VdSOX1 Negatively Regulates Verticillium dahliae Virulence via Enhancing Effector Expression and Suppressing Host Immune Responses
Abstract
1. Introduction
2. Results
2.1. VdSOX1 Encodes a Sarcosine Oxidase and Is Highly Conserved Within the Genus Verticillium
2.2. VdSOX1 Exhibits Tissue-Specific Expression and Is Induced by Infection and Sarcosine/Glyphosate
2.3. VdSOX1 Modulates Growth, Sporulation, Microsclerotia Formation, and Virulence in V. dahliae
2.4. VdSOX1 Negatively Regulates Carbon Metabolism in V. dahliae
2.5. VdSOX1 Gene Negatively Promotes Effector Expression to Enhance Pathogenicity
2.6. VdSOX1 Knockout Enhances Host Susceptibility by Downregulating Cotton Resistance-Related Genes
3. Discussion
4. Materials and Methods
4.1. V. dahliae Isolates and Growth Conditions
4.2. Cloning and Sequence Analysis of VdSOX1 Gene
4.3. Analysis of Gene Expression Patterns
4.4. Plasmid Construction and Transformation
4.5. Phenotype Assays
4.6. The Cotton Infection Assays
4.7. RNA-Sequencing
4.8. Read Mapping and Differential Expression Analysis
4.9. Exploratory Data Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Klosterman, S.J.; Atallah, Z.K.; Vallad, G.E.; Subbarao, K.V. Diversity, pathogenicity, and management of Verticillium species. Annu. Rev. Phytopathol. 2009, 47, 39–62. [Google Scholar] [CrossRef]
- Zhou, J.; Feng, Z.; Liu, S.; Wei, F.; Shi, Y.; Zhao, L.; Huang, W.; Zhou, Y.; Feng, H.; Zhu, H. CGTase, a novel antimicrobial protein from Bacillus cereus YUPP-10, suppresses Verticillium dahliae and mediates plant defence responses. Mol. Plant Pathol. 2021, 22, 130–144. [Google Scholar] [CrossRef]
- Fradin, E.F.; Thomma, B.P. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 2006, 7, 71–86. [Google Scholar] [CrossRef] [PubMed]
- Short, D.P.; Sandoya, G.; Vallad, G.E.; Koike, S.T.; Xiao, C.-L.; Wu, B.-M.; Gurung, S.; Hayes, R.J.; Subbarao, K.V. Dynamics of Verticillium species microsclerotia in field soils in response to fumigation, cropping patterns, and flooding. Phytopathology 2015, 105, 638–645. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Zhou, J.; Zhao, L.; Feng, Z.; Wei, F.; Bai, H.; Feng, H.; Zhu, H. A review of the pathogenicity mechanism of Verticillium dahliae in cotton. J. Cotton Res. 2022, 5, 3. [Google Scholar] [CrossRef]
- Tian, L.; Wang, Y.; Yu, J.; Xiong, D.; Zhao, H.; Tian, C. The mitogen-activated protein kinase kinase VdPbs2 of Verticillium dahliae regulates microsclerotia formation, stress response, and plant infection. Front. Microbiol. 2016, 7, 1532. [Google Scholar] [CrossRef]
- Wang, M.; Weiberg, A.; Lin, F.-M.; Thomma, B.P.; Huang, H.-D.; Jin, H. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2016, 2, 16151. [Google Scholar] [CrossRef]
- Wang, Y.; Tian, L.; Xiong, D.; Klosterman, S.J.; Xiao, S.; Tian, C. 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. [Google Scholar] [CrossRef]
- Tian, L.; Yu, J.; Wang, Y.; Tian, C. The C2H2 transcription factor VdMsn2 controls hyphal growth, microsclerotia formation, and virulence of Verticillium dahliae. Fungal Biol. 2017, 121, 1001–1010. [Google Scholar] [CrossRef]
