CoChat
Sign Up
Cited by 81Plant Pathogens and Fungal DiseasesFungal and yeast genetics researchMicrobial Metabolism and Applications

Transcription factor VdCmr1 is required for pigment production, protection from UV irradiation, and regulates expression of melanin biosynthetic genes in Verticillium dahliae

Open access
Wang, Yonglin, Hu, Xiaoping, Fang, Yulin, Anchieta, Amy, Goldman, Polly H., Hernandez, Gustavo, Klosterman, Steven J.·2018·Microbiology
DOI 10.1099/mic.0.000633PMC PMC5982140
Open this paper in CoChat — free account

Abstract

Verticillium dahliae is a soilborne fungus that causes vascular wilt diseases on numerous plant species worldwide. The production of darkly melanized microsclerotia is crucial in the disease cycle of V. dahliae, as these structures allow for long-term survival in soil. Previously, transcriptomic and genomic analysis identified a cluster of genes in V. dahliae that encodes some dihydroxynaphthalene (DHN) melanin biosynthetic pathway homologues found in related fungi. In this study, we explored the roles of cluster-specific transcription factor VdCmr1, as well as two other genes within the cluster encoding a polyketide synthase (VdPKS1) and a laccase (VdLac1), enzymes at initial and endpoint steps in DHN melanin production. The results revealed that VdCmr1 and VdPKS1 are required for melanin production, but neither is required for microsclerotia production. None of the three genes were required for pathogenesis on tobacco and lettuce. Exposure of Δ VdCmr1 and wild-type strains to UV irradiation, or to high temperature (40 °C), revealed an approx. 50 % reduction of survival in the Δ VdCmr1 strain, relative to the wild-type strain, in response to either condition. Expression profiles revealed that expression of some melanin biosynthetic genes are in part dependent on VdCmr1. Combined data indicate VdCmr1 is a key regulator of melanin biosynthesis, and that via regulation of melanogenesis, VdCmr1 affects survival of V. dahliae in response to abiotic threats. We conclude with a model showing regulation of VdCmr1 by a high osmolarity glycerol response (Hog)-type MAP kinase pathway.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1099/mic.0.000633

