Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (11): 1764-1769.doi: 10.3724/SP.J.1006.2019.82066

• RESEARCH NOTES • Previous Articles    

Pyramiding and evaluation of brown planthopper resistance genes in water-saving and drought-resistance restorer line

ZHANG An-Ning1,2,LIU Yi1,2,WANG Fei-Ming1,XIE Yue-Wen2,KONG De-Yan1,NIE Yuan-Yuan3,ZHANG Fen-Yun1,BI Jun-Guo1,YU Xin-Qiao1,LIU Guo-Lan1,LUO Li-Jun1,2,*()   

  1. 1 Shanghai Agrobiological Gene Center, Shanghai 201106, China
    2 College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China
    3 Jiangxi Super Rice Research and Development Center, Nanchang 330200, Jiangxi, China
  • Received:2018-12-20 Accepted:2019-06-12 Online:2019-11-12 Published:2019-07-09
  • Contact: Li-Jun LUO E-mail:lijun@sagc.org.cn
  • Supported by:
    This study was supported by the Shanghai Seed Industry Development Project(2019-02-08-00-08-F01110);the Shanghai Agriculture Applied Technology Development Program(2018-02-08-00-08-F01553);the National Key Research and Development Program of China(2017YFD0100304)


The brown planthopper (Nilaparvata lugens St?l, BPH) is the most serious pest threat to rice production across Asia. Increasing host-plant resistance is the most economical and ecological strategy for controlling this pest. The objective of this study was to survey the resistance effects of different R genes to brown planthopper, reveal its influence on agronomic traits, and provide insights into molecular breeding of rice with resistance to brown planthopper. In this research, the brown planthopper R genes Bph6, Bph9, Bph14, and Bph15 were introgressed into the water-saving and drought-resistant rice restorer line ‘Hanhui 3’ through marker-assisted backcrossing scheme. The standard seedling group screening method was used to identify the resistance of the improved lines. Among single-gene improved lines, the order of the R genes effects was Bph9 > Bph6 > Bph15 > Bph14, and among pyramiding improved lines, that was Bph6+Bph9+Bph14+Bph15 > Bph6+Bph9 > Bph6+Bph9+Bph14 > Bph6+Bph9+Bph15 > Bph6+Bph14+Bph15 > Bph9+Bph14+Bph15 > Bph14+Bph15. Furthermore, the survey of agronomic traits demonstrated that there were no significant differences between the 11 improved lines and recurrent parent ‘Hanhui 3’ in plant height, panicle number per plant and 1000-grain weight. These results suggest that the introgression of Bph6, Bph9, Bph14, and Bph15 genes by molecular marker-assisted selection technology could enhance the resistance to brown planthopper and improve breeding efficiency.

Key words: breeding, brown planthopper, resistance gene, marker-assisted selection, resistance evaluation, water-saving and drought-resistance rice

Fig. 1

Breeding restorer lines with resistance to brown planthopper"

Fig. 2

PCR analysis for brown planthopper resistance genes A: Bph6-linked marker RM5757; B: Bph9-linked marker InD28432; C: Bph14-linked marker 76-2; D: Bph15-linked marker MS5. M: D2000 marker; P1: recurrent parent Hanhui 3; P2: donor parent; 1-11: improved lines 18R1-18R11."

Table 1

Evaluation for brown planthopper resistance at seedling stage"

Identification no.
Resistance performance
Resistance level#
18R1 18FS30 Bph6 2.60±0.81 抗虫 R
18R2 18FS72 Bph9 2.40±0.35 抗虫 R
18R3 18FS32 Bph14 5.20±0.76 中抗 MR
18R4 18FS71 Bph15 4.30±0.97 中抗 MR
18R5 18FS86 Bph6+Bph9 1.10±0.21 高抗 HR
18R6 18FS83 Bph14+Bph15 1.93±0.41 高抗 HR
18R7 18FS90 Bph6+Bph9+Bph14 1.27±0.27 高抗 HR
18R8 18FS88 Bph6+Bph9+Bph15 1.50±0.38 高抗 HR
18R9 18FS92 Bph6+Bph14+Bph15 1.60±0.31 高抗 HR
18R10 18FS94 Bph9+Bph14+Bph15 1.70±0.35 高抗 HR
18R11 18FS97 Bph6+Bph9+Bph14+Bph15 0.53±0.24 高抗 HR
旱恢3号 Hanhui 3 18FS26 8.93±0.07 高感 HS
TN1 8.80±0.12 高感 HS

Table 2

Agronomic traits of improved lines"