- Qi, X.; Li, X.; Guo, H.; Guo, N.; Cheng, H. Vd PLP, a patatin-like phospholipase in Verticillium dahliae, is involved in cell wall integrity and required for pathogenicity. Genes 2018, 9, 162. [Google Scholar] [CrossRef]
- Zhang, T.; Zhang, B.; Hua, C.; Meng, P.; Wang, S.; Chen, Z.; Du, Y.; Gao, F.; Huang, J. VdPKS1 is required for melanin formation and virulence in a cotton wilt pathogen Verticillium dahliae. Sci. China Life Sci. 2017, 60, 868–879. [Google Scholar] [CrossRef]
- Wang, Y.; Hu, X.; Fang, Y.; Anchieta, A.; Goldman, P.H.; Hernandez, G.; Klosterman, S.J. Transcription factor VdCmr1 is required for pigment production, protection from UV irradiation, and regulates expression of melanin biosynthetic genes in Verticillium dahliae. Microbiology 2018, 164, 685–696. [Google Scholar] [CrossRef]
- Tzima, A.K.; Paplomatas, E.J.; Tsitsigiannis, D.I.; Kang, S. The G protein β subunit controls virulence and multiple growth-and development-related traits in Verticillium dahliae. Fungal Genet. Biol. 2012, 49, 271–283. [Google Scholar] [CrossRef] [PubMed]
- Gao, F.; Zhou, B.-J.; Li, G.-Y.; Jia, P.-S.; Li, H.; Zhao, Y.-L.; Zhao, P.; Xia, G.-X.; Guo, H.-S. A Glutamic Acid-Rich Protein Identified in Verticillium dahliae from an Insertional Mutagenesis Affects Microsclerotial Formation and Pathogenicity. PLoS ONE 2010, 5, e15319. [Google Scholar] [CrossRef] [PubMed]
- Li, J.J.; Zhou, L.; Yin, C.M.; Zhang, D.D.; Klosterman, S.J.; Wang, B.L.; Song, J.; Wang, D.; Hu, X.P.; Subbarao, K.V. The Verticillium dahliae Sho1-MAPK pathway regulates melanin biosynthesis and is required for cotton infection. Environ. Microbiol. 2019, 21, 4852–4874. [Google Scholar] [CrossRef]
- Sun, L.; Qin, J.; Rong, W.; Ni, H.; Guo, H.S.; Zhang, J. Cellophane surface-induced gene, VdCSIN1, regulates hyphopodium formation and pathogenesis via cAMP-mediated signalling in Verticillium dahliae. Mol. Plant Pathol. 2019, 20, 323–333. [Google Scholar] [CrossRef]
- Zhou, T.-T.; Zhao, Y.-L.; Guo, H.-S. Secretory proteins are delivered to the septin-organized penetration interface during root infection by Verticillium dahliae. PLoS Pathog. 2017, 13, e1006275. [Google Scholar] [CrossRef]
- Zhao, Y.-L.; Zhou, T.-T.; Guo, H.-S. Hyphopodium-specific VdNoxB/VdPls1-dependent ROS-Ca2+ signaling is required for plant infection by Verticillium dahliae. PLoS Pathog. 2016, 12, e1005793. [Google Scholar] [CrossRef]
- Yang, Y.; Zhang, Y.; Li, B.; Yang, X.; Dong, Y.; Qiu, D. A Verticillium dahliae pectate lyase induces plant immune responses and contributes to virulence. Front. Plant Sci. 2018, 9, 1271. [Google Scholar] [CrossRef]
- Maruthachalam, K.; Klosterman, S.; Kang, S.; Hayes, R.; Subbarao, K. Identification of pathogenicity-related genes in the vascular wilt fungus Verticillium dahliae by Agrobacterium tumefaciens-mediated T-DNA insertional mutagenesis. Mol. Biotechnol. 2011, 49, 209–221. [Google Scholar] [CrossRef]
- Tzima, A.K.; Paplomatas, E.J.; Rauyaree, P.; Ospina-Giraldo, M.D.; Kang, S. VdSNF1, the sucrose nonfermenting protein kinase gene of Verticillium dahliae, is required for virulence and expression of genes involved in cell-wall degradation. Mol. Plant-Microbe Interact. 2011, 24, 129–142. [Google Scholar] [CrossRef]
