Virulence Adaptation by Rice Planthoppers and Leafhoppers to Resistance Genes and Loci: A Review
Abstract
:Simple Summary
Abstract
1. Introduction
2. Literature Review
3. Results and Discussion
3.1. Resistance Genes—A Rare Genetic Resource
3.2. Resistance Genes—A Non-Renewable Resource
3.3. The Nature of Virulence Adaptation
3.3.1. Historical Evidence
3.3.2. Relict Populations
3.3.3. Selection Studies
3.3.4. Post-Selection Populations and the Utility of ‘Biotypes’
3.4. Mechanisms of Virulence Adaptation
3.4.1. Virulence Responses to Novel Hosts
3.4.2. Virulence Adaptation during Sustained Exposure to Resistant Rice
3.4.3. Microbiome Responses during Sustained Exposure to Resistant Rice
3.5. Deploying Resistance to Conserve Rare Genes
3.5.1. Gene Pyramiding and Durability
3.5.2. Varietal Deployment and Durability
4. Conclusions
Supplementary Materials
Funding
Data Availability Statement
Conflicts of Interest
References
- Pathak, M.D.; Khan, Z.R. Insect Pests of Rice; International Rice Research Institute: Los Baños, Philippines, 1994. [Google Scholar]
- Hu, G.; Lu, F.; Zhai, B.-P.; Lu, M.-H.; Liu, W.-C.; Zhu, F.; Wu, X.-W.; Chen, G.-H.; Zhang, X.-X. Outbreaks of the brown planthopper Nilaparvata lugens (Stål) in the Yangtze River Delta: Immigration or local reproduction? PLoS ONE 2014, 9, e88973. [Google Scholar] [CrossRef]
- Prenp, V.; Zalucki, M.P.; Jahn, G.C.; Nesbitt, H.J. Establishment of Nilaparvata lugens Stål in rice crop nurseries: A possible source of outbreaks. J. Asia-Pac. Entomol. 2002, 5, 75–83. [Google Scholar] [CrossRef]
- Hirano, K.; Fujii, K. The outbreak mechanisms of the green rice leafhopper, Nephotettix cincticeps Uhler, in northern Japan. Popul. Ecol. 1995, 37, 259–267. [Google Scholar] [CrossRef]
- Wu, Y.; Zhang, G.; Chen, X.; Li, X.-J.; Xiong, K.; Cao, S.-P.; Hu, Y.-Y.; Lu, M.-H.; Liu, W.-C.; Tuan, H.-A.; et al. The influence of Sogatella furcifera (Hemiptera: Delphacidae) migratory events on the Southern rice black-streaked dwarf virus epidemics. J. Econ. Entomol. 2017, 110, 854–864. [Google Scholar] [CrossRef]
- Escalada, M.M.; Luecha, M.; Heong, K.L. Social impacts of planthopper outbreaks: Case study from Thailand. In Rice Planthoppers: Ecology, Management, Socio-Economics and Policy; Heong, K.L., Escalada, M.M., Cheng, J., Eds.; Zhejiang University Press: Hangzhou, China, 2015; pp. 209–226. [Google Scholar]
- Bottrell, D.G.; Schoenly, K.G. Resurrecting the ghost of green revolutions past: The brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J. Asia-Pac. Entomol. 2012, 15, 122–140. [Google Scholar] [CrossRef]
- Dyck, V.A.; Thomas, B. The brown planthopper problem. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 3–17. [Google Scholar]
- Cheng, C.-H.; Chang, W.L. Studies on varietal resistance to the brown planthopper in Taiwan. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 251–272. [Google Scholar]
- Fernando, H.; Senadhera, D.; Elikawela, Y.; de Alwis, H.M.; Kudagamage, C. Varietal resistance to the brown planthopper in Sri Lanka. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 241–250. [Google Scholar]
- Pongprasert, S.; Weerapat, P. Varietal resistance to the brown planthopper in Thailand. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 273–282. [Google Scholar]
- Rashid, M.M.; Jahan, M.; Islam, K.S. Impact of nitrogen, phosphorus and potassium on brown planthopper and tolerance of its host rice plants. Rice Sci. 2016, 23, 119–131. [Google Scholar] [CrossRef]
- Horgan, F.G.; Srinivasan, T.S.; Naik, B.S.; Ramal, A.F.; Bernal, C.C.; Almazan, M.L.P. Effects of nitrogen on egg-laying inhibition and ovicidal response in planthopper-resistant rice varieties. Crop Prot. 2016, 89, 223–230. [Google Scholar] [CrossRef]
- Rashid, M.M.; Jahan, M.; Islam, K.S. Effects of nitrogen, phosphorous and potassium on host-choice behavior of brown planthopper, Nilaparvata lugens (Stål) on rice cultivar. J. Insect Behav. 2017, 30, 1–15. [Google Scholar] [CrossRef]
- Wu, J.; Ge, L.; Liu, F.; Song, Q.; Stanley, D. Pesticide-induced planthopper population resurgence in rice cropping systems. Annu. Rev. Entomol. 2020, 65, 409–429. [Google Scholar] [CrossRef]
- Visarto, P.; Zalucki, M.P.; Nesbitt, H.J.; Jahn, G.C. Effect of fertilizer, pesticide treatment, and plant variety on the realized fecundity and survival rates of brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae) generating outbreaks in Cambodia. J. Asia-Pac. Entomol. 2001, 4, 75–84. [Google Scholar] [CrossRef]
- Cuong, N.L.; Ben, P.T.; Phuong, L.T.; Chau, L.M.; Cohen, M.B. Effect of host plant resistance and insecticide on brown planthopper Nilaparvata lugens (Stål) and predator population development in the Mekong Delta, Vietnam. Crop Prot. 1997, 16, 707–715. [Google Scholar] [CrossRef]
- Matsukawa-Nakata, M.; Huy Chung, N.; Kobori, Y. Insecticide application and its effect on the density of rice planthoppers, Nilaparvata lugens and Sogatella furcifera, in paddy fields in the Red River Delta, Vietnam. J. Pestic. Sci. 2019, 44, 129–135. [Google Scholar] [CrossRef] [PubMed]
- Palmer, L.; Rao, P. Grassy stunt, ragged stunt and tungro diseases of rice in Indonesia. Int. J. Pest Manag. 1981, 27, 212–217. [Google Scholar] [CrossRef]
- Morinaka, T.; Putta, M.; Chettanachit, D.; Parejarearn, A.; Disthaporn, S. Transmission of rice ragged stunt disease in Thailand. JARQ 1983, 17, 138–144. [Google Scholar]
- Shikata, E.; Senboku, T.; Kamjaipai, K.; Chou, T.-G.; Tiongco, E.R.; Ling, K.C. Rice ragged stunt virus, a new member of plant reovirus group. Jpn. J. Phytopathol. 1979, 45, 436–443. [Google Scholar] [CrossRef]
- Nakasuji, F. Epidemiological study on rice dwarf virus transmitted by the green rice leafhopper Nephotettix cincticeps. JARQ 1974, 8, 84–91. [Google Scholar]
- Inoue, H.; Ruy-Aree, S. Bionomics of green rice leafhopper and epidemics of yellow orange leaf virus disease in Thailand. Trop. Agric. Res. Ser. 1977, 10, 117–121. [Google Scholar]
- Kobayashi, A.; Supaad, M.A.; Othman, B.O. Inheritance of resistance of rice to tungro and biotype selection of green leafhopper in Malaysia. JARQ 1983, 16, 306–311. [Google Scholar]
- Romena, A.M.; Rapusas, H.R.; Heinrichs, E.A. Evaluation of rice accessions for resistance to the whitebacked planthopper Sogatella furcifera (Horváth)(Homoptera: Delphacidae). Crop Prot. 1985, 5, 334–340. [Google Scholar] [CrossRef]
- Rath, P.C.; Prakash, A.; Rao, J.; Subudhi, H.N. Screening of rice varieties against white backed plant hopper (WBPH) Sogatella furcifera Horváth, in net house condition. J. Appl. Zool. Res. 2005, 16, 21–22. [Google Scholar]
- Ali, M.P.; Alghamdi, S.S.; Begum, M.A.; Anwar Uddin, A.B.M.; Alam, M.Z.; Huang, D. Screening of rice genotypes for resistance to the brown planthopper, Nilaparvata lugens Stål. Cereal Res. Commun. 2012, 40, 502–508. [Google Scholar] [CrossRef]
- Fujita, D.; Kohli, A.; Horgan, F.G. Rice resistance to planthoppers and leafhoppers. Crit. Rev. Plant Sci. 2013, 32, 162–191. [Google Scholar] [CrossRef]
- Mishra, A.; Barik, S.R.; Pandit, E.; Yadav, S.S.; Das, S.R.; Pradhan, S.K. Genetics, mechanisms and deployment of brown planthopper resistance genes in rice. Crit. Rev. Plant Sci. 2022, 41, 91–127. [Google Scholar] [CrossRef]
- Hu, J.; Xiao, C.; He, Y. Recent progress on the genetics and molecular breeding of brown planthopper resistance in rice. Rice 2016, 9, 30. [Google Scholar] [CrossRef]
- Muduli, L.; Pradhan, S.K.; Mishra, A.; Bastia, D.N.; Samal, K.C.; Agrawal, P.K.; Dash, M. Understanding brown planthopper resistance in rice: Genetics, biochemical and molecular breeding approaches. Rice Sci. 2021, 28, 532–546. [Google Scholar] [CrossRef]
- Horgan, F.G.; Almazan, M.L.P.; Vu, Q.; Ramal, A.F.; Bernal, C.C.; Yasui, H.; Fujita, D. Unanticipated benefits and potential ecological costs associated with pyramiding leafhopper resistance loci in rice. Crop Prot. 2019, 115, 47–58. [Google Scholar] [CrossRef]
- Claridge, M.F.; Den Hollander, J. The biotypes of the rice brown planthopper, Nilaparvata lugens. Entomol. Exp. Appl. 1980, 27, 23–30. [Google Scholar] [CrossRef]
- Sogawa, K. Biological and genetic nature of biotype populations of the brown planthopper, Nilaparvata lugens. JARQ 1980, 14, 187–190. [Google Scholar]
- Den Hollander, J.; Pathak, P.K. The genetics of the biotypes of the rice brown plantopper, Nilaparvata lugens. Entomol. Exp. Appl. 1981, 29, 76–86. [Google Scholar] [CrossRef]
- Ito, K.; Kisimoto, R. Selection of new biotypes of the brown planthopper, Nilaparvata lugens Stål, capable of surviving on resistant rice cultivars. J. Cent. Agric. Exp. Stn. 1981, 1, 139–154. [Google Scholar]
- Ferrater, J.B.; Naredo, A.I.; Almazan, M.L.P.; de Jong, P.W.; Dicke, M.; Horgan, F.G. Varied responses by yeast-like symbionts during virulence adaptation in a monophagous phloem-feeding insect. Arthropod-Plant Interact. 2015, 9, 215–224. [Google Scholar] [CrossRef]
- Horgan, F.G.; Ramal, A.F.; Bentur, J.S.; Kumar, R.; Bhanu, K.V.; Sarao, P.S.; Iswanto, E.H.; Chien, H.V.; Phyu, M.H.; Bernal, C.C.; et al. Virulence of brown planthopper (Nilaparvata lugens) populations from South and South East Asia against resistant rice varieties. Crop Prot. 2015, 78, 222–231. [Google Scholar] [CrossRef]
- Horgan, F.G.; Srinivasan, T.S.; Bentur, J.S.; Kumar, R.; Bhanu, K.V.; Sarao, P.S.; Chien, H.V.; Almazan, M.L.P.; Bernal, C.C.; Ramal, A.F.; et al. Geographic and research center origins of rice resistance to Asian planthoppers and leafhoppers: Implications for rice breeding and gene deployment. Agronomy 2017, 7, 62. [Google Scholar] [CrossRef] [PubMed]
- Priyadarshini, S.; Lakshmi, V.J.; Madhav, M.S.; Rajeswari, B.; Srinivas, C. Virulence of rice brown planthopper, Nilaparvata lugens (Stål) population from Khammam district of Telangana State against rice genotypes and its morphometrics. J. Res. PJTSAU 2021, 49, 16–22. [Google Scholar]
- Horgan, F.G. Slowing virulence adaptation in Asian rice planthoppers through migration-based deployment of resistance genes. Curr. Opin. Insect Sci. 2023, 55, 101004. [Google Scholar] [CrossRef]
- Habibuddin, H. Variation of brown planthopper population from major rice regions of Peninsular Malaysia. MARDI Res. J. 1989, 17, 218–224. [Google Scholar]
- Wada, T.; Ito, K.; Takahashi, A. Biotype comparisons of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae) collected in Japan and the Indochina Peninsula. Appl. Entomol. Zool. 1994, 29, 477–484. [Google Scholar] [CrossRef]
