A small RNA effector conserved in herbivore insects suppresses host plant defense by cross-kingdom gene silencing  

作　　者：Wen-Hao Han Shun-Xia Ji Feng-Bin Zhang Hong-Da Song Jun-Xia Wang Xiao-Ping Fan Rui Xie Shu-Sheng Liu Xiao-Wei Wang 

机构地区：[1]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 [2]LC-Bio Technology Co.,Ltd,Hangzhou,China

出　　处：《Molecular Plant》2025年第3期437-456,共20页分子植物(英文版)

基　　金：supported by National Natural Science Foundation of China(31925033,32161143008);National Key Research and Development Program(2021YFC2600100).

摘　　要：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.

关 键 词：cross-kingdom regulation plant-insect interaction salivary effector small RNA insect exosomes 

分 类 号：Q943[生物学—植物学]