Abstract
Insect Taiman (Tai) binds to methoprene-tolerant to form a heterodimeric complex, mediating juvenile hormone (JH) signaling to regulate larval development and to prevent premature metamorphosis. Tai also acts as a steroid receptor coactivator of 20-hydroxyecdysone (20E) receptor heterodimer, ecdysone receptor (EcR) and Ultraspiracle (USP), to control the differentiation of early germline cells and the migration of specific follicle cells and border cells in ovaries in several insect species. In holometabolous insects, however, whether Tai functions as the coactivator of EcR/USP to transduce 20E message during larval-pupal transition is unknown. In the present paper, we found that the LdTai mRNA levels were positively correlated with circulating JH and 20E titers in Leptinotarsa decemlineata; and ingestion of either JH or 20E stimulated the transcription of LdTai. Moreover, RNA interference (RNAi)-aided knockdown of LdTai at the fourth (final) instar stage repressed both JH and 20E signals, inhibited larval growth and shortened larval developing period. The knockdown caused 100% larval lethality due to failure of larval-pupal ecdysis. Under the apolysed larval cuticle, the LdTai RNAi prepupae possessed pupal thorax. In contrast, the process of tracheal ecdysis was uncompleted. Neither JH nor 20E rescued the aforementioned defectives in LdTai RNAi larvae. It appears that Tai mediates both JH and 20E signaling. Our results uncover a link between JH and 20E pathways during metamorphosis in L. decemlineata.
Highlights
Insect development and reproduction are essentially governed by the steroid 20-hydroxyecdysone (20E) and the sesquiterpenoid juvenile hormone (JH) (Jindra et al, 2013, 2015a; Santos et al, 2019)
We examined the defects after silence of LdTai using RNA interference (RNAi), and found that the silence repressed both JH and 20E signals and brought about lethality due to failure of larval-pupal ecdysis
Based on findings obtained from RNAi and hormone rescuing experiments, we established in the present paper that Tai was critical for the regulation of metamorphosis by mediating both JH and 20E signals in L. decemlineata
Summary
Insect development and reproduction are essentially governed by the steroid 20-hydroxyecdysone (20E) and the sesquiterpenoid juvenile hormone (JH) (Jindra et al, 2013, 2015a; Santos et al, 2019). During larval development in holometabolous insects, the presence of JH suppresses the expression of metamorphosis-initiation genes and 20E can only induce the larval-larval molt (Riddiford, 1994; Ureña et al, 2014). The binding of Met/Tai heterodimer to JH response element (JHRE) triggers the transcription of Krüppel-homolog 1 (Kr-h1) and Hairy to repress metamorphosis (Saha et al, 2016; Wu et al, 2016), partially by inhibition of prothoracicotropic hormone (PTTH) signaling (PTTH-Torso-MAPK) to repress 20E biosynthesis and release in Coleopteran for instance the Colorado potato beetle Leptinotarsa decemlineata, the most destructive insect defoliator of potatoes (Meng et al, 2018, 2019), and Lepidopteran such as the tobacco hornworm Manduca sexta (Rountree and Bollenbacher, 1986; Watson and Bollenbacher, 1988)
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