Liu Jiaqi, Ma Tao, Liang Jianxiang, Yang Bohan, Chen Shuyun, Li Xinlong, Wu Wei, Lu Jiang, Fu Peining
Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240, China.
Plant J. 2025 Apr;122(2):e70143. doi: 10.1111/tpj.70143.
Grapevine (Vitis vinifera L.) frequently faces challenges from various pathogens, among which Plasmopara viticola is the most devastating one hindering grape production. During infection, P. viticola secretes a series of effectors into host cells to manipulate plant immune responses. Here, an RXLR effector of P. viticola, PvRXLR13, was identified as one that could disrupt immune processes and thus promote pathogen colonization. PvRXLR13 contained a functional signal peptide and was highly conserved across different destructive oomycetes. PvRXLR13 was significantly induced during P. viticola infection and could suppress elicitor chitin-induced reactive oxygen species (ROS), callose deposition, and INF1-triggered cell death. Furthermore, PvRXLR13 could also inhibit P. viticola- and P. capsici-triggered HO accumulation and promote pathogen colonization in both grapevine and Nicotiana benthamiana, respectively. VvHY5, a basic leucine zipper (bZIP) transcription factor, was found to be the host target of PvRXLR13. Further analysis revealed that overexpression of VvHY5 enhanced grapevine resistance to P. viticola and P. viticola-triggered HO accumulation. Furthermore, we found that VvHY5 directly bound to the promoter of the positive immune factor VvEDS1 and activated its expression, whereas PvRXLR13 attenuated the DNA-binding activity of VvHY5 during P. viticola infection. Further analysis revealed that other members of grape bZIPs, VvbZIP6/9/21/32/34/37, were also involved in the defense response against P. viticola invasion. Just like HY5/HYH, all these bZIP family members were targeted by the effector PvRXLR13. Collectively, our findings suggest that P. viticola secretes a key effector PvRXLR13 to compromise the function in immune regulation of bZIP transcription factors to promote infection in grapevine.
葡萄（Vitis vinifera L.）经常面临各种病原体的挑战，其中葡萄霜霉病菌（Plasmopara viticola）是阻碍葡萄生产的最具破坏性的病原体。在感染过程中，葡萄霜霉病菌会向宿主细胞分泌一系列效应蛋白来操纵植物的免疫反应。在此，葡萄霜霉病菌的一种RXLR效应蛋白PvRXLR13被鉴定为能够破坏免疫过程从而促进病原体定殖的蛋白。PvRXLR13含有一个功能性信号肽，在不同的破坏性卵菌中高度保守。PvRXLR13在葡萄霜霉病菌感染期间显著诱导表达，并且能够抑制激发子几丁质诱导的活性氧（ROS）产生、胼胝质沉积以及INF1触发的细胞死亡。此外，PvRXLR13还能够分别抑制葡萄霜霉病菌和辣椒疫霉（Phytophthora capsici）触发的HO积累，并促进病原体在葡萄和本氏烟草（Nicotiana benthamiana）中的定殖。VvHY5是一种碱性亮氨酸拉链（bZIP）转录因子，被发现是PvRXLR13的宿主靶标。进一步分析表明，VvHY5的过表达增强了葡萄对葡萄霜霉病菌的抗性以及葡萄霜霉病菌触发的HO积累。此外，我们发现VvHY5直接结合到正向免疫因子VvEDS1的启动子上并激活其表达，而在葡萄霜霉病菌感染期间PvRXLR13会减弱VvHY5的DNA结合活性。进一步分析表明，葡萄bZIP家族的其他成员VvbZIP6/9/21/32/34/37也参与了对葡萄霜霉病菌入侵的防御反应。就像HY5/HYH一样，所有这些bZIP家族成员都被效应蛋白PvRXLR13靶向。总的来说，我们的研究结果表明，葡萄霜霉病菌分泌关键效应蛋白PvRXLR13来损害bZIP转录因子的免疫调节功能，从而促进其在葡萄中的感染。
