Han Wen-Hao, Ji Shun-Xia, Zhang Feng-Bin, Song Hong-Da, Wang Jun-Xia, Fan Xiao-Ping, Xie Rui, Liu Shu-Sheng, Wang Xiao-Wei
State Key Laboratory of Rice Biology and Breeding, Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China.
LC-Bio Technology Co., Ltd, Hangzhou, China.
Mol Plant. 2025 Mar 3;18(3):437-456. doi: 10.1016/j.molp.2025.01.001. Epub 2025 Jan 3.
Herbivore insects deploy salivary effectors to manipulate the defense of their host plants. However, it remains unclear whether small RNAs from insects can function as effectors in regulating plant-insect interactions. Here, we report that a microRNA (miR29-b) found in the saliva of the phloem-feeding whitefly (Bemisia tabaci) can transfer into the host plant phloem during feeding and fine-tune the defense response of tobacco (Nicotiana tabacum) plants. We show that the salivary gland-enriched BtmiR29-b is produced by BtDicer 1 and released into tobacco cells via salivary exosomes. Once inside the plant cells, BtmiR29-b hijacks tobacco Argonaute 1 to silence the defense gene Bcl-2-associated athanogene 4 (NtBAG4). In tobacco, NtBAG4 acts as the positive regulator of phytohormones salicylic acid (SA) and jasmonic acid (JA), enhancing plant defense against whitefly attacks. Interestingly, we also found that miR29-b acts as a salivary effector in another Hemipteran insect, the aphid Myzus persicae, which inhibits tobacco resistance by degrading NtBAG4. Moreover, miR29-b is highly conserved in Hemiptera and across other insect orders such as Coleoptera, Hymenoptera, Orthoptera, and Blattaria. Computational analysis suggests that miR29-b may also target the evolutionarily conserved BAG4 gene in other plant species. We further provide evidence showing BtmiR29-b-mediated BAG4 cleavage and defense suppression in tomato (Solanum lycopersicum). Taken together, our work reveals that a conserved miR29-b effector from insects fine-tunes plant SA- and JA-mediated defense by cross-kingdom silencing of the host plant BAG4 gene, providing new insight into the defense and counter-defense mechanisms between herbivores and their host plants.
植食性昆虫会分泌唾液效应蛋白来操控宿主植物的防御机制。然而，昆虫产生的小RNA是否能作为效应分子来调节植物与昆虫之间的相互作用仍不清楚。在此，我们报道，在取食韧皮部的烟粉虱（Bemisia tabaci）唾液中发现的一种微小RNA（miR29-b），在取食过程中可转移至宿主植物韧皮部，并微调烟草（Nicotiana tabacum）植株的防御反应。我们发现，在唾液腺中高度富集的BtmiR29-b由BtDicer 1产生，并通过唾液外泌体释放到烟草细胞中。一旦进入植物细胞，BtmiR29-b会利用烟草AGO1蛋白使防御基因Bcl-2相关死亡促进因子4（NtBAG4）沉默。在烟草中，NtBAG4作为植物激素水杨酸（SA）和茉莉酸（JA）的正向调节因子，增强植物对烟粉虱攻击的防御能力。有趣的是，我们还发现miR29-b在另一种半翅目昆虫——桃蚜（Myzus persicae）中也作为唾液效应分子发挥作用，它通过降解NtBAG4来抑制烟草的抗性。此外，miR29-b在半翅目以及鞘翅目、膜翅目、直翅目和蜚蠊目等其他昆虫目中高度保守。计算分析表明，miR29-b可能还靶向其他植物物种中进化保守的BAG4基因。我们进一步提供证据表明，BtmiR29-b可介导番茄（Solanum lycopersicum）中BAG4的切割并抑制其防御反应。综上所述，我们的研究揭示了一种来自昆虫的保守miR29-b效应分子，通过对宿主植物BAG4基因进行跨界沉默来微调植物SA和JA介导的防御反应，为食草动物及其宿主植物之间的防御和反防御机制提供了新的见解。
