Sains Malaysiana 53(5)(2024): 1067-1080

http://doi.org/10.17576/jsm-2024-5305-08

Exploring the Resistance of Pigmented Rice to Brown Planthopper (Nilaparvata lugensStål) by Phenotypic and Genotypic Analyses

(Mengkaji Kerintangan Beras Berpigmen terhadap Wereng Coklat (Nilaparvata lugens Stål) melalui Analisis Fenotip dan Genotip)

CHAERANI^1,*, MUHAMAD YUNUS², NURUL HIDAYATUN¹, TASLIAH², RINA SITI GALURINA¹, MATSOHAN¹, YUSI NURMALITA ANDARINI¹ & ANDARI RISLIAWATI¹

¹Research Center for Food Crops, National Research and Innovation Agency (BRIN), Jln. Raya Jakarta-Bogor Km. 46, Cibinong, Bogor 16911, Indonesia

²Research Center for Applied Botany, National Research and Innovation Agency (BRIN), Jln. Raya Jakarta-Bogor Km. 46, Cibinong, Bogor 16911, Indonesia

Received: 1 December 2023/Accepted: 17 April 2024

@rin.go.id

Abstract

Developing new pigmented rice varieties that meet consumers' preferences requires addressing resistance to brown planthopper (BPH), a highly destructive insect pest of rice.  To effectively manage this pest, it is essential to explore BPH resistance genes from rice germplasms and incorporate them into elite varieties. The objective of this study was to identify the source of resistance among local and improved pigmented rice varieties in Indonesia against field BPH. Furthermore, the study aimed to characterize their genetic diversity using molecular markers associated with Bph genes and functional markers for these genes.  Eighty-eight local varieties from the Indonesian Agricultural Gene Bank, collected across 18 provinces between 1971 and 2019, and four improved varieties, were evaluated using the standard seed box screening test method. Among these entries, 6 local accessions and 1 improved variety exhibited moderate resistance. Genetic analysis of these entries and three randomly selected susceptible entries using 12 SSR and InDel markers associated with Bph gene loci showed that the moderately resistant entries had higher allele numbers (11 to 13) compared to the susceptible entries (4 to 7). These markers could distinguish the resistant group from the susceptible ones in cluster analysis. Genotyping using functional markers further showed that the moderately resistant entries had 2 to 4 combinations of Bph genes. In contrast, the susceptible entries contained neither Bph genes nor only one gene. Local accessions with a 2 to 4 Bph gene combination can be donors of BPH resistance in improving pigmented rice varieties.

Keywords: Bph gene; brown planthopper resistance; local rice accession; screening

Abstrak

Membangunkan varieti padi berpigmen baharu yang memenuhi keutamaan pengguna memerlukan usaha menangani rintangan terhadap wereng coklat (BPH), serangga perosak pemusnah beras. Untuk menguruskan perosak ini dengan berkesan, adalah penting untuk mengkaji gen rintangan BPH daripada germplasma padi dan memasukkannya ke dalam varieti elit. Objektif kajian ini adalah untuk mengenal pasti punca rintangan dalam kalangan varieti padi tempatan dan padi berpigmen dipertingkat di Indonesia berbanding BPH ladang. Tambahan pula, penyelidikan ini bertujuan untuk mencirikan kepelbagaian genetik mereka menggunakan penanda molekul yang dikaitkan dengan gen Bph dan penanda berfungsi untuk gen ini. Lapan puluh lapan varieti tempatan daripada Bank Gene Pertanian Indonesia yang dikumpulkan daripada 18 wilayah antara 1971 dan 2019 dan empat varieti yang dipertingkat dinilai menggunakan kaedah ujian saringan kotak benih piawai. Antara entri ini, 6 aksesi tempatan dan 1 varieti dipertingkat menunjukkan rintangan yang sederhana. Analisis genetik bagi entri ini dan tiga entri rentan yang dipilih secara rawak menggunakan 12 penanda SSR dan InDel yang dikaitkan dengan lokus gen Bph menunjukkan bahawa entri tahan sederhana mempunyai nombor alel yang lebih tinggi (11 hingga 13) berbanding dengan entri rentan (4 hingga 7). Penanda ini boleh membezakan kumpulan rintangan daripada kumpulan rentan dalam analisis kelompok. Genotip menggunakan penanda berfungsi selanjutnya menunjukkan bahawa entri tahan sederhana mempunyai 2 hingga 4 gabungan gen Bph. Sebaliknya, entri yang rentan tidak mengandungi gen Bph atau hanya satu gen. Aksesi tempatan dengan gabungan gen 2 hingga 4 Bph boleh menjadi penderma rintangan BPH dalam meningkatkan varieti beras berpigmen.