Plant height (cm)
per plant
Panicle length
Grains per
Grain fertility
1000-Grain weight (g)
Grain yield
per plant (g)
18R1 Bph6 121.00±1.00 13.67±3.21 21.49±0.58 200.30±2.84** 83.35±3.04 26.35±0.88 32.34±0.70*
18R2 Bph9 119.68±1.64 9.88±0.55 25.53±0.87** 202.65±5.16** 77.62±1.78 24.79±1.66 33.94±1.74
18R3 Bph14 129.00±6.24 10.00±4.00 24.88±1.80 199.98±7.81** 90.37±1.14 25.00±1.20 29.04±0.73**
18R4 Bph15 120.48±1.36 10.70±1.00 26.13±0.45** 200.22±3.20** 79.16±2.39 24.32±0.54 34.94±1.47
18R5 Bph6+Bph9 120.65±2.67 10.58±0.64 25.75±0.57** 201.66±2.29** 76.68±0.98* 24.44±1.58 31.99±3.46*
18R6 Bph14+Bph15 119.71±2.21 9.88±0.64 26.08±0.49** 198.87±7.43** 80.37±1.66 26.07±1.82 30.64±1.71**
18R7 Bph6+Bph9+Bph14 118.12±1.46 10.50±1.04 24.90±0.48* 194.34±2.80** 71.64±1.30** 26.21±1.12 34.90±0.71
18R8 Bph6+Bph9+Bph15 124.19±0.13 10.04±0.69 25.13±0.85* 205.54±5.21** 71.86±1.73** 24.44±0.88 32.75±2.89
18R9 Bph6+Bph14+Bph15 119.89±1.59 10.95±0.23 24.94±0.61* 200.59±4.13** 68.69±1.13** 24.87±1.73 36.47±1.04
18R10 Bph9+Bph14+Bph15 118.41±3.68 10.99±0.53 26.14±0.62** 201.56±2.44** 69.90±3.57** 26.53±0.52 31.19±1.82*
18R11 Bph6+Bph9+Bph14+Bph15 121.12±2.63 11.33±0.56 25.82±0.36** 200.79±6.06** 57.26±2.73** 26.40±1.21 30.38±1.89**
Hanhui 3 117.00±4.90 10.00±0.82 22.80±0.41 240.69±21.35 86.24±6.49 25.84±1.62 42.11±6.78
[1] Khush G S . What it will take to feed 5.0 billion rice consumers in 2030. Plant Mol Biol, 2005,59:1-6.
[2] Xue J, Zhou X, Zhang C X, Yu L L, Fan H W, Wang Z, Xu H J, Xi Y, Zhu Z R, Zhou W W, Pan P L, Li B L, Colbourne J K, Noda H, Suetsugu Y, Kobayashi T, Zheng Y, Liu S, Zhang R, Liu Y, Luo Y D, Fang D M, Chen Y, Zhan D L, Lyu X D, Cai Y, Wang Z B, Huang H J, Cheng R L, Zhang X C, Lou Y H, Yu B, Zhuo J C, Ye Y X, Zhang W Q, Shen Z C, Yang H M, Wang J, Bao Y Y, Cheng J A . Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol, 2014,15:521.
[3] 姜辉, 林荣华, 刘亮, 瞿唯钢, 陶传江 . 稻飞虱的危害及再猖獗机制. 昆虫知识, 2005,42:612-615.
Jiang H, Lin R H, Liu L, Qu W G, Tao C J . Planthoppers damage to rice and the resurgence mechanism. Chin Bull Entomol, 2005,42:612-615 (in Chinese with English abstract).
[4] Heong K L, Hardy B . Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia. Los Baños (Philippines): International Rice Research Institute, 2009. pp 401-428.
[5] Hu J, Xiao C, He Y . Recent progress on the genetics and molecular breeding of brown planthopper resistance in rice. Rice, 2016,9:30.
[6] Huang Z, He G, Shu L, Li X, Zhang Q . Identification and mapping of two brown planthopper resistance genes in rice. Theor Appl Genet, 2001,102:929-934.
[7] Guo J P, Xu C X, Wu D, Zhao Y, Qiu Y F, Wang X X, Ou-Yang Y D, Cai B D, Liu X, Jing S L, Shang-Guan X X, Wang H Y, Ma Y H, Hu L, Wu Y, Shi S J, Wang W L, Zhu L L, Xu X, Chen R Z, Feng Y Q, Du B, He G C . Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat Genet, 2018,50:297-306.