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 44

  1. [2]Klosterman SJ Atallah ZK Vallad GE Subbarao KV Diversity, pathogenicity, and management of Verticillium species Annu Rev Phytopathol 2009 47 39 62 10.1146/annurev-phyto-080508-081748 19385730 · DOI
  2. [4]Bell AA Wheeler MH Biosynthesis and functions of fungal melanins Annu Rev Phytopathol 1986 24 411 451 10.1146/annurev.py.24.090186.002211 · DOI · Paper page
  3. [5]Chumley FG Genetic analysis of melanin-deficient, nonpathogenic mutants of Magnaporthe grisea Mol Plant-Microbe Interact 1990 3 135 143 10.1094/MPMI-3-135 · DOI · Paper page
  4. [6]Stipanovic RD Bell AA Pentaketide metabolites of Verticillium dahliae. 3. Identification of (-)-3,4-dihydro-3,8-dihydroxy-1(2h)-naphtalenone((-)-vermelone) as a precursor to melanin J Org Chem 1976 41 2468 2469 10.1021/jo00876a026 945335 · DOI
  5. [7]Duressa D Anchieta A Chen D Klimes A Garcia-Pedrajas MD RNA-seq analyses of gene expression in the microsclerotia of Verticillium dahliae BMC Genomics 2013 14 607 10.1186/1471-2164-14-607 24015849 PMC3852263 · DOI
  6. [8]Xiong D Wang Y Ma J Klosterman SJ Xiao S Deep mRNA sequencing reveals stage-specific transcriptome alterations during microsclerotia development in the smoke tree vascular wilt pathogen, Verticillium dahliae BMC Genomics 2014 15 324 10.1186/1471-2164-15-324 24884698 PMC4035056 · DOI
  7. [9]Bell AA Puhalla JE Tolmsoff WJ Stipanovic RD Use of mutants to establish (+)-scytalone as an intermediate in melanin biosynthesis by Verticillium dahliae Can J Microbiol 1976 22 787 799 10.1139/m76-115 945120 · DOI · Paper page
  8. [10]Stipanovic RD Bell AA Pentaketide metabolites of Verticillium dahliae. II. Accumulation of naphthol derivatives by the aberrant-melanin mutant BRM-2 Mycologia 1977 69 164 172 10.2307/3758627 557166 · DOI
  9. [11]Fan R Klosterman SJ Wang C Subbarao KV Xu X Vayg1 is required for microsclerotium formation and melanin production in Verticillium dahliae Fungal Genet Biol 2017 98 1 11 10.1016/j.fgb.2016.11.003 27866941 · DOI
  10. [12]Zhang T Zhang B Hua C Meng P Wang S VdPKS1 is required for melanin formation and virulence in a cotton wilt pathogen Verticillium dahliae Sci China Life Sci 2017 60 868 879 10.1007/s11427-017-9075-3 28755294 · DOI
  11. [13]Klimes A Dobinson KF Thomma BP Klosterman SJ Genomics spurs rapid advances in our understanding of the biology of vascular wilt pathogens in the genus Verticillium Annu Rev Phytopathol 2015 53 181 198 10.1146/annurev-phyto-080614-120224 26047557 · DOI
  12. [14]Wang Y Tian L Xiong D Klosterman SJ Xiao S The mitogen-activated protein kinase gene, VdHog1, regulates osmotic stress response, microsclerotia formation and virulence in Verticillium dahliae Fungal Genet Biol 2016 88 13 23 10.1016/j.fgb.2016.01.011 26812120 · DOI
  13. [15]Tian L Wang Y Yu J Xiong D Zhao H The mitogen-activated protein kinase kinase VdPbs2 ofVerticillium dahliae regulates microsclerotia formation, stress response, and plant infection Front Microbiol 2016 7 1532 10.3389/fmicb.2016.01532 27729908 PMC5037172 · DOI
  14. [16]Tian L Xu J Zhou L Guo W VdMsb regulates virulence and microsclerotia production in the fungal plant pathogen Verticillium dahliae Gene 2014 550 238 244 10.1016/j.gene.2014.08.035 25151308 · DOI
  15. [17]Xiong D Wang Y Tian L Tian C MADS-Box transcription factor VdMcm1 regulates conidiation, microsclerotia formation, pathogenicity, and secondary metabolism of Verticillium dahliae Front Microbiol 2016 7 1192 10.3389/fmicb.2016.01192 27536281 PMC4971026 · DOI
  16. [18]Xiong D Wang Y Tang C Fang Y Zou J VdCrz1 is involved in microsclerotia formation and required for full virulence in Verticillium dahliae Fungal Genet Biol 2015 82 201 212 10.1016/j.fgb.2015.07.011 26235044 · DOI
  17. [19]Tran VT Braus-Stromeyer SA Kusch H Reusche M Kaever A Verticillium transcription activator of adhesion Vta2 suppresses microsclerotia formation and is required for systemic infection of plant roots New Phytol 2014 202 565 581 10.1111/nph.12671 24433459 · DOI
  18. [20]Tsuji G Kenmochi Y Takano Y Sweigard J Farrall L 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 2000 38 940 954 10.1046/j.1365-2958.2000.02181.x 11123670 · DOI · Paper page
  19. [21]Eliahu N Igbaria A Rose MS Horwitz BA Lev S 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 2007 6 421 429 10.1128/EC.00264-06 17237364 PMC1828933 · DOI
  20. [22]Kihara J Moriwaki A Tanaka N Tanaka C Ueno M Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae FEMS Microbiol Lett 2008 281 221 227 10.1111/j.1574-6968.2008.01101.x 18312572 · DOI
  21. [23]Cho Y Srivastava A Ohm RA Lawrence CB Wang KH Transcription factor Amr1 induces melanin biosynthesis and suppresses virulence in Alternaria brassicicola PLoS Pathog 2012 8 e1002974 10.1371/journal.ppat.1002974 23133370 PMC3486909 · DOI · Paper page
  22. [24]Schumacher J DHN melanin biosynthesis in the plant pathogenic fungus Botrytis cinerea is based on two developmentally regulated key enzyme (PKS)-encoding genes Mol Microbiol 2016 99 729 748 10.1111/mmi.13262 26514268 · DOI · Paper page
