Advertisement

Molecular characterization of the Krüppel-homolog 1 and its role in ovarian development in Sogatella furcifera (Hemiptera: Delphacidae)

  • Kui Hu
  • Ping Tian
  • Lu Yang
  • Yan Tang
  • Lin Qiu
  • Hualiang He
  • Wenbing Ding
  • Youzhi LiEmail author
Original Article
  • 51 Downloads

Abstract

Juvenile hormone (JH) plays a pivotal role in insect reproduction. The Krüppel-homolog 1 (Kr-h1) is a JH-inducible zinc finger transcription factor that has also been found to play a role in insect reproduction, however, its function varies across species. In this study, we cloned SfKr-h1 from Sogatella furcifera and investigated its role in ovarian development. The open reading frame of SfKr-h1 is 1 800 bp encoding 599 amino acids. The putative amino acid sequence of SfKr-h1 contains eight putative C2H2-type zinc finger domains and is highly homologous with the Kr-h1s of other hemipteran species. Expression of SfKr-h1 peaked 96 h after adult emergence and was highest in the ovary. RNA interference (RNAi) knockdown of SfKr-h1 substantially reduced the transcription of SfVg, and arrested ovarian development. These results suggest that SfKr-h1 is critical for normal ovarian development in S. furcifera.

Keywords

Sogatella furcifera Krüppel-homolog 1 Reproduction Juvenile hormone RNA interference 

