Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Nijhout HF (1994) Insect hormones. Princeton University Press, Princeton

    Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

  1. Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Insect Pests, College of Plant Protection, Hunan Agricultural University, Changsha, 410128, China

    Kui Hu, Ping Tian, Lu Yang, Yan Tang, Lin Qiu, Hualiang He & Youzhi Li

  2. National Research Center of Engineering & Technology for Utilization of Botanical Functional Ingredients, Hunan Agricultural University, Changsha, 410128, China

    Wenbing Ding

  3. Hunan Provincial Engineering & Technology Research Center for Biopesticide and Formulation Processing, Hunan Agricultural University, Changsha, 410128, China

    Wenbing Ding & Youzhi Li

Authors
  1. Kui Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ping Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hualiang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wenbing Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Youzhi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Youzhi Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, K., Tian, P., Yang, L. et al. Molecular characterization of the Krüppel-homolog 1 and its role in ovarian development in Sogatella furcifera (Hemiptera: Delphacidae). Mol Biol Rep 47, 1099–1106 (2020). https://doi.org/10.1007/s11033-019-05206-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-019-05206-7

Keywords

Search

Navigation