Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (8): 2056-2064    DOI: 10.1016/S2095-3119(20)63196-3
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Identification of blast-resistance loci through genome-wide association analysis in foxtail millet (Setaria italica (L.) Beauv.)
LI Zhi-jiang1, 2*, JIA Guan-qing3*, LI Xiang-yu2, LI Yi-chu4, ZHI Hui3, TANG Sha3, MA Jin-feng2, ZHANG Shuo3, LI Yan-dong2, SHANG Zhong-lin1, DIAO Xian-min1, 3 
1 College of Life Sciences, Hebei Normal University, Shijiazhuang 050024, P.R.China
2 Institute of Crop Breeding, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, P.R.China
3 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
4 Institute of Plant Protection, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      

由瘟病菌引起的瘟病造成世界上多种粮食作物严重减产,但是到目前为止,在禾本科作物中,对抗瘟病基因的遗传研究仍然有限。本研究利用888份谷子核心种质资源,在苗期接种谷瘟病菌株HN-1,通过GWAS方法,寻找抗谷瘟病位点。表型鉴定结果表明,谷子种质资源中高抗资源不到1.6%,中抗资源占35.25%,中感资源占57.09%,高感资源占6.08%。通过表型鉴定发现,在地理分布上,谷子生长季降雨量较高的地区高抗资源比例相对较高。利用覆盖谷子全基因组的720 000个SNP标记进行全基因组关联分析,在第2和第9条染色体上找到了2个显著的谷瘟病抗性相关位点,对这2个位点的分析找到了8个可能的抗病候选基因。这些结果为抗谷瘟病遗传育种和相关基因的克隆奠定了基础,也为其他作物抗瘟病育种和相关基础研究提供了指导信息。

Blast disease caused by the fungus Magnaporthe grisea results in significant yield losses of cereal crops across the world.  To date, very few regulatory genes contributing to blast resistance in grass species have been identified and the genetic basis of blast resistance in cereals remains elusive.  Here, a core collection of foxtail millet (Setaria italica) containing 888 accessions was evaluated through inoculation with the blast strain HN-1 and a genome-wide association study (GWAS) was performed to detect regulators responsible for blast disease resistance in foxtail millet.  The phenotypic variation of foxtail millet accessions inoculated with the blast strain HN-1 indicated that less than 1.60% of the samples were highly resistant, 35.25% were moderately resistant, 57.09% were moderately susceptible, and 6.08% were highly susceptible.  The geographical pattern of blast-resistant samples revealed that a high proportion of resistant accessions were located in lower latitude regions where the foxtail millet growing season has higher rain precipitation.  Using 720 000 SNP markers covering the Setaria genome, GWAS showed that two genomic loci from chromosomes 2 and 9 were significantly associated with blast disease resistance in foxtail millet.  Finally, eight putative genes were identified using rice blast-related transcriptomic data.  The results of this work lay a foundation for the foxtail millet blast resistance biology and provide guidance for breeding practices in this promising crop species and other cereals.
Keywords:   foxtail millet        blast resistance        core collection        GWAS  
Received: 04 February 2020   Accepted:
Fund: This research was supported by the National Key R&D Program of China (2018YFD1000706 and 2018YFD1000700), the National Natural Science Foundation of China (31871630 and 31771807), the earmarked fund for China Agriculture Research System of MOF and MARA (CARS-06-13.5), the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences, and the Heilongjiang Academy of Agricultural Sciences Research Program, China (2018JJPY005).
Corresponding Authors:  Correspondence DIAO Xian-min, Tel/Fax: +86-10-62126889, E-mail:    
About author:  * These authors contributed equally to this study.

Cite this article: 

LI Zhi-jiang, JIA Guan-qing, LI Xiang-yu, LI Yi-chu, ZHI Hui, TANG Sha, MA Jin-feng, ZHANG Shuo, LI Yan-dong, SHANG Zhong-lin, DIAO Xian-min. 2021. Identification of blast-resistance loci through genome-wide association analysis in foxtail millet (Setaria italica (L.) Beauv.). Journal of Integrative Agriculture, 20(8): 2056-2064.

Austin D F. 2006. Foxtail millets (Setaria: Poaceae) - abandoned food in two hemispheres. Economic Botany, 60, 143–158.
Churchill G A, Doerge R W. 1994. Empirical threshold values for quantitative trait mapping. Genetics, 138, 963–971.
Couch B C, Fudal I, Lebrun M H, Tharreau D, Valent B, van Kim P, Notteghem J L, Kohn L M. 2005. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics, 170, 613–630.
Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z. 2017. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science, 355, 962–965.
