ความก้าวหน้าการพัฒนาพันธุ์ข้าวต้านทานเพลี้ยกระโดดสีน้ำตาลด้วยอณูพันธุศาสตร์

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ข้าว เพลี้ยกระโดดสีน้ำตาล ยีนต้านทาน ไบโอไทป์ อณูพันธุศาสตร์

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จิรพงศ์ ใจรินทร์
กองวิจัยและพัฒนาข้าว กรมการข้าว กรุงเทพฯ 10900

บทคัดย่อ

เพลี้ยกระโดดสีน้ำตาล Nilaparvata lugens (Stål) เป็นแมลงศัตรูข้าวที่สร้างความเสียหายในพื้นที่ปลูกข้าวนาชลประทานและนาน้ำฝนอย่างมาก แนวทางการควบคุมเพลี้ยกระโดดสีน้ำตาลด้วยการปลูกพันธุ์ข้าวต้านทานเป็นวิธีที่ดีที่สุดวิธีหนึ่ง เป็นกลยุทธ์ที่เป็นมิตรต่อสิ่งแวดล้อมและปลอดภัยต่อเกษตรกร อย่างไรก็ตาม การปรับเปลี่ยนไบโอไทป์ของประชากรเพลี้ยกระโดดสีน้ำตาลทำให้พันธุ์ต้านทานกลับกลายเป็นพันธุ์อ่อนแอได้ ไบโอไทป์จึงเป็นอุปสรรคของการใช้พันธุ์ต้านทาน การเร่งค้นหายีนต้านทานใหม่และพัฒนาแนวทางการสร้างพันธุ์ข้าวต่อสู้กับความหลากหลายของไบโอไทป์และต้านทานได้ยาวนาน เป็นสิ่งที่นักวิจัยพยายามดำเนินการอย่างต่อเนื่อง องค์ความรู้ทางพันธุกรรมความต้านทานและไบโอไทป์จึงมีความสำคัญสำหรับเป็นข้อมูลสนับสนุนการตัดสินใจเลือกและใช้ประโยชน์ยีนต้านทานอย่างมีประสิทธิภาพ ความก้าวหน้าด้านเทคโนโลยีการถอดรหัสพันธุกรรมและการปรับแต่งจีโนม เปิดโอกาสให้การค้นพบและใช้ประโยชน์ยีนต้านทานทำได้ง่ายและรวดเร็วขึ้น อีกทั้งยังสามารถเพิ่มประสิทธิภาพ ลดระยะเวลา และค่าใช้จ่ายในการพัฒนาพันธุ์ข้าว เนื้อหาในบทความได้กล่าวถึงความก้าวหน้าของการใช้ประโยชน์แหล่งพันธุกรรมความต้านทาน การค้นหาตำแหน่งยีนต้านทาน และแนวทางการพัฒนาพันธุ์ข้าวให้ต้านทานได้ยาวนานและครอบคลุมความหลากหลายของเพลี้ยกระโดดสีน้ำตาล

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ฉบับ
ปีที่ 53 ฉบับที่ 2 (2022): พฤษภาคม – สิงหาคม
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บทความวิจารณ์

References

Akama, K., N. Akter, H. Endo, M. Kanesaki, M. Endo and S. Toki. 2020. An in vivo targeted deletion of the calmodulin–binding domain from rice glutamate decarboxylase 3 (OsGAD3) increases γ–aminobutyric acid content in grains. Rice 13: 20.

Akula, S.H., M.A. Dass, S.K. Surapaneni and P. Balaravi. 2020. Mapping of quantitative trait loci associated with resistance to brown planthopper in background of Swarna from a traditional variety PTB33. Euphytica 216: 114.

Ali, M.P., D. Huang, G. Nachman, N. Ahmed, M.A. Begum and M.F. Rabbi. 2014. Will climate change affect outbreak patterns of plant hoppers in Bangladesh? PLoS ONE 9: e91678.

Balachiranjeevi, C.H., G.D. Prahalada, A. Mahender, M. Jamaloddin, M.A.L. Sevilla, C.M. Marfori–Nazarea, R. Vinarao, U. Sushanto, S.E. Baehaki, Z.K. Li and J. Ali. 2019. Identification of a novel locus, BPH38(t), conferring resistance to brown planthopper (Nilaparvata lugens Stal.) using early backcross population in rice (Oryza sativa L.). Euphytica 215: 185.

