Skip to main content
Log in

Differential expression of vitellogenin mRNA and protein in response to rice resistance genes in two strains of Nilaparvata lugens (Hemiptera: Delphacidae) with different levels of virulence

  • Original Research Paper
  • Published:
Applied Entomology and Zoology Aims and scope Submit manuscript

Abstract

Controlling the brown planthopper (BPH), Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is a difficult task in rice (Oryza sativa L.) production. We focused on vitellogenins (Vg), which are the major yolk protein precursors of vitellins and play an important role in the reproduction of oviparous species, including insects. We studied the accumulation of Vg mRNA and protein in a virulent BPH strain, Nagasaki-03, and a nonvirulent strain, Hatano-66, after rearing them on four rice lines. The rice lines used were two single resistance gene introgression lines, Norin-PL3 (Bph1 carrier) and Norin-PL4 (bph2 carrier), a pyramided line in which both genes were combined, and a susceptible japonica recurrent parent Tsukushibare. RT-PCR and quantitative RT-PCR analyses showed that the Vg mRNA level decreased greatly in Hatano-66 on the resistant lines. In contrast, the level of reduction on the resistant lines was much less in Nagasaki-03. Immunoblot analysis showed that Nagasaki-03 retained comparable levels of 175 kDa Vg protein on both the susceptible and resistant lines, whereas in Hatano-66, no Vg protein was detected on the resistant lines. Our results showed that BPH resistance genes caused differential reduction in the accumulation of Vg mRNA and protein, leading to the retardation of BPH reproduction on the resistant host rice plants.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ayoade O, Morooka S, Tojo S (1999) Enhancement of short wing formation and ovarian growth in the genetically defined macropterous strain of the brown planthopper, Nilaparvata lugens. J Insect Physiol 45:93–100

    Google Scholar 

  • Byrne BM, Gruber M, Ab G (1989) The evolution of egg yolk proteins. Prog Biophys Mol Biol 53:33–69

    Article  PubMed  CAS  Google Scholar 

  • Cheng DJ, Hou RF (2005) Determination and distribution of a female-specific protein in the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Tissue Cell 37:37–45

    Article  PubMed  CAS  Google Scholar 

  • Chen WJ, Wang L, Pang XF, Pan QH (2006) Genetic analysis and fine mapping of a rice brown planthopper (Nilaparvata lugens Stål) resistance gene bph19 (t). Mol Genet Genomics 275:321–329

    Article  PubMed  CAS  Google Scholar 

  • Deno RF, Perfect TJ (1994) Planthoppers: their ecology and management. Chapman and Hall, New York

    Google Scholar 

  • Engelmann F (1970) The physiology of insect reproduction. Pergamon, Oxford

  • Gallagher KD, Kenmore PE, Sogawa K (1994) Judicial use of insecticides deters planthopper outbreaks and extends the life of resistant varieties in Southeast Asian rice. In: Denno RF, Perfect JT (eds) Planthoppers: their ecology and management. Chapman and Hall, New York, London, pp 599–614

    Google Scholar 

  • Hare JD (1994) Status and prospects for an integrated approach to the control of rice planthoppers. In: Denno RF, Perfect TJ (eds) Planthoppers: their ecology and management. Chapman and Hall, New York, London, pp 615–632

    Google Scholar 

  • Hattori M, Sogawa K (2002) Oviposition behaviour of the rice brown planthopper, Nilaparvata lugens (Stål), and its electronic monitoring. J Insect Behav 15:283–293

    Article  Google Scholar 

  • Hayashi H, Chino M (1990) Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31:247–251

    CAS  Google Scholar 

  • Iwanaga K, Tojo S (1986) Effects of juvenile hormone and rearing density on wing dimorphism and oocyte development in the brown planthopper, Nilaparvata lugens. J Insect Physiol 32:585–590

    Article  CAS  Google Scholar 

  • Kaneda C, Nemoto H, Ikeda R, Yokoo M, Kobayashi A (1985) Breeding of rice Norin-PL3, a new germplasms with brown planthopper resistance. Bull Natl Agric Res Cent 5:93–103 (in Japanese)

    Google Scholar 

  • Kaneda C, Nemoto H, Ikeda R, Yokoo M, Kobayashi A, Ikehashi H, Takita T (1986) Breeding of rice Norin-PL4, a new germplasms with the brown planthopper resistance gene “bph2.” Bull Natl Agric Res Cent 6:19–32 (in Japanese)

    Google Scholar 

  • Khan ZR, Saxena RC (1988) Probing behavior of three biotypes of Nilaparvata lugens (Hemiptera: Delphacidae) on different resistant and susceptible rice varieties. J Econ Entomol 81:1338–1345

    Google Scholar 

  • Kunkel JG, Nordin JH (1985) Yolk proteins. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 1. Pergamon, New York, pp 83–111

  • Leal I, White EE, Sahota ST, Manville FJ (1997) Differential expression of the vitellogenin gene in the spruce terminal weevil feeding on resistant versus susceptible host trees. Insect Biochem Mol Biol 27:569–575

    Article  PubMed  CAS  Google Scholar 

  • Murai H, Hashimoto Z, Sharma PN, Shimuzu T, Murata K, Takumi S, Mori N, Kawasaki S, Nakamura C (2001) Construction of a high-resolution linkage map of rice brown planthopper (Nilparvata lugens Stål) resistance gene bph2. Theor Appl Genet 103:526–532