- Wang, D.; Tian, L.; Zhang, D.D.; Song, J.; Song, S.S.; Yin, C.M.; Zhou, L.; Liu, Y.; Wang, B.L.; Kong, Z.Q. Functional analyses of small secreted cysteine-rich proteins identified candidate effectors in Verticillium dahliae. Mol. Plant Pathol. 2020, 21, 667–685. [Google Scholar] [CrossRef]
- Zhang, Y.; Gao, Y.; Liang, Y.; Dong, Y.; Yang, X.; Qiu, D. Verticillium dahliae PevD1, an Alt a 1-like protein, targets cotton PR5-like protein and promotes fungal infection. J. Exp. Bot. 2019, 70, 613–626. [Google Scholar] [CrossRef]
- Gui, Y.J.; Chen, J.Y.; Zhang, D.D.; Li, N.Y.; Li, T.G.; Zhang, W.Q.; Wang, X.Y.; Short, D.P.; Li, L.; Guo, W. Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1. Environ. Microbiol. 2017, 19, 1914–1932. [Google Scholar] [CrossRef]
- Zhu, X.; Soliman, A.; Islam, M.R.; Adam, L.R.; Daayf, F. Verticillium dahliae’s isochorismatase hydrolase is a virulence factor that contributes to interference with potato’s salicylate and jasmonate defense signaling. Front. Plant Sci. 2017, 8, 399. [Google Scholar] [CrossRef]
- Santhanam, P.; Van Esse, H.P.; Albert, I.; Faino, L.; Nürnberger, T.; Thomma, B.P. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant-Microbe Interact. 2013, 26, 278–286. [Google Scholar] [CrossRef] [PubMed]
- Luo, X.; Mao, H.; Wei, Y.; Cai, J.; Xie, C.; Sui, A.; Yang, X.; Dong, J. The fungal-specific transcription factor Vdpf influences conidia production, melanized microsclerotia formation and pathogenicity in Verticillium dahliae. Mol. Plant Pathol. 2016, 17, 1364–1381. [Google Scholar] [CrossRef]
- Zhang, W.Q.; Gui, Y.J.; Short, D.P.; Li, T.G.; Zhang, D.D.; Zhou, L.; Liu, C.; Bao, Y.M.; Subbarao, K.V.; Chen, J.Y. Verticillium dahliae transcription factor VdFTF1 regulates the expression of multiple secreted virulence factors and is required for full virulence in cotton. Mol. Plant Pathol. 2018, 19, 841–857. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.; Li, T.; Klosterman, S.J.; Tian, C.; Wang, Y. The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae. New Phytol. 2020, 226, 1461–1479. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Deng, C.; Tian, L.; Xiong, D.; Tian, C.; Klosterman, S.J. The transcription factor VdHapX controls iron homeostasis and is crucial for virulence in the vascular pathogen Verticillium dahliae. Msphere 2018, 3, e00400-18. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Hoppenau, C.E.; Tran, V.-T.; Kusch, H.; Aßhauer, K.P.; Landesfeind, M.; Meinicke, P.; Popova, B.; Braus-Stromeyer, S.A.; Braus, G.H. Verticillium dahliae VdTHI4, involved in thiazole biosynthesis, stress response and DNA repair functions, is required for vascular disease induction in tomato. Environ. Exp. Bot. 2014, 108, 14–22. [Google Scholar] [CrossRef]
- Qin, T.; Hao, W.; Sun, R.; Li, Y.; Wang, Y.; Wei, C.; Dong, T.; Wu, B.; Dong, N.; Wang, W. Verticillium dahliae VdTHI20, involved in pyrimidine biosynthesis, is required for DNA repair functions and pathogenicity. Int. J. Mol. Sci. 2020, 21, 1378. [Google Scholar] [CrossRef]