- Cheng, J.A. Rice planthopper problems and relevant causes in China. In Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia; Heong, K.L., Hardy, B., Eds.; International Rice Research Institute: Los Baños, Philippines, 2009; pp. 157–178. [Google Scholar]
- Gallagher, K.D.; Kenmore, P.E.; Sogawa, K. Judicial use of insecticides deter planthopper outbreaks and extend the life of resistant varieties in Southeast Asian rice. In Planthoppers: Their Ecology and Management; Denno, R.F., Perfect, T.J., Eds.; Springer: Boston, MA, USA, 1994; pp. 599–614. [Google Scholar]
- Horgan, F.G. Mechanisms of resistance: A major gap in understanding planthopper-rice interactions. In Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia; Heong, K.L., Hardy, B., Eds.; International Rice Research Institute: Los Baños, Philippines, 2009; pp. 281–302. [Google Scholar]
- Shi, X.-h.; Hu, R.-f. Rice variety improvement and the contribution of foreign germplasms in China. J. Integr. Agric. 2017, 16, 2337–2345. [Google Scholar] [CrossRef]
- Gamalath, N.S.; Tufail, M.; Sharma, P.N.; Mori, N.; Takeda, M.; Nakamura, C. 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. 2012, 47, 9–16. [Google Scholar] [CrossRef]
- Horgan, F.G. Integrating gene deployment and crop management for improved rice resistance to Asian planthoppers. Crop Prot. 2018, 110, 21–33. [Google Scholar] [CrossRef]
- Horgan, F.G. Integrated pest management for sustainable rice cultivation: A holistic approach. In Achieving Sustainable Cultivation of Rice, Vol 2: Cultivation, Pest and Disease Management; Sasaki, T., Ed.; Burleigh Dodds Series in Agricultural Science; Burleigh Dodds Scientific Publishing: London, UK, 2017; pp. 309–341. [Google Scholar]
- Garrett, K.A.; Andersen, K.F.; Asche, F.; Bowden, R.L.; Forbes, G.A.; Kulakow, P.A.; Zhou, B. Resistance genes in global crop breeding networks. Phytopathology 2017, 107, 1268–1278. [Google Scholar] [CrossRef]
- Yamasaki, M.; Yoshimura, A.; Yasui, H. Genetic basis of ovicidal response to whitebacked planthopper (Sogatella furcifera Horváth) in rice (Oryza sativa L.). Mol. Breed. 2003, 12, 133–143. [Google Scholar] [CrossRef]
- Yang, Y.; Xu, J.; Leng, Y.; Xiong, G.; Hu, J.; Zhang, G.; Huang, L.; Wang, L.; Guo, L.; Li, J.; et al. Quantitative trait loci identification, fine mapping and gene expression profiling for ovicidal response to whitebacked planthopper (Sogatella furcifera Horváth) in rice (Oryza sativa L.). BMC Plant Biol. 2014, 14, 145. [Google Scholar] [CrossRef] [PubMed]
- Horgan, F.G.; Mundaca, E.A.; Quintana, R.; Naredo, A.I.; Almazan, M.L.P.; Bernal, C.C. Efficacy and cost-effectiveness of phenotyping for rice resistance and tolerance to planthoppers. Insects 2021, 12, 847. [Google Scholar] [CrossRef] [PubMed]
- Heinrichs, E. Genetic Evaluation for Insect Resistance in Rice; International Rice Research Institute: Los Baños, Philippines, 1985. [Google Scholar]
- Yang, T.; Gu, F.; Shi, S.; Gu, Z. Incorporation of brown planthopper (BPH) resistance genes from indica into japonica rice. IRRN 1988, 13, 11. [Google Scholar]
- Mui, P.T.; Bong, B. Evaluation of rice varieties for resistance to brown planthopper in the Mekong Delta. Omonrice 1999, 7, e7. [Google Scholar]
- Liu, Y.; Su, C.; Jiang, L.; He, J.; Wu, H.; Peng, C.; Wan, J. The distribution and identification of brown planthopper resistance genes in rice. Hereditas 2009, 146, 67–73. [Google Scholar] [CrossRef]
- Pathak, M.D.; Khush, G.S. Studies of varietal resistance in rice to the brown planthopper at the International Rice Research Institute. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 285–302. [Google Scholar]
- Kalode, M.B.; Krishna, T.S. Varietal resistance to brown planthopper in India. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 187–200. [Google Scholar]
- Misra, D.S.; Reddy, K.D.; Misra, B.C. Varietal screening for leafhopper and planthopper resistance at Varanasi, India. IRRN 1986, 11, 9–10. [Google Scholar]
- Rani, N.S.; Kalode, M.B.; Bentur, J.S.; Pati, D.; Siddiq, E.A. Genetic sources of resistance to whitebacked planthopper in scented quality rices. IRRN 1992, 17, 10. [Google Scholar]
- Roy, D.; Biswas, A.; Sarkar, S.; Chakraborty, G.; Gaber, A.; Kobeasy, M.I.; Hossain, A. Evaluation and characterization of indigenous rice (Oryza sativa L.) landraces resistant to brown planthopper Nilaparvata lugens (Stål.) biotype 4. PeerJ 2022, 10, e14360. [Google Scholar] [CrossRef]
- Krishna, T.S.; Seshu, D.V.; Kalode, M.B. Varietal screening for brown planthopper resistance. IRRN 1980, 5, 7. [Google Scholar]
- Kabir, M.A.; Alam, M.S. Varietal screening for resistance to brown planthopper and its biotype in Bangladesh. IRRN 1981, 6, 8–9. [Google Scholar]
- Reddy, K.V.; Kalode, M.B. Mechanism of resistance in rice varieties showing differential reaction to brown planthopper. Proc. Indian Acad. Sci. 1985, 94, 37–48. [Google Scholar] [CrossRef]
- Velusamy, R. Resistance of wild rices, Oryza spp., to the brown planthopper, Nilaparvata lugens (Stål)(Homoptera: Delphacidae). Crop Prot. 1988, 7, 403–408. [Google Scholar] [CrossRef]
- Pathak, K.A.; Heinrichs, E.A. Varietal screening of selected Indian rice cultivars to whitebacked planthopper Sogatella furcifera (Horváth). Indian J. Entomol. 1990, 52, 100–104. [Google Scholar]
- Oka, H.I. Genetic diversity of wild and cultivated rice. In Rice Biotechnology; Khush, G.S., Toenniessen, G.H., Eds.; CAB International: Wallingford, UK, 1991; pp. 55–83. [Google Scholar]
- Singh, J.; Sidhu, G.S.; Shukla, K.K.; Sharma, D.R. Screening entries in the International Rice Whitebacked Planthopper Nursery (IRWBPHN) 1991 for resistance to whitebacked planthopper (WBPH) in Ludhiana, India. IRRN 1993, 18, 25–26. [Google Scholar]
- Santhanalakshmi, S.; Shukla, K.K.; Kumar Prince, S.J. Evaluation of resistance of wild rices, Oryza spp. to the whitebacked planthopper, Sogatella furcifera (Horváth)(Homoptera: Delphacidae). Arch. Phytopathol. Plant Prot. 2010, 43, 1088–1097. [Google Scholar] [CrossRef]
- Velusamy, R. Resistance of wild rices, Oryza spp., to the whitebacked planthopper, Sogatella furcifera (Horváth)(Homoptera: Delphacidae). Crop Prot. 1989, 8, 265–270. [Google Scholar] [CrossRef]
- Duan, C.-x.; Zhang, S.-x.; Lei, C.-l.; Cheng, Z.-j.; Chen, Q.; Zhai, H.-q.; Wan, J.-m. Evaluation of rice germplasm for resistance to the small brown planthopper (Laodelphax striatellus) and analysis of resistance mechanism. Rice Sci. 2008, 15, 36–42. [Google Scholar] [CrossRef]
- Shao, L.Y.; Sun, F.Y.; Wang, X.Q.; Li, Z.Q.; Yu, F.Q.; Yang, M. Identification of rice varieties resistant to the small brown planthopper (Laodelphax striatellus) in Liaoning and an investigation of their resistance mechanisms. Chin. J. Appl. Entomol. 2013, 50, 1649–1659. [Google Scholar]
- Sunio, L.M.; Heinrichs, E.A. Varietal resistance to the green leafhopper, Nephotettix virescens in the world collection of rice [Oryza sativa](Philippines). In Proceedings of the 16 Annual Convention of Pest Control Council of the Philippines, La Trinidad, Philippines, 2–4 May 1985; p. 1. [Google Scholar]
- Cheng, C.-H.; Pathak, M.D. Resistance to Nephotettix virescens in rice varieties. J. Econ. Entomol. 1972, 65, 1148–1153. [Google Scholar] [CrossRef]
- Razzaque, Q.M.A.; Heinrichs, E.A. Evaluation of germplasm accessions for green leafhopper (GLH) resistance. IRRN 1985, 10, 9–10. [Google Scholar]
- Koshihara, T. Resistance of rice varieties against green rice leafhopper, Nephotettix cincticeps Uhler. Trop. Agric. Res. Ser. 1971, 5, 221–225. [Google Scholar]
- Van Mai, T.; Yoshimura, A.; Yasui, H. Characterization of resistance to the green rice leafhopper (Nephotettix cincticeps Uhler) in a core collection of landraces in rice (Oryza sativa L.). Am. J. Plant Sci. 2017, 8, 236–256. [Google Scholar]
- Razzaque, Q.M.A.; Heinrichs, E.A. Screening wild rices for resistance to green leafhopper (GLH) resistance. IRRN 1985, 10, 11–12. [Google Scholar]
- Pongprasert, S. Resistance to the zigzag leafhopper. In Recilia Dorsalis (Motschulsky), in Rice Varieties; University of the Philippines Los Baños: Los Baños, Philippines, 1974. [Google Scholar]
- Jennings, P.R.; Pineda, A.T. Screening rice for resistance to the planthopper Sogatodes orizicola (Muir). Crop Sci. 1970, 10, 687–689. [Google Scholar] [CrossRef]
- International Rice Research Institute. Standard Evaluation Systems (SES) for Rice; International Rice Research Institute: Los Baños, Philippines, 2002. [Google Scholar]
- Pathak, M.D. Resistance to leafhoppers and planthoppers in rice varieties. In Proceedings of the Symposium on Tropical Agriculture Researches, Tokyo, Japan, 19–24 July 1971; p. 179. [Google Scholar]
- Hajano, J.U.D.; Zhang, H.B.; Ren, Y.D.; Lu, C.T.; Wang, X.F. Screening of rice (Oryza sativa) cultivars for resistance to rice black streaked dwarf virus using quantitative PCR and visual disease assessment. Plant Pathol. 2016, 65, 1509–1517. [Google Scholar] [CrossRef]
- Feng, Z.; Kang, H.; Li, M.; Zou, L.; Wang, X.; Zhao, J.; Wei, L.; Zhou, N.; Li, Q.; Lan, Y.; et al. Identification of new rice cultivars and resistance loci against rice black-streaked dwarf virus disease through genome-wide association study. Rice 2019, 12, 49. [Google Scholar] [CrossRef] [PubMed]
- Yu, W.; He, J.; Wu, J.; Xu, Z.; Lai, F.; Zhong, X.; Zhang, M.; Ji, H.; Fu, Q.; Zhou, X.; et al. Resistance to planthoppers and Southern rice black-streaked dwarf virus in rice germplasms. Plant Dis. 2023, 108, 2321–2329. [Google Scholar] [CrossRef]
- Lee, S.-C. Towards integrated pest management of rice in Korea. Korean J. Appl. Entomol. 1992, 31, 205–240. [Google Scholar]
- Claridge, M.F.; Den Hollander, J.; Furet, I. Adaptations of brown planthopper (Nilaparvata lugens) populations to rice varieties in Sri Lanka. Entomol. Exp. Appl. 1982, 32, 222–226. [Google Scholar] [CrossRef]
- Rosida, N.; Kuswinanti, T.; Nasruddin, A.; Amin, N. Green leafhopper (Nephotettix virescens Distan) biotype and their ability to transfer tungro disease in South Sulawesi, Indonesia. IOP Conf. Ser. Earth Environ. Sci. 2020, 486, 012147. [Google Scholar] [CrossRef]
- Claridge, M.F.; Den Hollander, J. Virulence to rice cultivars and selection for virulence in populations of the brown planthopper Nilaparvata lugens. Entomol. Exp. Appl. 1982, 32, 213–221. [Google Scholar] [CrossRef]
- Alam, S.N.; Cohen, M.B. Durability of brown planthopper, Nilaparvata lugens, resistance in rice variety IR64 in greenhouse selection studies. Entomol. Exp. Appl. 1998, 89, 71–78. [Google Scholar] [CrossRef]