Bentur, J.S., R.M. Sundaram, S.K. Mangrauthia and S. Nair. 2021. Molecular approaches for insect pest management in rice. pp. 379–424. In: J. Ali and S.H. Wani, eds. Rice Improvement Physiological, Molecular Breeding and Genetic Perspectives. Springer, Switzerland.

Bottrell, D.G. and K.G. Schoenly. 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-Pac. Entomol. 15: 122–140.

Brar, D.S. and G.S. Khush. 2018. Wild relatives of rice: a valuable genetic resource for genomics and breeding research, pp. 1–25. In: T.K. Mondal and R.J. Henry, eds. The Wild Oryza Genomes. Compendium of Plant Genomes. Springer, Switzerland.

Brar, D.S., P.S. Virk, K.K. Jena and G.S. Khush. 2009. Breeding for resistance to planthoppers in rice, pp. 401–427. In: K.L. Heong and B. Hardy, eds. Planthopper: New Threats to the Sustainability of Intensive Rice Production Systems in Asia. International Rice Research Institute, Los Baños, Philippines.

Cheng, A., I. Ismail, M. Osman, H. Hashim and N.S. Mohd Zainual. 2017. Rapid and targeted introgression of fgr gene through marker-assisted backcrossing in rice (Oryza sativa L.). Genome 60(12): 1045–1050.

Claridge, M.F. and J. Den Hollander. 1980. The “biotypes” of the rice brown planthopper, Nilaparvata lugens. Entomol. Exp. Appl. 27(1): 23–30.

Claridge, M.F. and J. Den Hollander. 1983. The biotype concept and its application to insect pests of agriculture. Crop Prot. 2(1): 85–95.

Darvasi, A. and M. Soller. 1994. Selective DNA pooling for determination of linkage between a molecular marker and a quantitative trait locus. Genetics 138(4): 1365–1373.

Douglas, A.E. 1993. The nutritional quality of phloem sap utilized by natural aphid populations. Ecol. Entomol. 18(1): 31–38.

Du, B., R. Chen, J. Guo and G. He. 2020. Current understanding of the genomic, genetic, and molecular control of insect resistance in rice. Mol. Breeding 40: 24.

Du, B., W. Zhang, B. Liu, J. Hu, Z. Wei, Z. Shi, R. He, L. Zhu, R. Chen, B. Han and G. He. 2009. Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc. Natl. Acad. Sci. 106(52): 22163–22168.

Dyck, V.A. and B. Thomas. 1979. The brown planthopper problem, pp. 3–17. In: Brown Planthopper: Threat to Rice Production in Asia. International Rice Research Institute, Los Baños, The Philippines.

Endo, M., M. Mikami, A. Endo, H. Kaya, T. Itoh, H. Nishimasu, O. Nureki and S. Toki. 2019. Genome editing in plants by engineered CRISPR–Cas9 recognizing NG PAM. Nat. Plants 5: 14–17.

Farmer, B.H. 1986. Perspectives on the ‘green revolution’ in South Asia. Mod. Asian Stud. 20(1): 175–199.

Fu, Q., Z. Zhang, C. Hu, F. Lai and Z. Sun. 2001. A chemically defined diet enables continuous rearing of the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Appl. Entomol. Zool. 36(1): 111–116.

Fujita, D., A. Kohli and F.G. Horgan. 2013. Rice resistance to planthoppers and leafhoppers. Crit. Rev. Plant Sci. 32(3): 162–191.

Fujiwara, T., S. Maisonneuve, M. Isshiki, M. Mizutani, L. Chen, H.L. Wong, T. Kawasaki and K. Shimamoto. 2010. Sekiguchi lesion gene encodes a cytochrome P450 monooxygenase that catalyzes conversion of tryptamine to serotonin in rice. J. Biol. Chem. 285(15): 11308–11313.

Guan, W., J. Shan, M. Gao, J. Guo, D. Wu, Q. Zhang, J. Wang, R. Chen, B. Du, L. Zhu and G. He. 2022. Bulked segregant RNA sequencing revealed difference between virulent and avirulent brown planthoppers. Front. Plant Sci. 13: 843227.

Guru Pirasanna Pandi, G., S. Chander, M.P. Singh and H. Pathak. 2018. Impact of elevated CO2 and temperature on brown planthopper population in rice ecosystem. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 88(1): 57–64.