Notes

Funding

This work was funded by National Natural Science Foundation of China (31572005) and Double First-class Construction Project of Hunan Agricultural University (SYL2019029).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1.
    Nijhout HF (1994) Insect hormones. Princeton University Press, PrincetonGoogle Scholar
  2. 2.
    Kayukawa T, Jouraku A, Ito Y, Shinoda T (2017) Molecular mechanism underlying juvenile hormone-mediated repression of precocious larval-adult metamorphosis. Proc Natl Acad Sci USA 114(5):1057–1062.  https://doi.org/10.1073/pnas.1615423114 CrossRefPubMedGoogle Scholar
  3. 3.
    Belles X, Santos CG (2014) The MEKRE93 (Methoprene tolerant-Krüppel homolog 1-E93) pathway in the regulation of insect metamorphosis, and the homology of the pupal stage. Insect Biochem Mol Biol 52:60–68.  https://doi.org/10.1016/j.ibmb.2014.06.009 CrossRefPubMedGoogle Scholar
  4. 4.
    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 CrossRefPubMedGoogle Scholar
  5. 5.
    Roy S, Saha TT, Zou Z, Raikhel AS (2018) Regulatory pathways controlling female insect reproduction. Annu Rev Entomol 63:489–511.  https://doi.org/10.1146/annurev-ento-020117-043258 CrossRefPubMedGoogle Scholar
  6. 6.
    Miyakawa H, Watanabe M, Araki M, Ogino Y, Miyagawa S, Iguchi T (2018) Juvenile hormone-independent function of Krüppel homolog 1 in early development of water flea Daphnia pulex. Insect Biochem Mol Biol 93:12–18.  https://doi.org/10.1016/j.ibmb.2017.12.007 CrossRefPubMedGoogle Scholar
  7. 7.
    Santos CG, Humann FC, Hartfelder K (2019) Juvenile hormone signaling in insect oogenesis. Curr Opin Insect Sci 31:43–48.  https://doi.org/10.1016/j.cois.2018.07.010 CrossRefPubMedGoogle Scholar
  8. 8.
    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 Krüppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci USA 109(29):11729–11734.  https://doi.org/10.1073/pnas.1204951109 CrossRefPubMedGoogle Scholar
  9. 9.
    Jin M, Xue J, Yao Y, Lin X (2014) Molecular characterization and functional analysis of Krüppel-homolog 1 (Kr-h1) in the brown planthopper, Nilaparvata lugens (Stål). J Integr Agric 13(9):1972–1981.  https://doi.org/10.1016/s2095-3119(13)60654-1 CrossRefGoogle Scholar
  10. 10.
    Li KL, Yuan SY, Nanda S, Wang WX, Lai FX, Fu Q, Wan PJ (2018) The roles of E93 and Kr-h1 in metamorphosis of Nilaparvata lugens. Front Physiol 9:1677.  https://doi.org/10.3389/fphys.2018.01677 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Yue Y, Yang RL, Wang WP, Zhou QH, Chen EH, Yuan GR, Wang JJ, Dou W (2018) Involvement of Met and Kr-h1 in JH-mediated reproduction of female Bactrocera dorsalis (Hendel). Front Physiol 9:482.  https://doi.org/10.3389/fphys.2018.00482 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Mao Y, Li Y, Gao H, Lin X (2019) The direct interaction between E93 and Kr-h1 mediated their antagonistic effect on ovary development of the brown planthopper. Int J Mol Sci 20(10):2431.  https://doi.org/10.3390/ijms20102431 CrossRefPubMedCentralGoogle Scholar
  13. 13.
    Jiang J, Xu Y, Lin X (2017) Role of Broad-Complex (Br) and Krüppel homolog 1 (Kr-h1) in the ovary development of Nilaparvata lugens. Front Physiol 8:1013.  https://doi.org/10.3389/fphys.2017.01013 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Lin X, Yao Y, Wang B (2015) Methoprene-tolerant (Met) and Krüpple-homologue 1 (Kr-h1) are required for ovariole development and egg maturation in the brown plant hopper. Sci Rep 5:18064.  https://doi.org/10.1038/srep18064 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Song J, Wu Z, Wang Z, Deng S, Zhou S (2014) Krüppel-homolog 1 mediates juvenile hormone action to promote vitellogenesis and oocyte maturation in the migratory locust. Insect Biochem Mol Biol 52:94–101.  https://doi.org/10.1016/j.ibmb.2014.07.001 CrossRefPubMedGoogle Scholar
  16. 16.
    Parthasarathy R, Sun Z, Bai H, Palli SR (2010) Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 40(5):405–414.  https://doi.org/10.1016/j.ibmb.2010.03.006 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Smykal V, Bajgar A, Provaznik J, Fexova S, Buricova M, Takaki K, Hodkova M, Jindra M, Dolezel D (2014) Juvenile hormone signaling during reproduction and development of the linden bug, Pyrrhocoris apterus. Insect Biochem Mol Biol 45:69–76.  https://doi.org/10.1016/j.ibmb.2013.12.003 CrossRefPubMedGoogle Scholar
  18. 18.
    Liang AW, Zhang H, Lin J, Wang FH (2018) De novo assembly and analysis of the white-backed planthopper (Sogatella furcifera) transcriptome. J Insect Sci 18(4):11.  https://doi.org/10.1093/jisesa/iey074 CrossRefPubMedCentralGoogle Scholar
  19. 19.
    Zhou C, Yang H, Yang H, Wang Z, Long G, Jin D (2019) Effects of sublethal concentrations of deltamethrin on fitness of white-backed planthopper, Sogatella furcifera (Horváth). Int J Pest Manage 65(2):165–170.  https://doi.org/10.1080/09670874.2018.1493243 CrossRefGoogle Scholar
  20. 20.
    Zhou G, Wen J, Cai D, Li P, Xu D, Zhang S (2008) Southern rice black-streaked dwarf virus: A new proposed Fijivirus species in the family Reoviridae. Chin Sci Bull 53(23):3677–3685.  https://doi.org/10.1007/s11434-008-0467-2 CrossRefGoogle Scholar
  21. 21.
