CSP and Takeout Genes Modulate the Switch between Attraction and Repulsion during Behavioral Phase Change in the Migratory Locust

Behavioral plasticity is the most striking trait in locust phase transition. However, the genetic basis for behavioral plasticity in locusts is largely unknown. To unravel the molecular mechanisms underlying the behavioral phase change in the migratory locust Locusta migratoria, the gene expression patterns over the time courses of solitarization and gregarization were compared by oligonucleotide microarray analysis. Data analysis revealed that several gene categories relevant to peripheral olfactory perception are strongly regulated in a total of 1,444 differentially expressed genes during both time courses. Among these candidate genes, several CSP (chemosensory protein) genes and one takeout gene, LmigTO1, showed higher expression in gregarious and solitarious locusts, respectively, and displayed opposite expression trends during solitarization and gregarization. qRT-PCR experiments revealed that most CSP members and LmigTO1 exhibited antenna-rich expressions. RNA interference combined with olfactory behavioral experiments confirmed that the CSP gene family and one takeout gene, LmigTO1, are involved in the shift from repulsion to attraction between individuals during gregarization and in the reverse transition during solitarization. These findings suggest that the response to locust-emitted olfactory cues regulated by CSP and takeout genes is involved in the behavioral phase change in the migratory locust and provide a previously undescribed molecular mechanism linked to the formation of locust aggregations.

行为可塑性是蝗虫型变中最显著的特征，但目前对于蝗虫行为可塑性的遗传基础仍知之甚少。为解析迁飞飞蝗（Locusta migratoria）行为型变的潜在分子机制，本研究采用寡核苷酸微阵列（oligonucleotide microarray）分析方法，对比了独居化与群居化时序过程中的基因表达模式。数据分析结果显示，在两类时序过程中共有的1444个差异表达基因中，多个与外周嗅觉感知相关的基因类别受到显著调控。在这些候选基因中，多个化学感受蛋白（CSP, chemosensory protein）基因以及一个取食调控基因（takeout）LmigTO1，分别在群居型与散居型飞蝗中呈高表达，且在独居化与群居化过程中呈现相反的表达趋势。实时定量聚合酶链反应（qRT-PCR）实验结果表明，多数CSP家族成员与LmigTO1均在触角组织中富集表达。RNA干扰（RNA interference）结合嗅觉行为实验证实，CSP基因家族与取食调控基因（takeout）LmigTO1参与了群居化过程中个体间从排斥到吸引的转变，以及独居化过程中的反向转变。上述研究结果表明，由CSP与takeout基因调控的、对飞蝗释放的嗅觉信号的应答过程参与了迁飞飞蝗的行为型变，同时为飞蝗聚群形成的相关分子机制研究提供了此前未被报道的全新机制。