The secretome of Verticillium dahliae in collusion with plant defence responses modulates Verticillium wilt symptoms

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

Submitted to: Biological Reviews
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/14/2022
Publication Date: 4/27/2022
Citation: Zhang, D., Dai, X., Klosterman, S.J., Subbarao, K.V., Chen, J. 2022. The secretome of Verticillium dahliae in collusion with plant defence responses modulates Verticillium wilt symptoms. Biological Reviews. 97(5):1810-1822. https://doi.org/10.1111/brv.12863.
DOI: https://doi.org/10.1111/brv.12863

Interpretive Summary: Verticillium dahliae is a broad host range fungal pathogen that affects numerous economically important plants worldwide. One of the hallmark symptoms that this pathogen causes is foliar wilting, and hence the plant disease that it causes is known as Verticillium wilt. Because the pathogen resides for part of its disease cycle in the water conducting plant vascular tissue, one historical hypothesis included the physical occlusion of vascular system to cause wilting. The other hypothesis, that proteins and other molecules secreted from the pathogen play a prominent role in causing wilt, is also likely. This work suggests from a synthesis of the literature indicates that the two ideas are not mutually exclusive, and that the cause of Verticillium wilt symptoms is a combination of physical occlusion and the result of secreted components from the pathogen.

Technical Abstract: Verticillium dahliae is a notorious soil-borne pathogen that enters hosts through the roots and proliferates in the plant water-conducting elements to cause Verticillium wilt. Historically, Verticillium wilt symptoms have been explained by vascular occlusion, due to the accumulation of mycelia and plant biomacromolecule aggregation, and also by phytotoxicity caused by pathogen-secreted toxins. Beyond the direct cytotoxicity of some members of the secretome, this review systematically discusses the roles of the V. dahliae secretome in vascular occlusion, including the deposition of polysaccharides as an outcome of plant cell wall destruction, the accumulation of fungal mycelia, and modulation of plant defence responses. By modulating plant defences and hormone levels, the secretome manipulates the vascular environment to induce Verticillium wilt. Thus, the secretome of V. dahliae colludes with plant defence responses to modulate Verticillium wilt symptoms, and thereby bridges the historical concepts of both toxin production by the pathogen and vascular occlusion as the cause of wilting symptoms.