Two sex pheromone receptors for sexual communication in the American cockroach

Na Li; Renke Dong; Huanchao Zeng; Yan Zhang; Run Huang; Wei Liu; Fengming Cao; Jincong Yu; Mingtao Liao; Jingyou Chen; Wenlei Zhang; Zejian Huang; Jiahui Wang; Li Li; Shen Zhu; Danyan Huang; Zining Li; Xiaoshuai Zhang; Dongwei Yuan; Nan Chen; Yongliang Fan; Guirong Wang; Coby Schal; Yufeng Pan; Sheng Li

doi:10.1007/s11427-023-2548-3

Two sex pheromone receptors for sexual communication in the American cockroach

Sci China Life Sci. 2024 Mar 22. doi: 10.1007/s11427-023-2548-3. Online ahead of print.

Authors

Na Li^#^{1

2}, Renke Dong^#^{3

4}, Huanchao Zeng^#^{3

4}, Yan Zhang^#⁵, Run Huang^#³, Wei Liu⁵, Fengming Cao³, Jincong Yu³, Mingtao Liao³, Jingyou Chen³, Wenlei Zhang³, Zejian Huang³, Jiahui Wang³, Li Li³, Shen Zhu^{3

4}, Danyan Huang³, Zining Li³, Xiaoshuai Zhang³, Dongwei Yuan³, Nan Chen³, Yongliang Fan⁶, Guirong Wang⁵, Coby Schal⁷, Yufeng Pan⁸, Sheng Li^{9

10}

Affiliations

¹ Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal University, Guangzhou, 510631, China. lina5hs@m.scnu.edu.cn.
² Guangmeiyuan R&D Center, Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, South China Normal University, Meizhou, 514589, China. lina5hs@m.scnu.edu.cn.
³ Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal University, Guangzhou, 510631, China.
⁴ Guangmeiyuan R&D Center, Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, South China Normal University, Meizhou, 514589, China.
⁵ Lingnan Guangdong Laboratory of Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518000, China.
⁶ State Key Laboratory of Crop Stress Biology for Arid Areas, and Key Laboratory of Integrated Pest Management on the Loess Plateau of Ministry of Agriculture, Northwest A&F University, Yangling, 712100, China.
⁷ Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, 27695, USA.
⁸ The Key Laboratory of Developmental Genes and Human Disease, School of Life Science and Technology, Southeast University, Nanjing, 210096, China. pany@seu.edu.cn.
⁹ Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal University, Guangzhou, 510631, China. lisheng@scnu.edu.cn.
¹⁰ Guangmeiyuan R&D Center, Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, South China Normal University, Meizhou, 514589, China. lisheng@scnu.edu.cn.

^# Contributed equally.

PMID: 38523236
DOI: 10.1007/s11427-023-2548-3

Abstract

Volatile sex pheromones are vital for sexual communication between males and females. Females of the American cockroach, Periplaneta americana, produce and emit two sex pheromone components, periplanone-A (PA) and periplanone-B (PB). Although PB is the major sex attractant and can attract males, how it interacts with PA in regulating sexual behaviors is still unknown. In this study, we found that in male cockroaches, PA counteracted PB attraction. We identified two odorant receptors (ORs), OR53 and OR100, as PB/PA and PA receptors, respectively. OR53 and OR100 were predominantly expressed in the antennae of sexually mature males, and their expression levels were regulated by the sex differentiation pathway and nutrition-responsive signals. Cellular localization of OR53 and OR100 in male antennae further revealed that two types of sensilla coordinate a complex two-pheromone-two-receptor pathway in regulating cockroach sexual behaviors. These findings indicate distinct functions of the two sex pheromone components, identify their receptors and possible regulatory mechanisms underlying the male-specific and age-dependent sexual behaviors, and can guide novel strategies for pest management.

Keywords: cockroach; odorant receptor; sex differentiation; sex pheromone; sexual attraction.