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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (1): 121-137.doi: 10.3724/SP.J.1006.2022.02090

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Genetic dissection of the bacterial blight disease resistance in super hybrid rice RILs using genome-wide association study

ZHAO Hai-Han1(), LIAN Wang-Min1, ZHAN Xiao-Deng1, XU Hai-Ming3, ZHANG Ying-Xin1, CHENG Shi-Hua1, LOU Xiang-Yang1,*(), CAO Li-Yong1,2,*(), HONG Yong-Bo1,*()   

  1. 1China National Center for Rice Improvement and State Key Laboratory of Rice Biology / Zhejiang Key Laboratory of Superrice / China National Rice Research Institute, Hangzhou 311401, Zhejiang, China
    2Northern Rice Center, China National Rice Research Institute, Baoqing 155600, Hebei, China
    3Institute of Crop Science and Institute of Bioinformatics, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, Zhejiang, China
  • Received:2020-12-24 Accepted:2021-04-14 Online:2022-01-12 Published:2021-07-06
  • Contact: LOU Xiang-Yang,CAO Li-Yong,HONG Yong-Bo E-mail:haihan3354@163.com;louxiangyang01@caas.cn;caoliyong@caas.cn;hongyongbo@caas.cn
  • About author:First author contact:** Contributed equally to this work
  • Supported by:
    Natural Science Foundation of China(31961143016);Natural Science Foundation of China(31701338);National Key Research and Development Program(2018YFD0100806);Strategic Science and Technology Innovation Cooperation Project of the Ministry of Agriculture and Rural Affairs(2020FYE0202300)

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Abstract:

Bacterial blight caused by Xanthomonas oryzae pv. oryzae is the most destructive bacterial disease in rice production, and cultivating new disease-resistance variety by mining and utilizing the novel disease resistance genes is one of the most effective ways to control this disease. In our study, a population of 139 recombinant inbred lines (RILs) derived from super hybrid rice Xieyou 9308, between the parents of which there was genetic difference in resistance to bacterial blight, were inoculated with four Xoo strains. A genome-wide association study (GWAS) was carried out using 476,505 SNPs for the lesion length as a quantitative phenotype. The result revealed that a total of 109 significant SNPs including two genes encoding NBS-LRR containing proteins were detected to be significantly difference at P < 1×10-4 for four Xoo strains-treated lesions, accounting for phenotype variation of 59.78%-63.29%, respectively. Furthermore, 25 SNPs located in/nearby 19 candidate genes were identified by the CR4 inoculation, accounting for 61.00%. Relative expression analysis of two selected candidate genes, LOC_Os11g43420 and LOC_Os11g45930, demonstrated their higher expression levels in the resistant cultivar Zhonghui 9308 than in the susceptible variety Xieqingzao B, suggesting that these two genes might positively regulated bacterial blight resistance. Phylogenetic tree analysis indicated that these two genes were different from the previous cloned resistant genes in evolution, suggesting they were novel disease resistance genes. These results lays a theoretical basis and provides genetic resources for future resistant breeding in rice.

Key words: rice bacterial blight, GWAS, NBS-LRR, resistant breeding

Table 1

Phenotype of 139 RILs and two parents inoculated with four different Xoo strains"

Xoo菌株
Xoo strain		 年份/区域
Year/location		 协青早B病斑长度(P1)
Lesion length of XB (P1) (cm)		 中恢9308病斑长度(P2)
Lesion length of R9308 (P2) (cm)		 亲本差异(P1-P2)的显著性P值
Significant P-value of parental difference (P1-P2)		 重组自交系
Recombinant inbred line		 变异系数
CV (%)
均值±标准差
Mean ± SD (cm)		 变化范围
Range (cm)
PXO96 2019/Hangzhou 21.6 5.4 <0.001** 13.7±7.0 0.2-37.7 51.9
CR4 2019/Hangzhou 21.6 5.3 <0.001** 7.7±4.2 0.2-20.3 54.5
PXO61 2020/Hangzhou 19.4 0.2 0.002** 1.2±2.4 0-19.4 203.0
PXO99 2020/Hangzhou 10.4 0.8 <0.001** 5.6±3.6 0.1-21.8 64.2

