干旱区生态环境知识资源中心(Arid): Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts

Arid

DOI	10.1371/journal.pgen.1008762
	Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts
	Guo, Wei 1,2; Song, Juan 1,2; Yang, Pengcheng 3; Chen, Xiangyong 1; Chen, Dafeng 1; Ren, Dani 1; Kang, Le 1,2,3; Wang, Xianhui 1,2
通讯作者	Kang, Le ; Wang, Xianhui
来源期刊	PLOS GENETICS
ISSN	1553-7404
出版年	2020
卷号	16 期号:4
英文摘要	Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase polyphenism involving remarkably behavioral plasticity between gregarious and solitarious phases. Here, we report that a major insect hormone, juvenile hormone, is involved in the regulation of this behavioral plasticity related to phase change by influencing the expression levels of olfactory-related genes in the migratory locust. We found that the treatment of juvenile hormone analog, methoprene, can significantly shift the olfactory responses of gregarious nymphs from attraction to repulsion to the volatiles released by gregarious nymphs. In contrast, the repulsion behavior of solitarious nymphs significantly decreased when they were treated with precocene or injected with double-stranded RNA of JHAMT, a juvenile hormone acid O-methyltransferase. Further, JH receptor Met or JH-response gene Kr-h1 knockdown phenocopied the JH-deprivation effects on olfactory behavior. RNA-seq analysis identified 122 differentially expressed genes in antennae after methoprene application on gregarious nymphs. Interestingly, several olfactory-related genes were especially enriched, including takeout (TO) and chemosensory protein (CSP) which have key roles in behavioral phase change of locusts. Furthermore, methoprene application and Met or Kr-h1 knockdown resulted in simultaneous changes of both TO1 and CSP3 expression to reverse pattern, which mediated the transition between repulsion and attraction responses to gregarious volatiles. Our results suggest the regulatory roles of a pleiotropic hormone in locust behavioral plasticity through modulating gene expression in the peripheral olfactory system. Author summary A behavioral change from shy solitarious individuals to highly social gregarious individuals is critical to the formation of disastrous swarms of locusts. However, the underlying molecular mechanism of behavioral plasticity regulated by hormones is still largely unknown. Here, we investigated the effect of juvenile hormone (JH) on the behavioral transition in fourth-instar gregarious and solitarious locusts. We found that JH induced the behavioral shift of the gregarious locust from attraction to repulsion to the volatiles of gregarious locusts. The solitarious locust significantly decreased repulsion behavior after deprivation of JH by precocene or knockdown of JHAMT, a key enzyme to synthesize JH. JH application on gregarious locusts caused significant expression alteration of genes, especially the olfactory genes TO and CSP in the antennae. We further demonstrated that the JH signaling pathway suppressed aggregation behavior in gregarious locusts by increasing TO1 expression and decreasing CSP3 expression at the same time. Our results suggested that internal physiological factors can directly modulate periphery olfactory system to produce behavioral plasticity.
类型	Article
语种	英语
国家	Peoples R China
开放获取类型	gold, Green Published
收录类别	SCI-E
WOS记录号	WOS:000531363700003
WOS关键词	SCHISTOCERCA-GREGARIA ; PHASE-CHANGES ; MIGRATORY LOCUST ; DESERT LOCUST ; PHEROMONE ; PLASTICITY ; MODULATION ; EMISSION ; FAMILY
WOS类目	Genetics & Heredity
WOS研究方向	Genetics & Heredity
资源类型	期刊论文
条目标识符	http://119.78.100.177/qdio/handle/2XILL650/318943
作者单位	1.Chinese Acad Sci, Inst Zool, State Key Lab Integrated Management Pest Insects, Beijing, Peoples R China; 2.Univ Chinese Acad Sci, CAS Ctr Excellence Biot Interact, Beijing, Peoples R China; 3.Chinese Acad Sci, Beijing Inst Life Sci, Beijing, Peoples R China
推荐引用方式 GB/T 7714	Guo, Wei,Song, Juan,Yang, Pengcheng,et al. Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts[J],2020,16(4).
APA	Guo, Wei.,Song, Juan.,Yang, Pengcheng.,Chen, Xiangyong.,Chen, Dafeng.,...&Wang, Xianhui.(2020).Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts.PLOS GENETICS,16(4).
MLA	Guo, Wei,et al."Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts".PLOS GENETICS 16.4(2020).