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Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties

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Abstract

For over 50 years, host plant resistance has been the principal focus of public research to reduce planthopper and leafhopper damage to rice in Asia. Several resistance genes have been identified from native varieties and wild rice species, and some of these have been incorporated into high-yielding rice varieties through conventional breeding. However, adaptation by hoppers to resistant rice has been phenomenally rapid, and hopper populations with virulence against several resistance genes are now widespread. Directional genetic selection for virulent hoppers seems unlikely given the rapid pace of adaptation reported from field and laboratory studies. Among the alternative explanations for rapid hopper adaptation are changes (genetic, epigenetic, or community structure) in endosymbiont communities that become advantageous for planthoppers and leafhoppers that feed on resistant rice varieties. This review examines the nature of these symbiont communities and their functions in planthoppers and leafhoppers—focusing on their likely roles in mediating adaptation to plant resistance. Evidence from a small number of experimental studies suggests that bacterial and eukaryotic (including yeast-like) symbionts can determine or mediate hopper virulence on rice plants and that symbiont functions could change over successive generations of selection on both resistant and susceptible plants. The review highlights the potential complexity of rice hopper–symbiont interactions and calls for a more careful choice of research materials and methods to help reduce this complexity. Finally, the consequences of symbiont-mediated virulence adaptation for future rice breeding programs are discussed.

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References

  • Alam SN, Cohen MB (1998) Durability of brown planthopper, Nilaparvata lugens, resistance in rice variety IR64 in greenhouse selection studies. Entomol Exp Appl 89:71–78

    Article  CAS  Google Scholar 

  • Bae SD, Song YH, Park YD (1987) Effects of temperature conditions on the growth and oviposition of brown planthopper, Nilaparvata lugens Stål. J Plant Prot 26:13–23

    Google Scholar 

  • Barbosa P, Krischik VA, Jones CG (eds) (1991) Microbial mediation of plant-herbivore interactions. John Wiley and Sons, Inc, USA, p 530

    Google Scholar 

  • Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS ONE 596:e11339

    Article  CAS  Google Scholar 

  • Bing L, Hongxia D, Maoxin Z, Di X, Jingshu W (2007) Potential resistance of tricin in rice against brown planthopper, Nilaparvata lugens (Stål). Acta Ecologia Sinica 27:1300–1307

    Article  Google Scholar 

  • Botrell DG, Schoenly KG (2012) Resurrecting the ghost of green revolutions past: the brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J Asia-Pacific Entomol 15:122–140

    Article  Google Scholar 

  • Catindig JLA, Arida GS, Baehaki SE, Bentur JS, Cuong LQ, Norowi M, Rattanakam W, Sriratanasak W, Xia J, Lu Z (2009) Situation of planthoppers in Asia. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Los Baños, pp 191–220

    Google Scholar 

  • Chaves S, Neto M, Tenreiro R (2009) Insect-symbiont systems: from complex relationship to biotechnological applications. Biotechnol J 4:1753–1765

    Article  CAS  PubMed  Google Scholar 

  • Chen YH (2009) Variation in planthopper-rice interactions: possible interactions among three species. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Los Baños (Philippines), pp 315–326

    Google Scholar 

  • Chen CC, Cheng LL, Hou RF (1981a) Studies on the intracellular yeast-like symbiote in the brown planthopper, Nilaparvata lugens Stål. II. Effects of antibiotics and elevated temperature on the symbiotes and their host. Zeitschrift für Angewandte Entomologie 92:440–449

    Article  Google Scholar 

  • Chen CC, Cheng LL, Kuan CC, Hou RF (1981b) Studies on the intracellular yeast-like symbiote in the Brown Planthopper, Nilaparvata lugens Stål. I. Histological observations and population changes of the symbiote. Zeitschrift für Angewandete Entomologie 91:321–327

    Article  Google Scholar 

  • Chen FJ, Zhang JF, Xia ZE, Lu ZX (2006) Morphological observations on the yeast-like endosymbionts in brown planthopper Nilaparvata lugens. Acta Zootaxonomica Sinica 31:728–735

    Google Scholar 

  • Chen YH, Bernal CC, Tan J, Horgan FG, Fitzgerald MA (2011) Planthopper “adaptation” to resistant rice varieties: changes in amino acid composition over time. J Insect Physiol 57:1375–1384

