miR-31-5p regulates cold acclimation of the wood-boring beetle Monochamus alternatus via ascaroside signaling
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RESEARCH ARTICLE
Open Access
miR-31-5p regulates cold acclimation of the wood-boring beetle Monochamus alternatus via ascaroside signaling Bin Zhang1,2†, Lilin Zhao1,2†, Jing Ning1, Jacob D. Wickham1, Haokai Tian1,2, Xiaoming Zhang1, Meiling Yang1, Xiangming Wang3 and Jianghua Sun1,2*
Abstract Background: Survival to cold stress in insects living in temperate environments requires the deployment of strategies that lead to physiological changes involved in freeze tolerance or freeze avoidance. These strategies may consist of, for instance, the induction of metabolic depression, accumulation of cryoprotectants, or the production of antifreeze proteins, however, little is known about the way such mechanisms are regulated and the signals involved in their activation. Ascarosides are signaling molecules usually known to regulate nematode behavior and development, whose expression was recently found to relate to thermal plasticity in the Japanese pine sawyer beetle Monochamus alternatus. Accumulating evidence also points to miRNAs as another class of regulators differentially expressed in response to cold stress, which are predicted to target genes involved in cold adaptation of insects. Here, we demonstrate a novel pathway involved in insect cold acclimation, through miRNA-mediated regulation of ascaroside function. Results: We initially discovered that experimental cold acclimation can enhance the beetle’s cold hardiness. Through screening and functional verification, we found miR-31-5p, upregulated under cold stress, significantly contributes to this enhancement. Mechanistically, miR-31-5p promotes production of an ascaroside (asc-C9) in the beetle by negatively targeting the rate-limiting enzyme, acyl-CoA oxidase in peroxisomal β-oxidation cycles. Feeding experiments with synthetic asc-C9 suggests it may serve as a signal to promote cold acclimation through metabolic depression and accumulation of cryoprotectants with specific gene expression patterns. Conclusions: Our results point to important roles of miRNA-mediated regulation of ascaroside function in insect cold adaptation. This enhanced cold tolerance may allow higher survival of M. alternatus in winter and be pivotal in shaping its wide distribution range, greatly expanding the threat of pine wilt disease, and thus can also inspire the development of ascaroside-based pest management strategies. Keywords: Ascaroside, miRNAs, Phenotypic plasticity, Cold acclimation, Monochamus alternatus
* Correspondence: [email protected] † Bin Zhang and Lilin Zhao contributed equally to this work. 1 State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China 2 CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 10049, China Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing
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