- Vu, Q.; Quintana, R.; Fujita, D.; Bernal, C.C.; Yasui, H.; Medina, C.D.; Horgan, F.G. Responses and adaptation by Nephotettix virescens to monogenic and pyramided rice lines with Grh-resistance genes. Entomol. Exp. Appl. 2014, 150, 179–190. [Google Scholar] [CrossRef]
- Rezaul Karim, A.N.M.; Pathak, M.D. An alternate biotype of green leafhopper in Bangladesh. IRRN 1979, 4, 7–8. [Google Scholar]
- Khush, G.S.; Virk, P.S. IR Varieties and Their Impact; International Rice Research Institute: Los Baños, Philippines, 2005. [Google Scholar]
- Bai, N.R.; Nair, G.N. Sources of resistance to brown planthopper (BPH) in rice. IRRN 1992, 17, 14. [Google Scholar]
- Zhao, Y.; Huang, J.; Wang, Z.Z.; Jing, S.L.; Wang, Y.; Ouyang, Y.D.; Cai, B.D.; Xin, X.F.; Liu, X.; Zhang, C.X.; et al. Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proc. Natl. Acad. Sci. USA 2016, 113, 12850–12855. [Google Scholar] [CrossRef]
- Tan, G.X.; Weng, Q.M.; Ren, X.; Huang, Z.; Zhu, L.L.; He, G.C. Two whitebacked planthopper resistance genes in rice share the same loci with those for brown planthopper resistance. Heredity 2004, 92, 212–217. [Google Scholar] [CrossRef]
- Peñalver-Cruz, A.; Arida, A.; Heong, K.L.; Horgan, F.G. Aspects of brown planthopper adaptation to resistant rice varieties with the Bph3 gene. Entomol. Exp. Appl. 2011, 141, 245–257. [Google Scholar] [CrossRef]
- Srinivasan, T.S.; Almazan, M.L.P.; Bernal, C.C.; Fujita, D.; Ramal, A.F.; Yasui, H.; Subbarayalu, M.K.; Horgan, F.G. Current utility of the BPH25 and BPH26 genes and possibilities for further resistance against plant- and leafhoppers from the donor cultivar ADR52. Appl. Entomol. Zool. 2015, 50, 533–543. [Google Scholar] [CrossRef]
- Myint, K.K.M.; Yasui, H.; Takagi, M.; Matsumura, M. Virulence of long-term laboratory populations of the brown planthopper, Nilaparvata lugens (Stål), and whitebacked Planthopper, Sogatella furcifera (Horváth) (Homoptera: Delphacidae), on rice differential varieties. Appl. Entomol. Zool. 2009, 44, 149–153. [Google Scholar] [CrossRef]
- Ketipearachchi, Y.; Kaneda, C.; Nakamura, C. Adaptation of the brown planthopper (BPH), Nilaparvata lugens (Stål) (Homoptera: Delphacidae), to BPH resistant rice cultivars carrying bph8 or Bph9. Appl. Entomol. Zool. 1998, 33, 497–505. [Google Scholar] [CrossRef]
- Horgan, F.G.; Garcia, C.P.F.; Haverkort, F.; de Jong, P.W.; Ferrater, J.B. Changes in insecticide resistance and host range performance of planthoppers artificially selected to feed on resistant rice. Crop Prot. 2020, 127, 104963. [Google Scholar] [CrossRef] [PubMed]
- Myint, K.K.M.; Matsumura, M.; Takagi, M.; Yasui, H. 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. 2009, 54, 159–164. [Google Scholar] [CrossRef]
- Fujii, T.; Yoshida, K.; Kobayashi, T.; Myint, K.K.M.; Yasui, H.; Sanada-Morimura, S.; Matsumura, M. Long-term virulence monitoring of differential cultivars in Japan’s immigrant populations of Nilaparvata lugens (Hemiptera: Delphacidae) in 2001–2019. Appl. Entomol. Zool. 2021, 56, 407–418. [Google Scholar] [CrossRef]
- Dahal, G.; Hibino, H.; Aguiero, V.M. Population characteristics and tungro transmission by Nephotettix virescens (Hemiptera: Cicadellidae) on selected resistant rice cultivars. Bull. Entomol. Res. 1997, 87, 387–395. [Google Scholar] [CrossRef]
- Dahal, G.; Hibino, H.; Cabunagan, R.C.; Tiongco, E.R.; Flores, Z.M.; Aguiero, V.M. Changes in cultivar reactions to tungro due to changes in virulence of the leafhopper vector. Phytopathology 1990, 80, 659–665. [Google Scholar] [CrossRef]
- Bahagiawati, A.; Heinrichs, E.; Medrano, F. Effect of host plant on the level of virulence of Nilaparvata lugens (Homoptera: Delphacidae) on rice cultivars. Environ. Entomol. 1989, 18, 489–493. [Google Scholar] [CrossRef]
- Cheng, C.-H. Interactions between biotypes of the brown planthopper and rice varieties. J. Agric. Res. China 1985, 34, 299–314. [Google Scholar]
- Heinrichs, E.A. Perspectives and directions for the continued development of insect-resistant rice varieties. Agric. Ecosyst. Environ. 1986, 18, 9–36. [Google Scholar] [CrossRef]
- Ho, D.T.; Taro, A. Rice resistance to brown planthopper (BPH) in the Solomon Islands. IRRN 1985, 10, 6–7. [Google Scholar]
- Joshi, R.C.; Shepard, B.M.; Kenmore, P.E.; Lydia, R. Insecticide-induced resurgence of brown planthopper (BPH) on IR62. IRRN 1992, 17, 9–10. [Google Scholar]
- Chau, N.L.; Thuat, N.C.; Chai, V.T. Changes in brown planthopper (BPH) biotypes in the Mekong Delta of Vietnam. IRRN 1993, 18, 26–27. [Google Scholar]
- Chau, L.M. Virulence of a new biotype of brown planthopper (BPH) in Mekong Delta. IRRN 1990, 17, 14–15. [Google Scholar]
- Phuong, L.T.; Chau, L.M. Resistance of varieties derived from Oryza sativa/Oryza officinalis to brown planthopper in the Mekong Delta, Vietnam. IRRN 1997, 22, 26–27. [Google Scholar]
- Thuat, N.C.; Huong, N.T.; Binh, D.T.; Chien, H.V.; Chau, N.L. Virulence of brown planthopper (BPH) in Vietnam. IRRN 1992, 17, 11. [Google Scholar]
- Deng, Z.; Qin, P.; Liu, K.; Jiang, N.; Yan, T.; Zhang, X.; Fu, C.; He, G.; Wang, K.; Yang, Y. The development of multi-resistant rice restorer lines and hybrid varieties by pyramiding resistance genes against blast and brown planthopper. Agronomy 2024, 14, 878. [Google Scholar] [CrossRef]
- Heinrichs, E.A.; Rapusas, H.R. Response to selection for virulence of Nephotettix virescens (Homoptera: Cicadellidae) on resistant rice cultivars. Environ. Entomol. 1990, 19, 167–175. [Google Scholar] [CrossRef]
- Seo, B.Y.; Jung, J.K.; Choi, B.R.; Park, H.M.; Lee, S.W.; Lee, B.H. Survival rate and stylet penetration behavior of current Korean populations of the brown planthopper, Nilaparvata lugens, on resistant rice varieties. J. Asia-Pac. Entomol. 2010, 13, 1–7. [Google Scholar] [CrossRef]
- Claridge, M.F.; Den Hollander, J.; Haslam, D. The significance of morphometric and fecundity differences between the biotypes of the brown planthopper, Nilaparvata lugens. Entomol. Exp. Appl. 1984, 36, 107–114. [Google Scholar] [CrossRef]
- Horgan, F.G.; Peñalver-Cruz, A.; Arida, A.; Ferrater, J.B.; Bernal, C.C. Adaptation by the brown planthopper to resistant rice: A test of female-derived virulence and the role of yeast-like symbionts. Insects 2021, 12, 908. [Google Scholar] [CrossRef]
- Lu, Z.; Yu, X.; Wu, G.; Tao, L.; Chen, J.; Zheng, X. The virulence change and damage characteristics of various geographic populations of brown planthopper. Insect Sci. 1999, 6, 146–154. [Google Scholar] [CrossRef]
- Lu, Z.-x.; Yu, X.-p.; Chen, J.-m.; Zheng, X.-s.; Xu, H.-x.; Zhang, Z.-t. The bionomics of biotype 2 populations of brown planthopper collected in field and domesticated in greenhouse. Chin. J. Rice Sci. 2002, 16, 89. [Google Scholar]
- Kaneda, C.; Kisimoto, R. Status of varietal resistance to brown planthopper in Japan. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 209–218. [Google Scholar]
- Naeemullah, M.; Sharma, P.N.; Tufail, M.; Mori, N.; Matsumura, M.; Takeda, M.; Nakamura, C. Characterization of brown planthopper strains based on their differential responses to introgressed resistance genes and on mitochondrial DNA polymorphism. Appl. Entomol. Zool. 2009, 44, 475–483. [Google Scholar] [CrossRef]
- Tanaka, K.; Matsumura, M. Development of virulence to resistant rice varieties in the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae), immigrating into Japan. Appl. Entomol. Zool. 2000, 35, 529–533. [Google Scholar] [CrossRef]
- Takita, T.; Hashim, H. Relationship between laboratory-developed biotypes of green leafhopper and resistant varieties of rice in Malaysia. JARQ 1985, 19, 219–223. [Google Scholar]
- Rapusas, H.R.; Heinrichs, E.A. Plant age and levels of resistance to green leafhopper, Nephotettix virescens (Distant), and tungro virus in rice varieties. Crop Prot. 1982, 1, 91–98. [Google Scholar] [CrossRef]
- Horgan, F.G.; Bernal, C.C.; Vu, Q.; Almazan, M.L.P.; Ramal, A.F.; Yasui, H.; Fujita, D. Virulence adaptation in a rice leafhopper: Exposure to ineffective genes compromises pyramided resistance. Crop Prot. 2018, 113, 40–47. [Google Scholar] [CrossRef]
- Rapusas, H.R.; Heinrichs, E.A. Feeding behavior of Nephotettix virescens (Homoptera: Cicadellidae) on rice varieties with different levels of resistance. Environ. Entomol. 1990, 19, 594–602. [Google Scholar] [CrossRef]
- Herdt, R.W.; Capule, C. Adoption, Spread and Production Impact of Modern Rice Varieties in Asia; International Rice Reserach Institute: Los Baños, Philippines, 1983. [Google Scholar]
- Heinrichs, E.A. Varietal resistance to the brown planthopper and yellow stem borer. In Rice Improvement in China and Other Asian Countries; International Rice Research Institute: Los Baños, Philippines, 1980; pp. 195–217. [Google Scholar]
- Chaudhary, R.; Ahn, S. International network for genetic evaluation of rice (INGER) and its Modus operandi for multi-environment testing. In Plant Adaptation and Crop Improvement; CAB International: Wallingford, UK, 1996; pp. 139–164. [Google Scholar]
- Sogawa, K.; Kusumayadi, A. Monitoring brown planthopper (BPH) biotypes by rice garden in North Sumatra. IRRN 1984, 9, 15–16. [Google Scholar]
- Saxena, R.C.; Barrion, A.A. Biotypes of the brown planthopper Nilaparvata lugens (Stål) and strategies in development of host plant-resistance. Insect Sci. Appl. 1985, 6, 271–289. [Google Scholar] [CrossRef]
- Pathak, P.K.; Lal, M.N.; Pant, G.B. Varietal resistance to the brown planthopper Nilaparvata lugens (Stål) and its biotypes. IRRN 1976, 1, 8. [Google Scholar]
- Verma, S.K.; Pathak, P.K.; Singh, B.N.; Lal, M.N. Indian biotypes of the brown planthopper. IRRN 1979, 4, 7. [Google Scholar]
- Baskaran, B.; Narayanaswamy, P.; Sambasivam, A. BPH outbreak in South Arcot District, Tamil Nadu, India. IRRN 1983, 8, 18. [Google Scholar]
- Das, S.R.; Dhal, N.K.; Mohanty, H.K. IR13429-196-1-20 and IR17525-56-2-2-2: Two promising brown planthopper (BPH)-tolerant lines. IRRN 1984, 9, 7. [Google Scholar]
- Velusamy, R.; Chelliah, S.; Heinrichs, E.A.; Medrano, F. Brown planthopper biotypes in India. IRRN 1984, 9, 19. [Google Scholar]
- Prakasa Rao, P.S. Testing for field resistance in rice under induced brown planthopper (BPH) outbreaks. IRRN 1985, 10, 5–6. [Google Scholar]
- Velusamy, R.; Saxena, R.C. Genes conditioning resistance to brown planthopper (BPH). IRRN 1989, 14, 12–13. [Google Scholar]