    Article  CAS  PubMed  Google Scholar 

  • Cheng D, Hou RF (1996) Ultrastructure of the yeast-like endocytobiont in the brown planthopper, Nilaparvata lugens (Stål)(Homoptera: Delphacidae). Endocytobiosis Cell Res 11:107–117

    Google Scholar 

  • Cheng DJ, Hou RF (2001) Histological observations on transovarial transmission of a yeast-like symbiote in Nilaparvata lugens Stål (Homoptera, Delphacidae). Tissue Cell 33:273–279

    Article  CAS  PubMed  Google Scholar 

  • Claridge MF, Den Hollander J (1982) Virulence to rice cultivars and selection for virulence in populations of the brown planthopper Nilaparvata lugens. Entomol Exp Appl 32:213–221

    Article  Google Scholar 

  • Claridge MF, Den Hollander J (1983) The biotype concept and its application to insect pests of agriculture. Crop Prot 2:85–95

    Article  Google Scholar 

  • Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92

    Article  CAS  PubMed  Google Scholar 

  • Dong S, Pang K, Bai X, Yu X, Hao P (2011) Identification of two species of yeast-like symbiotes in the brown planthopper, Nilaparvata lugens. Curr Microbiol 62:1133–1138

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64:409–434

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (1992) Microbial brokers of insect-plant interactions. In: Proceedings of the 8th international symposium on insect-plant relationships series entomologica, vol 49. pp 329–336

  • Dowd PF (1989) In situ production of hydrolytic detoxifying enzymes by symbiotic yeasts in the cigarette beetle (Coleoptera: Anobiidae). J Econ Entomol 82:396–400

    CAS  Google Scholar 

  • Dowd PF (1992) Insect fungal symbionts: a promising source of detoxifying enzymes. J Ind Microbiol 9:149–161

    Article  CAS  Google Scholar 

  • Dowd PF, Shen SK (1990) The contribution of symbiotic yeast to toxin resistance of the cigarette beetle (Lasioderma serricorne). Entomol Exp Appl 56:241–248

    Article  CAS  Google Scholar 

  • Eya BK, Kenny PTM, Tamura SY, Ohnishi M, Naya Y, Nakanishi K, Sugiura M (1989) Chemical association in symbiosis sterol donors in planthoppers. J Chem Ecol 15:373–380

    Article  CAS  Google Scholar 

  • Fujita D, Yoshimura A, Yasui H (2010) Development of near-isogenic lines and pyramided lines carrying resistance genes to green rice leafhopper (Nephotettix cincticeps Uhler) with the Taichung 65 genetic background in rice (Oryza sativa L.). Breed Sci 60:18–27

    Article  CAS  Google Scholar 

  • Fujita D, Kohli A, Horgan FG (2013) Rice resistance to planthoppers and leafhoppers. Crit Rev Plant Sci 32:162–191

    Article  CAS  Google Scholar 

  • Ganter PF (2006) Yeast and invertebrate associations. In: Rosa CA, Peter G (eds) Biodiversity and ecophysiology of yeasts (The yeast handbook). Springer, Heidelberg, pp 303–370

    Chapter  Google Scholar 

  • Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism of host resistance. Plant Physiol 146:1810–1820

    Article  CAS  PubMed  Google Scholar 

  • Hirae M, Fukuta Y, Tamura K, Oya S (2007) Artificial selection of biotypes of green rice leafhopper, Nephotettix cincticeps Uhler (Homoptera: Cicadellidae), and virulence to resistant rice varieties. Appl Entomol Zool 42:97–107

    Article  Google Scholar 

  • Hongoh Y, Ishikawa H (1997) Uric acid as a nitrogen resource for the brown planthopper, Nilaparvata lugens: studies with synthetic diets and aposymbiotic insects. Zoolog Sci 14:581–586

    Article  CAS  Google Scholar 

  • Horgan FG (2009) Mechanisms of resistance: a major gap in understanding planthopper-rice interactions. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Los Baños (Philippines), pp 281–302

    Google Scholar 

  • Horgan FG (2012) Diversity and defence: plant-herbivore interactions at multiple scales and trophic levels. In: Gurr GM, Wratten SD, Snyder WE, Read DMY (eds) Biodiversity and insect pests: key issues for sustainable management. Wiley-Blackwell, Oxford, pp 241–258

