Yao Zhuotian, Sun Xiujia, Wu Xiaoshuang, Zhu Fengqin, Huang Jianhua, Zhang Wei, Ma Weihua, Hua Hongxia, Lin Yongjun
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.
State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing 100871, China.
Int J Biol Macromol. 2024 Dec;282(Pt 2):136861. doi: 10.1016/j.ijbiomac.2024.136861. Epub 2024 Oct 25.
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.
耐寒性是变温动物适应陆地环境和种内地理谱系多样化的重要生理特征，但目前对其潜在遗传机制和进化仍缺乏系统研究。为了解决这一问题，我们以广泛分布的水稻害虫二化螟为模型，探索耐寒性的遗传机制和进化历史。首先，我们通过对实验室饲养品系中的潜在关键基因进行功能验证，系统地描述了其抗冻机制。这揭示了甘油生物合成在耐寒性中的功能作用，包括通过三酰甘油脂肪酶（Tgl）水解的三酰甘油起源途径和通过α-淀粉酶（Aa）和麦芽糖酶（Ma）水解的糖原起源途径，以及细胞伴侣Hsc70和Hsf1的作用。然后，我们通过收集代表性地理样本并进行群体遗传分析来研究耐寒性的进化，这表明不同地理种群的冷适应策略有所不同。综上所述，我们的研究结果证明了二化螟抗寒的功能基础，揭示了自然种群中耐寒性的进化历史，为生物耐寒性提供了见解，并为害虫防治提供了线索。