Haliru, B.S., M.Y. Rafii, N. Mazlan, S.I. Ramlee, I. Muhammad, I.S. Akos, J. Halidu, S. Swaray and Y.R. Bashir. 2020. Recent strategies for detection and improvement of brown planthopper resistance genes in rice: a review. Plants 9(9): 1202.

Hayakawa, T., T. Yamaya, T. Mae and K. Ojima. 1993. Changes in the content of two glutamate synthase proteins in spikelets of rice (Oryza sativa) plants during ripening. Plant Physiol. 101(4): 1257–1262.

Hayashi, H., S. Nakamura, Y. Ishiwatari, S. Mori and M. Chino. 1993. Changes in the amino acid composition and protein modification in phloem sap of rice. Plant Soil. 155: 171–174.

Heinrichs, E.A., F.G. Medrano and H.R. Rapusas. 1985. Genetic Evaluation for Insect Resistance in Rice. International Rice Research Institute, Los Baños, The Philippines. 356 pp.

Heong, K.L. and B. Hardy. 2009. Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia. International Rice Research Institute, Los Baños, The Philippines. 460 pp.

Horgan, F.G., A. Arida, G. Ardestani and M.L.P. Almazan. 2021. Elevated temperatures diminish the effects of a highly resistant rice variety on the brown planthopper. Sci. Rep. 11: 262.

Hu, J., C. Xiao and Y. He. 2016. Recent progress on the genetics and molecular breeding of brown planthopper resistance in rice. Rice 9: 30.

Hu, J., X. Chang, L. Zou, W. Tang and W. Wu. 2018. Identification and fine mapping of Bph33, a new brown planthopper resistance gene in rice (Oryza sativa L.). Rice 11: 55.

Hu, J., X. Li, C. Wu, C. Yang, H. Hua, G. Gao, J. Xiao and Y. He. 2012. Pyramiding and evaluation of the brown planthopper resistance genes Bph14 and Bph15 in hybrid rice. Mol. Breeding 29: 61–69.

Huang, Z., G. He, L. Shu, X. Li and Q. Zhang. 2001. Identification and mapping of two brown planthopper resistance genes in rice. Theor. Appl. Genet. 102: 929–934.

Jaganathan, D., A. Bohra, M. Thudi and R.K. Varshney. 2020. Fine mapping and gene cloning in the post-NGS era: advances and prospects. Theor. Appl. Genet. 133: 1791–1810.

Jairin, J. 2008. High-resolution Mapping of a Brown Planthopper (BPH) Resistance Gene, Bph3, and Marker-assisted Selection for BPH Resistance in Rice. PhD Thesis, Kasetsart University, Bangkok.

Jairin, J. 2021. Towards understanding biotypes of the brown planthopper, Nilaparvata lugens (Stål). Thai Rice Res. J. 12(1): 97–118. (in Thai)

Jairin, J., K. Sansen, W. Wongboon and J. Kothcharerk. 2010. Detection of a brown planthopper resistance gene bph4 at the same chromosomal position of Bph3 using two different genetic backgrounds of rice. Breed. Sci. 60: 71–75.

Jairin, J., P. Pattawatang, V. Chamarerk, P. Leelakud and W. Khunnasut. 2014. Development of rice lines resistance to multiple biotypes of brown planthopper (Nilaparvata lugens Stål), pp. 179–197. In Proc. the 31st Rice and Temperate Cereal Crops Annual Conference, 23–24 May 2014. (in Thai)

Jairin, J., P. Vejchasarn, T. Somjai, K. Srivilai, K. Darwell, P. Leelagud, R. Kawichai, J. Kotcharerk, A. Suthanthangjai, N. Popa, S. Lachanthuek and V. Chamarerk. 2019. Identification of QTLs for blast, bacterial blight, and planthopper resistance using SNP-based linkage maps from two recombinant inbred rice lines. Am. J. Plant Sci. 10: 760–779.

Jairin, J., S. Teangdeerith, P. Leelagud, J. Kothcharerk, K. Sansen, M. Yi, A. Vanavichit and T. Toojinda. 2009. Development of rice introgression lines with brown planthopper resistance and KDML105 grain quality characteristics through marker-assisted selection. Field Crop Res. 110: 263–271.

Jairin, J., S. Teangdeerith, P. Leelagud, K. Phengrat, A. Vanavichit and T. Toojinda. 2007. Detection of brown planthopper resistance genes from different rice mapping populations in the same genomic location. ScienceAsia 33: 347–352.