  23. [25]Zhou Y Yang L Wu M Chen W Li G A single-nucleotide deletion in the transcription factor gene bcsmr1 causes sclerotial-melanogenesis deficiency in Botrytis cinerea Front Microbiol 2017 8 2492 10.3389/fmicb.2017.02492 29312200 PMC5733056 · DOI
  24. [26]Qin QM Vallad GE Wu BM Subbarao KV Phylogenetic analyses of phytopathogenic isolates of Verticillium spp Phytopathology 2006 96 582 592 10.1094/PHYTO-96-0582 18943175 · DOI
  25. [27]Klosterman SJ Subbarao KV Kang S Veronese P Gold SE Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens PLoS Pathog 2011 7 e1002137 10.1371/journal.ppat.1002137 21829347 PMC3145793 · DOI
  26. [28]Paz Z García-Pedrajas MD Andrews DL Klosterman SJ Baeza-Montañez L One step construction of Agrobacterium-recombination-ready-plasmids (OSCAR), an efficient and robust tool for ATMT based gene deletion construction in fungi Fungal Genet Biol 2011 48 677 684 10.1016/j.fgb.2011.02.003 21362493 · DOI
  27. [29]Dobinson KF Grant SJ Kang S Cloning and targeted disruption, via Agrobacterium tumefaciens-mediated transformation, of a trypsin protease gene from the vascular wilt fungus Verticillium dahliae Curr Genet 2004 45 104 110 10.1007/s00294-003-0464-6 14618375 · DOI
  28. [30]Faino L Seidl MF Datema E van den Berg GC Janssen A Single-molecule real-time sequencing combined with optical mapping yields completely finished fungal genome MBio 2015 6 e00936-15 10.1128/mBio.00936-15 26286689 PMC4542186 · DOI
  29. [31]Kabir Z Bhat RG Subbarao KV Comparison of media for recovery of Verticillium dahliae from soil Plant Disease 2004 88 49 55 10.1094/PDIS.2004.88.1.49 30812456 · DOI
  30. [32]Pfaffl MW Horgan GW Dempfle L Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR Nucleic Acids Res 2002 30 e36 10.1093/nar/30.9.e36 11972351 PMC113859 · DOI
  31. [33]Cheng XX Zhao LH Klosterman SJ Feng HJ Feng ZL The endochitinase VDECH from Verticillium dahliae inhibits spore germination and activates plant defense responses Plant Sci 2017 259 12 23 10.1016/j.plantsci.2017.03.002 28483050 · DOI
  32. [34]Sarmiento-Villamil JL García-Pedrajas NE Baeza-Montañez L García-Pedrajas MD The APSES transcription factor Vst1 is a key regulator of development in microsclerotium- and resting mycelium-producing Verticillium species Mol Plant Pathol 2018 19 59 76 10.1111/mpp.12496 27696683 PMC6638171 · DOI
  33. [35]Butler MJ Day AW Fungal melanins: a review Can J Microbiol 1998 44 1115 1136 10.1139/w98-119 · DOI
  34. [36]Brandt WH Morphogenesis in verticillium: effects of light and ultraviolet radiation on microsclerotia and melanin Can J Bot 1964 42 1017 1023 10.1139/b64-094 · DOI
  35. [37]Hawke MA Studies on the Survival of Microsclerotia of Verticillium dahliae Thesis University of Western Ontario Paper 2357, Ontario, Canada 1994
  36. [38]Gessler NN Egorova AS Belozerskaya TA Melanin pigments of fungi under extreme environmental conditions (review) Appl Biochem Microbiol 2014 50 105 113 10.1134/S0003683814020094 25272728 · DOI
  37. [39]Zhong Q Gvozdenovic-Jeremic J Webster P Zhou J Greenberg ML Loss of function of KRE5 suppresses temperature sensitivity of mutants lacking mitochondrial anionic lipids Mol Biol Cell 2005 16 665 675 10.1091/mbc.E04-09-0808 15563612 PMC545902 · DOI
  38. [40]Tamura K Stecher G Peterson D Filipski A Kumar S MEGA6: molecular evolutionary genetics analysis version 6.0 Mol Biol Evol 2013 30 2725 2729 10.1093/molbev/mst197 24132122 PMC3840312 · DOI
  39. [41]Tsuji G Sugahara T Fujii I Mori Y Ebizuka Y Evidence for involvement of two naphthol reductases in the first reduction step of melanin biosynthesis pathway of Colletotrichum lagenarium Mycol Res 2003 107 854 860 10.1017/S0953756203008001 12967213 · DOI
  40. [42]Perpetua NS Kubo Y Yasuda N Takano Y Furusawa I Cloning and characterization of a melanin biosynthetic THR1 reductase gene essential for appressorial penetration of Colletotrichum lagenarium Mol Plant Microbe Interact 1996 9 323 329 10.1094/MPMI-9-0323 8672814 · DOI
  41. [43]Kubo Y Takano Y Endo N Yasuda N Tajima S Cloning and structural analysis of the melanin biosynthesis gene SCD1 encoding scytalone dehydratase in Colletotrichum lagenarium Appl Environ Microbiol 1996 62 4340 4344 8953707 PMC168262
  42. [45]Takano Y Kubo Y Shimizu K Mise K Okuno T Structural analysis of PKS1, a polyketide synthase gene involved in melanin biosynthesis in Colletotrichum lagenarium Mol Gen Genet 1995 249 162 167 10.1007/BF00290362 7500937 · DOI
  43. [46]Tsuji G Fujikawa J Ishida H Horino O Kubo Y Laccase gene LAC1 of Colletotrichum lagenarium is not essential for melanin biosynthesis and pathogenicity J Gen Plant Pathol 2001 67 182 190 10.1007/PL00013009 · DOI
  44. [47]Wang G Liu Z Lin R Li E Mao Z Biosynthesis of antibiotic leucinostatins in bio-control fungus Purpureocillium lilacinum and their inhibition on Phytophthora revealed by genome mining PLoS Pathog 2016 12 e1005685 10.1371/journal.ppat.1005685 27416025 PMC4946873 · DOI