Kata kunci: Aksesi beras tempatan; gen Bph; ketahanan terhadap wereng coklat; penyaringan

REFERENCES

Abdullah, B. 2017. Peningkatan kadar antosianin beras merah dan beras hitam melalui biofortifikasi. Jurnal Litbang Pertanian 36(2): 91-98.

Afza, H. 2017. Peran konservasi dan karakterisasi plasma nutfah padi beras merah dalam pemuliaan tanaman. Jurnal Penelitian dan Pengembangan Pertanian 35(3): 143-153.

Ariefiansyah, R. 2018. Transformasi wereng batang cokelat dari ‘hama tidak penting’ menjadi ‘hama elite’ pada ekosistem padi sawah di Pulau Jawa: Sebuah pembahasan etnografi multispesies. Antropologi Indonesia 39(1): 15-38.

Baehaki, S.E. 2012. Perkembangan biotipe hama wereng coklat pada tanaman padi. IPTEK Tanaman Pangan 7(1): 8-17.

Baehaki, S.E. & Mejaya, I.M.J. 2014. Wereng cokelat sebagai hama global bernilai ekonomi tinggi dan strategi pengendaliannya. IPTEK Tanaman Pangan 9(1): 1-12.

Brar, D.S., Virk, P.S., Jena, K.K. & Khush, G.S. 2009. Breeding for resistance to planthoppers in rice. In Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia, edited by Heong, K.L. & Hardy, B. Los Baños: International Rice Research Institute. pp. 401-409.

Busniah, M., Kasim, M & Winarto, W. 2020. West Sumatera brown rice resistance to brown planthopper. In IOP Conference Series: Earth and Environmental Science 497: 1-6.

Chaerani, C., Damayanti, D., Trisnaningsih, T., Yuriyah, S., Kusumanegara, K., Dadang, A., Sutrisno, S. & Bahagiawati, B. 2016. Virulence of brown planthopper and development of core collection of the pest. Jurnal Penelitian Tanaman Pangan 35(2): 109-117.

Chen, J.W., Wang, L., Pang, X.F. & Pan, Q.H. 2006. Genetic analysis and fine mapping of a rice brown planthopper (Nilaparvata lugens Stål) resistance gene Bph19(t). Molecular Genetics and Genomics 275(4): 321-329.

Deng, G.F., Xu, X.R., Zhang, Y., Li, D., Gan, R.Y. & Li, H.B. 2013. Phenolic compounds and bioactivities of pigmented rice. Critical Reviews in Food Science and Nutrition 53(3): 296-306.

Dwipa, I., Syarif, A., Suliansyah, I. & Swasti, E. 2018. West Sumatra brown rice resistance to brown planthopper and blast disease. Biodiversitas 19(3): 839-844.

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

Effendi, B.S. & Munawar, D. 2013. Uji ketahanan galur padi terhadap wereng coklat biotipe 3 melalui population build-up. Jurnal Entomologi Indonesia 10(1): 7-17.

Haliru, B.S., Rafii, M.Y., Mazlan, N., Ramlee, S.I., Muhammad, I., Akos, I.S., Halidu, J., Swaray, S. & Bashir, Y.R. 2020. Recent strategies for detection and improvement of brown planthopper resistance genes in rice: A review. Plants 9(9): 1-18.

Harini, S., Kumar, S., Balaravi, P., Sharma, R., Dass, A. & Shenoy, V. 2013. Evaluation of rice genotypes for brown planthopper (BPH) resistance using molecular markers and phenotypic methods. African Journal of Biotechnology 12(19): 2515-2525.

Heinrichs, E.A., Medrano, F.G. & Rapusas, H.R. 1985. Genetic Evaluation for Insect Resistance in Rice. Int. Rice Res. Inst.

Horgan, F.G., Mundaca, E.A., Quintana, R., Naredo, A.I., Almazan, M.L.P. & Bernal, C.C. 2021. Efficacy and cost-effectiveness of phenotyping for rice resistance and tolerance to planthoppers. Insects 12(10): 847.

