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 lugens Stål) by Phenotypic and
Genotypic Analyses
(Mengkaji Kerintangan Beras Berpigmen
terhadap Wereng Coklat (Nilaparvata lugens Stål) melalui Analisis
Fenotip dan Genotip)
CHAERANI1,*, 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
Diserahkan: 1 Disember 2023/Diterima: 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
RUJUKAN
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
AgroBiogen 17(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.
*Pengarang
untuk surat-menyurat; email: chae007@brin.go.id
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