Jairin, J., T. Toojinda, S. Tragoonrungb, S. Tayapatc and A. Vanavichit. 2005. Multiple genes determining brown planthopper (Nilaparvata lugens Stal) resistance in backcross introgressed lines of Thai jasmine rice ‘KDML105’. ScienceAsia 31: 129–135.

Jairin, J., U. Kotchasatit, S. Saleeto, S. Jearakongman, K. Srivilai, V. Chamarerk, J. Kothcharerk, P. Pattawatang, S. Korinsak, C. Wongsaprom and T. Toojinda. 2017. Application of markerassisted breeding to improve biotic stress resistance for rainfed lowland rice in northeast Thailand. SABRAO J. Breed. Genet. 49(2): 168–178.

Jena, K.K. 2010. The species of the genus Oryza and transfer of useful genes from wild species into cultivated rice, O. sativa. Breed. Sci. 60: 518–523.

Jena, K.K. and S.M. Kim. 2010. Current status of brown planthopper (BPH) resistance and genetics. Rice 3: 161–171.

Jena, K.K., J.U. Jeung, J.H. Lee, H.C. Choi and D.S. Brar. 2006. High-resolution mapping of a new brown planthopper (BPH) resistance gene, Bph18(t), and marker-assisted selection for BPH resistance in rice (Oryza sativa L.). Theor. Appl. Genet. 112(2): 288–297.

Jena, K.K., S.L. Hechanova, H. Verdeprado, H. Verdeprado, G.D. Prahalada and S.M. Kim. 2017. Development of 25 near-isogenic lines (NILs) with ten BPH resistance genes in rice (Oryza sativa L.): production, resistance spectrum, and molecular analysis. Theor. Appl. Genet. 130: 2345–2360.

Jeon, Y.H., S.N. Ahn, H.C. Choi, T.R. Hahn and H.P. Moon. 1999. Identification of a RAPD marker linked to a brown planthopper resistance gene in rice. Euphytica 107: 23–28.

Joshi, R.K. and S. Nayak. 2010. Gene pyramiding-a broad spectrum technique for developing durable stress resistance in crops. Biotechnol. Mol. Biol. Rev. 5(3): 51–60.

Kamolsukyeunyong, W., S. Ruengphayak, P. Chumwong, L. Kusumawati, E. Chaichoompu, W. Jamboonsri, C. Saensuk, K. Phoonsiri, T. Toojinda and A. Vanavichit. 2019. Identification of spontaneous mutation for broad-spectrum brown planthopper resistance in a large, long-term fast neutron mutagenized rice population. Rice 12: 16.

Kamolsukyeunyong, W., W. Sukhaket, K. Pitija, P. Thorngkham, S. Mahatheeranont, T. Toojinda and A. Vanavichit. 2021. Rice sesquiterpene plays important roles in antixenosis against brown planthopper in rice. Plants. 10: 1049.

Karley, A.J., A.E. Douglas and W.E. Parker. 2002. Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J. Exp. Biol. 205: 3009–3018.

Ketipearachchi, Y., C. Kaneda and C. Nakamura. 1998. Adaptation of the brown planthopper (BPH), Nilaparvata lugens (Stål) (Homoptera: Delphacidae), to BPH resistant rice cultivars carrying bph8 or Bph9. Appl. Entomol. Zool. 33(4): 497–505.

Khan, M.M., R.M. Kaleem-Ullah, J.A. Siddiqui and S. Ali. 2020. Insecticide resistance and detoxification enzymes activity in Nilaparvata lugens Stål against neonicotinoids. J. Agric. Sci. 12(5): 24–36.

Khush, G.S. 1971. Rice breeding for disease and insect resistance at IRRI. Oryza 8: 111–119.

Khush, G.S. 1979. Genetics of and breeding for resistance to the brown planthopper, pp. 321–332. In Brown Planthopper: Threat to Rice Production in Asia. International Rice Research Institute, Los Baños, The Philippines.

Khush, G.S. and P.S. Virk. 2005. IR Varieties and Their Impact. International Rice Research Institute, Los Baños, The Philippines.

Kim, H., P.S. Miguel, W. Nelson, K. Collura, M. Wissotski, J.G. Walling, J.P. Kim, S.A. Jackson, C. Soderlund and R.A. Wing. 2007. Comparative physical mapping between Oryza sativa (AA genome type) and O. punctata (BB genome type). Genetics 176: 379–390.

Kobayashi, T. 2016. Evolving ideas about genetics underlying insect virulence to plant resistance in rice-brown planthopper interactions. J. Insect Physiol. 84: 32–39.

