MiR-276 and MiR-182013-5p Modulate Insect Metamorphosis and Reproduction Via Dually Regulating Juvenile Hormone Acid Methyltransferase

Overview

Journal Commun Biol

Specialty Biology

Date 2024 Dec 2

PMID 39623057

Authors

Jiasheng Song

Wanwan Li

Lulu Gao

Qiang Yan

Xinyan Zhang

Mingzhi Liu

Shutang Zhou

Affiliations

Soon will be listed here.

Abstract

Juvenile hormone (JH) represses insect metamorphosis and stimulates reproduction. JH titers are generally low in juveniles, drop to a nadir during metamorphosis, increase after eclosion and peak in vitellogenic phase. We found that Jhamt, a rate-limiting enzyme in JH biosynthesis, mirrors JH titer patterns in the migratory locust. Knocking down Jhamt reduced JH titers, led to precocious nymphal ecdysis, metamorphosis and impaired vitellogenesis. Jhamt is negatively regulated by miR-276 and positively by miR-182013-5p. miR-276 is abundant in late nymphal but low in adults, while miR-182013-5p shows the opposite pattern. In nymphs, miR-276 binds more to Jhamt, while in adults, miR-182013-5p dominates. Functionally, miR-276 reduced Jhamt and JH levels, shortening nymphal development and inhibiting Vg expression. Conversely, miR-182013-5p increased Jhamt and JH levels, prolonging nymphal development and enhancing Vg expression. Our findings identify miR-276 and miR-182013-5p as dual regulators in JH biosynthesis, acting as "brake" and "accelerator," respectively. This study provides new insights into JH titer fluctuations and miRNA regulation in insect metamorphosis and reproduction.

References

Huang J, Tian L, Peng C, Abdou M, Wen D, Wang Y . DPP-mediated TGFbeta signaling regulates juvenile hormone biosynthesis by activating the expression of juvenile hormone acid methyltransferase. Development. 2011; 138(11):2283-91. DOI: 10.1242/dev.057687. View

Qu Z, Bendena W, Nong W, Siggens K, Noriega F, Kai Z . MicroRNAs regulate the sesquiterpenoid hormonal pathway in and other arthropods. Proc Biol Sci. 2017; 284(1869). PMC: 5745405. DOI: 10.1098/rspb.2017.1827. View

Ishimaru Y, Tomonari S, Matsuoka Y, Watanabe T, Miyawaki K, Bando T . TGF-β signaling in insects regulates metamorphosis via juvenile hormone biosynthesis. Proc Natl Acad Sci U S A. 2016; 113(20):5634-9. PMC: 4878498. DOI: 10.1073/pnas.1600612113. View

Defelipe L, Dolghih E, Roitberg A, Nouzova M, Mayoral J, Noriega F . Juvenile hormone synthesis: "esterify then epoxidize" or "epoxidize then esterify"? Insights from the structural characterization of juvenile hormone acid methyltransferase. Insect Biochem Mol Biol. 2011; 41(4):228-35. PMC: 3057355. DOI: 10.1016/j.ibmb.2010.12.008. View

Riddiford L . Juvenile hormone: the status of its "status quo" action. Arch Insect Biochem Physiol. 1996; 32(3-4):271-86. DOI: 10.1002/(SICI)1520-6327(1996)32:3/4<271::AID-ARCH2>3.0.CO;2-W. View

Fu K, Li Q, Zhou L, Meng Q, Lu F, Guo W . Knockdown of juvenile hormone acid methyl transferase severely affects the performance of Leptinotarsa decemlineata (Say) larvae and adults. Pest Manag Sci. 2015; 72(6):1231-41. DOI: 10.1002/ps.4103. View

Song J, Zhou S . Post-transcriptional regulation of insect metamorphosis and oogenesis. Cell Mol Life Sci. 2019; 77(10):1893-1909. PMC: 11105025. DOI: 10.1007/s00018-019-03361-5. View

Song J, Li W, Zhao H, Zhou S . Clustered miR-2, miR-13a, miR-13b and miR-71 coordinately target Notch gene to regulate oogenesis of the migratory locust Locusta migratoria. Insect Biochem Mol Biol. 2018; 106:39-46. DOI: 10.1016/j.ibmb.2018.11.004. View

Pasquinelli A . MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet. 2012; 13(4):271-82. DOI: 10.1038/nrg3162. View

10.

Nam J, Rissland O, Koppstein D, Abreu-Goodger C, Jan C, Agarwal V . Global analyses of the effect of different cellular contexts on microRNA targeting. Mol Cell. 2014; 53(6):1031-1043. PMC: 4062300. DOI: 10.1016/j.molcel.2014.02.013. View

11.

Zhang J, Wen D, Li E, Palli S, Li S, Wang J . MicroRNA miR-8 promotes cell growth of corpus allatum and juvenile hormone biosynthesis independent of insulin/IGF signaling in Drosophila melanogaster. Insect Biochem Mol Biol. 2021; 136:103611. DOI: 10.1016/j.ibmb.2021.103611. View

12.

Li C, Wong A, Wang S, Jia Q, Chuang W, Bendena W . miRNA-Mediated Interactions in and between Plants and Insects. Int J Mol Sci. 2018; 19(10). PMC: 6213987. DOI: 10.3390/ijms19103239. View

13.

Wu Z, Yang L, Li H, Zhou S . Krüppel-homolog 1 exerts anti-metamorphic and vitellogenic functions in insects via phosphorylation-mediated recruitment of specific cofactors. BMC Biol. 2021; 19(1):222. PMC: 8499471. DOI: 10.1186/s12915-021-01157-3. View

14.

Belles X, Martin D, Piulachs M . The mevalonate pathway and the synthesis of juvenile hormone in insects. Annu Rev Entomol. 2004; 50:181-99. DOI: 10.1146/annurev.ento.50.071803.130356. View

15.

Asgari S . MicroRNA functions in insects. Insect Biochem Mol Biol. 2012; 43(4):388-97. DOI: 10.1016/j.ibmb.2012.10.005. View

16.

Daimon T, Uchibori M, Nakao H, Sezutsu H, Shinoda T . Knockout silkworms reveal a dispensable role for juvenile hormones in holometabolous life cycle. Proc Natl Acad Sci U S A. 2015; 112(31):E4226-35. PMC: 4534237. DOI: 10.1073/pnas.1506645112. View

17.

Song J, Li W, Zhao H, Gao L, Fan Y, Zhou S . The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene . Development. 2018; 145(24). DOI: 10.1242/dev.170670. View

18.

Place R, Li L, Pookot D, Noonan E, Dahiya R . MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci U S A. 2008; 105(5):1608-13. PMC: 2234192. DOI: 10.1073/pnas.0707594105. View

19.

Liu S, Li K, Gao Y, Liu X, Chen W, Ge W . Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in . Proc Natl Acad Sci U S A. 2017; 115(1):139-144. PMC: 5776822. DOI: 10.1073/pnas.1716897115. View

20.

Cruz J, Martin D, Pascual N, Maestro J, Piulachs M, Belles X . Quantity does matter. Juvenile hormone and the onset of vitellogenesis in the German cockroach. Insect Biochem Mol Biol. 2003; 33(12):1219-25. DOI: 10.1016/j.ibmb.2003.06.004. View