Involvement of Met and Kr-h1 in JH-Mediated Reproduction of Female Bactrocera dorsalis (Hendel)

Abstract

Juvenile hormone (JH) prevents metamorphosis during insect larval stages and promotes adult reproductive processes. Krüppel-homolog 1 (Kr-h1), a zinc finger transcription factor assumed to be induced by JH via the JH receptor methoprene-tolerant (Met), mediates the antimetamorphic effect of JH in insects, but its function in JH-mediated reproductive processes has not been fully explored. In this study, Met and Kr-h1 involved in the JH signaling pathway were first cloned and identified from the oriental fruit fly, Bactrocera dorsalis, an important pest infesting fruit and vegetables worldwide. Subsequent spatiotemporal expression analysis revealed that Met and Kr-h1 were both highly expressed in 7-day-old adults and fat body of female adults, respectively. Treatment with a JH analog (methoprene) significantly induced the expression of JH signaling and vitellogenin (Vg) genes and accelerated ovary development. RNA interference (RNAi) further revealed that either Met or Kr-h1 depletion at the adult stage of B. dorsalis impeded ovary development, with significantly lower egg production noted as well. In addition, rescue through methoprene application after RNAi stimulated the expression of JH signaling and Vg genes. Although there were still differences in ovary phenotype between rescued insects and the pre-RNAi control, ovary redevelopment with a larger surface area was observed, consistent with the spatiotemporal expression and phenotypes recorded in the original methoprene experiment. Our data reveal the involvement of Met and Kr-h1 in insect vitellogenesis and egg production, thus indicating the crucial role of the JH signaling pathway in insect reproduction.

RNA interference‐mediated knockdown of the transcription factor Krüppel homologue 1 suppresses vitellogenesis in Chilo suppressalis

“…Our RNAi experiment indicates that silencing of Kr‐h1 dramatically decreases Vg expression, oocyte maturation and ovarian growth, suggesting that Kr‐h1 is involved in insect vitellogenesis and the development of the ovary. Knockdown of Kr‐h1 in B. dorsalis , H. armigera and N. lugens also suppressed vitellogenesis (Jiang et al, ; Yue et al, ; Zhang et al, ). JH‐induced Met with its partner SRC [also called Taiman ( Tai ) or βFtz‐F1‐interacting steroid receptor coactivator ( FISC )] form a Met/SRC complex, and Kr‐h1 as a JH early‐inducible gene that interacts with JH /Met/SRC , the promoter region of Kr‐h1 was searched for a JH response element (JHRE), JHRE of Kr‐h1 ( k JHRE), which contains an E‐box to bind basic helix‐loop‐helix Per‐ARNT‐Sim (bHLH‐PAS) proteins thereby controlling the development and competence of the fat body during vitellogenesis (Kayukawa et al, ; Cui et al, ; Li et al, ; Song et al, ).…”

“…However, it also plays a major role in regulating Vg expression in the fat body of females, enhances the patency of the follicular epithelium and allow Vg uptake by oocytes (Ramaswamy et al, 1997). The Kr-h1 gene has been found to be a crucial promoter of the reproduction function regulated by the JH signalling pathway, and its roles in insect physiology and developmental biology have consequently been extensively studied (Lozano and Belles, 2011;Jiang et al, 2017;Yue et al, 2018). The results of our experiments on the rice striped stem borer indicate that Kr-h1 controls Vg expression, oocyte maturation and ovarian development in the fat body (Fig.…”

“…Kr-h1 also participates in many aspects of insect physiology including development and reproduction (Miyakawa et al, 2018;Yue et al, 2018) and has been closely associated with oogenesis (Roy et al, 2018). Recent studies revealed that ovarian development in Nilaparvata lugens is under the control of both BR-C and Kr-h1, which jointly determined of the number of ovarioles (Jiang et al, 2017).…”

Molecular Characterization of Vitellogenin and Its Receptor in Sogatella furcifera, and Their Function in Oocyte Maturation

“…KP735521) and elongation factor 1α (SfEF1α, accession No. KP735517) using the 2 − Ct method, like previous studies (Livak and Schmittgen, 2001;An et al, 2015;Yin et al, 2018;Yue et al, 2018). Each sample had three technological replicates.…”

Dual roles of juvenile hormone signaling during early oogenesis in Drosophila

“…In the fat body, JH binds to its receptor Methoprene‐tolerant (Met), and its paralog germ cell‐expressed basic helix‐loop‐helix‐PAS (Gce), to activate early JH‐response gene Krüppel‐homolog 1 ( Kr‐h1 ) which encodes a key transcription factor that mediates the JH signaling pathway (Jindra et al ., ; Li et al ., ). JH signaling pathway affects Vg synthesis in the fat body and has been proven in many insects, such as Drosophila melanogaster (Riddiford, ), Aedes aegypti (Raikhel et al ., ), Tribolium castaneum (Parthasarathy et al ., ), Pyrrhocoris apterus (Smykal et al ., ), Locusta migratoria (Song et al ., ), Bactrocera dorsalis (Yue et al ., ), and so on. Insulin‐like peptides, produced in insulin‐producing cells ( ilp2 , ilp3 and ilp5 ) or fat body ( ilp6 ), are released into the hemolymph to regulate JH synthesis in the CA and oogenesis (Tatar et al ., ; Tu et al ., ; Bai et al ., ; Gancz & Gilboa, ; Rauschenbach et al ., ).…”