Kobayashi, T., K. Yamamoto, S. Kuwazaki, Y. Suetsugu, M. Hattori, J. Jairin, S. Sanada-morimura and M. Matsumura. 2014. Genetic mapping of the rice-resistance-breaking gene of the brown planthopper Nilaparvata lugens. Proc. R. Soc. B. 281: 20140726.

Kotcharerk, J., P. Pattawatang, S. Palawisut and J. Jairin. 2015. Development of Pathum Thani 1 rice to resist brown planthopper using marker assisted selection, pp. 17–27. In Proc. the 8th Rice Research Symposium 2015: Rice Research Center Groups in Upper and Lower Northern Region, 25–27 February 2015, Chiang Rai, Thailand. (in Thai)

Kotcharerk, J., W. Prongprasert, T. Toojinda and S. Palawisut 2011. Development of brown planthopper resistance in rice variety Chainat 1 using marker assisted selection, pp. 374–375. In Proc. the 2nd Rice and Temperate Cereal Crops Annual Conference 2011: Rice and National Farmers’ Day, 3–4 June 2011, Bangkok, Thailand. (in Thai)

Kuang, Y.H., Y.F Fang, S.C. Lin, S.F. Tsai, Z.W. Yang, C.P. Li, S.H. Huang, S.L. Hechanova, K.K. Jena and W.P. Chuang. 2021. The impact of climate change on the resistance of rice nearisogenic lines with resistance genes against brown planthopper. Rice 2: 64.

Kumar, K., P. Kaur, A. Kishore, Y. Vikal, K. Singh and K. Neelam. 2020. Recent advances in genomicsassisted breeding of brown planthopper (Nilaparvata lugens) resistance in rice (Oryza sativa). Plant Breed. 139: 1052–1066.

Kumar, K., P.S. Sarao, D. Bhatia, K. Neelam, A. Kaur, G.S. Mangat, D.S. Brar and K. Singh. 2018. High-resolution genetic mapping of a novel brown planthopper resistance locus, Bph34 in Oryza sativa L. X Oryza nivara (Sharma & Shastry) derived interspecific F2 population. Theor. Appl. Genet. 131: 1163–1171.

Lakshmi, V.J., N.V. Krishnaiah, G. Katti, I.C. Pasalu and K. Bhanu. 2010. Development of insecticide resistance in rice brown planthopper and whitebacked planthopper in Godavari Delta of Andhra Pradesh. Indian J. Plant Prot. 38: 35–40.

Leelagud, P., S. Kongsila, P. Vejchasarn, K. Darwell, Y. Phansenee, A. Suthanthangjai, C. Uparang, R. Kawichai, P. Yajai, K. Boonsa-Nga, V. Chamarerk and J. Jairin. 2020. Genetic diversity of Asian rice gall midge based on mtCOI gene sequences and identification of a novel resistance locus gm12 in rice cultivar MN62M. Mol. Biol. Rep. 47: 4273–4283.

Li, S., X. Zhang, W. Wang, X. Guo, Z. Wu, W. Du, Y. Zhao and L. Xia. 2018. Expanding the scope of CRISPR/Cpf1-mediated genome editing in rice. Mol. Plant 11: 995–998.

Li, Z., Y. Xue, H. Zhou, Y. Li, B. Usman, X. Jiao, X. Wang, F. Liu, B. Qin, R. Li and Y. Qiu. 2019. High-resolution mapping and breeding application of a novel brown planthopper resistance gene derived from wild rice (Oryza. rufipogon Griff). Rice 12: 41.

Lu, H., T. Luo, H. Fu, L. Wang, Y. Tan, J. Huang, Q. Wang, G. Ye, A.M.R. Gatehouse, Y. Lou and Q. Shu. 2018. Resistance of rice to insect pests mediated by suppression of serotonin biosynthesis. Nat. Plants 4: 338–344.

Mae, T. and K. Ohira. 1981. The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol. 22(6): 1067–1074.

Mansur, L.M., J. Orf and K.G. Lark. 1993. Determining the linkage of quantitative trait loci to RFLP markers using extreme phenotypes of recombinant inbreds of soybean (Glycine max L. Merr.). Theor. Appl. Genet. 86: 914–918.

Matsumura, M. and S. Sanada-Morimura. 2010. Recent status of insecticide resistance in Asian rice planthopper. Jpn. Agric. Res. Q. 44(3): 225–230.