Cited by

Sorted by citations

Authors
Wang, Y., Hu, X., Fang, Y., Anchieta, A., Goldman, P. H., Hernandez, G., & Klosterman, S. J.
Affiliations
  • Beijing Forestry University (CN)
  • Northwest A&F University (CN)
  • Agricultural Research Service (US)
Corresponding author
Klosterman, Steven J.
ORCID
Venue
Microbiology
Publisher
Microbiology Society
Published
2018-04-01
Volume
164
Issue
4
Pages
685-696
ISSN
  • 1350-0872 (ISSN-L)
  • 1465-2080
DOI
10.1099/mic.0.000633
PMC
PMC5982140
OpenAlex
W2788463145
Cited by
81
References
1
Citations by year
2026: 8 · 2025: 7 · 2024: 8 · 2023: 10 · 2022: 20 · 2021: 11 · 2020: 6 · 2019: 9 · 2018: 2
FWCI
3.83
Type
journal article
Language
en
Open access
Licence
Locations
  • Microbiology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
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 › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Metabolism and Applications
Keywords
Verticillium dahliae, transcription factors, melanogenesis, polyketide synthase, laccase, microsclerotia, heat stress, abiotic stress tolerance, gene expression regulation, soil-borne fungal pathogens, vascular wilt
MeSH terms
Fungal Proteins, Melanins, Models, Biological, Naphthols, Plant Diseases, Temperature, Transcription Factors, Ultraviolet Rays, Gene Expression Regulation, Fungal, Gene Deletion, Verticillium, Laccase, Polyketide Synthases

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review