Fig. 1

Phenotype and lesion length of XB/R9308 after inoculating of four Xoo strains A-D indicate the phenotype of XB and R9308 after inoculating of four Xoo strains (PXO96, CR4, PXO61, and PXO99) and measure the lesion length after 15 dpi (days post inoculation) and 21 dpi. Bar: 10 cm. E-H indicate the average lesion length after inoculating four Xoo strains of parents, respectively. Data presents are the mean ± SD from the independent experiments. **: P ≤ 0.01 (Student’s t-test)."

Fig. 2

Histogram of phenotypic frequency distribution for four Xoo strains in 139 RILs and two parents A-D come from four Xoo strains of PXO96, CR4, PXO61, and PXO99, respectively. The X-axis represents a mean lesion length, and the Y-axis represents the corresponding frequency. Black and red arrows mean the lesion length of R9308 and XB, respectively. Light grey line indicates the normal distribution curve."

Fig. 3

Bar chart of bacterial blight resistance levels for four Xoo strains in 139 RILs and two parents Number of accessions in the following reactions to four Xoo races: LL = 0 cm, 0 cm ≤ LL < 3 cm, LL/Total Leaf Length < 25%, LL/Total Leaf Length < 50%, LL/Total Leaf Length < 75%, and LL/Total leaf lesion represented resistant (level 0), highly resistant (level 1), moderately resistant (level 2), moderately susceptible (level 3), highly susceptible (level 4), and susceptible (level 5), respectively. LL indicates mean lesion length of each accession."

Fig. 4

Pattern of LD decay with average distance Figure shows that decay of LD (r2) with distance (kb) between SNPs."

Fig. 5

Genome-wide association study of lesion length after inoculating four Xoo strains in 139 RILs and two parents Manhattan plot (A-D) are plotted with the leaf lesion length after inoculating four Xoo strains of PXO96, CR4, PXO61, and PXO99, respectively. The X-axis represents the whole rice genome and the y-axis represents the -log10 (P-value). The blue line represents a Bonferroni corrected P-value. The orange line representing a stringent criterion of -log10 (P-value) > 4.0 under four environments was used for determining the association significance of four Xoo strains. Q-Q plot (E-H): E: PXO96; F: CR4; G: PXO61; H: PXO99. The horizontal axis of Q-Q plot (E-H) represents the expected -log10 (P-value) while the vertical axis is the observed -log10 (P-value). Red line is the cutoff line."

Table 2

Genome-wide significant association signals of bacterial blight resistance using three Xoo stains (P ≤ 1×10-4)"