Michelmore, R.W., I. Paran and R.V. Kesseli. 1991. Identification of markers linked to diseaseresistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. 88: 9828–9832.

Murata, K., M. Fujiwara, C. Kaneda, S. Takumi, N. Mori and C. Nakamura. 1998. RFLP mapping of a brown planthopper (Nilaparvata lugens Stål) resistance gene bph2 of indica rice introgressed into a japonica breeding line ‘Norin-PL4’. Genes Genet. Syst. 73(6): 359–364.

Ohnishi, Y., T. Tanaka, K. Ozaki, R. Yamada, H. Suzuki and Y. Nakamura. 2001. A high-throughput SNP typing system for genome-wide association studies. J. Hum. Genet. 46: 471–477.

Otuka, A., S. Huang, S. Sanada-Morimura and M. Matsumura. 2012. Migration analysis of Nilaparvata lugens (Hemiptera: Delphacidae) from the Philippines to Taiwan under typhoon-induced windy conditions. Appl. Entomol. Zool. 47: 263–271.

Pan, Y., L. Huang, S. Song, M. Hu, S. Chang, Q. Lv, Y. Li, T. Wang, X. Ouyang, Y. Xiao and X. Fu. 2019. Identification of brown planthopper resistance gene Bph32 in the progeny of a rice dominant genic male sterile recurrent population using genome-wide association study and RNA-seq analysis. Mol. Breeding 39: 72.

Parts, L., A.F. Cubillos, J. Warringer, K. Jain, F. Salinas, S.J. Bumpstead, M. Molin, A. Zia, J.T. Simpson, M.A. Quail, A. Moses, E.J. Louis, R. Durbin and G. Liti. 2011. Revealing the genetic structure of a trait by sequencing a population under selection. Genome Res. 21: 1131–1138.

Qi, L., Y.B. Ding, X.M. Zheng, R. Xu, L.Z. Zhang, Y.Y. Wang, X.N. Wang, L.F. Zhang, Y.L. Cheng, W.H. Qiao and Q.W. Yang. 2018. Fine mapping and identification of a novel locus qGL12.2 control grain length in wild rice (Oryza rufipogon Griff.). Theor. Appl. Genet. 131: 1497–1508.

Qiu, Y., J. Guo, S. Jing, L. Zhu and G. He. 2010. High-resolution mapping of the brown planthopper resistance gene Bph6 in rice and characterizing its resistance in the 9311 and Nipponbare near isogenic backgrounds. Theor. Appl. Genet. 121: 1601–1611.

Qiu, Y., J. Guo, S. Jing, L. Zhu and G. He. 2012. Development and characterization of Japonica rice lines carrying the brown planthopper resistance genes BPH12 and BPH6. Theor. Appl. Genet. 124: 485–494.

Rahman, M.L., W. Jiang, S.H. Chu, Y. Qiao, T. Ham, M. Woo, J. Lee, M.S. Khanam, J. Chin, J. Jeung, D.S. Brar, K.K. Jena and H. Koh. 2009. High-resolution mapping of two rice brown planthopper resistance genes, Bph20(t) and Bph21(t), originating from Oryza minuta. Theor. Appl. Genet. 119: 1237–1246.

Rashid, M.M., M. Jahan, K.S. Islam and M.A. Latif. 2017. Ecological fitness of brown planthopper, Nilaparvata lugens (Stål), to rice nutrient management. Ecol. Process. 6: 15.

Ren, J., F. Gao, X. Wu, X. Lu, L. Zeng, J. Lv, X. Su, H. Luo and G. Ren. 2016. Bph32, a novel gene encoding an unknown SCR domain-containing protein, confers resistance against the brown planthopper in rice. Sci. Rep. 6: 37645.

Samanwong, S., S. Tanasinchakul, S. Tantakom and S. Chitrakon. 2005. Brown planthopper (Nilaparvata lugens Stål) resistance from Thai wild and weedy rice, pp. 137–143. In Proc. the Weedy Rice Symposium, 21 October 2005. Bangkok, Thailand. (in Thai).

Sandstrom, J. 2000. Nutritional quality of phloem sap in relation to host plant-alternation in the bird cherry-oat aphid. Chemoecology 10: 17–24.

Sarao, P.S., G.K. Sahi, K. Neelam, G.S. Mangat, B.C. Patra and K. Singh. 2016. Donors for resistance to brown planthopper Nilaparvata lugens (Stål) from wild rice species. Rice Sci. 23: 219–224.