[8] Zhao Y, Huang J, Wang Z Z, Jing S L, Wang Y, Ou-Yang Y D, Cai B D, Xin X F, Liu X, Zhang C X, Pan Y F, Ma R, Li Q F, Jiang W H, Zeng Y, Shang-Guan X X, Wang H Y, Du B, Zhu L L, Xu X, Feng Y Q, He S Y, Chen R Z, Zhang Q F, He G C . Allelic diversity in an NLR gene Bph9 enables rice to combat planthopper variation. Proc Natl Acad Sci USA, 2016,113:12850-12855.
[9] 陈英之, 陈乔, 孙荣科, 杨朗, 黄凤宽, 黄大辉, 韦素美, 张月雄, 刘丕庆, 李容柏 . 改良水稻对稻褐飞虱的抗性研究. 西南农业学报, 2010,23:1099-1106.
Chen Y Z, Chen Q, Sun R K, Yang L, Huang F K, Huang D H, Wei S M, Zhang Y X, Liu P Q, Li R B . Improvement of rice resistance to brown planthoppers. Southwest China J Agric Sci, 2011,23:1099-1106 (in Chinese with English abstract).
[10] 胡杰, 杨长举, 张庆路, 高冠军, 何予卿 . 基因聚合改良杂交稻组合的稻飞虱田间抗性表现. 应用昆虫学报, 2011,48:1341-1347.
Hu J, Yang C J, Zhang Q L, Gao G J, He Y Q . Resistance of pyramided rice hybrids to brown planthoppers. Chin J Appl Entomol, 2011,48:1341-1347 (in Chinese with English abstract).
[11] 李进波, 夏明元, 戚华雄, 何光存, 万丙良, 查中萍 . 水稻抗褐飞虱基因Bph14Bph15的分子标记辅助选择. 中国农业科学, 2006,39:2132-2137.
Li J B, Xia M Y, Qi H X, He G C, Wan B L, Zha Z P . Marker-assisted selection for brown planthopper (Nilaparvata lugens Stål) resistance gene Bph14 and Bph15 in rice. Sci Agric Sin, 2006,39:2132-2137 (in Chinese with English abstract).
[12] 李进波, 万丙良, 夏明元, 戚华雄, 石华胜, 辛复林 . 抗褐飞虱水稻品种的培育及其抗性表现. 应用昆虫学报, 2011,48:1348-1353.
Li J B, Wan B L, Xia M Y, Qi H X, Shi H S, Xin F L . Breeding of the brown planthopper resistant rice varieties. Chin J Appl Entomol, 2011,48:1348-1353 (in Chinese with English abstract).
[13] 罗世友, 陈红萍, 吴小燕, 胡兰香, 熊换金, 邓伟, 汪雨萍, 席建才, 喻凤, 陈明亮, 肖叶青, 陈大洲 . 应用分子标记辅助选育抗褐飞虱水稻恢复系. 分子植物育种, 2015,13:2404-2415.
Luo S Y, Chen H P, Wu X Y, Hu L X, Xiong H J, Deng W, Wang Y P, Xi J C, Yu F, Chen M L, Xiao Y Q, Chen D Z . Breeding restorer lines resistance to brown planthopper by marker-assisted selection. Mol Plant Breed, 2015,13:2404-2415 (in Chinese with English abstract).
[14] 罗利军, 梅捍卫, 余新桥, 刘鸿艳, 冯芳君 . 节水抗旱稻及其发展策略. 科学通报, 2011,56:804-811.
Luo L J, Mei H W, Yu X Q, Liu H Y, Feng F J . Water-saving and drought-resistance rice and its development strategy. Chin Sci Bull, 2011,56:804-811 (in Chinese with English abstract).
[15] 聂元元, 李霞, 毛凌华, 赵洪阳, 万鹏, 李瑶 . 节水抗旱稻在江西的试验示范及推广. 杂交水稻, 2018,33(2):38-39.
Nie Y Y, Li X, Mao L H, Zhao H Y, Wan P, Li Y . Experimental demonstration and extension of water-saving and drought-resistant rice in Jiangxi. Hybrid Rice, 2018,32(2):38-39 (in Chinese).
[16] 王震, 徐爱民, 朱敬乐, 赵洪阳 . 节水抗旱稻“旱优73”在蚌埠的示范表现及高产栽培技术. 安徽农学通报, 2018,24(2):42-44.
Wang Z, Xu A M, Zhu J L, Zhao H Y . Performance of water- saving and drought-resistant rice ‘Hanyou 73’ in Bengbu. Anhui Agric Sci Bull, 2018,24(2):42-44 (in Chinese).
[17] 柏秀芳, 贾琳, 胡超, 李柱, 周娟, 符建法, 贾先勇 . 节水抗旱稻在湖南的发展前景与策略. 湖南农业科学, 2016, ( 8):25-27.
Bai X F, Jia L, Hu C, Li Z, Zhou J, Fu J F, Jia X Y . Development prospect and strategies of water-saving and drought-resistance rice in Hunan. Hunan Agric Sci, 2016, ( 8):25-27 (in Chinese with English abstract).
