadevall A (1997) Melanization affects susceptibility of Cryptococcus neoformans to heat and cold. FEMS Microbiol Lett 153: 265– 272. 9271852
  24. [31]Moriwaki A, Kihara J, Kobayashi T, Tokunaga T, Arase S, et al (2004) Insertional mutagenesis and characterization of a polyketide synthase gene (PKS1) required for melanin biosynthesis in Bipolaris oryzae. FEMS Microbiol Lett 238: 1– 8. 15336395
  25. [32]Takano Y, Kubo Y, Kuroda I, Furusawa I (1997) Temporal transcriptional pattern of three melanin biosynthesis genes, PKS1, SCD1, and THR1, in appressorium-differentiating and nondifferentiating conidia of Colletotrichum lagenarium. Appl Environ Microbiol 63: 351– 354. 16535499 PMC1389113
  26. [33]Kubo Y, Takano Y, Tsuji G, Kenmochi Y, Kuroda I, et al (1998) Expression and regulation of melanin biosynthetic genes during appressorium formation of Collectotrichum lagenarium. In: Kohmoto K, Yoder OC, editors. Molecular Genetics of Host Specific Toxins in Plant Disease. Dordrecht: Kluwer Academic Publishers. pp. 253–260.
  27. [34]Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, et al (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26– 32. 22110030 PMC3245080
  28. [35]Ohm RA, Bradshaw RE, Condon BJ, Feau N, Henrissat B, et al (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog In Press. PMC3516569 23236275
  29. [36]Bateman A, Coin L, Durbin R, Finn RD, Hollich V, et al (2004) The Pfam protein families database. Nucleic Acids Res 32: D138– 141. 14681378 PMC308855
  30. [37]You BJ, Choquer M, Chung KR (2007) The Colletotrichum acutatum gene encoding a putative pH-responsive transcription regulator is a key virulence determinant during fungal pathogenesis on citrus. Mol Plant Microbe Interact 20: 1149– 1160. 17849717
  31. [38]Rollins JA (2003) The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact 16: 785– 795. 12971602
  32. [39]Arechiga-Carvajal ET, Ruiz-Herrera J (2005) The RIM101/pacC homologue from the basidiomycete Ustilago maydis is functional in multiple pH-sensitive phenomena. Eukaryot Cell 4: 999– 1008. 15947192 PMC1151993
  33. [40]Lorang JM, Tuori RP, Martinez JP, Sawyer TL, Redman RS, et al (2001) Green fluorescent protein is lighting up fungal biology. Appl Environ Microbiol 67: 1987– 1994. 11319072 PMC92827
  34. [41]Kihara J, Moriwaki A, Tanaka N, Tanaka C, Ueno M, et al (2008) Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae. FEMS Microbiol Lett 281: 221– 227. 18312572
  35. [42]Son H, Seo YS, Min K, Park AR, Lee J, et al (2011) A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog 7: e1002310. 22028654 PMC3197617
  36. [43]Wong Sak Hoi J, Dumas B (2010) Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryot Cell 9: 480– 485. 20139240 PMC2863410
  37. [44]Penalva MA, Arst HN Jr (2004) Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu Rev Microbiol 58: 425– 451. 15487944
  38. [45]Flaherty JE, Pirttila AM, Bluhm BH, Woloshuk CP (2003) PAC1, a pH-regulatory gene from Fusarium verticillioides. Appl Environ Microbiol 69: 5222– 5227. 12957906 PMC194909
  39. [46]Rollins JA, Dickman MB (2001) pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl Environ Microbiol 67: 75– 81. 11133430 PMC92519
  40. [47]Caracuel Z, Roncero MI, Espeso EA, Gonzalez-Verdejo CI, Garcia-Maceira FI, et al (2003) The pH signaling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol Microbiol 48: 765– 779. 12694620
  41. [48]Kihara J, Moriwaki A, Ito M, Arase S, Honda Y (2004) Expression of THR1, a 1,3,8-trihydroxynaphthalene reductase gene involved in melanin biosynthesis in the phytopathogenic fungus Bipolaris oryzae, is enhanced by near-ultraviolet radiation. Pigment Cell Res 17: 15– 23. 14717841
  42. [50]Kubo Y, Nakamura H, Kobayashi K, Okuno T, Furusawa I (1991) Cloning of a Melanin Biosynthetic Gene Essential for Appressorial Penetration of Colletotrichum lagenarium. Mol Plant Microbe Interact 4: 440– 445. 8672814
  43. [51]Howard RJ, Ferrari MA, Roach DH, Money NP (1991) Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci U S A 88: 11281– 11284. 1837147 PMC53118
  44. [52]Feng B, Wang X, Hauser M, Kaufmann S, Jentsch S, et al (2001) Molecular cloning and characterization of WdPKS1, a gene involved in dihydroxynaphthalene melanin biosynthesis and virulence in Wangiella (Exophiala) dermatitidis. Infect Immun 69: 1781– 1794. 11179356 PMC98085
  45. [53]Langfelder K, Jahn B, Gehringer H, Schmidt A, Wanner G, et al (1998) Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med Microbiol Immunol 187: 79– 89. 9832321