- Pophaly, D.J.; Rana, D.K. Virulence of brown planthopper (BPH) in Raipur, India. IRRN 1992, 17, 12–13. [Google Scholar]
- Pophaly, D.J.; Rana, D.K. Reaction of IR varieties to the brown planthopper (BPH) population in Raipur, Madhya Pradesh, India. IRRN 1993, 18, 27–28. [Google Scholar]
- Shrestha, G.L.; Adhikary, R.R. A new brown planthopper (BPH) biotype in Parwanipur, Nepal. IRRN 1987, 12, 34. [Google Scholar]
- Mochida, O. IR26 found susceptible to the brown planthopper in North Sumatra, Indonesia. IRRN 1977, 2, 10–11. [Google Scholar]
- Oka, I.N. Quick method for identifying brown planthopper biotypes in the field. IRRN 1978, 3, 11–12. [Google Scholar]
- Sogawa, K.; Kilin, D. Inheritance of virulence of the North Sumatra population of the brown planthopper (BPH) on IR42. IRRN 1984, 9, 14–15. [Google Scholar]
- Sogawa, K.; Kilin, D.; Bhagiawati, A.H. Characterization of the brown planthopper population on IR42 in North Sumatra, Indonesia. IRRN 1984, 9, 25. [Google Scholar]
- Sogawa, K.; Soekirno, S.; Raksadinata, Y. New genetic makeup of brown planthopper (BPH) populations in Central Java, Indonesia. IRRN 1987, 12, 29–30. [Google Scholar]
- Sogawa, K.; Kilin, D. Biotype shift in a brown planthopper (BPH) population on IR42. IRRN 1987, 12, 40. [Google Scholar]
- Erdiansyah, I.; Damanhuri. Performance of resistance of rice varieties recommendation of Jember Regency to brown planthopper pest (Nilaparvata lugens Stål.). IOP Conf. Ser. Earth Environ. Sci. 2018, 207, 012041. [Google Scholar] [CrossRef]
- Chaerani, C.; Damayanti, D.; Trisnaningsih, T.; Yuriyah, S.; Kusumanegara, K.; Dadang, A.; Sutrisno, S.; Bahagiawati., B. Virulence of brown planthopper and development of core collection of the pest. J. Penelit. Pertan. Tanam. Pangan 2016, 35, 125601. [Google Scholar] [CrossRef]
- Ito, K.; Wada, T.; Takahashi, A.; Salleh, N.; Hassim, H. Brown planthopper Nilaparvata lugens Stål (Homoptera, Delphacidae) biotypes capable of attacking resistant rice varieties in Malaysia. Appl. Entomol. Zool. 1994, 29, 523–532. [Google Scholar] [CrossRef]
- Feuer, R. Biotype 2 brown planthopper in the Philippines. IRRN 1976, 1, 15. [Google Scholar]
- Domingo, I.T. Pest incidence in Central Luzon, the rice granary of the Philippines. IRRN 1976, 1, 9. [Google Scholar]
- Heinrichs, E.A.; Viajante, V. Field reaction of rice to the brown planthopper and ragged stunt virus. IRRN 1978, 3, 9–10. [Google Scholar]
- Peralta, C.A.; Fontanilla, W.S.; Ferrer, L.S. Brown planthopper resurgence on IR36 in Mindanao, Philippines. IRRN 1983, 8, 13–14. [Google Scholar]
- Medrano, F.; Heinrichs, E.A. Responses of resistant rices to brown planthoppers (BPH) collected in Mindanao, Philippines. IRRN 1985, 10, 14–15. [Google Scholar]
- Medina, E.B.; Bernal, C.C.; Cohen, M.B. Role of host plant resistance in successful control of brown planthopper in Central Luzon, Philippines. IRRN 1996, 21, 53. [Google Scholar]
- Chansrisommai, N.; Katanyukul, W. Resistance of modern rice varieties to the brown planthopper in Thailand. IRRN 1982, 7, 9. [Google Scholar]
- Thanysiriwat, T.; Pattwatang, P.; Angeles, E.R. New biotypes of brown planthopper in Thailand. In Proceedings of the Rice and Temperate Cereal Crops Annual Conference, Chon Buri, Thailand, 9–11 June 2009; Bangkok, Thailand, 2009; pp. 386–389. [Google Scholar]
- Chaiyawat, P. Virulence of brown planthopper (Nilaparvata lugens Stål) against differential resistant and certified rice varieties in the major irrigated rice-growing areas of Thailand. In Proceedings of the 28th International Rice Research Conference, Hanoi, Vietnam, 8–12 November 2010; pp. 1–9. [Google Scholar]
- Sreewongchai, T.; Worede, F.; Phumichai, C.; Sripichitt, P. Evaluation of rice genotypes for resistance to brown planthopper (Nilaparvata lugens Stål) populations from the central region of Thailand. Agric. Nat. Resour. 2015, 49, 506–515. [Google Scholar]
- Huynh, N.V. New biotype of brown planthopper in the Mekong Delta of Vietnam. IRRN 1977, 2, 10. [Google Scholar]
- Thuat, N.C.; Thans, D.V. Population dynamics of the brown planthopper (BPH) in the Mekong Delta. IRRN 1984, 9, 14–15. [Google Scholar]
- Huynh, N.V.; Nhung, H.T. High virulence of new brown planthopper (BPH) populations in the Mekong Delta, Vietnam. IRRN 1987, 13, 16. [Google Scholar]
- Chau, L.M. Development of a brown planthopper (BPH) biotype and change in varietal resistance in Mekong Delta. IRRN 1990, 15, 12. [Google Scholar]
- Stapley, J.; May-Jackson, Y.Y.; Golden, W. Varietal resistance to the brown planthopper in the Solomon Islands. In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Banõs, Philippines, 1979; pp. 233–239. [Google Scholar]
- Ho, D.T. Effect of sequential release of resistant rices on brown planthopper (BPH) biotype development in the Solomon Islands. IRRN 1985, 10, 16–17. [Google Scholar]
- Wu, G.R.; Chen, F.Y.; Tao, L.Y.; Huang, C.W.; Fen, B.C. Studies on the biotypes of the brown planthopper, Nilaparvata lugens (Stål). Acta Entomol. Sin. 1983, 26, 154–160. [Google Scholar]
- Wu, J.-T.; Qiu, X. Screening rice for brown planthopper (BPH) resistance. IRRN 1984, 9, 6. [Google Scholar]
- Lei, H.; Liu, G.; Wu, M.; Jiang, J. Biotype populations of Nilaparvata lugens in Hunan, China. IRRN 1987, 12, 22–23. [Google Scholar]
- Lei, H.; Liu, G.; Wu, M.; Tian, J. Varietal screening for brown planthopper resistance in China. IRRN 1984, 9, 1–12. [Google Scholar]
- Yu, X.; Lu, Z.; Wu, G.; Tao, L.; Chen, J.; Zheng, X.; Xu, H. The biotypes, wing-forms and the immigration of brown planthopper, Nilaparvata lugens Stål, in Zhejiang Province, China. J. Asia-Pac. Entomol. 2001, 4, 201–207. [Google Scholar] [CrossRef]
- Zhang, Y.; Tan, Y.; Huang, B. Monitoring variation in brown planthopper biotype in Guangdong, China. IRRN 1995, 20, 19–20. [Google Scholar]
- Yu, X.; Wu, G.; Tao, L. Virulence of brown planthopper (BPH) populations collected in China. IRRN 1991, 16, 26. [Google Scholar]
- Takahashi, A.; Ito, K.; Tang, J.; Hu, G.W.; Wada, T. Biotypical property in the populations of the brown planthopper, Nilaparvata lugens Stål (Homoptera, Delphacidae), collected in China and Japan. Appl. Entomol. Zool. 1994, 29, 461–463. [Google Scholar] [CrossRef]
- Li, B.; He, J.; Wan, P.; Lai, F.; Wang, W.; Sun, Y.; Jiang, F.Q.; Chen, B.; Fu, Q. Studies on the virulence of different geographic populations of Nilaparvata lugens (Stål) collected from China. J. Environ. Entomol. 2019, 41, 9–16. [Google Scholar]
- Chen, L.C.; Chang, W.L. Inheritance of resistance to brown planthopper in rice variety, Mudgo. J. Taiwan Agr. Res. 1971, 20, 57–60. [Google Scholar]
- Chang, W.L. Tainung 68, the first BPH-resistant japonica cultivar developed in Taiwan. IRRN 1982, 7, 8. [Google Scholar]
- Sogawa, K. Rice brown planthopper (BPH) immigrants in Japan change biotype. IRRN 1992, 17, 26–27. [Google Scholar]
- Lippold, P.C.; Lee, J.O.; Kim, Y.H.; Park, J.; Chung, K.H.; Davis, M.D.; Steenberg, K. Feeding of brown planthopper on rice varieties labled with 32P. IRRN 1978, 3, 8–9. [Google Scholar]
- Lee, J.O.; Goh, H.G. Yield losses of a susceptible rice variety to brown planthopper (BPH) in Korea. IRRN 1984, 9, 9. [Google Scholar]
- Lee, J.O.; Goh, H.G.; Kim, C.C.; Park, J.S. Brown planthopper biotypes in Korea. IRRN 1983, 8, 15. [Google Scholar]
- Lee, J.O.; Goh, H.G.; Kim, Y.H.; Kim, C.G. Brown planthopper-resistant japonica varieties developed in Korea. IRRN 1983, 8, 5. [Google Scholar]
- Veronica, B.K.; Kalode, M.B. Virulence in brown planthopper populations from different sources in Andhra-Prasesh. Indian J. Agric. Sci. 1983, 53, 1084–1086. [Google Scholar]
- Lee, J.O.; Goh, H.G.; Kim, Y.H.; Kim, C.G.; Park, J.S. Reactions of some Koran rice varieties to brown planthopper biotype 2. IRRN 1982, 7, 10–11. [Google Scholar]
- Namoto, H.; Yoloo, M.; Kaneda, C. Breeding japonica lines with brown planthopper (BPH) resistance. IRRN 1986, 11, 9. [Google Scholar]
- Nguyen, C.D.; Zheng, S.-H.; Sanada-Morimura, S.; Matsumura, M.; Yasui, H.; Fujita, D. Substitution mapping and characterization of brown planthopper resistance genes from indica rice variety, ‘PTB33’ (Oryza sativa L.). Breed. Sci. 2021, 71, 497–509. [Google Scholar] [CrossRef] [PubMed]
- Azzam, O.; Chancellor, T.C.B. The biology, epidemiology, and management of rice tungro disease in Asia. Plant Dis. 2002, 86, 88–100. [Google Scholar] [CrossRef]
- Pannak, S.; Wanchana, S.; Aesomnuk, W.; Pitaloka, M.K.; Jamboonsri, W.; Siangliw, M.; Meyers, B.C.; Toojinda, T.; Arikit, S. Functional Bph14 from Rathu Heenati promotes resistance to BPH at the early seedling stage of rice (Oryza sativa L.) as revealed by QTL-seq. Theor. Appl. Genet. 2023, 136, 25. [Google Scholar] [CrossRef] [PubMed]
- Sun, L.; Su, C.; Wang, C.; Zhai, H.; Wan, J. Mapping of a major resistance gene to the brown planthopper in the rice cultivar Rathu Heenati. Breed. Sci. 2005, 55, 391–396. [Google Scholar] [CrossRef]
- Jairin, J.; Phengrat, K.; Teangdeerith, S.; Vanavichit, A.; Toojinda, T. Mapping of a broad-spectrum brown planthopper resistance gene, Bph3, on rice chromosome 6. Mol. Breed. 2007, 19, 35–44. [Google Scholar] [CrossRef]
- Ren, J.; Gao, F.; Wu, X.; Lu, X.; Zeng, L.; Lv, J.; Su, X.; Luo, H.; Ren, G. Bph32, a novel gene encoding an unknown SCR domain-containing protein, confers resistance against the brown planthopper in rice. Sci. Rep. 2016, 6, 37645. [Google Scholar] [CrossRef]
- Pathak, P.K.; Verma, S.K.; Lal, M.N. Varietal resistance to brown planthopper, and problems of its biotypes. Indian J. Genet. Plant Breed. 1979, A39, 141–142. [Google Scholar]
- Gould, F. Evolutionary biology and genetically engineered crops. BioScience 1988, 38, 26–33. [Google Scholar] [CrossRef]
- Sogawa, K. Shifts in population characteristics of brown planthopper (BPH) immigrants to Japan. IRRN 1993, 18, 35–36. [Google Scholar]
- Tanaka, K. Recent status in virulence to resistant rice varieties of brown planthopper Nilaparvata lugens immigrating into Japan. Annu. Rep. Kanto-Tosan Plant Prot. Soc. 1999, 46, 85–88. [Google Scholar]
- Tanaka, K. A simple method for evaluating the virulence of the brown planthopper. IRRN 2000, 25, 18–19. [Google Scholar]
- Tabata, S.; Yamagata, Y.; Fujita, D.; Sanada-Morimura, S.; Matsumura, M.; Yasui, H. Genetic Dissection of the Breakdown of Durable Resistance in indica Rice Variety PTB33 to Brown Planthoppers Nilaparvata Lugens (Stål). Research Square (Preprint). Available online: https://www.researchsquare.com/article/rs-1131675/v1 (accessed on 1 August 2024).