[18] Jena K K, Hechanova S L, Verdeprado H, Prahalada G D, Kim S R . 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, 2017,130:2345-2360.
[19] Xiao C, Hu J, Ao Y T, Cheng M X, Gao G J, Zhang Q L, He G C, He Y Q . Development and evaluation of near-isogenic lines for brown planthopper resistance in rice cv. 9311. Sci Rep, 2016,6:38159.
[20] Qiu Y F, Guo J P, Jing S L, Zhu L L, He G C . Development and characterization of japonica rice lines carrying the brown planthopper-resistance genes Bph12 and Bph6. Theor Appl Genet, 2012,124:485-894.
[21] 曾盖 . 利用MAS改良水稻两用核不育系的稻瘟病和褐飞虱抗性. 湖南农业大学硕士学位论文, 2017. pp 22-30.
Zeng G . Improving Blast and BPH Resistance of Dual-purpose Genic Sterile Rice Using Molecular Marker-assisted Selection. MS Thesis of Hunan Agricultural University, Changsha, Hunan, China, 2017. pp 22-30 (in Chinese with English abstract).
[22] 胡杰 . 水稻褐飞虱抗性基因的遗传定位和聚合效应分析. 华中农业大学博士学位论文, 湖北武汉, 2013. pp 85-92.
Hu J . Mapping and Pyramiding Brown Planthopper Resistance Genes in Rice. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hubei, China, 2013. pp 85-92 (in Chinese with English abstract).
[23] 楼珏, 杨文清, 李仲惺, 罗天宽, 谢永楚, 郑国楚, 岳高红, 徐建龙, 卢华金 . 聚合稻瘟病、白叶枯病和褐飞虱抗性基因的三系恢复系改良效果的评价. 作物学报, 2016,42:31-42.
Lou J, Yang W Q, Li Z X, Luo T K, Xie Y C, Zheng G C, Yue G H, Xu J L, Lu H J . Evaluation of improvement effect of restorer lines on pyramiding genes resistant to rice blast, bacterial leaf blight and brown planthopper. Acta Agron Sin, 2016,42:31-42 (in Chinese with English abstract).
[1] HU Wen-Jing, LI Dong-Sheng, YI Xin, ZHANG Chun-Mei, ZHANG Yong. Molecular mapping and validation of quantitative trait loci for spike-related traits and plant height in wheat [J]. Acta Agronomica Sinica, 2022, 48(6): 1346-1356.
[2] DENG Zhao, JIANG Nan, FU Chen-Jian, YAN Tian-Zhe, FU Xing-Xue, HU Xiao-Chun, QIN Peng, LIU Shan-Shan, WANG Kai, YANG Yuan-Zhu. Analysis of blast resistance genes in Longliangyou and Jingliangyou hybrid rice varieties [J]. Acta Agronomica Sinica, 2022, 48(5): 1071-1080.
[3] ZHU Zheng, WANG Tian-Xing-Zi, CHEN Yue, LIU Yu-Qing, YAN Gao-Wei, XU Shan, MA Jin-Jiao, DOU Shi-Juan, LI Li-Yun, LIU Guo-Zhen. Rice transcription factor WRKY68 plays a positive role in Xa21-mediated resistance to Xanthomonas oryzae pv. oryzae [J]. Acta Agronomica Sinica, 2022, 48(5): 1129-1140.
[4] YANG Xin, LIN Wen-Zhong, CHEN Si-Yuan, DU Zhen-Guo, LIN Jie, QI Jian-Min, FANG Ping-Ping, TAO Ai-Fen, ZHANG Li-Wu. Molecular identification of a geminivirus CoYVV and screening of resistant germplasms in jute [J]. Acta Agronomica Sinica, 2022, 48(3): 624-634.
[5] MA Hong-Bo, LIU Dong-Tao, FENG Guo-Hua, WANG Jing, ZHU Xue-Cheng, ZHANG Hui-Yun, LIU Jing, LIU Li-Wei, YI Yuan. Application of Fhb1 gene in wheat breeding programs for the Yellow-Huai Rivers valley winter wheat zone of China [J]. Acta Agronomica Sinica, 2022, 48(3): 747-758.