    Article  CAS  Google Scholar 

  • Murata K, Fujiwara M, Kaneda C, Takumi S, Mori N, Nakamura C (1998) RFLP mapping of a brown planthopper (Nilaparvata lugens Stål) resistance gene bph2 of indica rice introgressed into a japonica breeding line “Norin-PL4.” Genes Genet Syst 73:359–364

  • Myint KKM, Yasui H, Takagi M, Matsumura M (2009) Virulence of long-term laboratory populations of the brown planthopper, Nilaparvata lugens (Stal), and whitebacked planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacidae), on rice differential varieties. Appl Entomol Zool 44:149–153

    Article  Google Scholar 

  • Naeemullah M, Sharma PN, Tufail M, Mori N, Matsumura M, Takeda M, Nakamura C (2009) Characterization of brown planthopper strains based on their differential responses to introgressed resistance genes and on mitochondrial DNA polymorphism. Appl Entomol Zool 44:475–483

    Article  CAS  Google Scholar 

  • Nagaba Y, Tufail M, Inui H, Takeda M (2011) Hormonal regulation and effects of four environmental pollutants on vitellogenin gene transcription in the giant water bug, Lethocerus deyrollei (Heteroptera: Belostomatidae). J Insect Conserv 15:421–431

    Article  Google Scholar 

  • Raabe M (1989) Recent development in insect neurohormones. Plenum, New York

  • Raikhel AS, Dhadialla TS (1992) Accumulation of yolk proteins in insect oocytes. Annu Rev Entomol 37:217–251

    Article  PubMed  CAS  Google Scholar 

  • Sahota TS, Manville JF, White E (1994) Interactions between Sitka spruce terminal weevil and its host, Picea sitchensis (Bong) Carr.: a new mechanism for resistance. Can Entomol 126:1067–1074

    Article  Google Scholar 

  • Sharma PN, Murata K, Torii A, Takumi S, Mori N, Nakamura C (2003a) Towards molecular cloning of resistance genes against brown planthopper (Nilaparvata lugens Stål) in rice: a case study of natural insect resistance genes. Trends Entomol 3:87–96

    Google Scholar 

  • Sharma PN, Torii A, Takumi S, Mori N, Nakamura C (2003b) Marker-assisted pyramiding of two brown planthopper (Nilaparvata lugens Stål) resistance genes Bph1 and Bph2 in rice (Oryza sativa L.). Hereditas 140:61–69

    Article  Google Scholar 

  • Sharma PN, Ketipearachchi Y, Murata K, Torii A, Takumi S, Mori N, Nakamura C (2003c) RFLP/AFLP mapping of a brown planthopper (Nilaparvata lugens Stål) resistance gene Bph1 in rice (Oryza sativa L.). Euphytica 129:109–117

    Article  CAS  Google Scholar 

  • Sogawa K (1982) The rice brown planthopper: feeding physiology and host plant interactions. Annu Rev Entomol 27:49–73

    Google Scholar 

  • Sogawa K, Pathak MD (1970) Mechanisms of brown planthopper (Hemiptera: Delphacidae) resistance in Mudgo variety of rice. Appl Ent Zool 53:145–158

    Google Scholar 

  • Tanaka K (2000) A simple method for evaluating the virulence of the brown planthopper. Int Rice Res Newslett 25:18–19

    Google Scholar 

  • Tufail M, Raikhel AS, Takeda M (2005) Biosynthesis and processing of insect vitellogenins. In: Raikhel AS, Sappington TW (eds) Progress in vitellogenesis. Reproductive biology of invertebrates, vol XII, part B. Science Publishers, Inc., Enfield, pp 1–32

  • Tufail M, Takeda M (2008) Molecular characteristics of insect vitellogenins. J Insect Physiol 54:1447–1458

    Article  PubMed  CAS  Google Scholar 

  • Tufail M, Naeemullah M, Elmogy M, Sharma PN, Takeda M, Nakamura C (2010) Molecular cloning, transcriptional regulation, and differential expression profiling of vitellogenin in two wing-morphs of the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Insect Mol Biol 19:787–798

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Kitagawa H (2000) Photosynthesis and translocation of assimilates in rice plants following phloem feeding by the planthopper Nilaparvata lugens (Hemiptera: Delphacidae). J Econ Entomol 93:1192–1198

    Article  PubMed  CAS  Google Scholar 

  • Zhang QF (2007) Strategies for developing green super rice. Proc Natl Acad Sci USA 104:16402–16409

    Google Scholar 

Download references

Acknowledgments

This work was supported in part by the Ministry of Education, Culture, Sports, Science and Technology, Japan. We thank Dr. Roger F. Hou for his generous gift of chicken anti-175-kD NlVg primary antibody.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chiharu Nakamura.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gamalath, N.S., Tufail, M., Sharma, P.N. et al. Differential expression of vitellogenin mRNA and protein in response to rice resistance genes in two strains of Nilaparvata lugens (Hemiptera: Delphacidae) with different levels of virulence. Appl Entomol Zool 47, 9–16 (2012). https://doi.org/10.1007/s13355-011-0082-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13355-011-0082-6

Keywords

Navigation