Functional analysis of the mating type genes in Verticillium dahliae

Authors: ZHANG, YA-DUO - Chinese Academy Of Agricultural Sciences; JI, XIAO-BIN - Chinese Academy Of Agricultural Sciences; ZONG, JUAN - Chinese Academy Of Agricultural Sciences; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; SUBBARAO, KRISHNA - University Of California; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/22/2024
Publication Date: 5/7/2024
Citation: Zhang, Y.D., Ji, X.B., Zong, J., Dai, X.F., Klosterman, S.J., Subbarao, K.V., Zhang, D.D., Chen, J.Y. 2024. Functional analysis of the mating type genes in Verticillium dahliae. BMC Biology. 22. Article 108. https://doi.org/10.1186/s12915-024-01900-6.
DOI: https://doi.org/10.1186/s12915-024-01900-6

Interpretive Summary: Sexual reproduction in fungi is governed in part by the presence of mating (MAT) type genes, which confer mating types within a species. In the soilborne plant pathogenic fungus Verticillium dahliae, there are two mating type genes found within the population. Yet the function of these gene products has not been fully characterized because V. dahliae is considered asexual. In this study, V. dahliae was shown to respond to fungal pheromone produced by V. dahliae and another fungal species. The products of the two mating type genes in V. dahliae bound to gene regulatory regions of pheromone and pheromone receptor genes involved in mating. In addition to potential roles in regulating mating within V. dahliae, the study further revealed that the two mating type gene products in V. dahliae regulate vegetative growth, carbon source utilization, and resistance to stressors, while negatively regulating virulence. The findings provide new insight into the functional roles of the two MAT genes in V. dahliae.

Technical Abstract: Populations of the plant pathogenic fungus Verticillium dahliae display a complex and rich genetic diversity, yet the existence of sexual reproduction in the fungus remains contested. As pivotal genes, MAT genes play a crucial role in regulating cell differentiation, morphological development, and mating of compatible cells. However, the functions of the two mating type genes in V. dahliae, VdMAT1-1-1, and VdMAT1-2-1, remain poorly understood. In this study, we confirmed that the MAT loci in V. dahliae are highly conserved, including both VdMAT1-1-1 and VdMAT1-2-1 which share high collinearity. The conserved core transcription factor encoded by the two MAT loci may facilitate the regulation of pheromone precursor and pheromone receptor genes by directly binding to their promoter regions. Additionally, peptide activity assays demonstrated that the signal peptide of the pheromone VdPpg1 possessed secretory activity, while VdPpg2, lacked a predicted signal peptide. Chemotactic growth assays revealed that V. dahliae senses and grows towards the pheromones FO-a and FO-a of Fusarium oxysporum, as well as towards VdPpg2 of V. dahliae, but not in response to VdPpg1. The findings herein also revealed that VdMAT1-1-1 and VdMAT1-2-1 regulate vegetative growth, carbon source utilization, and resistance to stressors in V. dahliae, while negatively regulating virulence. These findings underscore the potential roles of VdMAT1-1-1 and VdMAT1-2-1 in sexual reproduction and confirm their involvement in various asexual processes of V. dahliae, offering novel insights into the functions of mating type genes in this species.