    Cheng Z, Li S, Gao R, Sun F, Liu W, Zhou G, Wu J, Zhou X, Zhou Y (2013) Distribution and genetic diversity of Southern rice black-streaked dwarf virus in China. Virol J 10(1):307.  https://doi.org/10.1186/1743-422X-10-307 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Lv MF, Xie L, Wang HF, Wang HD, Chen JP, Zhang HM (2017) Biology of Southern rice black-streaked dwarf virus: a novel Fijivirus emerging in East Asia. Plant Pathol 66(4):515–521.  https://doi.org/10.1111/ppa.12630 CrossRefGoogle Scholar
  23. 23.
    Xu Y, Zhou W, Zhou Y, Wu J, Zhou X (2012) Transcriptome and comparative gene expression analysis of Sogatella furcifera (Horváth) in response to southern rice black-streaked dwarf virus. PLoS ONE 7(4):e36238.  https://doi.org/10.1371/journal.pone.0036238 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Higgins DG (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266(1):383–402.  https://doi.org/10.1016/S0076-6879(96)66024-8 CrossRefPubMedGoogle Scholar
  25. 25.
    Hu K, Yang H, Liu S, He H, Ding W, Qiu L, Li Y (2019) Odorant-binding protein 2 is involved in the preference of Sogatella furcifera (Hemiptera: Delphacidae) for rice plants infected with the southern rice black-streaked dwarf virus. Fla Entomol 102(2):353–358.  https://doi.org/10.1653/024.102.0210 CrossRefGoogle Scholar
  26. 26.
    Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45.  https://doi.org/10.1093/nar/29.9.e45 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Hu K, Liu S, Qiu L, Li Y (2019) Three odorant-binding proteins are involved in the behavioral response of Sogatella furcifera to rice plant volatiles. PeerJ 7:e6576.  https://doi.org/10.7717/peerj.6576 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Li K, Jia QQ, Li S (2019) Juvenile hormone signaling—a mini review. Insect Sci 26(4):600–606.  https://doi.org/10.1111/1744-7917.12614 CrossRefPubMedGoogle Scholar
  29. 29.
    Kayukawa T, Nagamine K, Ito Y, Nishita Y, Ishikawa Y, Shinoda T (2016) Krüppel homolog 1 inhibits insect metamorphosis via direct transcriptional repression of Broad-Complex, a pupal specifier gene. J Biol Chem 291(4):1751–1762.  https://doi.org/10.1074/jbc.M115.686121 CrossRefPubMedGoogle Scholar
  30. 30.
    Xie X, Liu M, Jiang Q, Zheng H, Zheng L, Zhu D (2018) Role of Krüppel homolog 1 (Kr-h1) in methyl farnesoate-mediated vitellogenesis in the swimming crab Portunus trituberculatus. Gene 679:260–265.  https://doi.org/10.1016/j.gene.2018.08.046 CrossRefPubMedGoogle Scholar
  31. 31.
    Liu S, Li K, Gao Y, Liu X, Chen W, Ge W, Feng Q, Palli SR, Li S (2018) Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. Proc Natl Acad Sci USA 115(1):139–144.  https://doi.org/10.1073/pnas.1716897115 CrossRefPubMedGoogle Scholar
  32. 32.
    Jindra M, Belles X, Shinoda T (2015) Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci 11:39–46.  https://doi.org/10.1016/j.cois.2015.08.004 CrossRefPubMedGoogle Scholar
  33. 33.
    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 Krüppel homolog 1, a repressor of metamorphosis, in the silkworm Bombyx mori. Dev Biol 388(1):48–56.  https://doi.org/10.1016/j.ydbio.2014.01.022 CrossRefPubMedGoogle Scholar
  34. 34.
    Zhang T, Song W, Li Z, Qian W, Wei L, Yang Y, Wang W, Zhou X, Meng M, Peng J, Xia Q, Perrimon N, Cheng D (2018) Krüppel homolog 1 represses insect ecdysone biosynthesis by directly inhibiting the transcription of steroidogenic enzymes. Proc Natl Acad Sci USA 115(15):3960–3965.  https://doi.org/10.1073/pnas.1800435115 CrossRefPubMedGoogle Scholar
  35. 35.
    Gujar H, Palli SR (2016) Krüppel homolog 1 and E93 mediate Juvenile hormone regulation of metamorphosis in the common bed bug, Cimex lectularius. Sci Rep 6:26092.  https://doi.org/10.1038/srep26092 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Fussnecker B, Grozinger C (2008) Dissecting the role of Kr-h1 brain gene expression in foraging behavior in honey bees (Apis mellifera). Insect Mol Biol 17(5):515–522.  https://doi.org/10.1111/j.1365-2583.2008.00819.x CrossRefPubMedGoogle Scholar
  37. 37.
    Moda LM, Vieira J, Guimarães Freire AC, Bonatti V, Bomtorin AD, Barchuk AR, Simões ZL (2013) Nutritionally driven differential gene expression leads to heterochronic brain development in honeybee castes. PLoS ONE 8(5):e64815.  https://doi.org/10.1371/journal.pone.0064815 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Duportets L, Bozzolan F, Abrieux A, Maria A, Gadenne C, Debernard S (2012) The transcription factor Krüppel homolog 1 is linked to the juvenile hormone-dependent maturation of sexual behavior in the male moth, Agrotis ipsilon. Gen Comp Endocrinol 176(2):158–166.  https://doi.org/10.1016/j.ygcen.2012.01.005 CrossRefPubMedGoogle Scholar
  39. 39.
    Song J, Guo W, Jiang F, Kang L, Zhou S (2013) Argonaute 1 is indispensable for juvenile hormone mediated oogenesis in the migratory locust, Locusta migratoria. Insect Biochem Mol Biol 43(9):879–887.  https://doi.org/10.1016/j.ibmb.2013.06.004 CrossRefPubMedGoogle Scholar
  40. 40.
    Song J, Li W, Zhao H, Gao L, Fan Y, Zhou S (2018) The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Krüppel-homolog 1. Development 145(24):170670.  https://doi.org/10.1242/dev.170670 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, College of Plant ProtectionHunan Agricultural UniversityChangshaChina
  2. 2.National Research Center of Engineering & Technology for Utilization of Botanical Functional IngredientsHunan Agricultural UniversityChangshaChina
  3. 3.Hunan Provincial Engineering & Technology Research Center for Biopesticide and Formulation ProcessingHunan Agricultural UniversityChangshaChina

Personalised recommendations