Satturu, V., J.L. Vattikuti, D.S. J, A. Kumar, R.K. Singh, S.P. M, H. Zaw, M.L. Jubay, L. Satish, A. Rathore, S. Mulinti, I.L. Vg, R. Abdul Fiyaz, A. Chakraborty and N. Thirunavukkarasu. 2020. Multiple genome wide association mapping models identify quantitative trait nucleotides for brown planthopper (Nilaparvata lugens) resistance in MAGIC Indica population of rice. Vaccines 8: 608.

Schenke, D. and D. Cai. 2020. Applications of CRISPR/Cas to improve crop disease resistance: beyond inactivation of susceptibility factors. iScience 23: 101478.

Shabanimofrad, M., M.Y. Rafii, S. Ashkani, M.M. Hanafi, N.A. Adam, M.A. Latif, A.R. Harun and M. Sahebi. 2015. Analysis of SSR markers linked with brown planthopper resistance genes (Bph) using high-resolution melting (HRM) in rice. Plant Omics. 8(3): 212–219.

Sharma, P.N., A. Torii, S. Takumi, N. Mori and C. Nakamura. 2004. Marker-assisted pyramiding of brown planthopper (Nilaparvata lugens Stål) resistance genes Bph1 and Bph2 on rice chromosome 12. Hereditas 140(1): 61–69.

Shigematsu, Y., N. Murofushi, K. Ito, C. Kanedaand and S. Kawabe. 1982. Sterols and asparagine in the rice plant, endogenous factors related to resistance against the brown planthopper (Nilaparvata lugens). Agric. Biol. Chem. 46(11): 2877–2879.

Shimatani, Z., S. Kashojiya, M. Takayama, R. Terada, T. Arazoe, H. Ishii, H. Teramura, T. Yamamoto, H. Komatsu, K. Miura, H. Ezura, K. Nishida, T. Ariizumi and A. Kondo. 2017. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 35: 441–443.

Sogawa, K. 2015. Planthopper outbreaks in different paddy ecosystems in Asia: man-made hopper plagues that threatened the green revolution in rice, pp. 33–63. In: K. Heong, J. Cheng and M. Escalada, eds. Rice Planthoppers. Springer, Dordrecht.

Sun, L., L. Yang, J. Wang, H. Liu, H. Zheng, D. Xie, M. Zhang, M. Feng, Y. Jia, H. Zhao and D. Zou. 2018. Identification of a cold-tolerant locus in rice (Oryza sativa L.) using bulked segregant analysis with a next-generation sequencing strategy. Rice 11: 24.

Sun, Z., J.H. Shi, T. Fan, C. Wang, L. Liu, H. Jin, C.N. Foba and M.Q. Wang. 2020. The control of the brown planthopper by the rice Bph14 gene is affected by nitrogen. Pest Manag. Sci. 76(11): 3649–3656.

Swinnen, S., K. Schaerlaekens, T. Pais, J. Claesen, G. Hubmann, Y. Yang, M. Demeke, M.R. Foulquié-Moreno, A. Goovaerts, K. Souvereyns, L. Clement, F. Dumortier and J.M. Thevelein. 2012. Identification of novel causative genes determining the complex trait of high ethanol tolerance in yeast using pooled-segregant whole-genome sequence analysis. Genome Res. 22: 975–984.

Takagi, H., A. Abe, K. Yoshida, S. Kosugi, S. Natsume, C. Mitsuoka, A. Uemura, H. Utsushi, M. Tamiru, S. Takuno, H. Innan, L.M. Cano, S. Kamoun and R. Terauchi. 2013. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J. 74: 174–183.

Tanaka, K. 1999. Quantitative genetic analysis of biotypes of the brown planthopper Nilaparvata lugens: heritability of virulence to resistant rice varieties. Entomol. Exp. Appl. 90: 279–287.

Thanyasiriwat, T., P. Pattawatang and E.R. Angeles. 2009. New biotypes of brown planthopper in Thailand. In Proc. the 6th International IPM Symposium, 24–26 March 2009. Portland, Oregon, USA.

Tobin, A.K. and T. Yamaya. 2001. Cellular compartmentation of ammonium assimilation in rice and barley. J. Exp. Bot. 52: 591–604.

Vejchasarn, P., J.R. Shearman, U. Chaiprom, Y. Phansenee, T. Tulyananda, J. Jairin and C. Amornbunchornvej. 2021. Population structure of nation-wide rice in Thailand. Rice 14: 88.

