J Integr Plant Biol ›› 2022, Vol. 64 ›› Issue (10): 1994-2008.DOI: 10.1111/jipb.13344

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  • 收稿日期:2022-06-22 接受日期:2022-08-15 出版日期:2022-10-01 发布日期:2022-10-20

The Xanthomonas type III effector XopAP prevents stomatal closure by interfering with vacuolar acidification

Longyu Liu1,2, Ying Li1, Zhengyin Xu1, Huan Chen2,3, Jingyi Zhang2,3, Brittany Manion2, Fengquan Liu3, Lifang Zou1, Zheng Qing Fu2* and Gongyou Chen1*   

  1. 1 State Key Laboratory of Microbial Metabolism/Shanghai Collaborative Innovation Center of Agri‐Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200240, China
    2 Department of Biological Sciences, University of South Carolina, Columbia 29208, USA
    3 Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China

    *Correspondences: Gongyou Chen (gyouchen@sjtu.edu.cn, Dr. Chen is fully responsible for the distribution of the materials associated with this article); Zheng Qing Fu (zfu@mailbox.sc.edu)
  • Received:2022-06-22 Accepted:2022-08-15 Online:2022-10-01 Published:2022-10-20

Abstract: Plant stomata close rapidly in response to a rise in the plant hormone abscisic acid (ABA) or salicylic acid (SA) and after recognition of pathogen-associated molecular patterns (PAMPs). Stomatal closure is the result of vacuolar convolution, ion efflux, and changes in turgor pressure in guard cells. Phytopathogenic bacteria secrete type III effectors (T3Es) that interfere with plant defense mechanisms, causing severe plant disease symptoms. Here, we show that the virulence and infection of Xanthomonas oryzae pv. oryzicola (Xoc), which is the causal agent of rice bacterial leaf streak disease, drastically increased in transgenic rice (Oryza sativa L.) plants overexpressing the Xoc T3E gene XopAP, which encodes a protein annotated as a lipase. We discovered that XopAP binds to phosphatidylinositol 3,5-bisphosphate (PtdIns(3,5)P2), a membrane phospholipid that functions in pH control in lysosomes, membrane dynamics, and protein trafficking. XopAP inhibited the acidification of vacuoles by competing with vacuolar H+-pyrophosphatase (V-PPase) for binding to PtdIns(3,5)P2, leading to stomatal opening. Transgenic rice overexpressing XopAP also showed inhibition of stomatal closure when challenged by Xoc infection and treatment with the PAMP flg22. Moreover, XopAP suppressed flg22-induced gene expression, reactive oxygen species burst and callose deposition in host plants, demonstrating that XopAP subverts PAMP-triggered immunity during Xoc infection. Taken together, these findings demonstrate that XopAP overcomes stomatal immunity in plants by binding to lipids.

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