CoChat
Sign Up
Cited by 54Plant Pathogens and Fungal DiseasesFungal and yeast genetics researchPlant pathogens and resistance mechanisms

The Verticillium dahliae Sho1‐MAPK pathway regulates melanin biosynthesis and is required for cotton infection

Open access
Li, Jun‐Jiao, Zhou, Lei, Yin, Chun‐Mei, Zhang, Dan‐Dan, Klosterman, Steven J., Wang, Bao‐Li, Song, Jian, Wang, Dan +4 more·2019·Environmental Microbiology
DOI 10.1111/1462-2920.14846PMC PMC6916341
Open this paper in CoChat — free accountOpen PDF

Abstract

Summary: Verticillium dahliae is a soil‐borne fungus that causes vascular wilt on numerous plants worldwide. The fungus survives in the soil for up to 14 years by producing melanized microsclerotia. The protective function of melanin in abiotic stresses is well documented. Here, we found that the V . dahliae tetraspan transmembrane protein VdSho1, a homolog of the Saccharomyces cerevisiae Sho1, acts as an osmosensor, and is required for plant penetration and melanin biosynthesis. The deletion mutant Δ Sho1 was incubated on a cellophane membrane substrate that mimics the plant epidermis, revealing that the penetration of Δ Sho1 strain was reduced compared to the wild‐type strain. Furthermore, VdSho1 regulates melanin biosynthesis by a signalling mechanism requiring a kinase‐kinase signalling module of Vst50‐Vst11‐Vst7. Strains, Δ Vst50 , Δ Vst7 and Δ Vst11 also displayed defective penetration and melanin production like the Δ Sho1 strain. Defects in penetration and melanin production in Δ Sho1 were restored by overexpression of Vst50 , suggesting that Vst50 lies downstream of VdSho1 in the regulatory pathway governing penetration and melanin biosynthesis. Data analyses revealed that the transmembrane portion of VdSho1 was essential for both membrane penetration and melanin production. This study demonstrates that Vst50‐Vst11‐Vst7 module regulates VdSho1‐mediated plant penetration and melanin production in V . dahliae , contributing to virulence.

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 · 10.1111/1462-2920.14846

Cites

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?

  • VdSho1 regulates melanin biosynthesis through the Vst50-Vst11-Vst7 kinase signaling module, thereby enhancing the pathogen's penetration capacity and modulating its pathogenicity in V. dahliae.

    “VdSho1 regulates melanin biosynthesis through the Vst50-Vst11-Vst7 kinase signaling module, thereby enhancing the pathogen’s penetration capacity and modulating its pathogenicity [68].”

    From Fungal Melanin in Plant Pathogens: Complex Biosynthesis Pathways and Diverse Biological Functions (2025) · cites this paper as [68]

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

No references could be resolved yet.