Wang, H.Y., Y. Yang, J.Y. Su, J.L. Shen, C.F. Gao and Y.C. Zhu. 2008. Assessment of the impact of insecticides on Anagrus nilaparvatae (Pang et Wang) (Hymenoptera: Mymanidae), an egg parasitoid of the rice planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Crop Prot. 27: 514–522.

Weibull, J.H.W. 1988. Free amino acids in the phloem sap from oats and barley resistant to Rhopalosiphum padi. Phytochem. 27: 2069–2072.

Wenger, W.J., K. Schwartz and G. Sherlock. 2010. Bulk segregant analysis by high-throughput sequencing reveals a novel xylose utilization gene from Saccharomyces cerevisiae. PLOS Genet. 6: e1000942.

Wu, H., Y. Liu, J. He, Y. Liu, L. Jiang, L. Liu, C. Wang, X. Cheng and J. Wan. 2014. Fine mapping of brown planthopper (Nilaparvata lugens Stål) resistance gene Bph28(t) in rice (Oryza sativa L.). Mol. Breeding 33: 909–918.

Xu, H.J., J. Xue, B. Lu, X.C. Zhang, J.C. Zhuo, S.F. He, X.F. Ma, Y.Q. Jiang, H.W. Fan, J.Y. Xu, Y.X. Ye, P.L. Pan, Q. Li, Y.Y. Bao, H.F. Nijhout and C.X. Zhang. 2015. Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519: 464–467.

Xue, W., N. Xu, X. Yuan, H. Chen, J. Zhang, S. Fu, C. Zhang and H. Xu. 2018. CRISPR/Cas9-mediated knockout of two eye pigmentation genes in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Biochem. Mol. Biol. 93: 19–26.

Yamasaki, M., A. Yoshimura and H. Yasui. 2003. Genetic basis of ovicidal response to whitebacked planthopper (Sogatella furcifera Horváth) in rice (Oryza sativa L.). Mol. Breeding 12: 133–143.

Yamaya, T., M. Obara, H. Nakajima, S. Sasaki, T. Hayakawa and T. Sato. 2002. Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. J. Exp. Bot. 53: 917–925.

Yang, H., X. Ren, Q. Weng, L. Zhu and G. He. 2002. Molecular mapping and genetic analysis of a rice brown planthopper (Nilaparvata lugens Stål) resistance gene. Hereditas 136: 39–43.

Yang, M., J. Lin, L. Cheng, H. Zhou, S. Chen, F. Liu, R. Li and Y. Qiu. 2020a. Identification of a novel planthopper resistance gene from wild rice (Oryza rufipogon Griff.). Crop J. 8: 1057–1070.

Yang, M., W. He, Y. Li, J. Qiu, F. Liu, R. Li and Y. Qiu. 2021. Effects of low levels of nitrogen or phosphorus provided in hydroponic culture on brown planthopper feeding and survival. Int. J. Pest Manag. 67: 89–98.

Yang, S., Y. Bao, C. Chen, M. Lu, W. Liu and S. Hong. 2020b. Analysis of atmospheric circulation situation and source areas for brown planthopper immigration to Korea: a case study. Ecosphere 11: e03079.

Yuexiong, Z., Q. Gang, M. Qianqian, W. Minyi, Y. Xinghai, M. Zengfeng, L. Haifu, L. Chi, L. Zhenjing, L. Fang, H. Dahui and L. Rongbai. 2020. Identification of major locus Bph35 resistance to brown planthopper in rice. Rice Sci. 27: 237–245.

Zhao, Y., G. Huang and W. Zhang. 2019. Mutations in NlInR1 affect normal growth and lifespan in the brown planthopper Nilaparvata lugens. Insect Biochem. Mol. Biol. 115: 103246.

Zheng, W.J., Y. Wang, L.L. Wang, Z.B. Ma, J.M. Zhao, P. Wang, L.X. Zhang, Z.H. Liu and X.C. Lu. 2016. Genetic mapping and molecular marker development for Pi65(t), a novel broadspectrum resistance gene to rice blast using next-generation sequencing. Theor. Appl. Genet. 129: 1035–1044.

Zong, Y., Y. Wang, C. Li, R. Zhang, K. Chen, Y. Ran, J.L. Qiu, D. Wang and C. Gao. 2017. Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat. Biotechnol. 35: 438–440.