Horgan, F.G., Ramal, A.F., Bentur, J.S., Kumar, R., Bhanu, K.V., Sarao, P.S., Iswanto, E.H., Van Chien, H., Phyu, M.H., Bernal, C.C., Almazan, M.L.P., Alam, M.Z., Lu, Z. & Huang, S.H. 2015. Virulence of brown planthopper (Nilaparvata lugens) populations from South and South East Asia against resistant rice varieties. Crop Protection 78(December): 222-231.

Hou, L.Y., Yu, P., Xu, Q., Yuan, X.P., Yu, H.Y., Wang, Y.P., Wang, C.H., Guo, W., Tang, S.X., Peng, S.T. & Wei, X.H. 2011. Genetic analysis and preliminary mapping of two recessive resistance genes to brown planthopper, Nilaparvata lugens Stål in Rice. Rice Science 18(3): 238-242.

Hu, J., Cheng, M., Gao, G., Zhang, Q., Xiao, J. & He, Y. 2013. Pyramiding and evaluation of three dominant brown planthopper resistance genes in the elite indica rice 9311 and its hybrids. Pest Management Science 69(7): 802-808.

Jairin, J., Phengrat, K., Teangdeerith, S., Vanavichit, A. & Toojinda, T. 2007. Mapping of a broad-spectrum brown planthopper resistance gene, Bph3, on rice chromosome 6. Molecular Breeding 19: 35-44

Jena, M., Panda, R.S., Sahu, R.K., Mukherjee, A.K. & Dhua, U. 2015. Evaluation of rice genotypes for rice brown plant hopper resistance through phenotypic reaction and genotypic analysis. Crop Protection 78: 119-126.

Kamal, M.M., Nguyen, C.D., Sanada-Morimura, S., Zheng, S.H. & Fujita, D. 2023. Development of pyramided lines carrying brown planthopper resistance genes in the genetic background of indica group rice (Oryza sativa L.) variety 'IR64'. Breeding Science. http://dx.doi.org/10.1270/jsbbs.23028

Kim, J., An, X., Yang, K., Miao, K.S., Qin, Y., Hu, Y., Du, B., Zhu, L., He, G. & Chen, R. 2022. Molecular mapping of a new brown planthopper resistance gene Bph43 in rice (Oryza sativa L.). Agronomy 12(4): 808.

Kumar, K., Sarao, P.S., Bhatia, D., Neelam, K., Kaur, A., Mangat, G.S., Brar, D.S. & Singh, K. 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. Theoretical and Applied Genetics 131(5): 1163-1171.

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

Ling, Y. & Weilin, Z. 2016. Genetic and biochemical mechanisms of rice resistance to planthopper. Plant Cell Reports 35(8): 1559-1572.

Liu, G., Yan, H., Fu, Q., Qian, Q., Zhang, Z., Zhai, W. & Zhu, L. 2001. Mapping of a new gene for brown planthopper resistance in cultivated rice introgressed from Oryza eichingeri. Chinese Science Bulletin 46(17): 1459-1462.

Liu, K. & Muse, S.V. 2005. PowerMarker: An integrated analysis environment for genetic marker analysis. Bioinformatics 21(9): 2128-2129.

Muduli, L., Dash, M., Das Mohapatra, S., Mohapatra, K.K., Nayak, H.S., Bastia, D.N., Pradhan, B., Tripathy, S.K., Jena, R.C. & Pradhan, S.K. 2023. Phenotypic and genotypic assessment of elite rice varieties for brown plant hopper (Nilaparvata lugens Stål.) resistance. Cereal Research Communications 51: 821-833.

Myint, K.K.M., Fujita, D., Matsumura, M., Sonoda, T., Yoshimura, A. & Yasui, H. 2012. Mapping and pyramiding of two major genes for resistance to the brown planthopper (Nilaparvata lugens [Stål]) in the rice cultivar ADR52. Theoretical and Applied Genetics 124: 495-504.

Naik, S.B., Divya, D., Sahu, N., Sundaram, R.M., Sarao, P.S., Singh, K., Lakshmi, V.J. & Bentur, J.S. 2018. A new gene Bph33(t) conferring resistance to brown planthopper (BPH), Nilaparvata lugens (Stål) in rice line RP2068-18-3-5. Euphytica 214: 53.