菌株
Xoo		 SNP标记
SNP		 染色体
Chr.		 物理位置
Position		 P值
P-value		 基因名称(MSU)
Gene ID (MSU)		 基因注释
Gene annotation
CR4 11_26502942_C_A 11 26502942 1.71260×10-5 LOC_Os11g43890 WD domain, G-beta repeat domain containing protein, expressed
CR4 9_1843902_G_A 9 1843902 1.83954×10-5 LOC_Os09g03660 Retrotransposon protein, putative, unclassified, expressed
CR4 7_23436266_C_T 7 23436266 1.88459×10-5 LOC_Os07g39114 Expressed protein
CR4 7_23436267_C_G 7 23436267 1.88459×10-5
CR4 7_23436291_C_T 7 23436291 1.88459×10-5
CR4 5_1383235_C_A 5 1383235 1.92989×10-5 LOC_Os05g03360 Retrotransposon protein, putative, unclassified, expressed
CR4 7_23436858_C_T 7 23436858 2.13921×10-5 LOC_Os07g39114 Expressed protein
CR4 7_23436871_A_T 7 23436871 2.13921×10-5
CR4 8_26662359_G_A 8 26662359 2.44334×10-5 LOC_Os08g42210 Expressed protein
CR4 11_27792921_A_G 11 27792921 2.70257×10-5 LOC_Os11g45930 NBS-LRR type disease resistance protein, putative, expressed
CR4 11_26056269_A_G 11 26056269 2.90443×10-5 LOC_Os11g43200 Tropinone reductase 2, putative, expressed
CR4 2_11969901_C_T 2 11969901 3.20777×10-5 LOC_Os02g20330 Expressed protein
CR4 11_23030967_G_A 11 23030967 3.55194×10-5 LOC_Os11g38760 Retrotransposon protein, putative, LINE subclass, expressed
CR4 12_10252946_G_T 12 10252946 4.65692×10-5 LOC_Os12g17880 Armadillo/beta-catenin repeat protein-related, putative, expressed
CR4 11_26220673_C_T 11 26220673 5.00378×10-5 LOC_Os11g43420 LZ-NBS-LRR class RGA, putative, expressed
CR4 6_23077582_G_A 6 23077582 6.20380×10-5 LOC_Os06g38890 Transposon protein, putative, unclassified, expressed
CR4 11_26410429_C_A 11 26410429 6.81889×10-5 LOC_Os11g43740 OsMADS68 - MADS-box family gene with MIKC* type-box
CR4 11_25840166_C_A 11 25840166 7.97330×10-5 LOC_Os11g42900 Expressed protein
CR4 11_25849255_T_C 11 25849255 8.02272×10-5
CR4 6_23441121_G_C 6 23441121 8.04677×10-5 LOC_Os06g39470 Transferase family protein, putative, expressed
CR4 2_1831384_A_G 2 1831384 8.31200×10-5 LOC_Os02g04180 Transposon protein putative CACTA En/Spm sub-class expressed
CR4 4_3331408_G_A 4 3331408 8.31200×10-5 LOC_Os04g06374 Retrotransposon protein putative Ty3-gypsy subclass expressed
CR4 7_9599243_T_C 7 9599243 8.31200×10-5 LOC_Os07g16400 Retrotransposon protein putative Ty3-gypsy subclass expressed
CR4 8_20838490_G_A 8 20838490 9.02380×10-5 LOC_Os08g33410 Hypothetical protein
CR4 8_20838500_T_C 8 20838500 9.02380×10-5 LOC_Os02g21320 Retrotransposon protein putative unclassified expressed
PXO96 6_25611297_T_C 6 25611297 8.66084×10-7 LOC_Os10g05510
PXO96 5_14854774_G_A 5 14854774 3.83500×10-6 LOC_Os06g42010
PXO96 2_12653706_C_A 2 12653706 4.27352×10-6 LOC_Os03g35500 Expressed protein
PXO96 10_2723114_A_G 10 2723114 6.44760×10-6 LOC_Os10g20020 Expressed protein
PXO96 6_25220112_T_G 6 25220112 1.45559×10-5 LOC_Os06g37790 Transposon protein putative unclassified expressed
PXO96 3_19680871_T_C 3 19680871 2.49545×10-5 LOC_Os10g01510 Retrotransposon protein putative Ty3-gypsy subclass
PXO96 10_10043595_C_T 10 10043595 2.53663×10-5 LOC_Os03g28010 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO96 6_22366894_G_A 6 22366894 2.89696×10-5 LOC_Os06g42010 Expressed protein
PXO96 10_330955_C_T 10 330955 2.98270×10-5 LOC_Os06g42250 Transposon protein putative CACTA En/Spm sub-class expressed
