Juvenile hormone induces reproduction via miR‐1175‐3p in the red imported fire ant, Solenopsis invicta

• Published in: Insect science 2024-04, Vol.31 (2), p.371-386
• Main Authors: Chen, Jie, Guan, Ziying, Ma, Yunjie, Shi, Qingxing, Chen, Ting, Waris, Muhammad Irfan, Lyu, Lihua, Lu, Yongyue, Qi, Guojun
• Format: Article
• Language: English
• Subjects: C protein; Caste differentiation; Fecundity; Fertility; Insects; Invasive insects; juvenile hormone; Juvenile hormones; MicroRNAs; miRNA; miR‐1175‐3p; Molecular modelling; Oogenesis; Ovaries; Queens; red imported fire ant; Regulatory mechanisms (biology); reproduction; Ribonucleic acid; RNA; social insects; Solenopsis invicta; Vitellin; Vitellogenin; Workers (insect caste)
• ISSN: 1672-9609; 1744-7917
• DOI: 10.1111/1744-7917.13291

Juvenile hormone (JH) acts in the regulation of caste differentiation between queens and workers (i.e., with or without reproductive capacity) during vitellin synthesis and oogenesis in social insects. However, the regulatory mechanisms have not yet been elucidated. Here, we identified a highly expressed microRNA (miRNA), miR‐1175‐3p, in the red imported fire ant, Solenopsis invicta. We found that miR‐1175‐3p is prominently present in the fat bodies and ovaries of workers. Furthermore, miR‐1175‐3p interacts with its target gene, broad‐complex core (Br‐C), in the fat bodies. By utilizing miR‐1175‐3p agomir, we successfully suppressed the expression of the Br‐C protein in queens, resulting in reduced vitellogenin expression, fewer eggs, and poorly developed ovaries. Conversely, decreasing miR‐1175‐3p levels led to the increased expression of Br‐C and vitellogenin in workers, triggering the “re‐development” of the ovaries. Moreover, when queens were fed with JH, the expression of miR‐1175‐3p decreased, whereas the expression of vitellogenin‐2 and vitellogenin‐3 increased. Notably, the suppression of fertility in queens caused by treatment with agomir miR‐1175‐3p was completely rescued by the increased vitellogenin expression induced by being fed with JH. These results suggest the critical role of miR‐1175‐3p in JH‐regulated reproduction, shedding light on the molecular mechanism underlying miRNA‐mediated fecundity in social insects and providing a novel strategy for managing S. invicta. We first identified a highly expressed miRNA, miRNA‐1175‐3p, and found that miR‐1175‐3p interacts with its target gene, broad‐complex core (Br‐C) in the fat bodies. miR‐1175‐3p regulates the reproduction of queens and workers in Solenopsis invicta. Juvenile hormone (JH) could reduce miR‐1175‐3p and increase Vg‐2 and Vg‐3 to enhance the fertility of the queens.