    Chapter  Google Scholar 

  • Hosokawa T, Kikuchi Y, Fukatsu T (2007) How many symbionts are provided by mothers, acquired by offspring, and needed for successful vertical transmission in an obligate insect–bacterium mutualism? Mol Ecol 16:5316–5325

    Article  PubMed  Google Scholar 

  • Hou RF (2008) Symbiosis between planthoppers and microorganisms. In: Capinera J (ed) Encyclopedia of entomology, 2nd edn. Springer, Dordrect, The Netherlands, pp 3657–3660

  • Hou Y, Ma Z, Dong S, Chen YH, Xiaoping Y (2013) Analysis of yeast-like symbiote diversity in the brown planthopper (BPH), Nilaparvata lugens Stål, using a novel nested PCR-DGGE protocol. Curr Microbiol 67:263–270

  • Ishikawa H (2003) Insect symbiosis: an introduction. In: Bourtzis K, Miller TA (eds) Insect symbiosis. CRC, Boca Raton, FL, pp 1–21

    Chapter  Google Scholar 

  • Jones CG (1984) Microorganisms as mediators of plant resource exploitation by insect herbivores. In: Price PW, Slobodchikoff CN, Gaud WS (eds) A new ecology. Novel approaches to interactive systems. John Wiley and Sons, Inc, New York, pp 53–99

    Google Scholar 

  • Jung JK, Im DJ (2005) Feeding inhibition of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae), on a resistant rice variety. J Asia-Pacific Entomol 8:301–308

    Article  Google Scholar 

  • Kagayama K, Shiragami N, Nagamine T, Umehara T, Mitsui T (1993) Isolation and classification of intracellular symbiotes from the rice brown planthopper, Nilaparvata lugens, based on analysis of 18S-ribosomal DNA. J Pestic Sci 18:231–237

    Article  Google Scholar 

  • Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664

    Article  Google Scholar 

  • Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci 109:8618–8622

    Article  CAS  PubMed  Google Scholar 

  • Kiyonaga T, Watanabe T, Miyamoto K, Suzuki Y (1997) Varietal differences in the brown planthopper egg mortality caused by antibiotic response of rice plants. Kyushu Agric Res 59:75 (In Japanese.)

    Google Scholar 

  • Koyama K (1985) Nutritional physiology of the brown rice planthopper, Nilaparvata lugens Stål (Hemiptera:Delphacidae). II. Essential amino acids for nymphal development. Appl Entomol Zool 20:424–430

    CAS  Google Scholar 

  • Koyama K (1986) Nutritional physiology of the brown rice planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). II. Essential amino acids for nymphal development. Appl Entomol Zool 20:424–430

    Google Scholar 

  • Latif MA, Guan TS, Yusoh OM, Siraj SS (2008) Evidence of sibling species in the brown planthopper complex (Nilaparvata lugens) detected from short and long primer random amplified polymorphic DNA fingerprints. Biochem Genet 46:520–537

    Article  CAS  PubMed  Google Scholar 

  • Latif MA, Rafii MY, Mazid MS, Ali ME, Ahmed F, Omar MY, Tan SG (2012) Genetic dissection of sympatric populations of brown planthopper, Nilaparvata lugens (Stål), using DALP-PCR molecular markers. Sci World J 2012:586831

    Article  CAS  Google Scholar 

  • Lee YH, Hou RF (1987) Physiological roles of a yeast-like symbiote in reproduction and embryonic development of the brown planthopper, Nilaparvata lugens Stål. J Insect Physiol 33:851–860

    Article  Google Scholar 

  • Lu Z, Yu X, Chen J, Zheng X, Xu H, Zhang J, Chen L (2004) Dynamics of yeast-like symbiote and its relationship with the virulence of brown planthopper, Nilaparvata lugens Stål, to resistant rice varieties. J Asia-Pacific Entomol 7:317–323

    Article  Google Scholar 

  • Mitsuhashi J, Kono Y (1975) Intercellular microorganisms in green rice leafhopper, Nephotettix cincticeps Uhler (Hemiptera; Deltocephalidae). Appl Entomol Zool 10:1–9