Research works printed but not linked: 67

  1. Bahn, Y.S., Xue, C., Idnurm, A., Rutherford, J.C., Heitman, J., et al (2007) Sensing the environment: lessons from fungi. Nat Rev Microbiol 5: 57– 69. 17170747
  2. Boisnard, S., Ruprich‐Robert, G., Florent, M., Da Silva, B., Chapeland‐Leclerc, F., et al (2008) Role of Sho1p adaptor in the pseudohyphal development, drugs sensitivity, osmotolerance and oxidant stress adaptation in the opportunistic yeast Candida lusitaniae. Yeast 25: 849– 859. 19061190
  3. Butler, M.J., and Day, A.W. (1998) Fungal melanins: A review. Can J Microbiol 44: 1115– 1136.
  4. Chen, J.Y., Liu, C., Gui, Y.J., Si, K.W., Zhang, D.D., et al (2018) Comparative genomics reveals cotton‐specific virulence factors in flexible genomic regions in Verticillium dahliae and evidence of horizontal gene transfer from Fusarium. New Phytol 217: 756– 770. 29084346 PMC5765495
  5. dos Santos, A.G., Marquês, J.T., Carreira, A.C., Castro, I.R., Viana, A.S., et al (2017) The molecular mechanism of Nystatin action is dependent on the membrane biophysical properties and lipid composition. Phys Chem Chem Phys 19: 30078– 30088. 29098221
  6. Duressa, D., Anchieta, A., Chen, D., Klimes, A., Garcia‐Pedrajas, M.D., et al (2013) RNA‐seq analyses of gene expression in the microsclerotia of Verticillium dahliae. BMC Genomics 14: 607. 24015849 PMC3852263
  7. Fang, Y., Klosterman, S.J., Tian, C., and Wang, Y. (2019) Insights into VdCmr1‐mediated protection against high temperature stress and UV irradiation in Verticillium dahliae. Environ Microbiol. 21: 2977– 2996. 10.1111/1462-2920.14695. 31136051 · DOI
  8. Fradin, E.F., and Thomma, B.P. (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo‐atrum. Mol Plant Pathol 7: 71– 86. 20507429
  9. Griffiths, S.A., Cox, R.J., Overdijk, E.J.R., Mesarich, C.H., Saccomanno, B., et al (2018) Assignment of a dubious gene cluster to melanin biosynthesis in the tomato fungal pathogen Cladosporium fulvum. PLoS One 13: e0209600. 30596695 PMC6312243
  10. Gu, Q., Chen, Y., Liu, Y., Zhang, C., and Ma, Z. (2015) The transmembrane protein FgSho1 regulates fungal development and pathogenicity via the MAPK module Ste50‐Ste11‐Ste7 in Fusarium graminearum. New Phytol 206: 315– 328. 25388878
  11. Gui, Y.J., Chen, J.Y., Zhang, D.D., Li, N.Y., Li, T.G., et al (2017) Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate‐binding module 1. Environ Microbiol 19: 1914– 1932. 28205292
  12. Gustin, M.C., Albertyn, J., Alexander, M., and Davenport, K. (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62: 1264– 1300. 9841672 PMC98946
  13. Henson, J.M., Butler, M.J., and Day, A.W. (1999) The dark side of the mycelium: melanins of phytopathogenic fungi. Annu Rev Phytopathol 37: 447– 471. 11701831
  14. Howard, R.J., and Valent, B. (1996) Breaking and entering: host penetration by the fungal rice blast pathogen Magnaporthe grisea. Annu Rev Microbiol 50: 491– 512. 8905089
  15. Hu, X.P., Gurung, S., Short, D.P., Sandoya, G.V., Shang, W.J., et al (2015) Nondefoliating and defoliating strains from cotton correlate with races 1 and 2 of Verticillium dahliae. Plant Dis 99: 150511060006009. 30699524
  16. Inderbitzin, P., and Subbarao, K.V. (2014) Verticillium systematics and evolution: how confusion impedes Verticillium wilt management and how to resolve It. Phytopathology 104: 564– 574. 24548214
  17. Jacobson, E.S. (2000) Pathogenic roles for fungal melanins. Clin Microbiol Rev 13: 708– 717. 11023965 PMC88958
  18. Jin, S., Kanagaraj, A., Verma, D., Lange, T., and Daniell, H. (2011) Release of hormones from conjugates: chloroplast expression of beta‐glucosidase results in elevated phytohormone levels associated with significant increase in biomass and protection from aphids or whiteflies conferred by sucrose esters. Plant Physiol 155: 222– 235. 21068365 PMC3075761
  19. Klimes, A., Dobinson, K.F., Thomma, B.P., and Klosterman, S.J. (2015) Genomics spurs rapid advances in our understanding of the biology of vascular wilt pathogens in the genus Verticillium. Annu Rev Phytopathol 53: 181– 198. 26047557
  20. Klosterman, S.J., Atallah, Z.K., Vallad, G.E., and Subbarao, K.V. (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47: 39– 62. 19385730
  21. Kou, Y., and Naqvi, N.I. (2016) Surface sensing and signaling networks in plant pathogenic fungi. Sem Cell Dev Biol 57: 84– 92. 27133541
  22. Lanver, D., Mendoza‐Mendoza, A., Brachmann, A., and Kahmann, R. (2010) Sho1 and Msb2‐related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22: 2085– 2101. 20587773 PMC2910971