- Rehman, L.; Su, X.; Li, X.; Qi, X.; Guo, H.; Cheng, H. FreB is involved in the ferric metabolism and multiple pathogenicity-related traits of Verticillium dahliae. Curr. Genet. 2018, 64, 645–659. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Su, X.; Lu, G.; Sun, G.; Zhang, Z.; Guo, H.; Guo, N.; Cheng, H. VdOGDH is involved in energy metabolism and required for virulence of Verticillium dahliae. Curr. Genet. 2020, 66, 345–359. [Google Scholar] [CrossRef] [PubMed]
- Shi-Kunne, X.; van Kooten, M.; Depotter, J.R.; Thomma, B.P.; Seidl, M.F. The genome of the fungal pathogen Verticillium dahliae reveals extensive bacterial to fungal gene transfer. Genome Biol. Evol. 2019, 11, 855–868. [Google Scholar] [CrossRef] [PubMed]
- de Jonge, R.; Bolton, M.D.; Kombrink, A.; van den Berg, G.C.; Yadeta, K.A.; Thomma, B.P. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 2013, 23, 1271–1282. [Google Scholar] [CrossRef]
- Su, X.; Lu, G.; Li, X.; Rehman, L.; Liu, W.; Sun, G.; Guo, H.; Wang, G.; Cheng, H. Host-induced gene silencing of an adenylate kinase gene involved in fungal energy metabolism improves plant resistance to Verticillium dahliae. Biomolecules 2020, 10, 127. [Google Scholar] [CrossRef]
- Wei, C.; Qin, T.; Li, Y.; Wang, W.; Dong, T.; Wang, Q. Host-induced gene silencing of the acetolactate synthases VdILV2 and VdILV6 confers resistance to Verticillium wilt in cotton (Gossypium hirsutum L.). Biochem. Biophys. Res. Commun. 2020, 524, 392–397. [Google Scholar] [CrossRef]
- Lahham, M.; Jha, S.; Goj, D.; Macheroux, P.; Wallner, S. The family of sarcosine oxidases: Same reaction, different products. Arch. Biochem. Biophys. 2021, 704, 108868. [Google Scholar] [CrossRef]
- Lee, S.; Jia, B.; Pham, B.P.; Shao, Y.; Kwak, J.M.; Cheong, G.-W. Architecture and characterization of sarcosine oxidase from Thermococcus kodakarensis KOD1. Extremophiles 2012, 16, 87–93. [Google Scholar] [CrossRef]
- Wagner, M.A.; Trickey, P.; Chen, Z.-w.; Mathews, F.S.; Jorns, M.S. Monomeric sarcosine oxidase: 1. Flavin reactivity and active site binding determinants. Biochemistry 2000, 39, 8813–8824. [Google Scholar] [CrossRef]
- Chikayama, M.; Ohsumi, M.; Yokota, S. Enzyme cytochemical localization of sarcosine oxidase activity in the liver and kidney of several mammals. Histochem. Cell Biol. 2000, 113, 489–495. [Google Scholar] [CrossRef] [PubMed]
- Goyer, A.; Johnson, T.L.; Olsen, L.J.; Collakova, E.; Shachar-Hill, Y.; Rhodes, D.; Hanson, A.D. Characterization and metabolic function of a peroxisomal sarcosine and pipecolate oxidase from Arabidopsis. J. Biol. Chem. 2004, 279, 16947–16953. [Google Scholar] [CrossRef]
- Guo, K.; Ma, X.; Sun, G.; Zhao, Y.; Li, X.; Zhao, W.; Kai, L. Expression and characterization of a thermostable sarcosine oxidase (SOX) from Bacillus sp. in Escherichia coli. Appl. Microbiol. Biotechnol. 2006, 73, 559–566. [Google Scholar] [CrossRef] [PubMed]
- HAYASHI, S. Mechanism of reduction of Corynebacterium sarcosine oxidase by dithiothreitol. J. Biochem. 1984, 95, 1201–1207. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, K.; Ogishima, M.; Sugiyama, M.; Inouye, Y.; Nakamura, S.; Imamura, S. Molecular cloning and expression of a Streptomyces sarcosine oxidase gene in Streptomyces lividans. Biosci. Biotechnol. Biochem. 1992, 56, 432–436. [Google Scholar] [CrossRef]
