The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae

ABSTRACT The ascomycete fungus Verticillium dahliae infects over 400 plant species and causes serious losses of economically important crops, such as cotton and tomato, and also of woody plants, such as smoke tree, maple, and olive. Melanized long-term survival structures known as microsclerotia pla...

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Main Authors: Meijun Lai, Zhuo Cheng, Luyao Xiao, Steven J. Klosterman, Yonglin Wang
Format: Article
Language:English
Published: American Society for Microbiology 2022-04-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02581-21
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author Meijun Lai
Zhuo Cheng
Luyao Xiao
Steven J. Klosterman
Yonglin Wang
author_facet Meijun Lai
Zhuo Cheng
Luyao Xiao
Steven J. Klosterman
Yonglin Wang
author_sort Meijun Lai
collection DOAJ
description ABSTRACT The ascomycete fungus Verticillium dahliae infects over 400 plant species and causes serious losses of economically important crops, such as cotton and tomato, and also of woody plants, such as smoke tree, maple, and olive. Melanized long-term survival structures known as microsclerotia play crucial roles in the disease cycle of V. dahliae, enabling this soilborne fungus to survive for years in the soil in the absence of a host. Previously, we identified VdMRTF1 (microsclerotia-related transcription factor) encoding a bZip transcription factor which is downregulated during microsclerotial development in V. dahliae. In the present study, we showed that VdMRTF1 negatively controls melanin production and virulence by genetic, biological, and transcriptomic analyses. The mutant strain lacking VdMRTF1 (ΔVdMRTF1) exhibited increased melanin biosynthesis and the defect also promoted microsclerotial development and sensitivity to Ca2+. In comparison with the wild-type strain, the ΔVdMRTF1 strain showed a significant enhancement in virulence and displayed an increased capacity to eliminate reactive oxygen species in planta. Furthermore, analyses of transcriptomic profiles between the ΔVdMRTF1 and wild-type strains indicated that VdMRTF1 regulates the differential expression of genes associated with melanin biosynthesis, tyrosine metabolism, hydrogen peroxide catabolic processes, and oxidoreductase activity in V. dahliae. Taken together, these data show that VdMRTF1 is a negative transcriptional regulator of melanin biosynthesis, microsclerotia formation, and virulence in V. dahliae. IMPORTANCE Verticillium wilt is difficult to manage because the pathogen colonizes the plant xylem tissue and produces melanized microsclerotia which survive for more than 10 years in soil without a host. The molecular mechanisms underlying microsclerotia formation are of great importance to control the disease. Here, we provide evidence that a bZip transcription factor, VdMRTF1, plays important roles in melanin biosynthesis, microsclerotial development, resistance to elevated Ca2+ levels, and fungal virulence of V. dahliae. The findings extend and deepen our understanding of the complexities of melanin biosynthesis, microsclerotia formation, and virulence that are regulated by bZip transcription factors in V. dahliae.
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spelling doaj.art-6eefc53bcdb64bc1ac0fbba9fc6f4bd42022-12-22T01:51:03ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-04-0110210.1128/spectrum.02581-21The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliaeMeijun Lai0Zhuo Cheng1Luyao Xiao2Steven J. Klosterman3Yonglin Wang4Beijing Key Laboratory for Forest Pest Control, College of Forestry, Beijing Forestry University, Beijing, ChinaBeijing Key Laboratory for Forest Pest Control, College of Forestry, Beijing Forestry University, Beijing, ChinaBeijing Key Laboratory for Forest Pest Control, College of Forestry, Beijing Forestry University, Beijing, ChinaUnited States Department of Agriculture, Agricultural Research Service, Salinas, California, USABeijing Key Laboratory for Forest Pest Control, College of Forestry, Beijing Forestry University, Beijing, ChinaABSTRACT The ascomycete fungus Verticillium dahliae infects over 400 plant species and causes serious losses of economically important crops, such as cotton and tomato, and also of woody plants, such as smoke tree, maple, and olive. Melanized long-term survival structures known as microsclerotia play crucial roles in the disease cycle of V. dahliae, enabling this soilborne fungus to survive for years in the soil in the absence of a host. Previously, we identified VdMRTF1 (microsclerotia-related transcription factor) encoding a bZip transcription factor which is downregulated during microsclerotial development in V. dahliae. In the present study, we showed that VdMRTF1 negatively controls melanin production and virulence by genetic, biological, and transcriptomic analyses. The mutant strain lacking VdMRTF1 (ΔVdMRTF1) exhibited increased melanin biosynthesis and the defect also promoted microsclerotial development and sensitivity to Ca2+. In comparison with the wild-type strain, the ΔVdMRTF1 strain showed a significant enhancement in virulence and displayed an increased capacity to eliminate reactive oxygen species in planta. Furthermore, analyses of transcriptomic profiles between the ΔVdMRTF1 and wild-type strains indicated that VdMRTF1 regulates the differential expression of genes associated with melanin biosynthesis, tyrosine metabolism, hydrogen peroxide catabolic processes, and oxidoreductase activity in V. dahliae. Taken together, these data show that VdMRTF1 is a negative transcriptional regulator of melanin biosynthesis, microsclerotia formation, and virulence in V. dahliae. IMPORTANCE Verticillium wilt is difficult to manage because the pathogen colonizes the plant xylem tissue and produces melanized microsclerotia which survive for more than 10 years in soil without a host. The molecular mechanisms underlying microsclerotia formation are of great importance to control the disease. Here, we provide evidence that a bZip transcription factor, VdMRTF1, plays important roles in melanin biosynthesis, microsclerotial development, resistance to elevated Ca2+ levels, and fungal virulence of V. dahliae. The findings extend and deepen our understanding of the complexities of melanin biosynthesis, microsclerotia formation, and virulence that are regulated by bZip transcription factors in V. dahliae.https://journals.asm.org/doi/10.1128/spectrum.02581-21bZip transcription factorVdMRTF1Verticillium dahliaemelanized microsclerotiavirulence
spellingShingle Meijun Lai
Zhuo Cheng
Luyao Xiao
Steven J. Klosterman
Yonglin Wang
The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae
Microbiology Spectrum
bZip transcription factor
VdMRTF1
Verticillium dahliae
melanized microsclerotia
virulence
title The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae
title_full The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae
title_fullStr The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae
title_full_unstemmed The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae
title_short The bZip Transcription Factor VdMRTF1 is a Negative Regulator of Melanin Biosynthesis and Virulence in Verticillium dahliae
title_sort bzip transcription factor vdmrtf1 is a negative regulator of melanin biosynthesis and virulence in verticillium dahliae
topic bZip transcription factor
VdMRTF1
Verticillium dahliae
melanized microsclerotia
virulence
url https://journals.asm.org/doi/10.1128/spectrum.02581-21
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