Diao X, Schnable J, Bennetzen J L, Li J. 2014. Initiation of Setaria as a model plant. Frontiers of Agricultural Science & Engineering, 1, 16–20.
Doust A, Diao X M. 2017. Genetics and Genomics of Setaria. Springer International Publishing, Switzerland.
Farfan I D, De La Fuente G N, Murray S C, Isakeit T, Huang P C, Warburton M, Williams P, Windham G L, Kolomiets M. 2015. Genome wide association study for drought, aflatoxin resistance, and important agronomic traits of maize hybrids in the sub-tropics. PLoS ONE, 10, e0117737.
Feng Z, Kang H, Li M, Zou L, Wang X, Zhao J, Wei L, Zhou N, Li Q, Lan Y, Zhang Y, Chen Z, Liu W, Pan X, Wang G, Zuo S. 2019. Identification of new rice cultivars and resistance loci against rice black-streaked dwarf virus disease through genome-wide association study. Rice, 12, 49.
Hoang G T, Van Dinh L, Nguyen T T, Ta N K, Gathignol F, Mai C D, Jouannic S, Tran K D, Khuat T H, Do V N, Lebrun M, Courtois B, Gantet P. 2019. Genome-wide association study of a panel of vietnamese rice landraces reveals new QTLs for tolerance to water deficit during the vegetative phase. Rice, 12, 4.
Huang X, Zhao Y, Wei X, Li C, Wang A, Zhao Q, Li W, Guo Y, Deng L, Zhu C, Fan D, Lu Y, Weng Q, Liu K, Zhou T, Jing Y, Si L, Dong G, Huang T, Lu T, et al. 2012. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nature Genetics, 44, 32–41.
Hwang E Y, Song Q, Jia G, Specht J E, Hyten D L, Costa J, Cregan P B. 2014. A genome-wide association study of seed protein and oil content in soybean. BMC Genomics, 15, 1.
Jia G, Huang X, Zhi H, Zhao Y, Zhao Q, Li W, Chai Y, Yang L, Liu K, Lu H, Zhu C, Lu Y, Zhou C, Fan D, Weng Q, Guo Y, Huang T, Zhang L, Lu T, Feng Q, et al. 2013. A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nature Genetics, 45, 957–961.
Kato H, Yamamoto M, Yamaguchi-Ozaki T, Kadouchi H, Iwamoto Y, Nakayashiki H, Tosa Y, Yayama S, Mori N. 2000. Pathogenicity, mating ability and DNA restriction fragment length polymorphisms of Pyricularia populations isolated from Gramineae, Bambusideae and Zingiberaceae plants. Journal of General Plant Pathology, 66, 30–47.
Li B, Zhang H, Yang X, Lv Y, Jiang P, Hao Z, Lv X, Wang H, Weng J. 2013. Genome-wide association study and candidate gene prediction of ear height in maize (Zea mays L.). Crops, 2, 35–40.
Li C, Wang D, Peng S, Chen Y, Su P, Chen J, Zheng L, Tan X, Liu J, Xiao Y, Kang H, Zhang D, Wang G, Liu Y. 2019. Genome-wide association mapping of resistance against rice blast strains in South China and identification of a new Pik allele. Rice, 12, 47.
Li W, Liu Y, Wang J, He M, Zhou X, Yang C, Yuan C, Wang J, Chern M, Yin J, Chen W, Ma B, Wang Y, Qin P, Li S, Ronald P, Chen X. 2016. The durably resistant rice cultivar Digu activates defense gene expression before the full maturation of Magnaporthe oryzae appressorium. Molecular Plant Pathology, 17, 354–368.
Li W, Zhu Z, Chern M, Yin J, Yang C, Ran L, Cheng M, He M, Wang K, Wang J, Zhu X, Chen Z, Wang J, Zhao W, Ma B, Qin P, Chen W, Wang Y, Liu J, Wang W, et al. 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell, 170, 114–126.
Li Z, Jia G, Li X, Li Y, Ma J, Zhi H, Tang S, Zhang S, Chai Y, Li Y, Diao X. 2016. Determination of standard varieties for identifying physiological races of foxtail millet blast fungus. Scientia Agricultura Sinica, 49, 3308–3318. (in Chinese)
Liang P, Li Y, Shen L. 1959. Studies on millet blast caused by Piricularia setariae Nishikado. Acta Phytopathologica Sinica, 5, 89–99. (in Chinese)
Liu H, Lin R, Xu A, Yang S, Li Z. 1990. Identification of millet blast resistance to foxtail millet germplasm resoures. Shanxi Agricultural Sciences, 3, 24–25. (in Chinese)
Liu P, Jin Y, Liu J, Liu C, Yao H, Luo F, Guo Z, Xia X, He Z. 2019. Genome-wide association mapping of root system architecture traits in common wheat (Triticum aestivum L.). Euphytica, 215, 121.