PXO96 3_16101988_G_T 3 16101988 3.07716×10-5 LOC_Os06g42370 Retrotransposon protein putative unclassified expressed
PXO96 6_25219787_G_A 6 25219787 3.14674×10-5 LOC_Os06g33630 Transposon protein putative unclassified expressed
PXO96 6_25373580_A_G 6 25373580 3.85706×10-5 LOC_Os02g32680 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO96 6_25462404_C_T 6 25462404 4.00401×10-5 LOC_Os06g49185 Retrotransposon protein putative unclassified expressed
PXO96 6_19579269_C_T 6 19579269 4.66700×10-5 LOC_Os06g45410 Retrotransposon protein putative Ty3-gypsy subclass
PXO96 2_19389629_A_G 2 19389629 4.76090×10-5 LOC_Os06g42310 Lectin receptor-type protein kinase putative expressed
PXO96 6_29801791_T_C 6 29801791 4.82490×10-5 LOC_Os06g42010 Expressed protein
PXO96 6_27455797_A_T 6 27455797 5.46665×10-5 LOC_Os06g42370 MYB family transcription factor putative expressedMYB
PXO96 6_25409464_C_T 6 25409464 6.23488×10-5 LOC_Os07g33300 Beta-galactosidase precursor putative expressed
PXO96 6_25226687_G_C 6 25226687 6.81127×10-5 LOC_Os05g40940 Transposon protein putative unclassified expressed
PXO96 6_25465479_C_T 6 25465479 6.91484×10-5 LOC_Os06g41120 Retrotransposon protein putative unclassified expressed
PXO96 7_19906050_T_A 7 19906050 7.23635×10-5 LOC_Os02g32520 Expressed protein
PXO96 5_24009603_G_A 5 24009603 7.38552×10-5 LOC_Os06g42350 Retrotransposon protein putative unclassified expressed
PXO96 6_24594013_A_C 6 24594013 7.54406×10-5 LOC_Os06g42560 Expressed protein
PXO96 2_19249914_C_T 2 19249914 7.84868×10-5 LOC_Os06g42020 ERD1 protein chloroplast precursor putative expressed
PXO96 6_25451288_C_G 6 25451288 9.02863×10-5 LOC_Os06g42350 Transposon protein putative CACTA En/Spm sub-class expressed
PXO96 6_25592476_C_T 6 25592476 9.10497×10-5 LOC_Os06g42560 Tryptophan synthase beta chain 2 putative expressed
PXO96 6_25233994_G_A 6 25233994 9.17863×10-5 LOC_Os06g42020 CSLA9 - cellulose synthase-like family A expressed
PXO96 6_25446478_G_A 6 25446478 9.81605×10-5 LOC_Os06g42350 Transposon protein putative CACTA En/Spm sub-class expressed
PXO96 6_25226517_G_A 6 25226517 9.81690×10-5 LOC_Os06g42010 Transposon protein putative unclassified expressed
PXO96 6_25226850_C_T 6 25226850 9.81690×10-5
PXO96 6_28762618_T_C 6 28762618 9.93356×10-5 LOC_Os06g47500 Retrotransposon protein putative Ty3-gypsy subclass
PXO96 6_27492113_G_A 6 27492113 9.99334×10-5 LOC_Os06g45470 Expressed protein
PXO99 1_19343496_G_A 1 19343496 2.88795×10-7 LOC_Os01g34960 Retrotransposon putative centromere-specific
PXO99 1_29753419_G_A 1 29753419 2.88795×10-7 LOC_Os01g51740 Expressed protein
PXO99 1_33782923_T_C 1 33782923 2.88795×10-7 LOC_Os01g58444 Expressed protein
PXO99 2_5398259_G_A 2 5398259 2.88795×10-7 LOC_Os02g10280 Transposon protein putative unclassified expressed
PXO99 3_13482702_G_A 3 13482702 2.88795×10-7 LOC_Os03g23790 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 4_1315077_T_C 4 1315077 2.88795×10-7 LOC_Os04g03150 Retrotransposon protein putative unclassified expressed
PXO99 4_25911404_C_T 4 25911404 2.88795×10-7 LOC_Os04g43770 Expressed protein
PXO99 4_35500148_C_A 4 35500148 2.88795×10-7 LOC_Os04g59630 Prenylcysteine oxidase 1 precursor putative expressed
PXO99 7_26936907_G_A 7 26936907 2.88795×10-7 LOC_Os07g45120 Expressed protein