    Google Scholar 

  • Myint KKM, Matsumura M, Takagi M, Yasui H (2009a) Demographic parameters of long-term laboratory strains of the brown planthopper, Nilaparvata lugens Stål (Homoptera: Delphacidae) on resistance genes bph20(t) and Bph21(t) in rice. J Fac Agric Kyushu Univ 54:159–164

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Nagamine T, Miyake T, Matsumoto S, Mitsui T (1993) Intracellular yeast-like symbiotes of a brown planthopper, Nilaparvata lugens. Riken Rev 3:31–32

    Google Scholar 

  • Nasu S (1963) Studies on some leafhoppers and planthoppers which transmit virus disease of rice plant in Japan. Bull Kyushu Agric Exp Stn 8:153–349

    Google Scholar 

  • Nasu S (1965) Studies on some leafhoppers and planthoppers which transmit virus diseases of rice plant in Japan. Bull Kyushu Agric Exp Stn 3:13–349

    Google Scholar 

  • Noda H (1974) Preliminary histological observations and population dynamics of intracellular yeast-like symbionts in the smaller brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Appl Entomol Zool 9:275–277

    Google Scholar 

  • Noda H (1977) Histological and histochemical observation of intracellular yeastlike symbiotes in the fat body of the smaller brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Appl Entomol Zool 12:134–141

    Google Scholar 

  • Noda H, Omura T (1992) Purification of yeast-like symbiotes of planthoppers. J Invertebr Pathol 59:104–105

    Article  Google Scholar 

  • Noda H, Saito T (1979) The role of intracellular yeast-like symbiotes in the development of Laodelphax striatellus. Appl Entomol Zool 14:453–458

    CAS  Google Scholar 

  • Noda H, Wada K, Saito T (1979) Sterols in Laodelphax striatellus with special reference to the intracellular yeastlike symbiotes as a sterol source. J Insect Physiol 25:443–447

    Article  CAS  Google Scholar 

  • Noda H, Nakashima N, Koizumi M (1995) Phylogenetic position of yeast-like symbiotes of rice planthoppers based on partial 18s rDNA sequences. Insect Biochem Mol Biol 25:639–646

    Article  CAS  PubMed  Google Scholar 

  • Noda H, Watanabe K, Kawai S, Yukuhiro F, Miyoshi T, Tomizawa M, Koizumi Y, Nikoh N, Fukatsu T (2012) Bacteriome-associated endosymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae). Appl Entomol Zool 47:217–225

    Article  CAS  Google Scholar 

  • Padgham DE (1983) The influence of the host-plant on the development of the adult brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), and its significance in migration. Bull Entomol Res 73:117–128

    Article  Google Scholar 

  • Pang K, Dong S, Hou Y, Bian Y, Yang K, Yu X (2012) Cultivation, identification and quantification of one species of yeast-like symbiote, Candida, in the rice brown planthopper, Nilaparvata lugens. Insect Sci 19:477–484

    Article  CAS  Google Scholar 

  • Pathak MD, Kalode MB (1980) Influence of nutrient chemicals on the feeding behaviour of the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Mimeographed manuscript. IRRI

  • Peñalver Cruz A, Arida A, Heong KL, Horgan FG (2011) Aspects of brown planthopper adaptation to resistant rice varieties with the Bph3 gene. Entomol Exp Appl 141:245–257

    Article  CAS  Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  CAS  PubMed  Google Scholar 

  • Piyaphongkul J, Pritchard J, Bale J (2012) Can tropical insects stand the heat? A case study with the brown planthopper Nilaparvata lugens (Stål). PLoS ONE 7:e29409

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Kawamura M, Ishikawa H (1996) Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J Insect Physiol 42:125–129

    Article  CAS  Google Scholar 

  • Saxena RC, Okech SH (1985) Role of plant volatiles in resistance of selected rice varieties to brown planthopper, Nilaparvata lugens (Stål) (Homoptera; Delphacidae). J Chem Ecol 11:1601–1616

    Article  CAS  Google Scholar 

  • Seino Y, Suzuki Y, Sogawa K (1996) An ovicidal substance produced by rice plants in response to oviposition by the whitebacked planthopper, Sogatella furcifera (Horvath) (Homoptera:Delphacidae). Appl Entomol Zool 31:467–473