Lu P. 2006. Descriptors and Data Standard for Foxtail Millet Setaria Italica (L.) Beuauv.]. China Agriculture Press, Beijing. p. 18. (in Chinese)
de Oliveira L F V, Christoff A P, de Lima J C, de Ross B C F, Sachetto-Martins G, Margis-Pinheiro M, Margis R. 2014. The wall-associated Kinase gene family in rice genomes. Plant Science, 229, 181–192.
Ou S H. 1987. Rice Diseases Surrey. The Commonwealth Mycological Institute, China. pp. 109–201. (in Chinese)
Samayoa L F, Malvar R A, Olukolu B A, Holland J B, Butron A. 2015. Genome-wide association study reveals a set of genes associated with resistance to the Mediterranean corn borer (Sesamia nonagrioides L.) in a maize diversity panel. BMC Plant Biology, 15, 35.
Tosa Y, Chuma I. 2014. Classification and parasitic specialization of blast fungi. Journal of General Plant Pathology, 80, 202–209.
Tosa Y, Tamba H, Tanaka K, Mayama S. 2006. Genetic analysis of host species specificity of Magnaporthe oryzae isolates from rice and wheat. Phytopathology, 96, 480–484.
Turner S D. 2014. qqman: An R package for visualizing GWAS results using QQ and manhattan plots. Biorxiv, 005165.
Valent B, Khang C H. 2010. Recent advances in rice blast effector research. Current Opinion in Plant Biology, 13, 434–441.
Wang C, Yang Y, Yuan X, Xu Q, Feng Y, Yu H, Wang Y, Wei X. 2014. Genome-wide association study of blast resistance in indica rice. BMC Plant Biology, 14, 311.
Wang Y, Chu J, Song Y, Xie S, Yan W, Jin L, Liu H, Xie S. 1985. Screening tests of millet varieties for resistance to blast pathogen. Acta Phytophylacica Sinica, 12, 175–180. (in Chinese)
Weng J, Xie C, Hao Z, Wang J, Liu C, Li M, Zhang D, Bai L, Zhang S, Li X. 2011. Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS ONE, 6, e29229.
Wu X. 1985. A preliminary study on the identification and screening of Millet Blast. Heilongjiang Agricultural Sciences, 46–50. (in Chinese)
Xiao N, Wu Y, Pan C, Yu L, Chen Y, Liu G, Li Y, Zhang X, Wang Z, Dai Z, Liang C, Li A. 2017. Improving of rice blast resistances in japonica by pyramiding major R genes. Frontiers in Plant Science, 7, 1918.
Xie S, Yan W, Jin X, Liu H, Hu J. 1984. A preliminary study on the varieties from Jilin Province resistance to Millet Blast. Jilin Agricultural Sciences, 2, 74–77. (in Chinese)
Yan W, Xie S, Jin X, Liu H, Hu J. 1985. A preliminary study on the physiological races of Millet Blast (Piricularia setariae Nishikado). Scientia Agricultura Sinica, 18, 57–62. (in Chinese)
Yan W, Xie S, Liu H, Li N. 1988. Evaluation for the specialized resistance of millet germplasm resources and elite Chinese varieties to Millet Blast in Jilin Province. Jilin Agricultural Sciences, 1, 6–10. (Chinese)
Yang K, Qi L, Zhang Z. 2014. Isolation and characterization of a novel wall-associated kinase gene TaWAK5 in wheat (Triticum aestivum). The Crop Journal, 2, 255–266.
Yang X, Zhang J, Perry L, Ma Z, Wan Z, Li M, Diao X, Lu H. 2012. From the modern to the archaeological: Starch grains from millets and their wild relatives in China. Journal of Archaeological Science, 39, 247–254.
Ye X, Li J, Cheng Y, Yao F, Long L, Wang Y, Wu Y, Li J, Wang J, Jiang Q, Kang H, Li W, Qi P, Lan X, Ma J, Liu Y, Jiang Y, Wei Y, Chen X, Liu C, et al. 2019. Genome-wide association study reveals new loci for yield-related traits in Sichuan wheat germplasm under stripe rust stress. BMC Genomics, 20, 640.
You Q, Zhang L, Yi X, Zhang Z, Xu W, Su Z. 2015. SIFGD: Setaria italica functional genomics database. Molecular Plant, 8, 967–970.
Zhang P, Zhong K, Zhong Z, Tong H. 2019. Genome-wide association study of important agronomic traits within a core collection of rice (Oryza sativa L.). BMC Plant Biology, 19, 259–271.