- Nishiya, Y.; Imanaka, T. Analysis of interaction between the Arthrobacter sarcosine oxidase and the coenzyme flavin adenine dinucleotide by site-directed mutagenesis. Appl. Environ. Microbiol. 1996, 62, 2405–2410. [Google Scholar] [CrossRef]
- Hassan-Abdallah, A.; Zhao, G.; Eschenbrenner, M.; Chen, Z.-w.; Mathews, F.S.; Jorns, M.S. Cloning, expression and crystallization of heterotetrameric sarcosine oxidase from Pseudomonas maltophilia. Protein Expr. Purif. 2005, 43, 33–43. [Google Scholar] [CrossRef]
- Dijkman, W.P.; de Gonzalo, G.; Mattevi, A.; Fraaije, M.W. Flavoprotein oxidases: Classification and applications. Appl. Microbiol. Biotechnol. 2013, 97, 5177–5188. [Google Scholar] [CrossRef]
- González-Valenzuela, L.E.; Dussán, J. Molecular assessment of glyphosate-degradation pathway via sarcosine intermediate in Lysinibacillus sphaericus. Environ. Sci. Pollut. Res. 2018, 25, 22790–22796. [Google Scholar] [CrossRef]
- Duressa, D.; Anchieta, A.; Chen, D.; Klimes, A.; Garcia-Pedrajas, M.D.; Dobinson, K.F.; Klosterman, S.J. RNA-seq analyses of gene expression in the microsclerotia of Verticillium dahliae. BMC Genom. 2013, 14, 607. [Google Scholar] [CrossRef] [PubMed]
- Santhanam, P.; Thomma, B.P. Verticillium dahliae Sge1 differentially regulates expression of candidate effector genes. Mol. Plant-Microbe Interact. 2013, 26, 249–256. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef]
- Zhou, B.-J.; Jia, P.-S.; Gao, F.; Guo, H.-S. Molecular characterization and functional analysis of a necrosis-and ethylene-inducing, protein-encoding gene family from Verticillium dahliae. Mol. Plant-Microbe Interact. 2012, 25, 964–975. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.; Xiong, D.; Fang, Y.; Tian, C.; Wang, Y. The two-component response regulator VdSkn7 plays key roles in microsclerotial development, stress resistance and virulence of Verticillium dahliae. Fungal Genet. Biol. 2017, 108, 26–35. [Google Scholar] [CrossRef]
- Zhang, J.; Zhang, Y.; Yang, J.; Kang, L.; EloRM, A.M.; Zhou, H.; Zhao, J. The α-1, 6-mannosyltransferase VdOCH1 plays a major role in microsclerotium formation and virulence in the soil-borne pathogen Verticillium dahliae. Fungal Biol. 2019, 123, 539–546. [Google Scholar] [CrossRef]
- Geng, Q.; Li, H.; Wang, D.; Sheng, R.-C.; Zhu, H.; Klosterman, S.J.; Subbarao, K.V.; Chen, J.-Y.; Chen, F.-M.; Zhang, D.-D. The Verticillium dahliae Spt-Ada-Gcn5 acetyltransferase complex subunit Ada1 is essential for conidia and microsclerotia production and contributes to virulence. Front. Microbiol. 2022, 13, 852571. [Google Scholar] [CrossRef]
- Chen, L.; Ma, X.; Sun, T.; Zhu, Q.-H.; Feng, H.; Li, Y.; Liu, F.; Zhang, X.; Sun, J.; Li, Y. VdPT1 encoding a neutral trehalase of Verticillium dahliae is required for growth and virulence of the pathogen. Int. J. Mol. Sci. 2023, 25, 294. [Google Scholar] [CrossRef]
- Del Sorbo, G.; Schoonbeek, H.-j.; De Waard, M.A. Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet. Biol. 2000, 30, 1–15. [Google Scholar] [CrossRef]
- Zhou, Y.; Yan, K.; Qin, Q.; Raimi, O.G.; Du, C.; Wang, B.; Ahamefule, C.S.; Kowalski, B.; Jin, C.; van Aalten, D.M. Phosphoglucose isomerase is important for Aspergillus fumigatus cell wall biogenesis. Mbio 2022, 13, e01426-22. [Google Scholar] [CrossRef]
