Thioredoxin VdTrx1, an unconventional secreted protein, is a virulence factor in Verticillium dahliae

Frontiers in Microbiology · 9 authors, 6 centres

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Deletion of VdTrx1 reduced disease symptoms and fungal biomass in three host plants, indicating it is required for full virulence.

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The authors demonstrated VdTrx1 is unconventionally secreted into culture filtrate and localizes to host apoplastic space, with secretion depending on VdVps36 (an ESCRT-II complex component) rather than VdGRASP. Deletion of VdTrx1 also impaired sulfite assimilation and sporulation. Plant infection assays across three hosts demonstrated that ΔVdTrx1 alleviated disease symptoms and reduced fungal biomass while maintaining penetration ability, suggesting reduced viability in host vascular tissue underlies attenuated virulence.

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preclinical research

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ORIGINAL PAPER

PMC10102666

Thioredoxin VdTrx1, an unconventional secreted protein, is a virulence factor in Verticillium dahliae

Frontiers in Microbiology

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ABSTRACT

Abstract Understanding how plant pathogenic fungi adapt to their hosts is of critical importance to securing optimal crop productivity. In response to pathogenic attack, plants produce reactive oxygen species (ROS) as part of a multipronged defense response. Pathogens, in turn, have evolved ROS scavenging mechanisms to undermine host defense. Thioredoxins (Trx) are highly conserved oxidoreductase enzymes with a dithiol-disulfide active site, and function as antioxidants to protect cells against free radicals, such as ROS. However, the roles of thioredoxins in Verticillium dahliae , an important vascular pathogen, are not clear. Through proteomics analyses, we identified a putative thioredoxin (VdTrx1) lacking a signal peptide. VdTrx1 was present in the exoproteome of V. dahliae cultured in the presence of host tissues, a finding that suggested that it plays a role in host-pathogen interactions. We constructed a VdTrx1 deletion mutant Δ VdTrx1 that exhibited significantly higher sensitivity to ROS stress, H 2 O 2 , and tert -butyl hydroperoxide ( t -BOOH). In vivo assays by live-cell imaging and in vitro assays by western blotting revealed that while VdTrx1 lacking the signal peptide can be localized within V. dahliae cells, VdTrx1 can also be secreted unconventionally depending on VdVps36, a member of the ESCRT-II protein complex. The Δ VdTrx1 strain was unable to scavenge host-generated extracellular ROS fully during host invasion. Deletion of VdTrx1 resulted in higher intracellular ROS levels of V. dahliae mycelium, displayed impaired conidial production, and showed significantly reduced virulence on Gossypium hirsutum , and model plants, Arabidopsis thaliana and Nicotiana benthamiana . Thus, we conclude that VdTrx1 acts as a virulence factor in V. dahliae . Keywords: Verticillium dahliae , unconventional secreted protein, thioredoxin, ROS scavenging, virulence factor

CITATION EXPORT

Li Tian, Jing Zhuang, Jun-Jiao Li et al.. Thioredoxin VdTrx1, an unconventional secreted protein, is a virulence factor in Verticillium dahliae. Frontiers in Microbiology. (2023). https://doi.org/10.3389/fmicb.2023.1130468

AUTHORS

9 · 6 CENTRES

Li Tian, Jing Zhuang, Jun-Jiao Li, He Zhu, Steven J Klosterman, Xiao-Feng Dai, Jie-Yin Chen, Krishna V Subbarao, Dan-Dan Zhang

1School of Life Science, Qufu Normal University, Qufu, China
2State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
3National Cotton Industry Technology System Liaohe Comprehensive Experimental Station, The Cotton Research Center of Liaoning Academy of Agricultural Sciences, Liaoning Provincial Institute of Economic Crops, Liaoyang, China
4United States Department of Agriculture, Agricultural Research Service, Salinas, CA, United States
5Western Agricultural Research Center, Chinese Academy of Agricultural Sciences, Changji, China
6Department of Plant Pathology, University of California, Davis, c/o United States Agricultural Research Station, Salinas, CA, United States