Zhao H, Wang X, Jia Y, Minkenberg B, Wheatley M, Fan J, Jia M H, Famoso A, Edwards J D, Wamishe Y, Valent B, Wang G, Yang Y. 2018. The rice blast resistance gene Ptr encodes an atypical protein required for broad-spectrum disease resistance. Nature Communications, 9, 2039.
Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B, Xing Y, Zhang B, Liu H, Fengler K A, Zhao J, Zhao X, Chen Y, Lai J, Yan J, Xu M. 2015. A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics, 47, 151–157.
[1] ZHANG Hua, WU Hai-yan, TIAN Rui, KONG You-bin, CHU Jia-hao, XING Xin-zhu, DU Hui, JIN Yuan, LI Xi-huan, ZHANG Cai-ying. Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of phosphorus utilization in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2521-2537.
[2] XU Xin, YE Jun-hua, YANG Ying-ying, LI Ruo-si, LI Zhen, WANG Shan, SUN Yan-fei, ZHANG Meng-chen, XU Qun, FENG Yue, WEI Xing-hua, YANG Yao-long. Genetic diversity analysis and GWAS reveal the adaptive loci of milling and appearance quality of japonica (oryza sativa L.) in Northeast China[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1539-1550.
[3] SHI Mei-qi, LIAO Xi-liang, YE Qian, ZHANG Wei, LI Ya-kai, Javaid Akhter BHAT, KAN Gui-zhen, YU De-yue. Linkage and association mapping of wild soybean (Glycine soja) seeds germinating under salt stress[J]. >Journal of Integrative Agriculture, 2022, 21(10): 2833-2847.
[4] WU Ping-xian, ZHOU Jie, WANG Kai, CHEN De-juan, YANG Xi-di, LIU Yi-hui, JIANG An-an, SHEN Lin-yuan, JIN Long, XIAO Wei-hang, JIANG Yan-zhi, LI Ming-zhou, ZHU Li, ZENG Yang-shuang, XU Xu, QIU Xiao-tian, LI Xue-wei, TANG Guo-qing. Identifying SNPs associated with birth weight and days to 100 kg traits in Yorkshire pigs based on genotyping-by-sequencing[J]. >Journal of Integrative Agriculture, 2021, 20(9): 2483-2490.
[5] ZHANG Zhe, CHEN Zi-tao, DIAO Shu-qi, YE Shao-pan, WANG Jia-ying, GAO Ning, YUAN Xiao-long, CHEN Zan-mou, ZHANG Hao, LI Jia-qi. Identifying the complex genetic architecture of growth and fatness traits in a Duroc pig population[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1607-1614.
[6] NIE Xing-hua, WANG Ze-hua, LIU Ning-wei, SONG Li, YAN Bo-qian, XING Yu, ZHANG Qing, FANG Ke-feng, ZHAO Yong-lian, CHEN Xin, WANG Guang-peng, QIN Ling, CAO Qing-qin. Fingerprinting 146 Chinese chestnut (Castanea mollissima Blume) accessions and selecting a core collection using SSR markers[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1277-1286.
[7] Sher MUHAMMAD, Muhammad SAJJAD, Sultan Habibullah KHAN, Muhammad SHAHID, Muhammad ZUBAIR, Faisal Saeed AWAN, Azeem Iqbal KHAN, Muhammad Salman MUBARAK, Ayesha TAHIR, Muhammad Umer, Rumana KEYANI, Muhammad Inam AFZAL, Irfan MANZOOR, Javed Iqbal WATTOO, Aziz-ur REHMAN. Genome-wide association analysis for stripe rust resistance in spring wheat (Triticum aestivum L.) germplasm[J]. >Journal of Integrative Agriculture, 2020, 19(8): 2035-2043.
[8] XIAO Wu-ming, PENG Xin, LUO Li-xin, LIANG Ke-qin, WANG Jia-feng, HUANG Ming, LIU Yong-zhu, GUO Tao, LUO Wen-long, YANG Qi-yun, ZHU Xiao-yuan, WANG Hui, CHEN Zhi-qiang. Development of elite restoring lines by integrating blast resistance and low amylose content using MAS[J]. >Journal of Integrative Agriculture, 2018, 17(01): 16-27.
[9] XIE Li-na, CHEN Ming, MIN Dong-hong, FENG Lu, XU Zhao-shi, ZHOU Yong-bin, XU Dong-bei, LI Lian-cheng, MA You-zhi, ZHANG Xiao-hong. The NAC-like transcription factor SiNAC110 in foxtail millet (Setaria italica L.) confers tolerance to drought and high salt stress through an ABA independent signaling pathway[J]. >Journal of Integrative Agriculture, 2017, 16(03): 559-571.
No Suggested Reading articles found!