  23. Li, N., Zhang, D.S., Liu, H.S., Yin, C.S., Li, X.X., et al (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999– 3014. 17138695 PMC1693939
  24. Liu, S.Y., Chen, J.Y., Wang, J.L., Li, L., Xiao, H.L., et al (2013) Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating Verticillium dahliae. Gene 529: 307– 316. 23891822
  25. Liu, W., Zhou, X., Li, G., Li, L., Kong, L., et al (2011) Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathogens 7: e1001261. 21283781 PMC3024261
  26. Ma, D., and Li, R. (2013) Current understanding of HOG‐MAPK pathway in Aspergillus fumigatus. Mycopathologia 175: 13– 23. 23161019
  27. Ma, Y., Qiao, J., Liu, W., Wan, Z., Wang, X., et al (2008) The sho1 sensor regulates growth, morphology, and oxidant adaptation in Aspergillus fumigatus but is not essential for development of invasive pulmonary aspergillosis. Infect Immun 76: 1695– 1701. 18227163 PMC2292864
  28. Nosanchuk, J.D., and Casadevall, A. (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5: 203– 223. 12675679
  29. O'Rourke, S.M., and Herskowitz, I. (1998) The Hog1 MAPK prevents cross talk between the HOG and pheromone response MAPK pathways in Saccharomyces cerevisiae. Genes Dev 12: 2874– 2886. 9744864 PMC317168
  30. O'Rourke, S.M., Herskowitz, I., and O'Shea, E.K. (2002) Yeast go the whole HOG for the hyperosmotic response. Trends Genet 18: 405– 412. 12142009
  31. Perez‐Nadales, E., and Di Pietro, A. (2015) The transmembrane protein Sho1 cooperates with the mucin Msb2 to regulate invasive growth and plant infection in Fusarium oxysporum. Mol Plant Pathol 16: 593– 603. 25382187 PMC6638380
  32. Raitt, D.C., Posas, F., and Saito, H. (2000) Yeast Cdc42 GTPase and Ste20 PAK‐like kinase regulate Sho1‐dependent activation of the Hog1 MAPK pathway. EMBO J 19: 4623– 4631. 10970855 PMC302074
  33. Reiser, V., Raitt, D.C., and Saito, H. (2003) Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure. J Cell Biol 161: 1035– 1040. 12821642 PMC2172993
  34. Ren, W., Liu, N., Yang, Y., Yang, Q., Chen, C., et al (2019) The sensor proteins BcSho1 and BcSln1 are involved in, though not essential to, vegetative differentiation, pathogenicity and osmotic stress tolerance in Botrytis cinerea. Front Microbiol 10: 328. 30858841 PMC6397835
  35. Román, E., Nombela, C., and Pla, J. (2005) The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol Cell Biol 25: 10611– 10627. 16287872 PMC1291223
  36. Saito, H. (2010) Regulation of cross‐talk in yeast MAPK signaling pathways. Curr Opin Microbiol 13: 677– 683. 20880736
  37. Saito, H., and Tatebayashi, K. (2004) Regulation of the osmoregulatory HOG MAPK cascade in yeast. J Biochem 136: 267– 272. 15598881
  38. Santhanam, P., and Thomma, B.P. (2013) Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Mol Plant‐Microbe Interact 26: 249– 256. 22970788
  39. Sarmiento‐Villamil, J.L., García‐Pedrajas, N.E., Baeza‐Montañez, L., and García‐Pedrajas, M.D. (2018a) The APSES transcription factor Vst1 is a key regulator of development in microsclerotium and resting mycelium‐producing Verticillium species. Mol Plant Pathol 19: 59– 76. 27696683 PMC6638171
  40. Sarmiento‐Villamil, J.L., Prieto, P., Klosterman, S.J., and García‐Pedrajas, M.D. (2018b) Characterization of two homeodomain transcription factors with critical but distinct roles in virulence in the vascular pathogen Verticillium dahliae. Mol Plant Pathol 19: 986– 1004. 28727279 PMC6638091
  41. Seet, B.T., and Pawson, T. (2004) MAPK signaling: Sho business. Curr Biol 14: 708– 810. 15341761
  42. So, Y.S., Jang, J., Park, G., Xu, J., Olszewski, M.A., et al (2018) Sho1 and Msb2 play complementary but distinct roles in stress responses, sexual differentiation, and pathogenicity of Cryptococcus neoformans. Front Microbiol 9: 2958. 30564211 PMC6288190
  43. Tang, W., Wang, W., Chen, D., Ji, Q., Jing, Y., et al (2012) Transposase derived proteins FHY3/FAR1 interact with phytochrome‐interacting factor1 to regulate chlorophyll biosynthesis by modulating HEMB1 during deetiolation in Arabidopsis. Plant Cell 24: 1984– 2000. 22634759 PMC3442582
  44. Tatebayashi, K., Tanaka, K., Yang, H.Y., Yamamoto, K., Matsushita, Y., et al (2007) Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26: 3521– 3533. 17627274 PMC1949007
  45. Tatebayashi, K., Yamamoto, K., Nagoya, M., Takayama, T., Nishimura, A., et al (2015) Osmosensing and scaffolding functions of the oligomeric four‐transmembrane domain osmosensor Sho1. Nat Commun 6: 6975. 25898136 PMC4411306
  46. Tian, L., Wang, Y., Yu, J., Xiong, D., Zhao, H., et al (2016) The mitogen‐activated protein kinase kinase VdPbs2 of Verticillium dahliae regulates microsclerotia formation, stress response, and plant infection. Front Microbiol 7: 1532. 27729908 PMC5037172
