褐飞虱繁殖和免疫介导的生活史性状的权衡

doi:10.1016/j.jia.2024.03.062

摘要/Abstract

摘要： 繁殖和免疫防御均具有高昂的适合度代价，两者之间的权衡往往推动进化。褐飞虱隶属于半翅目，飞虱科，是一种全球性超级害虫，主要危害水稻作物。类酵母共生体（YLS）存在于褐飞虱的腹部脂肪体中，与褐飞虱的生长、发育和繁殖密切相关。我们之前的研究表明，交配行为会促进褐飞虱将YLS从脂肪体释放到血淋巴中，从而引发免疫反应。此外，褐飞虱生命史特征（如存活率）相关的适合度代价与 YLS 的相对丰度密切相关。然而，褐飞虱的繁殖和免疫可能存在的模式尚未确定。本研究采用组学的方法对羽化后72 h交配和未交配的褐飞虱脂肪体组织的转录组进行分析，从中筛选出了两个在褐飞虱交配后高表达的抗菌肽基因NlDefensin A (NlDfA)和NlDefensin (NlDfB)。随后，克隆并分析了NlDfA和NlDfB基因的全长CDs序列。qPCR 结果表明，与未交配的褐飞虱相比，交配后的褐飞虱体内NlDfA和NlDfB基因显著上调。时空表达分析表明，NlDfA和NlDfB基因在所有组织和发育阶段均有表达，且在羽化后24 h的脂肪体中表达量最高。NlDfA和NlDfB蛋白的体外表达对褐飞虱中的共生菌有明显的抑制作用。此外，通过RNA干扰技术沉默NlDfA和NlDfB基因的表达，显著增加了脂肪体中YLS的相对丰度，而血淋巴中的YLS则明显减少，与适合度代价相关的生物学参数（如存活率、繁殖力、孵化率等）均显著下降，同时，YLS从血淋巴到卵的垂直传递也受到抑制。我们的研究结果表明，交配行为可以通过上调NlDfA和NlDfB基因的表达来提高褐飞虱的免疫力，从而保护宿主在繁殖过程中免受病原体的攻击，然而，YLS含量的降低可能会成为褐飞虱生命史性状的一个不利因素。这项工作对于以关键靶基因为导向的褐飞虱精准绿色防控技术以及昆虫的"以菌治虫"策略的提出具有重要的理论和实践意义。

Abstract:

Reproduction and immune defense are costly functions, and they are expected to tradeoff with each other to drive evolution. The brown planthopper (BPH), Nilaparvata lugens Stål (Hemiptera, Delphacidae), is a global superpest that mostly damages rice crops. Yeast-like symbionts (YLS) exist in the abdominal fat body tissue and are tightly associated with the development, growth, and reproduction of BPH. Our previous research demonstrated that mating behavior promotes the release of YLS from the fat body into the hemolymph in the BPH, thereby triggering an immune response. Additionally, the fitness costs related to life-history traits of BPH (such as survival rate) have a strong dependence on the relative abundance of YLS. However, the possible relationship between reproduction and the immune response in BPH has not been identified. In this study, an omics-based approach was used to analyze the transcriptome of fat body tissues in mated and unmated BPH at 72 h post-eclosion, from which two antimicrobial peptide genes, NlDefensin A (NlDfA) and NlDefensin B (NlDfB), were selected since they were highly expressed in mated BPH. Subsequently, the full-length cDNA sequences of the NlDfA and NlDfB genes were cloned and analyzed. qPCR results showed up-regulation of the NlDfA and NlDfB genes in mated BPH when compared to unmated BPH. Spatial-temporal expression analysis indicated that the NlDfA and NlDfB genes were expressed in all tissues and developmental stages, and they were most highly expressed in the fat body at 24 h post-eclosion. Moreover, the symbionts in BPH were significantly inhibited by the in vitro expression of the NlDfA and NlDfB proteins. Furthermore, RNA interference (RNAi)-mediated suppression of NlDfA and NlDfB dramatically increased the relative abundance of YLS in the fat body, while YLS in the hemolymph decreased significantly. These BPHs also displayed some fitness disadvantages in survival, fecundity, hatchability, and possibly the vertical transmission of YLS from hemolymph to egg. Our results indicated that mating could heighten the immunity of BPH by up-regulating the expression of the NlDfA and NlDfB genes, which protect the host from pathogen challenges during reproduction. However, the reduced content of YLS may act as a fitness disadvantage in dictating the life-history traits of BPH. This work has significant theoretical and practical implications for the precise green control technology that involves crucial gene targeting, as well as for the “endosymbionts for pest control” strategy in insects.

Key words: Nilaparvata lugens , reproduction , immune defense , trade-off

中图分类号:

. 褐飞虱繁殖和免疫介导的生活史性状的权衡[J]. Journal of Integrative Agriculture, 2024, 23(6): 2018-2032.

Dan Sun, Hongfeng Wang, Jiahui Zeng, Qiuchen Xu, Mingyun Wang, Xiaoping Yu, Xuping Shentu. The life-history trait trade-offs mediated by reproduction and immunity in the brown planthopper, Nilaparvata lugens Stål[J]. Journal of Integrative Agriculture, 2024, 23(6): 2018-2032.

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