- Pathak, P.K.; Heinrichs, E.A. Selection of biotype populations 2 and 3 of Nilaparvata lugens by exposure to resistant rice varieties. Environ. Entomol. 1982, 11, 85–90. [Google Scholar] [CrossRef]
- Nemoto, H.; Yokoo, M. Experimental selection of a brown planthopper population on mixtures of resistant rice lines. Breed. Sci. 1994, 44, 133–136. [Google Scholar] [CrossRef]
- Ketipearachchi, Y.; Nakamura, C.; Kaneda, C. Biotype shifting of brown planthopper (BPH) on rice cultivars. Kinki J. Crop Sci. Breed. 1997, 42, 7–9. [Google Scholar]
- Hwang, I.; Kim, J.; Song, Y. Changes in the fitness of brown planthopper, Nilaparvata lugens Stål (Homoptera: Delphacidae) to several resistant rice varieties after multi-generational selection. Korean J. Appl. Entomol. 2002, 41, 113–121. [Google Scholar]
- Lu, Z.-X.; Yu, X.-P.; Chen, J.-M.; Zheng, X.-S.; Xu, H.-X.; Zhang, J.-F.; Chen, L.-Z. Dynamics of yeast-like symbiote and its relationship with the virulence of brown planthopper, Nilaparvata lugens Stål, to resistant rice varieties. J. Asia-Pac. Entomol. 2004, 7, 317–323. [Google Scholar] [CrossRef]
- Li, J.; Shang, K.; Liu, J.; Jiang, T.; Hu, D.; Hua, H. Multi-generational effects of rice harboring Bph15 on brown planthopper, Nilaparvata lugens. Pest Manag. Sci. 2014, 70, 310–317. [Google Scholar] [CrossRef]
- Chen, Y.H.; Bernal, C.C.; Tan, J.; Horgan, F.G.; Fitzgerald, M.A. Planthopper “adaptation” to resistant rice varieties: Changes in amino acid composition over time. J. Insect Physiol. 2011, 57, 1375–1384. [Google Scholar] [CrossRef]
- Shen, J.-h.; Wang, Y.; Sogawa, K.; Hattori, M.; Liu, G.-j. Monitoring the changes in virulence of different populations of the whitebacked planthopper, Sogatella furcifera rearing on resistant rice varieties. Chin. J. Rice Sci. 2003, 17, 84. [Google Scholar]
- Horgan, F.G.; Srinivasan, T.S.; Crisol-Martinez, E.; Almazan, M.L.P.; Ramal, A.F.; Oliva, R.; Quibod, I.L.; Bernal, C.C. Microbiome responses during virulence adaptation by a phloem-feeding insect to resistant near-isogenic rice lines. Ecol. Evol. 2019, 9, 11911–11929. [Google Scholar] [CrossRef]
- Hirae, M.; Fukuta, Y.; Tamura, K.; Oya, S. Artificial selection of biotypes of green rice leafhopper, Nephotettix cincticeps Uhler (Homoptera: Cidadellidae), and virulence to resistant rice varieties. Appl. Entomol. Zool. 2007, 42, 97–107. [Google Scholar] [CrossRef]
- Hirae, M.; Tamura, K.; Fukuta, Y. Development and reproduction of biotypes of green rice leafhopper, Nephotettix cincticeps (Uhler) (Homoptera: Cicadellidae) virulent to resistant rice varieties. Jpn. J. Appl. Entomol. Zool. 2008, 52, 207–213. [Google Scholar] [CrossRef]
- Heinrichs, E.A.; Rapusas, H.R. Cross-virulence of Nephotettix virescens (Homoptera: Cicadellidae) biotypes among some rice cultivars with the same major-resistance gene. Environ. Entomol. 1985, 14, 696–700. [Google Scholar] [CrossRef]
- Horgan, F.G.; Ferrater, J.B. Benefits and potential trade-offs associated with yeast-like symbionts during virulence adaptation in a phloem-feeding planthopper. Entomol. Exp. Appl. 2017, 163, 112–125. [Google Scholar] [CrossRef]
- Guirong, W.; Fengxiang, L.; Qiang, F.; Zhitao, Z.; Lanfang, G. Virulent shift in populations of Nilaparvata lugens (Homptera: Delphacidae). Chin. J. Rice Sci. 1999, 13, 229. [Google Scholar]
- Khan, Z.R.; Saxena, R.C. Probing behavior of three biotypes of Nilaparvata lugens (Homoptera: Delphacidae) on different resistant and susceptible rice varieties. J. Econ. Entomol. 1988, 81, 1338–1345. [Google Scholar] [CrossRef]
- Rapusas, H.R.; Chen, J.M.; Heinrichs, E.A. Behavior of two green leafhopper (GLH) colonies on three rice varieties. IRRN 1985, 10, 8. [Google Scholar]
- Khan, Z.R.; Saxena, R.C. Purification of biotype-1 population of brown planthopper Nilaparvata lugens (Homoptera, Delphacidae). Insect Sci. Appl. 1990, 11, 55–62. [Google Scholar] [CrossRef]
- Lin, T.F. Varietal improvement on resistance to biotypes of brown planthopper (Nilaparvata lugens Stål) in indica rice. J. Agric. Assoc. China 1982, 121, 38–47. [Google Scholar]
- Lin, T.F. The breeding for resistance to biotypes for brown planthopper (Nilaparvata lugens Stål). J. Agric. Assoc. China 1983, 122, 36–45. [Google Scholar]
- Saxena, R.C.; Barrion, A.A. Biotypes of the brown planthopper, Nilaparvara lugens (Stål). Korean J. Appl. Entomol. 1983, 22, 52–66. [Google Scholar]
- Tanaka, K. Quantitative genetic analysis of biotypes of the brown planthopper Nilaparvata lugens: Heritability of virulence to resistant rice varieties. Entomol. Exp. Appl. 1999, 90, 279–287. [Google Scholar] [CrossRef]
- Sezer, M.; Butlin, R.K. The genetic basis of host plant adaptation in the brown planthopper (Nilaparvata lugens). Heredity 1998, 80, 499–508. [Google Scholar] [CrossRef]
- Latif, M.A.; Omar, M.Y.; Rafii, M.Y.; Malek, M.A.; Tan, S.G. Evidence of sibling species between two host-associated populations of brown planthopper, N. lugens (Stål)(Homoptera: Delphacidea) complex based on morphology and host–plant relationship studies. Comptes Rendus. Biol. 2013, 336, 354–363. [Google Scholar] [CrossRef]
- Claridge, M.F.; Den Hollander, J.; Morgan, J.C. The status of weed-associated populations of the brown planthopper, Nilaparvata lugens (Stål)—Host race or biological species? Zool. J. Linn. Soc. 2008, 84, 77–90. [Google Scholar] [CrossRef]
- Latif, M.A.; Soon Guan, T.; Yusoh, O.M.; Siraj, S.S. Evidence of sibling species in the brown planthopper complex (Nilaparvata lugens) detected from short and long primer random amplified polymorphic DNA fingerprints. Biochem. Genet. 2008, 46, 520–537. [Google Scholar] [CrossRef]
- Saxena, R.C.; Demayo, C.G.; Barrion, A.A. Allozyme variation among biotypes of the brown plathopper Nilaparvata lugens in the Philippines. Biochem. Genet. 1991, 29, 115–123. [Google Scholar] [CrossRef]
- Mochida, O.; Okada, T. Taxonomy and biology of Nilaparvata lugens (Hom., Delphacidae). In Brown Planthopper: Threat to Rice Production in Asia; International Rice Research Institute, Ed.; International Rice Research Institute: Los Baños, Philippines, 1979; pp. 21–44. [Google Scholar]
- Khan, Z.R.; Saxena, R.C.; Rueda, B.P. Responses of rice-infesting and grass-infesting populations of Nilaparvata lugens (Homoptera: Delphacidae) to rice plants and Leersia grass and to their steam distillate extracts. J. Econ. Entomol. 1988, 81, 1080–1088. [Google Scholar] [CrossRef]
- Renganayaki, K.; Fritz, A.K.; Sadasivam, S.; Pammi, S.; Harrington, S.E.; McCouch, S.R.; Kumar, S.M.; Reddy, A.S. Mapping and progress toward map-based cloning of brown planthopper biotype-4 resistance gene introgressed from Oryza officinalis into cultivated rice, O. sativa. Crop Sci. 2002, 42, 2112–2117. [Google Scholar] [CrossRef]
- Huang, F.; Wei, S.; Luo, S.; Huang, S.; Li, Q. Studies on the virulence characteristics of different rice brown planthopper biotypes. Guangxi Nongye Shengwu Kexue 2003, 22, 84–88. [Google Scholar]
- Prahalada, G.D.; Shivakumar, N.; Lohithaswa, H.C.; Gowda, D.K.S.; Ramkumar, G.; Kim, S.R.; Ramachandra, C.; Hittalmani, S.; Mohapatra, T.; Jena, K.K. Identification and fine mapping of a new gene, BPH31 conferring resistance to brown planthopper biotype 4 of India to improve rice, Oryza sativa L. Rice 2017, 10, 41. [Google Scholar] [CrossRef]
- Saxena, R.C.; Barrion, A.A. Classification of the three Korean biotypes of the brown planthopper, Nilaparvata lugens (Stål), by morphological variation. Korean J. Appl. Entomol. 1993, 32, 317–322. [Google Scholar]
- Saxena, R.C.; Barrion, A.A. Variations in leg characters among three biotypes of the brown planthopper, Nilaparvata lugens (Stål), in Korea. Korean J. Appl. Entomol. 1993, 32, 68–75. [Google Scholar]
- Saxena, R.C.; Rueda, L.M. Morphological variations among 3 biotypes of the brown planthopper Nilaparvata lugens in the Philippines. Insect Sci. Appl. 1982, 3, 193–210. [Google Scholar] [CrossRef]
- Sogawa, K. Hybridization experiments on 3 biotypes of the brown planthopper, Nilaparvata lugens (Homoptera, Delphaciae) at the IRRI, the Philippines. Appl. Entomol. Zool. 1981, 16, 193–199. [Google Scholar] [CrossRef]
- Sogawa, K. Electrophoretic variations in esterase among biotypes of the brown planthopper. IRRN 1978, 3, 8–9. [Google Scholar]
- Sogawa, K. Variations in gustatory response to amino acid-sucrose solutions among biotypes of the brown planthopper. IRRN 1978, 3, 9. [Google Scholar]
- Sogawa, K. Quantitative morphological variations among biotypes of the brown planthopper. IRRN 1978, 3, 9–10. [Google Scholar]
- Daniel, D.J.E.; Rajendram, G.F. Chromatographic analysis of free amino-acids in eggs of Nilaparvata lugens in Sri Lanka and biotype-1, biotype-2 and biotype-3 of the Philippines. Entomol. Exp. Appl. 1983, 33, 226–228. [Google Scholar] [CrossRef]
- Guru-Pirasanna-Pandi, G.; Babu, S.B.; Choudhary, J.S.; Asad, M.; Chidambaranathan, P.; Basana-Gowda, G.; Rath, P.C.; Naaz, N.; Jaremko, M.; Qureshi, K.A.; et al. Genome organization and comparative evolutionary mitochondriomics of brown planthopper, Nilaparvata lugens biotype 4 using next generation sequencing (NGS). Life 2022, 12, 1289. [Google Scholar] [CrossRef]
- Shufran, K.; Whalon, M. Genetic analysis of brown planthopper biotypes using random amplified polymorphic DNA-polymerase chain reaction (RAPD-PCR). Int. J. Trop. Insect Sci. 1995, 16, 27–33. [Google Scholar] [CrossRef]
- Jing, S.; Liu, B.; Peng, L.; Peng, X.; Zhu, L.; Fu, Q.; He, G. Development and use of EST-SSR markers for assessing genetic diversity in the brown planthopper (Nilaparvata lugens Stål). Bull. Entomol. Res. 2012, 102, 113–122. [Google Scholar] [CrossRef]
- Chaerani, C.; Dadang, A.; Fatimah, F.; Husin, B.A.; Sutrisno, S.; Yunus, M. SRAP analysis of brown planthopper (Nilaparvata lugens) populations maintained on differential rice host varieties. Biodiversitas J. Biol. Divers. 2021, 22, 18. [Google Scholar] [CrossRef]
- Guan, W.; Shan, J.H.; Gao, M.Y.; Guo, J.P.; Wu, D.; Zhang, Q.; Wang, J.; Chen, R.Z.; Du, B.; Zhu, L.L.; et al. Bulked segregant RNA sequencing revealed difference between virulent and avirulent brown planthoppers. Front. Plant Sci. 2022, 13, 843227. [Google Scholar] [CrossRef] [PubMed]
- Dadang, A.; Yunus, M. Virulence and SSR diversity of brown planthopper (Nilaparvata lugens) adapted on differential rice host varieties. HAYATI J. Biosci. 2021, 28, 293–303. [Google Scholar]
