The Verticillium dahliae small cysteine-rich protein VdSCP23 manipulates host immunity

Authors: WANG, JIE - Shanxi Agriculture University; WANG, DAN - Chinese Academy Of Agricultural Sciences; JI, XIAOBIN - Chinese Academy Of Agricultural Sciences; WANG, JUN - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; DAI, XIAOFENG - Chinese Academy Of Agricultural Sciences; CHEN, JIEYIN - Chinese Academy Of Agricultural Sciences; SUBBARAO, KRISHNA - University Of California; HAO, XIAOJUAN - Shanxi Agriculture University; ZHANG, DANDAN - Chinese Academy Of Agricultural Sciences

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/24/2023
Publication Date: 5/28/2023
Citation: Wang, J., Wang, D., Ji, X., Wang, J., Klosterman, S.J., Dai, X., Chen, J., Subbarao, K.V., Hao, X., Zhang, D. 2023. The Verticillium dahliae small cysteine-rich protein VdSCP23 manipulates host immunity. International Journal of Molecular Sciences. 24(11). Article 9403. https://doi.org/10.3390/ijms24119403.
DOI: https://doi.org/10.3390/ijms24119403

Interpretive Summary: The fungus Verticillium dahliae is the cause of devastating vascular wilt diseases on hundreds of plant species worldwide, from trees to shrubs to high value crops. Determining how this pathogen causes disease, and specifically the mechanisms at the cellular and molecular level by which the pathogen is perceived by the plant immune system is very important for developing plant disease resistance. In this study, a gene from V. dahliae was determined to encode a protein product named VdSCP23 that is capable of translocating from the fungus to the plant cell, where it is believed to modulate plant immunity by inhibiting plant defense responses.

Technical Abstract: Verticillium wilt caused by Verticillium dahliae is a notorious soil-borne fungal disease and seriously threatens the yield of economic crops worldwide. During host infection, V. dahliae secretes many effectors that manipulate host immunity, among which small cysteine-rich proteins (SCPs) play an important role. However, the exact roles of many SCPs from V. dahliae are unknown and varied. In this study, we show that the small cysteine-rich protein VdSCP23 inhibits cell necrosis in Nicotiana benthamiana leaves, as well as the reactive oxygen species (ROS) burst, electrolyte leakage and the expression of defense-related genes. VdSCP23 is mainly localized in the plant cell plasma membrane and nucleus, but its inhibition of immune responses was independent of its nuclear localization. Site-directed mutagenesis and peptide truncation showed that the inhibition function of VdSCP23 was independent of cysteine residues but was dependent on the N-glycosylation sites and the integrity of VdSCP23 protein structure. Deletion of VdSCP23 did not affect the growth and development of mycelia or conidial production in V. dahliae. Unexpectedly, VdSCP23 deletion strains still maintained their virulence for N. benthamiana, Gossypium hirsutum and Arabidopsis thaliana seedlings. This study demonstrates an important role for VdSCP23 in the inhibition of plant immune responses; however, it is not required for normal growth or virulence in V. dahliae.