    CAS  Google Scholar 

  • Shigematsu Y, Murofushi N, Ito K, Kaneda C, Kawabe S, Takahashi N (1982) Sterols and asparagine in the rice plant, endogenous factors related to resistance against the brown planthopper (Nilaparvata lugens). Agric Biol Chem 46:2877–2879

    Article  CAS  Google Scholar 

  • Sogawa K (1991) Super-susceptibility to the white-backed planthopper in japonica-indica hybrid rice. Kyushu Agric Res 53:92 (In Japanese)

    Google Scholar 

  • Sogawa K, Pathak MD (1970) Mechanism of brown planthopper resistance in Mudgo variety of rice (Hemiptera: Delphacid). Appl Entomol Zool 5:145–158

    Google Scholar 

  • Stevenson PC, Kimmins FM, Grayer RJ, Raveendranath S (1996) Schaftosides from rice phloem as feeding inhibitors and resistance factors to brown planthopper, Nilaparvata lugens. Entomol Exp Appl 80:246–249

    Article  Google Scholar 

  • Suzuki Y, Sogawa K, Seino Y (1996) Ovicidal reaction of rice plants against the whitebacked planthopper Sogatella furcifera Horvath (Homoptera: Delphacidae). Appl Entomol Zool 31:111–118

    Google Scholar 

  • Tanaka K, Matsumura M (2000) Development of virulence to resistant rice varieties in the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae), immigrating into Japan. Appl Entomol Zool 35:529–533

    Article  Google Scholar 

  • Tang M, Lv L, Jing S, Zhu L, He G (2010) Bacterial symbionts of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Appl Environ Microbiol 76:1740–1745

    Article  CAS  PubMed  Google Scholar 

  • Thanysiriwat T, Pattwatang P, Angeles ER (2009) New biotypes of brown planthopper in Thailand. In: Proceedings of the rice and temperate cereal crops annual conference 2009, Bangkok, Thailand, pp 386–389

  • Vega FE, Dowd PF (2005) The role of yeasts as insect endosymbionts. In: Vega FE, Blackwell M (eds) Insect-fungal associations: ecology and evolution. Oxford University Press, New York, USA, pp 211–243

    Google Scholar 

  • Verma SK, Pathak PK, Singh BN, Lal MN (1979) Indian biotypes of the brown planthopper. Int Rice Res Newsl 4:6

    Google Scholar 

  • Wang X, Zhou G, Xiang CY, Du MH, Cheng JA, Luis SS, Lou YG (2008a) β-glucosidase treatment and infestation by the rice brown planthopper, Nilaparvata lugens, elicit similar signaling pathways in rice plants. Chin Sci Bull 53:53–57

    Article  CAS  Google Scholar 

  • Wang Y, Tang M, Hao P, Yang Z, Zhu L, He G (2008b) Penetration into rice tissues by brown planthopper and fine structure of the salivary sheaths. Entomol Exp Appl 129:295–307

    Article  Google Scholar 

  • Wang Y, Wang X, Yuan H, Chen R, Zhu L, He R, He G (2008c) Responses of two contrasting genotypes of rice to brown planthopper. Mol Plant-Microbe Interact 21:122–132

    Article  CAS  PubMed  Google Scholar 

  • Wang WX, Luo J, Lai FX, Fu Q (2010) Identification and phylogenetic analysis of symbiotic bacteria Arsenophonus from the rice brown planthopper, Nilaparvata lugens (Stal) (Homoptera:Delphacidae). Acta Entomologia Sinica 53(6):647–654

    CAS  Google Scholar 

  • Weng Q, Huang Z, Wang X, Zhu L, He G (2003) In situ localization of proteinase inhibitor mRNA in rice plant challenged by brown planthopper. Chin Sci Bull 48:979–982

    CAS  Google Scholar 

  • Wetzel JM, Ohnishi M, Fujita T, Nakanishi K, Naya Y, Noda H, Sugiura M (1992) Diversity in steroidogenesis of symbiotic microorganisms from planthoppers. J Chem Ecol 18:2083–2094

    Article  CAS  Google Scholar 

  • Wilkinson TL, Ishikawa H (2001) On the functional significance of symbiotic microorganisms in the Homoptera: a comparative study of Acyrthosiphon pisum and Nilaparvata lugens. Physiol Entomol 26:86–93