[6] ZHAO Mei-Cheng, DIAO Xian-Min. Phylogeny of wild Setaria species and their utilization in foxtail millet breeding [J]. Acta Agronomica Sinica, 2022, 48(2): 267-279.
[7] ZHAO Hai-Han, LIAN Wang-Min, ZHAN Xiao-Deng, XU Hai-Ming, ZHANG Ying-Xin, CHENG Shi-Hua, LOU Xiang-Yang, CAO Li-Yong, HONG Yong-Bo. Genetic dissection of the bacterial blight disease resistance in super hybrid rice RILs using genome-wide association study [J]. Acta Agronomica Sinica, 2022, 48(1): 121-137.
[8] XI Ling, WANG Yu-Qi, ZHU Wei, WANG Yi, CHEN Guo-Yue, PU Zong-Jun, ZHOU Yong-Hong, KANG Hou-Yang. Identification of resistance to wheat and molecular detection of resistance genes to wheat stripe rust of 78 wheat cultivars (lines) in Sichuan province [J]. Acta Agronomica Sinica, 2021, 47(7): 1309-1323.
[9] HAN Yu-Zhou, ZHANG Yong, YANG Yang, GU Zheng-Zhong, WU Ke, XIE Quan, KONG Zhong-Xin, JIA Hai-Yan, MA Zheng-Qiang. Effect evaluation of QTL Qph.nau-5B controlling plant height in wheat [J]. Acta Agronomica Sinica, 2021, 47(6): 1188-1196.
[10] JIANG Wei, PAN Zhe-Chao, BAO Li-Xian, ZHOU Fu-Xian, LI Yan-Shan, SUI Qi-Jun, LI Xian-Ping. Genome-wide association analysis for late blight resistance of potato resources [J]. Acta Agronomica Sinica, 2021, 47(2): 245-261.
[11] ZHANG Rong-Yue, WANG Xiao-Yan, YANG Kun, SHAN Hong-Li, CANG Xiao-Yan, LI Jie, WANG Chang-Mi, YIN Jiong, LUO Zhi-Ming, LI Wen-Feng, HUANG Ying-Kun. Identification of brown rust resistance and molecular detection of Bru1 gene in new and main cultivated sugarcane varieties [J]. Acta Agronomica Sinica, 2021, 47(2): 376-382.
[12] ZHANG Huan, LUO Huai-Yong, LI Wei-Tao, GUO Jian-Bin, CHEN Wei-Gang, ZHOU Xiao-Jing, HUANG Li, LIU Nian, YAN Li-Ying, LEI Yong, LIAO Bo-Shou, JIANG Hui-Fang. Genome-wide identification of peanut resistance genes and their response to Ralstonia solanacearum infection [J]. Acta Agronomica Sinica, 2021, 47(12): 2314-2323.
[13] HUANG Yi-Wen, DAI Xu-Ran, LIU Hong-Wei, YANG Li, MAI Chun-Yan, YU Li-Qiang, YU Guang-Jun, ZHANG Hong-Jun, LI Hong-Jie, ZHOU Yang. Relationship between the allelic variations at the Ppo-A1 and Ppo-D1 loci and pre-harvest sprouting resistance in wheat [J]. Acta Agronomica Sinica, 2021, 47(11): 2080-2090.
[14] CHE Yang, CHENG Shuang, TIAN Jin-Yu, TAO Yu, LIU Qiou-Yuan, XING Zhi-Peng, DOU Zhi, XU Qiang, HU Ya-Jie, GUO Bao-Wei, WEI Hai-Yan, GAO Hui, ZHANG Hong-Cheng. Characteristics and differences of rice yield, quality, and economic benefits under different modes of comprehensive planting-breeding in paddy fields [J]. Acta Agronomica Sinica, 2021, 47(10): 1953-1965.
[15] ZHAO Xu-Yang, YAO Fang-Jie, LONG Li, WANG Yu-Qi, KANG Hou-Yang, JIANG Yun-Feng, LI Wei, DENG Mei, LI Hao, CHEN Guo-Yue. Evaluation of resistance to stripe rust and molecular detection of resistance genes of 93 wheat landraces from the Qinghai-Tibet spring and winter wheat zones [J]. Acta Agronomica Sinica, 2021, 47(10): 2053-2063.
Full text



No Suggested Reading articles found!