  46. [55]Karkehabadi S, Hansson H, Kim S, Piens K, Mitchinson C, et al (2008) The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1.6 A resolution. J Mol Biol 383: 144– 154. 18723026
  47. [56]Lev S, Horwitz BA (2003) A mitogen-activated protein kinase pathway modulates the expression of two cellulase genes in Cochliobolus heterostrophus during plant infection. Plant Cell 15: 835– 844. 12671080 PMC152332
  48. [57]Cramer RA, La Rota CM, Cho Y, Thon M, Craven KD, et al (2006) Bioinformatic analysis of expressed sequence tags derived from a compatible Alternaria brassicicola-Brassica oleracea interaction. Mol Plant Pathol 7: 113– 124. 20507432
  49. [58]Noda J, Brito N, Gonzalez C (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10: 38. 20184750 PMC2844071
  50. [60]Anderson R, May R (1982) Coevolution of hosts and parasites. Parasitology 85: 411– 426. 6755367
  51. [61]Sacristan S, Garcia-Arenal F (2008) The evolution of virulence and pathogenicity in plant pathogen populations. Mol Plant Pathol 9: 369– 384. 18705877 PMC6640236
  52. [62]Lenski RE, May RM (1994) The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J Theor Biol 169: 253– 265. 7967617
  53. [63]Di Stasio M, Brefort T, Mendoza-Mendoza A, Munch K, Kahmann R (2009) The dual specificity phosphatase Rok1 negatively regulates mating and pathogenicity in Ustilago maydis. Mol Microbiol 73: 73– 88. 19486294
  54. [64]Potter SC, Clarke L, Curwen V, Keenan S, Mongin E, et al (2004) The Ensembl analysis pipeline. Genome Res 14: 934– 941. 15123589 PMC479123
  55. [65]Cho Y, Davis JW, Kim KH, Wang J, Sun QH, et al (2006) A high throughput targeted gene disruption method for Alternaria brassicicola functional genomics using linear minimal element (LME) constructs. Mol Plant Microbe Interact 19: 7– 15. 16404948
  56. [66]Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Dominguez Y, et al (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41: 973– 981. 15465386
  57. [67]Hamer JE, Timberlake WE (1987) Functional organization of the Aspergillus nidulans trpC promoter. Mol Cell Biol 7: 2352– 2359. 3039345 PMC365366
  58. [68]Malonek S, Rojas MC, Hedden P, Gaskin P, Hopkins P, et al (2004) The NADPH-cytochrome P450 reductase gene from Gibberella fujikuroi is essential for gibberellin biosynthesis. J Biol Chem 279: 25075– 25084. 15037621
  59. [69]Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105– 1111. 19289445 PMC2672628
  60. [70]Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. 19261174 PMC2690996
  61. [71]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511– 515. 20436464 PMC3146043

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Authors
Cho, Y., Srivastava, A., Ohm, R. A., Lawrence, C. B., Wang, K.-H., Grigoriev, I. V., & Marahatta, S. P.
Affiliations
  • University of Hawaiʻi at Mānoa (US)
  • Joint Genome Institute (US)
  • Virginia Tech (US)
Corresponding author
Cho, Yangrae
ORCID
Venue
PLoS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2012-10-25
Volume
8
Issue
10
Pages
e1002974
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
DOI
10.1371/journal.ppat.1002974
PMC
PMC3486909
OpenAlex
W2006884119
Cited by
106
References
1
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FWCI
3.39
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Pathogens (publishedVersion, public-domain)
  • Europe PMC (PubMed Central) (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • VTechWorks (Virginia Tech) (submittedVersion)
Funders
  • U.S. Department of Energy (-AC02-05CH11231, 05CH11231, DE AC02 05CH11231, DE-AC02-)
  • U.S. Department of Agriculture (DE-AC02-05CH11231)
  • Joint Genome Institute (AC02-05CH11231, DE–AC02–05CH11231)
  • Office of Science (DEAC02–05CH11231, AC02-05CH11231, DE-AC02, 05CH11231)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Plant Pathogens and Fungal Diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant pathogens and resistance mechanisms
Keywords
Alternaria brassicicola, melanogenesis, fungal virulence, plant pathogenic fungi, saprotrophic fungi, hydrolytic enzymes, UV sensitivity, gene disruption mutants, plant cell wall degradation
MeSH terms
Alternaria, Brassica, Fungal Proteins, Genes, Fungal, Melanins, Mutation, Pectins, Phenotype, Plant Diseases, Transcription Factors, Gene Expression Regulation, Fungal, Gene Deletion

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