Functional and evolutionary analysis of key enzymes triacylglycerol lipase, glycogen hydrolases in the glycerol and glucose biosynthesis pathway and cellular chaperones for freeze-tolerance of the Rice stem borer, Chilo suppressalis

Zhuotian Yao; Xiujia Sun; Xiaoshuang Wu; Fengqin Zhu; Jianhua Huang; Wei Zhang; Weihua Ma; Hongxia Hua; Yongjun Lin

doi:10.1016/j.ijbiomac.2024.136861

Functional and evolutionary analysis of key enzymes triacylglycerol lipase, glycogen hydrolases in the glycerol and glucose biosynthesis pathway and cellular chaperones for freeze-tolerance of the Rice stem borer, Chilo suppressalis

Int J Biol Macromol. 2024 Oct 25:136861. doi: 10.1016/j.ijbiomac.2024.136861. Online ahead of print.

Authors

Zhuotian Yao¹, Xiujia Sun², Xiaoshuang Wu³, Fengqin Zhu⁴, Jianhua Huang⁵, Wei Zhang⁶, Weihua Ma⁷, Hongxia Hua⁸, Yongjun Lin⁹

Affiliations

¹ National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Hubei Hongshan Laboratory, College of Plant Science and Technology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China. Electronic address: yaozhuotian@webmail.hzau.edu.cn.
² State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing 100871, China. Electronic address: sunxj@pku.edu.cn.
³ National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Hubei Hongshan Laboratory, College of Plant Science and Technology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China. Electronic address: wuxiaoshuang@webmail.hzau.edu.cn.
⁴ National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Hubei Hongshan Laboratory, College of Plant Science and Technology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China. Electronic address: zhufengqin@webmail.hzau.edu.cn.
⁵ Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China. Electronic address: jhhuang@zju.edu.cn.
⁶ State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing 100871, China. Electronic address: weizhangvv@pku.edu.cn.
⁷ National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Hubei Hongshan Laboratory, College of Plant Science and Technology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China. Electronic address: weihuama@mail.hzau.edu.cn.
⁸ National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Hubei Hongshan Laboratory, College of Plant Science and Technology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China. Electronic address: huahongxia@mail.hzau.edu.cn.
⁹ National Key Laboratory of Crop Genetic Improvement and National Centre of Plant Gene Research, Hubei Hongshan Laboratory, College of Plant Science and Technology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei, China. Electronic address: yongjunlin@mail.hzau.edu.cn.

PMID: 39490866
DOI: 10.1016/j.ijbiomac.2024.136861

Abstract

Freeze-tolerance is an important physiological trait for terrestrial environmental adaptation and intraspecific geographic-lineage diversification in ectothermic animals, yet there remains a lack of systematic studies on its underlying genetic mechanisms and evolution. To address this problem, we employed the widely distributed rice pest, the Chilo suppressalis, as a model to explore the genetic mechanisms and evolutionary history of freeze-tolerance. First, we systematically characterized its antifreeze mechanisms by performing functional validation of potential key genes in laboratory-reared lines. This revealed the functional roles of glycerol biosynthesis in freeze-tolerance, including the triacylglycerol-originated pathway via triacylglycerol lipase (Tgl) hydrolysis and the glycogen-originated pathway via α-amylase (Aa) and maltase (Ma) hydrolysis, as well as the roles of the cellular chaperones Hsc70 and Hsf1. Then, we investigated the evolution of freeze-tolerance by collecting representative geographical samples and performing population genetic analyses, which suggested differentiated strategies of cold adaptation in different geographic populations. Taken together, our findings demonstrate the functional basis of cold resistance in Chilo suppressalis and reveal the evolutionary history of freeze-tolerance in natural populations, providing insights into organismal freeze-tolerance and clues for pest control.

Keywords: Cold adaptation; Cryoprotectant; Diversification; Evolution; Geographical populations; Overwintering; Protein chaperone.