- Kobayashi, T. Evolving ideas about genetics underlying insect virulence to plant resistance in rice-brown planthopper interactions. J. Insect Physiol. 2016, 84, 32–39. [Google Scholar] [CrossRef]
- Sun, Z.X.; Zhai, Y.F.; Zhang, J.Q.; Kang, K.; Cai, J.H.; Fu, Y.; Qiu, J.Q.; Shen, J.W.; Zhang, W.Q. The genetic basis of population fecundity prediction across multiple field populations of Nilaparvata lugens. Mol. Ecol. 2015, 24, 771–784. [Google Scholar] [CrossRef]
- Jairin, J.; Kobayashi, T.; Yamagata, Y.; Sanada-Morimura, S.; Mori, K.; Tashiro, K.; Kuhara, S.; Kuwazaki, S.; Urio, M.; Suetsugu, Y.; et al. A simple sequence repeat- and single-nucleotide polymorphism-based genetic linkage map of the brown planthopper, Nilaparvata lugens. DNA Res. 2013, 20, 17–30. [Google Scholar] [CrossRef]
- Babu, S.B.; Guru-Pirasanna-Pandi, G.; Parameswaran, C.; Padhi, J.; Basana-Gowda, G.; Annamalai, M.; Patil, N.; Meher, C.; Sabarinathan, S.; Rath, P.C. Genetic analysis of brown planthopper, Nilaparvata lugens (Stål)(Hemiptera: Delphacidae) based on microsatellite markers. Curr. Sci. 2023, 125, 777. [Google Scholar]
- Hereward, J.P.; Cai, X.; Matias, A.M.A.; Walter, G.H.; Xu, C.; Wang, Y. Migration dynamics of an important rice pest: The brown planthopper (Nilaparvata lugens) across Asia—Insights from population genomics. Evol. Appl. 2020, 13, 2449–2459. [Google Scholar] [CrossRef] [PubMed]
- Guru-Pirasanna-Pandi, G.; Choudhary, J.S.; Anant, A.K.; Parameswaran, C.; Basana-Gowda, G.; Adak, T.; Paneerselvam, P.; Annamalai, M.; Patil, N.; Rath, P.C. Population genetic structure and migration pattern of Nilaparvata lugens (Stål.) (Hemiptera: Delphacidae) populations in India based on mitochondrial COI gene sequences. Curr. Sci. 2022, 123, 461–470. [Google Scholar] [CrossRef]
- Guru-Pirasanna-Pandi, G.; Anant, A.K.; Choudhary, J.S.; Babu, S.B.; Basana-Gowda, G.; Annamalai, M.; Patil, N.; Adak, T.; Panneerselvam, P.; Rath, P.C. Molecular diversity of Nilaparvata lugens (Stål.) (Hemiptera: Delphacidae) from India based on internal transcribed spacer 1 gene. Curr. Sci. 2022, 122, 1392–1400. [Google Scholar] [CrossRef]
- Claridge, M.F.; Den Hollander, J. The biotype concept and its application to insect pests of agriculture. Crop Prot. 1983, 2, 85–95. [Google Scholar] [CrossRef]
- Downie, D.A. Baubles, bangles, and biotypes: A critical review of the use and abuse of the biotype concept. J. Insect Sci. 2010, 10, 176. [Google Scholar] [CrossRef]
- Saxena, R.C.; Barrion, A.A. Biotypes of insect pests of agricultural crops. Int. J. Trop. Insect Sci. 2011, 8, 453–458. [Google Scholar] [CrossRef]
- Taggar, G.K.; Arora, R. Insect biotypes and host plant resistance. In Breeding Insect Resistant Crops for Sustainable Agriculture; Arora, R., Sandhu, S., Eds.; Springer: Singapore, 2017; pp. 387–421. [Google Scholar]
- Uawisetwathana, U.; Chevallier, O.P.; Xu, Y.; Kamolsukyeunyong, W.; Nookaew, I.; Somboon, T.; Toojinda, T.; Vanavichit, A.; Goodacre, R.; Elliott, C.T.; et al. Global metabolite profiles of rice brown planthopper-resistant traits reveal potential secondary metabolites for both constitutive and inducible defenses. Metabolomics 2019, 15, 151. [Google Scholar] [CrossRef] [PubMed]
- Bing, L.; Hongxia, D.; Maoxin, Z.; Di, X.; Jingshu, W. Potential resistance of tricin in rice against brown planthopper Nilaparvata lugens (Stål). Acta Ecol. Sin. 2007, 27, 1300–1306. [Google Scholar] [CrossRef]
- Yoshihara, T.; Sogawa, K.; Pathak, M.D.; Juliano, B.O.; Sakamura, S. Soluble silicic acid as a sucking inhibitory substance in rice against the brown planthopper (Delphacidae, Homoptera). Entomol. Exp. Appl. 1979, 26, 314–322. [Google Scholar] [CrossRef]
- Yoshihara, T.; Sogawa, K.; Pathak, M.D.; Juliano, B.O.; Sakamura, S. Oxalic acid as a sucking inhibitor ot the brown planthopper in rice (Delphacidae, Homoptera). Entomol. Exp. Appl. 1980, 27, 149–155. [Google Scholar] [CrossRef]
- Stevenson, P.C.; Kimmins, F.M.; Grayer, R.J.; Raveendranath, S. Schaftosides from rice phloem as feeding inhibitors and resistance factors to brown planthoppers, Nilaparvata lugens. Entomol. Exp. Appl. 1996, 80, 246–249. [Google Scholar] [CrossRef]
- Kang, K.; Yue, L.; Xia, X.; Liu, K.; Zhang, W. Comparative metabolomics analysis of different resistant rice varieties in response to the brown planthopper Nilaparvata lugens Hemiptera: Delphacidae. Metabolomics 2019, 15, 62. [Google Scholar] [CrossRef]
- Alam, S.N.; Cohen, M.B. Detection and analysis of QTLs for resistance to the brown planthopper, Nilaparvata lugens, in a doubled-haploid rice population. Theor. Appl. Genet. 1998, 97, 1370–1379. [Google Scholar] [CrossRef]
- Cohen, M.B.; Alam, S.N.; Medina, E.B.; Bernal, C.C. Brown planthopper, Nilaparvata lugens, resistance in rice cultivar IR64: Mechanism and role in successful N. lugens management in Central Luzon, Philippines. Entomol. Exp. Appl. 1997, 85, 221–229. [Google Scholar] [CrossRef]
- Ferrater, J.B.; de Jong, P.W.; Dicke, M.; Chen, Y.H.; Horgan, F.G. Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties. Arthropod-Plant Interact. 2013, 7, 591–605. [Google Scholar] [CrossRef]
- Gupta, A.; Nair, S. Heritable epigenomic modifications influence stress resilience and rapid adaptations in the brown planthopper (Nilaparvata lugens). Int. J. Mol. Sci. 2022, 23, 8728. [Google Scholar] [CrossRef] [PubMed]
- Zheng, X.H.; Zhu, L.L.; He, G.C. Genetic and molecular understanding of host rice resistance and Nilaparvata lugens adaptation. Curr. Opin. Insect Sci. 2021, 45, 14–20. [Google Scholar] [CrossRef] [PubMed]
- Jing, S.L.; Zhao, Y.; Du, B.; Chen, R.Z.; Zhu, L.L.; He, G.C. Genomics of interaction between the brown planthopper and rice. Curr. Opin. Insect Sci. 2017, 19, 82–87. [Google Scholar] [CrossRef] [PubMed]
- Peng, L.; Zhao, Y.; Wang, H.Y.; Song, C.P.; Shangguan, X.X.; Ma, Y.H.; Zhu, L.L.; He, G.C. Functional study of cytochrome P450 enzymes from the brown planthopper (Nilaparvata lugens Stål) to analyze its adaptation to BPH-resistant rice. Front. Physiol. 2017, 8, 972. [Google Scholar] [CrossRef]
- Peng, L.; Zhao, Y.; Wang, H.; Zhang, J.; Song, C.; Shangguan, X.; Zhu, L.; He, G. Comparative metabolomics of the interaction between rice and the brown planthopper. Metabolomics 2016, 12, 1–15. [Google Scholar] [CrossRef]
- Chen, L.; Chen, J.M.; He, Y.P.; Zhang, J.F. Comparison of feeding behaviors of imidacloprid-resistant and-susceptible brown planthopper (BPH, Nilaparvata lugens Stål) on different rice varieties. Acta Agric. Zhejiangensis 2011, 23, 924–931. [Google Scholar]
- Oya, S.; Sato, A. Differences in feeding habits of the green rice leafhopper, Nephotettix cincticeps Uhler (Hemiptera: Deltocephalidae), on resistant and susceptible rice varieties. Appl. Entomol. Zool. 1981, 16, 451–457. [Google Scholar] [CrossRef]
- Zhu, J.; Zhu, K.; Li, L.; Li, Z.; Qin, W.; Park, Y.; He, Y. Proteomics of the honeydew from the brown planthopper and green rice leafhopper reveal they are rich in proteins from insects, rice plant and bacteria. Insects 2020, 11, 582. [Google Scholar] [CrossRef]
- Auclair, J.L.; Baldos, E.; Heinrichs, E.A. Biochemical evidence for the feeding sites of the leafhopper Nephotettix virescens within susceptible and resistant rice plants. Int. J. Trop. Insect Sci. 1982, 3, 29–34. [Google Scholar] [CrossRef]
- Padgham, D.E.; Woodhead, S. Variety-related feeding patterns in the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), on its host, the rice plant. Bull. Entomol. Res. 2009, 78, 339–349. [Google Scholar] [CrossRef]
- Paguia, P.; Pathak, M.D.; Heinrichs, E.A. Honeydew excretion measurement techniques for determining differential feeding-activity of biotypes of Nilaparvata lugens on rice varieties. J. Econ. Entomol. 1980, 73, 35–40. [Google Scholar] [CrossRef]
- Pompon, J.; Quiring, D.; Giordanengo, P.; Pelletier, Y. Role of xylem consumption on osmoregulation in Macrosiphum euphorbiae (Thomas). J. Insect Physiol. 2010, 56, 610–615. [Google Scholar] [CrossRef]
- Pompon, J.; Quiring, D.; Goyer, C.; Giordanengo, P.; Pelletier, Y. A phloem-sap feeder mixes phloem and xylem sap to regulate osmotic potential. J. Insect Physiol. 2011, 57, 1317–1322. [Google Scholar] [CrossRef]
- Horgan, F.G.; Naik, B.S.; Iswanto, E.H.; Almazan, M.L.P.; Ramal, A.F.; Bernal, C.C. Responses by the brown planthopper, Nilaparvata lugens, to conspecific density on resistant and susceptible rice varieties. Entomol. Exp. Appl. 2016, 158, 284–294. [Google Scholar] [CrossRef]
- Jairin, J.; Leelagud, P.; Saejueng, T.; Chamarerk, V. Loss of resistance to Nilaparvata lugens may be due to the low-level expression of BPH32 in rice panicles at the heading stage. Am. J. Plant Sci. 2017, 8, 2825–2836. [Google Scholar] [CrossRef]
- Ferrater, J.B.; Horgan, F.G. Does Nilaparvata lugens gain tolerance to rice resistance genes through conspecifics at shared feeding sites? Entomol. Exp. Appl. 2016, 160, 77–82. [Google Scholar] [CrossRef]
- Srinivasan, T.S.; Almazan, M.L.P.; Bernal, C.C.; Ramal, A.F.; Subbarayalu, M.K.; Horgan, F.G. Interactions between nymphs of Nilaparvata lugens and Sogatella furcifera (Hemiptera: Delphacidae) on resistant and susceptible rice varieties. Appl. Entomol. Zool. 2016, 51, 81–90. [Google Scholar] [CrossRef]
- Liu, C.X.; Du, B.; Hao, F.H.; Lei, H.H.; Wan, Q.F.; He, G.C.; Wang, Y.L.; Tang, H.R. Dynamic metabolic responses of brown planthoppers towards susceptible and resistant rice plants. Plant Biotechnol. J. 2017, 15, 1346–1357. [Google Scholar] [CrossRef]
- Nanda, S.; Wan, P.J.; Yuan, S.Y.; Lai, F.X.; Wang, W.X.; Fu, Q. Differential responses of OsMPKs in IR56 rice to two BPH populations of different virulence levels. Int. J. Mol. Sci. 2018, 19, 4030. [Google Scholar] [CrossRef]
- Wan, P.J.; Zhou, R.N.; Nanda, S.; He, J.C.; Yuan, S.Y.; Wang, W.X.; Lai, F.X.; Fu, Q. Phenotypic and transcriptomic responses of two Nilaparvata lugens populations to the Mudgo rice containing Bph1. Sci. Rep. 2019, 9, 14049. [Google Scholar] [CrossRef]