- Zhang, X.; Zhao, L.; Liu, S.; Zhou, J.; Wu, Y.; Feng, Z.; Zhang, Y.; Zhu, H.; Wei, F.; Feng, H. Identification and functional analysis of a novel hydrophobic protein VdHP1 from Verticillium dahliae. Microbiol. Spectr. 2022, 10, e02478-21. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Li, J.; Wang, Z.; Zhou, H.; Wang, Y.; Qin, W.; Duan, H.; Zhao, H.; Ge, X. Suppression of plant immunity by Verticillium dahliae effector Vd6317 through AtNAC53 association. Plant J. 2024, 119, 1767–1781. [Google Scholar] [CrossRef] [PubMed]
- Song, Q.; Han, S.; Hu, S.; Xu, Y.; Zuo, K. The Verticillium dahliae effector VdPhb1 promotes pathogenicity in cotton and interacts with the immune protein GhMc4. Plant Cell Physiol. 2024, 65, 1173–1183. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Huang, Y.; Shang, W.; Chen, J.; Klosterman, S.J.; Subbarao, K.V.; Qin, J.; Hu, X. A glycine-rich nuclear effector VdCE51 of Verticillium dahliae suppresses plant immune responses by inhibiting the accumulation of GhTRXH2. Crop J. 2024, 12, 1137–1149. [Google Scholar] [CrossRef]
- Marchingo, J.M.; Cantrell, D.A. Protein synthesis, degradation, and energy metabolism in T cell immunity. Cell. Mol. Immunol. 2022, 19, 303–315. [Google Scholar] [CrossRef]
- Qin, J.; Wang, K.; Sun, L.; Xing, H.; Wang, S.; Li, L.; Chen, S.; Guo, H.-S.; Zhang, J. The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. eLife 2018, 7, e34902. [Google Scholar] [CrossRef]
- Madan, M.; Thind, K. Physiology of Fungi; University of London Press: London, UK, 1998; Chapter 3; pp. 64–75. [Google Scholar]
- Shao, S.; Li, B.; Sun, Q.; Guo, P.; Du, Y.; Huang, J. Acetolactate synthases regulatory subunit and catalytic subunit genes VdILVs are involved in BCAA biosynthesis, microscletotial and conidial formation and virulence in Verticillium dahliae. Fungal Genet. Biol. 2022, 159, 103667. [Google Scholar] [CrossRef]
- Wang, S.; Xing, H.; Hua, C.; Guo, H.-S.; Zhang, J. An improved single-step cloning strategy simplifies the Agrobacterium tumefaciens-mediated transformation (ATMT)-based gene-disruption method for Verticillium dahliae. PhytoPathology 2016, 106, 645–652. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Xu, D.; Zhao, X.; Xu, C.; Zhang, C.; Huang, J. VdSOX1 Negatively Regulates Verticillium dahliae Virulence via Enhancing Effector Expression and Suppressing Host Immune Responses. J. Fungi 2025, 11, 576. https://doi.org/10.3390/jof11080576
Xu D, Zhao X, Xu C, Zhang C, Huang J. VdSOX1 Negatively Regulates Verticillium dahliae Virulence via Enhancing Effector Expression and Suppressing Host Immune Responses. Journal of Fungi. 2025; 11(8):576. https://doi.org/10.3390/jof11080576
Chicago/Turabian StyleXu, Di, Xiaoqiang Zhao, Can Xu, Chongbo Zhang, and Jiafeng Huang. 2025. "VdSOX1 Negatively Regulates Verticillium dahliae Virulence via Enhancing Effector Expression and Suppressing Host Immune Responses" Journal of Fungi 11, no. 8: 576. https://doi.org/10.3390/jof11080576
APA StyleXu, D., Zhao, X., Xu, C., Zhang, C., & Huang, J. (2025). VdSOX1 Negatively Regulates Verticillium dahliae Virulence via Enhancing Effector Expression and Suppressing Host Immune Responses. Journal of Fungi, 11(8), 576. https://doi.org/10.3390/jof11080576