The Acyl-CoA-binding protein VdAcb1 is essential for carbon starvation response and contributes to virulence in Verticillium dahliae

Authors: ZHUANG, JING - Chinese Academy Of Agricultural Sciences; ZHANG, YA-DUO - Chinese Academy Of Agricultural Sciences; SUN, WEI-XIA - Chinese Academy Of Agricultural Sciences; ZONG, JUAN - Qufu Normal University; LI, JUN-JIAO - Chinese Academy Of Agricultural Sciences; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences; TIAN, LI - Qufu Normal University; SUBBARAO, KRISHNA - University Of California; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences

Submitted to: aBIOTECH
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/22/2024
Publication Date: 7/13/2024
Citation: Zhuang, J., Zhang, Y.D., Sun, W.X., Zong, J., Li, J.-J., Dai, X.-F., Klosterman, S.J., Chen, J.-Y., Tian, L., Subbarao, K.V., Zhang, D.-D. 2024. The Acyl-CoA-binding protein VdAcb1 is essential for carbon starvation response and contributes to virulence in Verticillium dahliae. aBIOTECH. https://doi.org/10.1007/s42994-024-00175-3.
DOI: https://doi.org/10.1007/s42994-024-00175-3

Interpretive Summary: The fungus Verticillium dahliae is a soilborne plant pathogen that penetrates plant roots, invades the water conducting xylem tissue of the plant to cause wilt. This work characterizes a mechanism in the pathogen required for an adaptive response to carbon starvation. This research shows that the same mechanism is required for full pathogenicity on plants. The work provides evidence for the role of a gene encoding a protein that binds to a key metabolic protein and pathogenesis. The work further indicates that the binding protein is secreted from the fungus and interacts with a protein involved in signaling growth responses in this fungus. This study dissects role of several genes in V. dahliae whose products play roles in regulating signaling for nutrient starvation responses and plant pathogenesis. Knowledge on how these products function may be useful to devise alternative approaches to kill or inhibit the fungus for disease control.

Technical Abstract: In the face of carbon, nitrogen, and phosphorus starvation, microorganisms have evolved adaptive mechanisms to maintain growth. In a previous study, we identified a protein predicted to contain acyl-CoA-binding domains in the plant pathogenic fungus Verticillium dahliae. The predicted protein, designated VdAcb1, possesses an atypical signal peptide. However, the functions of this acyl-CoA-binding protein in V. dahliae are not clear. In this research, in vivo or in vitro assays confirmed that VdAcb1 is secreted extracellularly from V. dahliae, although it does not have the typical signal peptide. Furthermore, the unconventional secretion of VdAcb1 was dependent on VdGRASP, a member of the compartment for unconventional protein secretion (CUPS). The deletion mutant strain of VdAcb1 ('VdAcb1) exhibited significant sensitivity to carbon starvation. RNA-seq revealed that the expression of genes related to filamentous growth (MSB2 pathway) and sugar transport were regulated by VdAcb1 under conditions of carbon starvation. Yeast one-hybrid experiments further showed that the expression of VdAcb1 was positively regulated by the transcription factor VdMsn4. The 'VdAcb1 strain showed significantly reduced virulence on Gossypium hirsutum and Nicotiana benthamiana. We hypothesize that under conditions of carbon starvation, the expression of VdAcb1 is activated by VdMsn4 and VdAcb1 is secreted into the extracellular space. In turn, this activates the downstream MAPK pathway to enhance filamentous growth and virulence of V. dahliae.