- Zha, W.J.; You, A.Q. Comparative iTRAQ proteomic profiling of proteins associated with the adaptation of brown planthopper to moderately resistant vs. susceptible rice varieties. PLoS ONE 2020, 15, e0238549. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Yan, S.Y.; Li, G.C.; Guo, H.; Tang, R.; Ma, R.Y.; Cai, Q.N. The brown planthopper NlDHRS11 is involved in the detoxification of rice secondary compounds. Pest Manag. Sci. 2023, 79, 4828–4838. [Google Scholar] [CrossRef] [PubMed]
- Xiao, H.M.; Yuan, Z.T.; Guo, D.H.; Hou, B.F.; Yin, C.L.; Zhang, W.Q.; Li, F. Genome-wide identification of long noncoding RNA genes and their potential association with fecundity and virulence in rice brown planthopper, Nilaparvata lugens. BMC Genom. 2015, 16, 749. [Google Scholar] [CrossRef]
- Zha, W.J.; Li, S.H.; Xu, H.S.; Chen, J.X.; Liu, K.; Li, P.D.; Liu, K.; Yang, G.C.; Chen, Z.J.; Shi, S.J.; et al. Genome-wide identification of long non-coding (lncRNA) in Nilaparvata lugens’s adaptability to resistant rice. PeerJ 2022, 10, e13587. [Google Scholar] [CrossRef] [PubMed]
- Liu, K.; Su, Q.; Kang, K.; Chen, M.; Wang, W.X.; Zhang, W.Q.; Pang, R. Genome-wide analysis of alternative gene splicing associated with virulence in the brown planthopper Nilaparvata lugens (Hemiptera: Delphacidae). J. Econ. Entomol. 2021, 114, 2512–2523. [Google Scholar] [CrossRef] [PubMed]
- Yuan, L.Y.; Hao, Y.H.; Chen, Q.K.; Pang, R.; Zhang, W.Q. Pancreatic triglyceride lipase is involved in the virulence of the brown planthopper to rice plants. J. Integr. Agric. 2020, 19, 2758–2766. [Google Scholar] [CrossRef]
- Hao, P.; Liu, C.; Wang, Y.; Chen, R.; Tang, M.; Du, B.; Zhu, L.; He, G. Herbivore-induced callose deposition on the sieve plates of rice: An important mechanism for host resistance. Plant Physiol. 2008, 146, 1810–1820. [Google Scholar] [CrossRef]
- Yang, Z.; Zhang, F.; Zhu, L.; He, G. Identification of differentially expressed genes in brown planthopper Nilaparvata lugens (Hemiptera: Delphacidae) responding to host plant resistance. Bull. Entomol. Res. 2007, 96, 53–59. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.F.; Yang, H.Y.; He, G.C. Cloning and characterization of two cytochrome P450 CYP6AX1 and CYP6AY1 cDNAs from Nilaparvata lugens Stål (Homoptera: Delphacidae). Arch. Insect Biochem. Physiol. 2007, 64, 88–99. [Google Scholar] [CrossRef]
- Gupta, A.; Nair, S. Methylation patterns of Tf2 retrotransposons linked to rapid adaptive stress response in the brown planthopper (Nilaparvata lugens). Genomics 2021, 113, 4214–4226. [Google Scholar] [CrossRef]
- Gupta, A.; Nair, S. Epigenetic diversity underlying seasonal and annual variations in brown planthopper (BPH) populations as revealed by methylation- sensitive restriction assay. Curr. Genom. 2023, 24, 354–367. [Google Scholar] [CrossRef]
- Pang, R.; Li, S.H.; Chen, W.W.; Yuan, L.Y.; Xiao, H.X.; Xing, K.; Li, Y.F.; Zhang, Z.F.; He, X.L.; Zhang, W.Q. Insecticide resistance reduces the profitability of insect-resistant rice cultivars. J. Adv. Res. 2024, 60, 1–12. [Google Scholar] [CrossRef]
- Shimada, M.; Ishii, Y.; Shibao, H. Rapid adaptation: A new dimension for evolutionary perspectives in ecology. Popul. Ecol. 2010, 52, 5–14. [Google Scholar] [CrossRef]
- Lee, Y.-M.; Lee, H.-R.; Yi, B.-Y.; Choi, S.-Y.; Sim, J.-W.; Ro, C.-J. Inheritance of adult emergence in artficially induced biotypes of brown planthopper (Nilaparvata lugens STAL) on the resistant rice varieties. Korean J. Appl. Entomol. 1981, 20, 15–20. [Google Scholar]
- Jing, S.L.; Zhang, L.; Ma, Y.H.; Liu, B.F.; Zhao, Y.; Yu, H.J.; Zhou, X.; Qin, R.; Zhu, L.L.; He, G.C. Genome-wide mapping of virulence in brown planthopper identifies loci that break down host plant resistance. PLoS ONE 2014, 9, e98911. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, T.; Yamamoto, K.; Suetsugu, Y.; Kuwazaki, S.; Hattori, M.; Jairin, J.; Sanada-Morimura, S.; Matsumura, M. Genetic mapping of the rice resistance-breaking gene of the brown planthopper Nilaparvata lugens. Proc. R. Soc. B-Biol. Sci. 2014, 281, 20140726. [Google Scholar] [CrossRef]
- Liu, F.; Fu, Q.; Lai, F.X.; Zhang, Z.T. A linkage between inheritance of virulence and sex in the brown planthopper, Nilaparvata lugens (Stål). Acta Entomol. Sin. 2005, 48, 892–897. [Google Scholar]
- Pan, H.-B.; Li, M.-Y.; Wu, W.; Wang, Z.-L.; Yu, X.-P. Host-plant induced shifts in microbial community structure in small brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). J. Econ. Entomol. 2021, 114, 937–946. [Google Scholar] [CrossRef]
- Yan, X.T.; Ye, Z.X.; Wang, X.; Zhang, C.X.; Chen, J.P.; Li, J.M.; Huang, H.J. Insight into different host range of three planthoppers by transcriptomic and microbiomic analysis. Insect Mol. Biol. 2021, 30, 287–296. [Google Scholar] [CrossRef]
- Ren, Z.; Zhang, Y.; Cai, T.; Mao, K.; Xu, Y.; Li, C.; He, S.; Li, J.; Wan, H. Dynamics of microbial communities across the life stages of Nilaparvata lugens (Stål). Microb. Ecol. 2022, 83, 1049–1058. [Google Scholar] [CrossRef]
- Tang, M.; Lv, L.; Jing, S.L.; Zhu, L.L.; He, G.C. Bacterial symbionts of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Appl. Environ. Microbiol. 2010, 76, 1740–1745. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Tang, M.; Hao, P.; Yang, Z.; Zhu, L.; He, G. Penetration into rice tissues by brown planthopper and fine structure of the salivary sheaths. Entomol. Exp. Appl. 2008, 129, 295–307. [Google Scholar] [CrossRef]
- Ojha, A.; Zhang, W.Q. A comparative study of microbial community and dynamics of Asaia in the brown planthopper from susceptible and resistant rice varieties. BMC Microbiol. 2019, 19, 139. [Google Scholar] [CrossRef]
- Wari, D.; Kabir, M.A.; Mujiono, K.; Hojo, Y.; Shinya, T.; Tani, A.; Nakatani, H.; Galis, I. Honeydew-associated microbes elicit defense responses against brown planthopper in rice. J. Exp. Bot. 2019, 70, 1683–1696. [Google Scholar] [CrossRef]
- Gong, G.; Yuan, L.Y.; Li, Y.F.; Xiao, H.X.; Li, Y.F.; Zhang, Y.; Wu, W.J.; Zhang, Z.F. Salivary protein 7 of the brown planthopper functions as an effector for mediating tricin metabolism in rice plants. Sci. Rep. 2022, 12, 3205. [Google Scholar] [CrossRef] [PubMed]
- Huang, H.J.; Liu, C.W.; Xu, H.J.; Bao, Y.Y.; Zhang, C.X. Mucin-like protein, a saliva component involved in brown planthopper virulence and host adaptation. J. Insect Physiol. 2017, 98, 223–230. [Google Scholar] [CrossRef] [PubMed]
- Premachandran, K.; Srinivasan, T.S. In silico modelling and interactive profiling of BPH resistance NBS-LRR proteins with salivary specific proteins of rice planthoppers. Gene Rep. 2022, 28, 101648. [Google Scholar] [CrossRef]
- Ji, R.; Yu, H.X.; Fu, Q.; Chen, H.D.; Ye, W.F.; Li, S.H.; Lou, Y.G. Comparative transcriptome analysis of salivary glands of two populations of rice brown planthopper, Nilaparvata lugens, that differ in virulence. PLoS ONE 2013, 8, e79612. [Google Scholar] [CrossRef]
- Wang, W.X.; Zhu, T.H.; Lai, F.X.; Fu, Q. Diversity and infection frequency of symbiotic bacteria in different populations of the rice brown planthopper in China. J. Entomol. Sci. 2015, 50, 47–66. [Google Scholar] [CrossRef]
- Xu, H.X.; Zheng, X.S.; Yang, Y.J.; Tian, J.C.; Fu, Q.; Ye, G.Y.; Lu, Z.X. Changes in endosymbiotic bacteria of brown planthoppers during the process of adaptation to different resistant rice varieties. Environ. Entomol. 2015, 44, 582–587. [Google Scholar] [CrossRef]
- Wang, Z.L.; Pan, H.B.; Wu, W.; Li, M.Y.; Yu, X.P. The gut bacterial flora associated with brown planthopper is affected by host rice varieties. Arch. Microbiol. 2021, 203, 325–333. [Google Scholar] [CrossRef]
- Xu, X.R.; Chen, L.; Zhou, H.T.; Tang, M. The effect of antibiotic treatment on the bacterial community of the brown planthopper and its correlation with rice virulence. Agronomy 2021, 11, 2327. [Google Scholar] [CrossRef]
- Deng, Z.Y.; Lai, C.L.; Zhang, J.; Sun, F.; Li, D.T.; Hao, P.Y.; Shentu, X.; Pang, K.; Yu, X.P. Effects of secondary metabolites of rice on brown planthopper and its symbionts. Int. J. Mol. Sci. 2024, 25, 386. [Google Scholar] [CrossRef]
- Hou, Y.; Ma, Z.; Dong, S.; Chen, Y.H.; Yu, X. Analysis of yeast-like symbiote diversity in the brown planthopper (BPH), Nilaparvata lugens Stål, using a novel nested PCR-DGGE protocol. Curr. Microbiol. 2013, 67, 263–270. [Google Scholar] [CrossRef] [PubMed]
- Hongoh, Y.; Ishikawa, H. Evolutionary studies on uricases of fungal endosymbionts of aphids and planthoppers. J. Mol. Evol. 2000, 51, 265–277. [Google Scholar] [CrossRef] [PubMed]
- Sasaki, T.; Kawamura, M.; Ishikawa, H. Nitrogen recycling in the brown planthopper, Nilaparvata lugens: Involvement of yeast-like endosymbionts in uric acid metabolism. J. Insect Physiol. 1996, 42, 125–129. [Google Scholar] [CrossRef]
- Lai, C.L.; Hou, Y.; Hao, P.Y.; Pang, K.; Yu, X.P. Detection of yeast-like symbionts in brown planthopper reared on different resistant rice varieties combining DGGE and absolute quantitative real-time PCR. Insects 2022, 13, 85. [Google Scholar] [CrossRef]
- Yang, M.; Cheng, L.; Yan, L.; Shu, W.; Wang, X.; Qiu, Y. Mapping and characterization of a quantitative trait locus resistance to the brown planthopper in the rice variety IR64. Hereditas 2019, 156, 22. [Google Scholar] [CrossRef] [PubMed]
- Horgan, F.G.; de Freitas, T.F.S.; Crisol-Martinez, E.; Mundaca, E.A.; Bernal, C.C. Nitrogenous fertilizer reduces resistance but enhances tolerance to the brown planthopper in fast-growing, moderately resistant rice. Insects 2021, 12, 989. [Google Scholar] [CrossRef]
- Horgan, F.G.; Bernal, C.C.; Ramal, A.F.; Almazan, M.L.P.; Mundaca, E.A.; Crisol-Martínez, E. Heterosis for interactions between insect herbivores and 3-line hybrid rice under low and high soil nitrogen conditions. Insects 2024, 15, 416. [Google Scholar] [CrossRef]
- Jairin, J.; Sansen, K.; Wongboon, W.; Kothcharerk, J. Detection of a brown planthopper resistance gene bph4 at the same chromosomal position of Bph3 using two different genetic backgrounds of rice. Breed. Sci. 2010, 60, 71–75. [Google Scholar] [CrossRef]
- Yang, K.; Liu, H.M.; Jiang, W.H.; Hu, Y.X.; Zhou, Z.Y.; An, X.; Miao, S.; Qin, Y.S.; Du, B.; Zhu, L.L.; et al. Large scale rice germplasm screening for identification of novel brown planthopper resistance sources. Mol. Breed. 2023, 43, 70. [Google Scholar] [CrossRef]
- Zhou, C.; Zhang, Q.; Chen, Y.; Huang, J.; Guo, Q.; Li, Y.; Wang, W.S.; Qiu, Y.F.; Guan, W.; Zhang, J.; et al. Balancing selection and wild gene pool contribute to resistance in global rice germplasm against planthopper. J. Integr. Plant Biol. 2021, 63, 1695–1711. [Google Scholar] [CrossRef]