Prahalada, G.D., Shivakumar, N., Lohithaswa, H.C., Sidde Gowda, D.K., Ramkumar, G., Kim, S.R., Ramachandra, C., Hittalmani, S., Mohapatra, T. & Jena, K.K. 2017. 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 (N Y) 10(1): 41.

Qiu, Y., Guo, J., Jing, S., Zhu, L. & He, G. 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. Theoretical and Applied Genetics 121(8): 1601-1611.

Rahman, M.L., Jiang, W., Chu, S.H., Qiao, Y., Ham, T.H., Woo, M.O., Lee, J., Khanam, M.S., Chin, J.H., Jeung, J.U., Brar, D.S., Jena, K.K. & Koh, H.J. 2009. High-resolution mapping of two rice brown planthopper resistance genes, Bph20(t) and Bph21(t), originating from Oryza minuta. Theoretical and Applied Genetics 119(7): 1237-1246.

Ramkumar, G., Prahalada, G.D., Hechanova, S.L., Kim, S.R. & Jena, K.K. 2016. Exploring genetic diversity of rice cultivars for the presence of brown planthopper (BPH) resistance genes and development of SNP marker for Bph18. Plant Breeding 135(3): 301-308.

Risliawati, A., Andarini, Y.N., Terryana, R.T., Nugroho, K. & Lestari, P. 2021. Analisis diversitas genetik aksesi padi warna Indonesia berdasarkan marka molekuler fungsional. Jurnal AgroBiogen17(1): 25-34.

Smith, C.M. 1999. Plant resistance to insects. In Biological and Biotechnological Control of Insect Pests, edited by Rechcigl, J.E. & Rechcigl, N.A. Boca Raton: CRC Press. pp. 171-208.

Sun, L., Su, C., Wang, C., Zhai, H. & Wan, J. 2005. Mapping of a major resistance gene to the brown planthopper in the rice cultivar Rathu Heenati. Breeding Science 55: 391-396.

Tiozon Jr., R.N., Sartagoda, K.J.D. & Sreenivasulu, N. 2023. The nutritional profile and human health benefit of pigmented rice and the impact of post-harvest processes and product development on the nutritional components: A review. Critical Reviews in Food Science and Nutrition 63(19): 3867-3894.

Wang, H., Shi, S., Guo, Q., Nie, L., Du, B., Chen, R., Zhu, L. & He, G. 2018. High-resolution mapping of a gene conferring strong antibiosis to brown planthopper and developing resistant near-isogenic lines in 9311 background. Molecular Breeding 38(8): 107.

Yang, K., Liu, H., Jiang, W., Hu, Y., Zhou, Z., An, X., Miao, S., Qin, Y., Du, B., Zhu, L., He, G. & Chen, R. 2023. Large scale rice germplasm screening for identification of novel brown planthopper resistance sources. Molecular Breeding 43(9): 70.

Yang, M., Cheng, L., Yan, L., Shu, W., Wang, X. & Qiu, Y. 2019. Mapping and characterization of a quantitative trait locus resistance to the brown planthopper in the rice variety IR64. Hereditas 156: 22.

Yunus, M., Dadang, A., Slamet, S., Warsun, A., Satyawan, D. & Chaerani, C. 2023. Segregation of molecular markers associated with Bph3 gene in BC5F2 population derived from Ciherang rice variety as the recipient parent. IOP Conference Series: Earth and Environmental Science 1255: 012044.

Zhang, Y., Qi, G., Ma, Q., Wei, M., Yang, X., Ma, Z., Liang, H., Liu, C., Li, Z., Liu, F., Huang, D. & Li, R. 2020. Identification of major locus Bph35 resistance to brown planthopper in rice. Rice Science 27(3): 237-245.

Zhao, Y., Huang, J., Wang, Z., Jing, S., Wang, Y., Ouyang, Y., Cai, B., Xin, X.F., Liu, X., Zhang, C., Pan, Y., Ma, R., Li, Q., Jiang, W., Zeng, Y. Shangguan, X., Wang, H., Du, B., Zhu, L., Xu, X., Feng, Y.Q., He, S.Y., Chen, R., Zhang, Q. & He, G. 2016. Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. Proceedings of the National Academy of Sciences of the United States of America 113(45): 12850-12855.

*Corresponding author; email: chae007@brin.go.id