  47. Tian, L., Xu, J., Zhou, L., and Guo, W. (2014) VdMsb regulates virulence and microsclerotia production in the fungal plant pathogen Verticillium dahliae. Gene 550: 238– 244. 25151308
  48. Tong, A.H., Drees, B., Nardelli, G., Bader, G.D., Brannetti, B., et al (2002) A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295: 321– 324. 11743162
  49. Turrà, D., Segorbe, D., and Di Pietro, A. (2014) Protein kinases in plant‐pathogenic fungi: conserved regulators of infection. Annu Rev Phytopathol 52: 267– 288. 25090477
  50. Tzima, A., Paplomatas, E.J., Rauyaree, P., and Kang, S. (2010) Roles of the catalytic subunit of cAMP‐dependent protein kinase A in virulence and development of the soilborne plant pathogen Verticillium dahliae. Fungal Genet Biol 47: 406– 415. 20144723
  51. Wang, Y., Hu, X., Fang, Y., Anchieta, A., Goldman, P.H., et al (2018) Transcription factor VdCmr1 is required for pigment production, protection from UV irradiation, and regulates expression of melanin biosynthetic genes in Verticillium dahliae. Microbiology 164: 685– 696. 29485393 PMC5982140
  52. Wang, Y., Tian, L., Xiong, D., Klosterman, S.J., Xiao, S., et al (2016) The mitogen‐activated protein kinase gene, VdHog1, regulates osmotic stress response, microsclerotia formation and virulence in Verticillium dahliae. Fungal Genet Biol 88: 13– 23. 26812120
  53. Westfall, P.J., Ballon, D.R., and Thorner, J. (2004) When the stress of your environment makes you go HOG wild. Science 306: 1511– 1512. 15567851
  54. Wheeler, M.H., and Bell, A.A. (1988) Melanins and their importance in pathogenic fungi. Curr Top Med Mycol 2: 338– 387. 3288360
  55. Xiong, D., Wang, Y., Ma, J., Klosterman, S.J., Xiao, S., et al (2014) Deep mRNA sequencing reveals stage‐specific transcriptome alterations during microsclerotia development in the smoke tree vascular wilt pathogen, Verticillium dahliae. BMC Genomics 15: 324. 24884698 PMC4035056
  56. Xiong, D., Wang, Y., Tang, C., et al (2015) VdCrz1 is involved in microsclerotia formation and required for full virulence in Verticillium dahliae. Fungal Genet Biol 82: 201– 212. 26235044
  57. Xu, H., Zhang, Q., Cui, W., Zhang, X., Liu, W., et al (2016) AbSte7, a MAPKK gene of Alternaria brassicicola, is involved in conidiation, salt/oxidative stress, and pathogenicity. J Microbiol Biotechnol 26: 1311– 1319. 27160581
  58. Xu, J.R., and Hamer, J.E. (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes 10: 2696– 2706. 8946911
  59. Yu, J., Li, T., Tian, L., Tang, C., Klosterman, S.J., et al (2019) Two Verticillium dahliae MAPKKKs, VdSsk2 and VdSte11, have distinct roles in pathogenicity, microsclerotial formation, and stress adaptation. mSphere 4: e00426. 31292234 PMC6620378
  60. Yu, P.L., Chen, L.H., and Chung, K.R. (2016) How the pathogenic fungus Alternaria alternata copes with stress via the response regulators SSK1 and SHO1. PLoS One 11: e0149153. 26863027 PMC4749125
  61. Zhang, D.D., Wang, J., Wang, D., Kong, Z.Q., Zhou, L., et al (2019) Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae. New Phytol 222: 1012– 1029. 30609067 PMC6594092
  62. Zhang, H., Liu, K., Zhang, X., Song, W., Zhao, Q., et al (2010) A two‐component histidine kinase, MoSLN1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Curr Genet 56: 517– 528. 20848286
  63. Zhang, T., Zhang, B., Hua, C., Meng, P., Wang, S., et al (2017) VdPKS1 is required for melanin formation and virulence in a cotton wilt pathogen Verticillium dahliae. Sci China‐Life Sci 60: 868– 879. 28755294
  64. Zhang, W.Q., Gui, Y.J., Short, D.P., Zhou, L., Li, T.G., et al (2017b) Verticillium dahliae transcription factor VdFTF1 regulates the expression of multiple secreted virulence factors and is required for full virulence in cotton. Mol Plant Pathol 19: 841– 857. 28520093 PMC6638078
  65. Zhao, Y.L., Zhou, T.T., and Guo, H.S. (2016) Hyphopodium‐specific VdNoxB/VdPls1‐dependent ROS‐Ca2+ signaling is required for plant infection by Verticillium dahliae. PLoS Pathogens 12: e1005793. 27463643 PMC4962994
  66. Zheng, J., Tang, C., Deng, C., and Wang, Y. (2019) Involvement of a response regulator VdSsk1 in stress response, melanin biosynthesis and full virulence in Verticillium dahliae. Front Microbiol 10: 606. 30967857 PMC6439524
  67. Zhou, L., Zhao, J., Guo, W.Z., and Zhang, T.Z. (2013) Functional analysis of autophagy genes via Agrobacterium‐mediated transformation in the vascular Wilt fungus Verticillium dahliae. J Genet Genomics 40: 421– 431. 23969251