- Jiang, H.; Hu, J.; Li, Z.; Liu, J.; Gao, G.; Zhang, Q.; Xiao, J.; He, Y. Evaluation and breeding application of six brown planthopper resistance genes in rice maintainer line Jin 23B. Rice 2018, 11, 22. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Zeng, G.; Hao, M.; Jiang, H.; Xiao, Y. Improvement of rice blast and brown planthopper resistance of PTGMS line C815S in two-line hybrid rice through marker-assisted selection. Mol. Breed. 2020, 40, 21. [Google Scholar] [CrossRef]
- Li, F.; Yan, L.; Shen, J.; Liao, S.; Ren, X.; Cheng, L.; Li, Y.; Qiu, Y. Fine mapping and breeding application of two brown planthopper resistance genes derived from landrace rice. PLoS ONE 2024, 19, e0297945. [Google Scholar] [CrossRef] [PubMed]
- Thakur, A. Pyramiding of Brown Plant Hopper Resistance Genes Bph34 and Bph33 in Rice. Ph.D. Thesis, Punjab Agricultural University, Ludhiana, India, 2022. [Google Scholar]
- Vignesh, M.; Valarmathi, M.; Rakshana, P.; Bharathi, A.; Dilip, K.R.; Sudha, M.; Manonmani, S.; Raveendran, M. Marker assisted pyramiding of major brown plant hopper resistance genes in an elite culture CBMAS14065. Electron. J. Plant Breed. 2023, 14, 1–8. [Google Scholar]
- Han, Y.; Wu, C.; Yang, L.; Zhang, D.; Xiao, Y. Resistance to Nilaparvata lugens in rice lines introgressed with the resistance genes Bph14 and Bph15 and related resistance types. PLoS ONE 2018, 13, e0198630. [Google Scholar] [CrossRef]
- Sharma, N.P.; Torii, A.; Takumi, S.; Mori, N.; Nakamura, C. Marker-assisted pyramiding of brown planthopper (Nilaparvata lugens Stål) resistance genes Bph1 and Bph2 on rice chromosome 12. Hereditas 2004, 140, 61–69. [Google Scholar] [CrossRef]
- Kamal, M.M.; Nguyen, C.D.; Sanada-Morimura, S.; Zheng, S.H.; Fujita, D. Development of pyramided lines carrying brown planthopper resistance genes in the genetic background of indica group rice (Oryza sativa L.) variety ‘IR64’. Breed. Sci. 2023, 73, 450–456. [Google Scholar] [CrossRef]
- Nguyen, C.D.; Verdeprado, H.; Zita, D.; Sanada-Morimura, S.; Matsumura, M.; Virk, P.S.; Brar, D.S.; Horgan, F.G.; Yasui, H.; Fujita, D. The development and characterization of near-isogenic and pyramided lines carrying resistance genes to brown planthopper with the genetic background of Japonica rice (Oryza sativa L.). Plants 2019, 8, 498. [Google Scholar] [CrossRef]
- Haley, S.D.; Peairs, F.B.; Walker, C.B.; Rudolph, J.B.; Randolph, T.L. Occurrence of a new Russian wheat aphid biotype in Colorado. Crop Sci. 2004, 44, 1589–1592. [Google Scholar] [CrossRef]
- Weiland, A.A.; Peairs, F.B.; Randolph, T.L.; Rudolph, J.B.; Haley, S.D.; Puterka, G.J. Biotypic diversity in Colorado Russian wheat aphid (Hemiptera: Aphididae) populations. J. Econ. Entomol. 2008, 101, 569–574. [Google Scholar] [CrossRef]
- Horgan, F.G.; Peñalver-Cruz, A.; Bernal, C.C.; Ramal, A.F.; Almazan, M.L.P.; Wilby, A. Resistance and tolerance to the brown planthopper, Nilaparvata lugens (Stål), in rice infested at different growth stages across a gradient of nitrogen applications. Field Crops Res. 2018, 217, 53–65. [Google Scholar] [CrossRef]
- You, L.L.; Wu, Y.; Xu, B.; Ding, J.; Ge, L.Q.; Yang, G.Q.; Song, Q.S.; Stanley, D.; Wu, J.C. Driving pest insect populations: Agricultural chemicals lead to an adaptive syndrome in Nilaparvata Lugens Stål (Hemiptera: Delphacidae). Sci. Rep. 2016, 6, 37430. [Google Scholar] [CrossRef]
- Suri, K.; Singh, G. Insecticide-induced resurgence of the whitebacked planthopper Sogatella furcifera (Horváth)(Hemiptera: Delphacidae) on rice varieties with different levels of resistance. Crop Prot. 2011, 30, 118–124. [Google Scholar] [CrossRef]
- Horgan, F.G.; Peñalver-Cruz, A. Compatibility of insecticides with rice resistance to planthoppers as influenced by the timing and frequency of applications. Insects 2022, 13, 106. [Google Scholar] [CrossRef] [PubMed]
- Horgan, F.G.; Peñalver-Cruz, A.; Almazan, M.L.P. Rice resistance buffers against the induced enhancement of brown planthopper fitness by some insecticides. Crops 2021, 1, 166–184. [Google Scholar] [CrossRef]
- Azzam, S.; Wang, F.; Wu, J.-C.; Shen, J.; Wang, L.-P.; Yang, G.-Q.; Guo, Y.-R. Comparisons of stimulatory effects of a series of concentrations of four insecticides on reproduction in the rice brown planthopper Nilaparvata lugens Stål (Homoptera: Delphacidae). Int. J. Pest Manag. 2009, 55, 347–358. [Google Scholar] [CrossRef]
- Yin, J.-L.; Xu, H.-W.; Wu, J.-C.; Hu, J.-H.; Yang, G.-Q. Cultivar and insecticide applications affect the physiological development of the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae). Environ. Entomol. 2008, 37, 206–212. [Google Scholar] [CrossRef]
- Rane, R.V.; Walsh, T.K.; Pearce, S.L.; Jermiin, L.S.; Gordon, K.H.J.; Richards, S.; Oakeshott, J.G. Are feeding preferences and insecticide resistance associated with the size of detoxifying enzyme families in insect herbivores? Curr. Opin. Insect Sci. 2016, 13, 70–76. [Google Scholar] [CrossRef]
- Valmorbida, I.; Muraro, D.S.; Hodgson, E.W.; O’Neal, M.E. Soybean aphid (Hemiptera: Aphididae) response to lambda-cyhalothrin varies with its virulence status to aphid-resistant soybean. Pest Manag. Sci. 2020, 76, 1464–1471. [Google Scholar] [CrossRef]
- Pym, A.; Singh, K.S.; Nordgren, Å.; Davies, T.G.E.; Zimmer, C.T.; Elias, J.; Slater, R.; Bass, C. Host plant adaptation in the polyphagous whitefly, Trialeurodes vaporariorum, is associated with transcriptional plasticity and altered sensitivity to insecticides. BMC Genom. 2019, 20, 996. [Google Scholar] [CrossRef]
- Heinrichs, E.A.; Valencia, S.L. Contact toxicity of insecticides to the three biotypes of brown planthopper. IRRN 1978, 3, 19–20. [Google Scholar]
- Yang, Y.-j.; Dong, B.-q.; Xu, H.-x.; Zheng, X.-s.; Heong, K.; Lu, Z.-x. Susceptibility to insecticides and ecological fitness in resistant rice varieties of field Nilaparvata lugens Stål population free from insecticides in laboratory. Rice Sci. 2014, 21, 181–186. [Google Scholar] [CrossRef]
- Fujii, T.; Matsukura, K.; Van Chien, H.; Cuong, L.Q.; Loc, P.M.; Estoy Jr, G.F.; Matsumura, M.; Sanada-Morimura, S. Insecticide resistance triggers a reduction of virulence to host-plant defenses in the brown planthopper. Entomol. Exp. Appl. 2024, 172, 301–311. [Google Scholar] [CrossRef]
- Kamal, M.M.; Nguyen, C.D.; Sanada-Morimura, S.; Zheng, S.H.; Fujita, D. Near-isogenic lines for resistance to brown planthopper with the genetic background of Indica group elite rice (Oryza sativa L.) variety ‘IR64’. Breed. Sci. 2023, 73, 278–289. [Google Scholar] [CrossRef]
- Van Mai, T.; Fujita, D.; Matsumura, M.; Yoshimura, A.; Yasui, H. Genetic basis of multiple resistance to the brown planthopper (Nilaparvata lugens Stål) and the green rice leafhopper (Nephotettix cincticeps Uhler) in the rice cultivar ‘ASD7’ (Oryza sativa L. ssp. indica). Breed. Sci. 2015, 65, 420–429. [Google Scholar] [CrossRef] [PubMed]
- Liu, G.-j.; Chen, S.-g.; Wang, J.-y.; Shen, J.-h.; Sogawa, K.; Xie, X.-m.; Qiao, Q.-c.; Pu, Z.-g.; Shi, D.-g.; Liu, X.-g. Preliminary study on suppression of the whitebacked planthopper, Sogatella furcifera by cultivating the mixture of the resistant and susceptible rice varieties. Chin. J. Rice Sci. 2003, 17, 103. [Google Scholar]
- Nanthakumar, M.; Lakshmi, V.J.; Bhushan, V.S.; Balachandran, S.; Mohan, M. Decrease of rice plant resistance and induction of hormesis and carboxylesterase titre in brown planthopper, Nilaparvata lugens (Stål) by xenobiotics. Pestic. Biochem. Physiol. 2012, 102, 146–152. [Google Scholar] [CrossRef]
- Li, Z.; Wan, G.; Wang, L.; Parajulee, M.N.; Zhao, Z.; Chen, F. Effects of seed mixture sowing with resistant and susceptible rice on population dynamics of target planthoppers and non-target stemborers and leaffolders. Pest Manag. Sci. 2018, 74, 1664–1676. [Google Scholar] [CrossRef]
- Nemoto, H.; Habibuddin, H. Adaptation of green leafhopper, Nephotettix virescens, populations reared on a mixed cropping of two rice cultivars resistant to rice tungro disease. Jpn. J. Trop. Agric. 1995, 39, 190–194. [Google Scholar] [CrossRef]
- Gong, G.; Zhang, Y.D.; Zhang, Z.F.; Wu, W.J. Alternately rearing with susceptible variety can delay the virulence development of insect pests to resistant varieties. Agriculture 2022, 12, 991. [Google Scholar] [CrossRef]
Herbivores Species 1 | Origin of Herbivore Population | Origin of Rice Accessions 2 | |||
---|---|---|---|---|---|
East Asia | South Asia | Global Cultivated 3 | Wild Species | ||
Nilaparvata lugens (Stål), brown planthopper [BPH] 4 | East Asia | 3.8% (13,917) [11,56,57,58] | - | 0.2% (ca 26,000) [59] | 68.2% (88) [56] |
South Asia | - | 8.7% (17,194) [10,27,60,61,62,63] | 7.7% (3880) [64,65,66] | 64.8% (128) [67] | |
Sogatella furcifera (Horváth), whitebacked planthopper [WBPH] 5 | East Asia | - | 25.4% (71) [68] | 0.8% (46,488) [25] | 37.7% (228) [69] |
South Asia | - | 24.8% (514) [26,61,62] | 29.9% (67) [70] | 56.6% (297) [71,72] | |
Laodelphax striatellus Fallén, small brown planthopper [SBPH] 6 | East Asia | 20.6% (180) [73,74] | |||
Nephotettix virescens (Distant), green leafhopper [GLH] 7 | East Asia | - | - | 2.2% (50,333) [75,76] | 67.2% (826) [69,75,77] |
South Asia | - | 37.5% (24) [61] | - | - | |
Nephotettix cincticeps Uhler, green rice leafhopper (GRL) | East Asia | 34.8% (164) [78,79] | |||
Nephotettix nigropictus (Stål) 7 | East Asia | - | - | - | 95.3% (91) [80] |
South Asia | - | 33.3% (24) [61] | - | - | |
Maiestas dorsalis Motschulsky, zig-zag leafhopper [ZLH] 8 | East Asia | - | - | 2.1% (3870) [25,81] | 55.2% (208) [69] |
Tagosodes orizicolus (Muir) 9 | Colombia | - | - | 59.9% (534) [82] | - |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Horgan, F.G. Virulence Adaptation by Rice Planthoppers and Leafhoppers to Resistance Genes and Loci: A Review. Insects 2024, 15, 652. https://doi.org/10.3390/insects15090652
Horgan FG. Virulence Adaptation by Rice Planthoppers and Leafhoppers to Resistance Genes and Loci: A Review. Insects. 2024; 15(9):652. https://doi.org/10.3390/insects15090652
Chicago/Turabian StyleHorgan, Finbarr G. 2024. "Virulence Adaptation by Rice Planthoppers and Leafhoppers to Resistance Genes and Loci: A Review" Insects 15, no. 9: 652. https://doi.org/10.3390/insects15090652