    Article  Google Scholar 

  • Woodhead S, Padgham DE (1988) The effect of plant surface characteristics on resistance of rice to the brown planthopper, Nilaparvata lugens. Entomol Exp Appl 47:15–22

    Article  Google Scholar 

  • Xet-Mull AM, Quesada T, Espinosa AM (2004) Phylogenetic position of the yeast-like symbiotes of Tagosodes orizicolus (Homoptera: Delphacidae) based on 18S ribosomal DNA partial sequences. Revista de Biología Tropical 52:777–785

    PubMed  Google Scholar 

  • Xu J (2010) Metagenomics and ecosystems biology: conceptual frameworks, tools and methods. In: Marco D (ed) Metagenomics: theory, methods and applications. Caister Academic Press, Norfolk, pp 1–14

    Google Scholar 

  • Xu XF, Mei HW, Luo LJ, Cheng XN, Li ZK (2002) RFLP-facilitated investigation of the quantitative resistance of rice to brown planthopper (Nilaparvata lugens). Theor Appl Genet 104:248–253

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki M, Yoshimura A, Yasui H (2000) Mapping of quantitative trait loci of ovicidal response to brown planthopper (Nilaparvata lugens Stål) in rice (Oryza sativa L.). Breed Sci 50:291–296

    Article  CAS  Google Scholar 

  • Yang Z, Zhang F, Zhu L, He G (2006) Identification of differentially expressed genes in brown planthopper Nilaparvata lugens (Hemiptera: Delphacidae) responding to host plant resistance. Bull Entomol Res 96:53–59

    Article  CAS  PubMed  Google Scholar 

  • Yin JL, Xu HW, Wu JC, Hu JH, Yang GQ (2008) Cultivar and insecticide applications affect the physiological development of the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae). Environ Entomol 37:206–212

    Article  CAS  PubMed  Google Scholar 

  • Yoshihara T, Sogawa K, Pathak MD, Juliano BO, Sakamura S (1980) Oxalic acid as sucking inhibitor of the brown planthopper in rice (Delphacidae, Homoptera). Entomol Exp Appl 27:149–155

    Article  CAS  Google Scholar 

  • Zeigler RS, Pantoja A, Duque MC, Weber G (1994) Characteristics of resistance in rice to Hoja Blanca Virus (VHB) and its vector. Ann Appl Biol 124:429–440

    Article  Google Scholar 

  • Zhang F, Zhu L, He G (2004) Differential gene expression in response to brown planthopper feeding in rice. J Plant Physiol 161:53–62

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Wu H, Chen J, Zheng X, Chen L, Yu X (2007) A strain isolated from brown planthopper and its molecular identification. Chin J Rice Sci 21:551–554

    CAS  Google Scholar 

  • Zhang J, Chen J, Chen F, Zheng X, Chen L, Yu X (2009) The isolation of yeast-like symbiotes in the brown planthopper and the sequences analysis of its 26S rDNA. Scientia Agricultura Sinica 42:2211–2216

    CAS  Google Scholar 

  • Zhongxian L, Xiaoping Y, Jianming C, Xusong Z, Hongxing X (2001) Effects of endosymbiote on feeding, development and reproduction of brown planthopper, Nilaparvata lugens. Chin Rice Res Newsl 9:11–12

    Google Scholar 

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Acknowledgments

We wish to thank DuPont Pioneer, the Bill and Melinda Gates Foundation (Cereal System Initiative for South Asia—CSISA) and the Asian Development Bank (Reta 6489) for funding to undertake this research. Ajay Kohli (IRRI) and two anonymous reviewers gave many helpful comments on the manuscript. This is paper #3 from the New Paradigms in Ricehopper Resistance Workshop held at IRRI, Los Baños, Philippines, in October 2010. Funding for the workshop was provided by the Japanese Ministry of Agriculture and the Research Directorate of IRRI.

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Correspondence to Finbarr G. Horgan.

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Communicated by Handling Editor: Joseph Dickens.

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Ferrater, J.B., de Jong, P.W., Dicke, M. et al. Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties. Arthropod-Plant Interactions 7, 591–605 (2013). https://doi.org/10.1007/s11829-013-9277-9

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