Abstract
Because juvenile hormone (JH) controls insect development and its analogs are used as insecticides, juvenile hormone disruptors (JHDs) represent potential sources from which novel pesticides can be developed. Many plant species harbor JHD activity, which has previously been attributed plant secondary metabolites (i.e., diterpenes) that disrupt insect development by interfering with the JH-mediated heterodimer formation of insect juvenile receptor complexes. The results of the present study indicate that plant JHD activity is also concentrated in certain plant groups and families and that plant metabolites have insect group-specific activity. These findings suggest that reciprocal diversification has occurred between plants and insects through the evolution of the plant metabolites and JH receptors, respectively, and that plant metabolites could be developed into insect group-specific pesticides with limited effects on non-target species.
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References
Ashok M, Turner C, Wilson TG (1998) Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc Natl Acad Sci U S A 95:2761–2766. https://doi.org/10.1073/pnas.95.6.2761
Bauernfeind RJ, Chapman RK (1984) Effect of some insect growth regulators on green peach aphids (Homoptera: Aphididae) under greenhouse conditions. J Econ Entomol 77:211–215. https://doi.org/10.1093/jee/77.1.211
Blackman RL, Eastop VF (1984) Aphids on the World's crops: an identification and information guide. John Wiley, United Kingdom
Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M (2011) Ligand-binding properties of a juvenile hormone receptor. Methoprene-tolerant Proc Natl Acad Sci USA 108:21128–21133. https://doi.org/10.1073/pnas.1116123109
Cui Y, Sui Y, Xu J, Zhu F, Palli SR (2014) Juvenile hormone regulates Aedes aegypti Kruppel homolog 1 through a conserved E box motif. Insect Biochem Molec 52:23–32. https://doi.org/10.1016/j.ibmb.2014.05.009
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181–204. https://doi.org/10.1146/annurev-ento-120811-153700
Kamata N, Kamata N (2002) Outbreaks of forest defoliating insects in Japan, 1950–2000. In: Outbreaks of forest defoliating insects in Japan, 1950–2000. B Entomol Research. https://doi.org/10.1079/ber2002159
Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M, Mita K, Imanishi S, Kiuchi M, Ishikawa Y, Shinoda T (2012) Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci U S A 109:11729–11734. https://doi.org/10.1073/pnas.1204951109
Kayukawa T, Murata M, Kobayashi I, Muramatsu D, Okada C, Uchino K, Sezutsu H, Kiuchi M, Tamura T, Hiruma K, Ishikawa Y, Shinoda T (2014) Hormonal regulation and developmental role of Kruppel homolog 1, a repressor of metamorphosis, in the silkworm Bombyx mori. Dev Biol 388:48–56. https://doi.org/10.1016/j.ydbio.2014.01.022
Keeling CI, Bohlmann J (2006) Diterpene resin acids in conifers. Phytochemistry 67:2415–2423. https://doi.org/10.1016/j.phytochem.2006.08.019
Kimura M (1991) The neutral theory of molecular evolution: a review of recent evidence. Idengaku zasshi 66:367-386. 10.1266.Jjg.66.367
Kobayashi F, Yamane A, Ikeda T (1984) The Japanese pine sawyer beetle as the vector of pine wilt disease. Annu Rev Entomol 29:115–135. https://doi.org/10.1146/annurev.en.29.010184.000555
Lee SH, Oh HW, Fang Y, An SB, Park DS, Song HH, Oh SR, Kim SY, Kim S, Kim N, Raikhel AS, Je YH, Shin SW (2015) Identification of plant compounds that disrupt the insect juvenile hormone receptor complex. Proc Natl Acad Sci U S A 112:1733–1738. https://doi.org/10.1073/pnas.1424386112
Li M, Mead EA, Zhu J (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci U S A 108:638–643. https://doi.org/10.1073/pnas.1013914108
Li M, Liu P, Wiley JD, Ojani R, Bevan DR, Li J, Zhu J (2014) A steroid receptor coactivator acts as the DNA-binding partner of the methoprene-tolerant protein in regulating juvenile hormone response genes. Mol Cell Endocrinol 394:47–58. https://doi.org/10.1016/j.mce.2014.06.021
Lozano J, Kayukawa T, Shinoda T, Belles X (2014) A role for Taiman in insect metamorphosis. PLoS Genet 10:e1004769. https://doi.org/10.1371/journal.pgen.1004769
Minakuchi C, Zhou X, Riddiford LM (2008) Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125:91–105. https://doi.org/10.1016/j.mod.2007.10.002
Minakuchi C, Namiki T, Shinoda T (2009) Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Dev Biol 325:341–350. https://doi.org/10.1016/j.ydbio.2008.10.016
Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspock U, Aspock H, Bartel D, Blanke A, Berger S, Bohm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, Grobe P, Gu S, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, von Reumont BM, Schutte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TKF, Wu Q, Wu G, Xie Y, Yang S, Yang Q, Yeates DK, Yoshizawa K, Zhang Q, Zhang R, Zhang W, Zhang Y, Zhao J, Zhou C, Zhou L, Ziesmann T, Zou S, Li Y, Xu X, Zhang Y, Yang H, Wang J, Wang J, Kjer KM, Zhou X (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767. https://doi.org/10.1126/science.1257570
Miura K, Oda M, Makita S, Chinzei Y (2005) Characterization of the Drosophila Methoprene-tolerant gene product. Juvenile hormone binding and ligand-dependent gene regulation FEBS J 272:1169–1178. https://doi.org/10.1111/j.1742-4658.2005.04552.x
Nel A, Roques P, Nel P, Prokin AA, Bourgoin T, Prokop J, Szwedo J, Azar D, Desutter-Grandcolas L, Wappler T, Garrouste R, Coty D, Huang D, Engel MS, Kirejtshuk AG (2013) The earliest known holometabolous insects. Nature 503:257–261. https://doi.org/10.1038/nature12629
Oh HW, Yun CS, Jeon JH, Kim JA, Park DS, Ryu HW, Oh SR, Song HH, Shin Y, Jung CS, Shin SW (2017) Conifer diterpene resin acids disrupt juvenile hormone-mediated endocrine regulation in the indian meal moth Plodia interpunctella. J Chem Ecol 43:703–711. https://doi.org/10.1007/s10886-017-0861-9
Shin SW, Zou Z, Saha TT, Raikhel AS (2012) bHLH-PAS heterodimer of Methoprene-tolerant and cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proc Natl Acad Sci U S A 109:16576–16581. https://doi.org/10.1073/pnas.1214209109
Slama K (1971) Insect juvenile hormone analogues. Annu Rev Biochem 40:1079–1102. https://doi.org/10.1146/annurev.bi.40.070171.005243
Wilson TG, Ashok M (1998) Insecticide resistance resulting from an absence of target-site gene product. Proc Natl Acad Sci U S A 95:14040–14044. https://doi.org/10.1073/pnas.95.24.14040
Zhang Z, Xu J, Sheng Z, Sui Y, Palli SR (2011) Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J Biol Chem 286:8437–8447. https://doi.org/10.1074/jbc.M110.191684
Acknowledgements
This work was supported by the KRIBB Research Initiative Program (KGM4981713), awarded to H.O., and the National Research Foundation of Korea Grant (NRF-2008-2004725), awarded to D.P.
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Shin, S.W., Jeon, J.H., Yun, CS. et al. Species-Specific Interactions between Plant Metabolites and Insect Juvenile Hormone Receptors. J Chem Ecol 44, 1022–1029 (2018). https://doi.org/10.1007/s10886-018-1001-x
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DOI: https://doi.org/10.1007/s10886-018-1001-x