Cited by

Sorted by citations

Authors
Li, J., Zhou, L., Yin, C., Zhang, D., Klosterman, S. J., Wang, B., Song, J., Wang, D., Hu, X., Subbarao, K. V., Chen, J., & Dai, X.
Affiliations
  • Laboratory of Cotton Disease Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences Beijing 100193 China
  • Institute of Food Science and Technology (CN)
  • University of California, Davis (US)
  • Northwest A&F University (CN)
  • Agricultural Research Service (US)
Corresponding author
Subbarao, Krishna V.
ORCID
Venue
Environmental Microbiology
Publisher
Wiley
Published
2019-11-24
Volume
21
Issue
12
Pages
4852-4874
ISSN
  • 1462-2912 (ISSN-L)
  • 1462-2920
DOI
10.1111/1462-2920.14846
PMC
PMC6916341
OpenAlex
W2984549809
Cited by
54
References
0
Citations by year
2026: 1 · 2025: 9 · 2024: 12 · 2023: 9 · 2022: 13 · 2021: 8 · 2020: 1 · 2019: 1
FWCI
3.28
Type
journal article
Language
en
Open access
Licence
Locations
  • Environmental Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders
  • Agricultural Science and Technology Innovation Program
  • National Key Research and Development Program of China (2017YFD0200601, 2017YFD0201904)
  • Foundation for Innovative Research Groups of the National Natural Science Foundation of China (31471759, 31501600, 31671986, 31772245, 31870138)
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
Verticillium dahliae, MAPK signaling, melanogenesis, osmosensor, microsclerotia, fungal virulence, transmembrane proteins, plant-pathogen interaction
MeSH terms
Gossypium, Fungal Proteins, Melanins, Plant Diseases, Virulence, Signal Transduction, Gene Expression Regulation, Fungal, Sequence Deletion, Verticillium, Mitogen-Activated Protein Kinase Kinases, Secondary Metabolism

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