State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo 315211, China.
Department of Plant Pathology, College of Plant Protection, Henan Agricultural University, Zhengzhou 450002, China.
Proc Natl Acad Sci U S A. 2024 Apr 16;121(16):e2318783121. doi: 10.1073/pnas.2318783121. Epub 2024 Apr 8.
Communication between insects and plants relies on the exchange of bioactive molecules that traverse the species interface. Although proteinic effectors have been extensively studied, our knowledge of other molecules involved in this process remains limited. In this study, we investigate the role of salivary microRNAs (miRNAs) from the rice planthopper in suppressing plant immunity. A total of three miRNAs were confirmed to be secreted into host plants during insect feeding. Notably, the sequence-conserved miR-7-5P is specifically expressed in the salivary glands of and is secreted into saliva, distinguishing it significantly from homologues found in other insects. Silencing miR-7-5P negatively affects feeding on rice plants, but not on artificial diets. The impaired feeding performance of miR-7-5P-silenced insects can be rescued by transgenic plants overexpressing miR-7-5P. Through target prediction and experimental testing, we demonstrate that miR-7-5P targets multiple plant genes, including the immune-associated bZIP transcription factor 43 (OsbZIP43). Infestation of rice plants by miR-7-5P-silenced insects leads to the increased expression of , while the presence of miR-7-5P counteracts this upregulation effect. Furthermore, overexpressing OsbZIP43 confers plant resistance against insects which can be subverted by miR-7-5P. Our findings suggest a mechanism by which herbivorous insects have evolved salivary miRNAs to suppress plant immunity, expanding our understanding of cross-kingdom RNA interference between interacting organisms.
昆虫与植物之间的通讯依赖于跨越物种界面的生物活性分子的交换。尽管蛋白效应物已被广泛研究,但我们对参与这一过程的其他分子的了解仍然有限。在这项研究中,我们研究了水稻褐飞虱唾液中的 microRNAs(miRNAs)在抑制植物免疫中的作用。共有 3 种 miRNA 被证实可在昆虫取食过程中分泌到宿主植物中。值得注意的是,序列保守的 miR-7-5P 特异性表达于 唾液腺中,并分泌到唾液中,与其他昆虫中发现的同源物明显不同。沉默 miR-7-5P 会负向影响 对水稻植株的取食,但对人工饲料没有影响。miR-7-5P 沉默昆虫的取食性能受损可以通过过表达 miR-7-5P 的转基因植物得到挽救。通过靶标预测和实验验证,我们证明 miR-7-5P 靶向多个植物基因,包括免疫相关的 bZIP 转录因子 43(OsbZIP43)。miR-7-5P 沉默的昆虫侵害水稻植株会导致 表达增加,而 miR-7-5P 的存在则抵消了这种上调效应。此外,过表达 OsbZIP43 赋予植物对昆虫的抗性,而 miR-7-5P 可以削弱这种抗性。我们的研究结果表明,植食性昆虫进化出唾液 miRNA 来抑制植物免疫的机制,扩展了我们对相互作用生物之间跨物种 RNA 干扰的理解。