PXO99 8_10707525_C_A 8 10707525 2.88795×10-7 LOC_Os08g17480 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 9_13062864_A_G 9 13062864 2.88795×10-7 LOC_Os09g21580 OsFBX324 - F-box domain containing protein expressed
PXO99 10_770633_A_C 10 770633 2.88795×10-7 LOC_Os10g02220 Peptide transporter PTR2 putative expressed
PXO99 10_4768566_T_C 10 4768566 1.88802×10-6 LOC_Os10g08820 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 5_25082791_T_C 5 25082791 3.02499×10-6 LOC_Os05g43190 Expressed protein
PXO99 9_682155_C_T 9 682155 3.65396×10-6 LOC_Os09g01980 Retrotransposon protein putative unclassified expressed
PXO99 1_35729850_C_T 1 35729850 3.96584×10-6 LOC_Os01g61780 Vacuolar ATP synthase 98 kDa subunit putative expressed
PXO99 3_20089598_G_A 3 20089598 4.86058×10-6 LOC_Os03g36220 Retrotransposon protein putative unclassified expressed
PXO99 4_23009161_T_C 4 23009161 5.65336×10-6 LOC_Os04g38730 Hypothetical protein
PXO99 10_10280800_G_A 10 10280800 8.21681×10-6 LOC_Os10g20430 Transposon protein putative CACTA En/Spm sub-class expressed
PXO99 4_22488159_C_T 4 22488159 8.54439×10-6 LOC_Os04g37830 Retrotransposon protein putative unclassified expressed
PXO99 1_6763731_G_A 1 6763731 1.45237×10-5 LOC_Os01g12381 GDSL-like lipase/acylhydrolase putative expressed
PXO99 10_10622194_C_T 10 10622194 2.05682×10-5 LOC_Os10g20980 Transposon protein putative CACTA En/Spm sub-class expressed
PXO99 11_19490121_G_C 11 19490121 2.45252×10-5 LOC_Os11g32980 Transposon protein putative unclassified expressed
PXO99 6_15683763_C_T 6 15683763 2.50426×10-5 LOC_Os06g27700 Retrotransposon protein putative unclassified expressed
PXO99 2_11530742_G_A 2 115307424 2.50426×10-5 LOC_Os02g19710 Retrotransposon protein putative unclassified expressed
PXO99 8_14551707_C_T 8 14551707 2.58147×10-5 LOC_Os08g24080 Retrotransposon protein putative unclassified
PXO99 1_37300757_C_T 1 37300757 2.64067×10-5 LOC_Os01g64230 Long cell-linked locus protein putative expressed
PXO99 4_29550982_A_G 4 29550982 2.67698×10-5 LOC_Os04g49550 RING-H2 finger protein ATL2A putative expressed
PXO99 4_29550988_A_T 4 29550988 2.67698×10-5
PXO99 4_29550990_T_C 4 29550990 2.67698×10-5
PXO99 8_20326896_C_T 8 20326896 2.96673×10-5 LOC_Os08g32790 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 7_9714575_A_T 7 9714575 3.05773×10-5 LOC_Os07g16560 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 12_23369262_A_G 12 23369262 3.32972×10-5 LOC_Os12g38030 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 6_9880157_A_G 6 9880157 3.68628×10-5 LOC_Os06g17040 Retrotransposon protein putative unclassified expressed
PXO99 6_27238355_G_T 6 27238355 3.79721×10-5 LOC_Os06g45030 Transposon protein putative unclassified expressed
PXO99 10_2015605_G_A 10 2015605 3.98789×10-5 LOC_Os10g04290 Transposon protein putative CACTA En/Spm sub-class expressed
PXO99 10_2015606_T_C 10 2015606 3.98789×10-5
PXO99 10_2015616_T_C 10 2015616 3.98789×10-5
PXO99 7_9797928_A_T 7 9797928 4.00610×10-5 LOC_Os07g16710 Retrotransposon protein putative Ty3-gypsy subclass
PXO99 12_23610190_C_T 12 23610190 4.37810×10-5 LOC_Os12g38460 RNA recognition motif family protein expressed
PXO99 11_3704859_G_A 11 3704859 4.37973×10-5 LOC_Os11g07350 Expressed protein
PXO99 6_27238423_T_C 6 27238423 4.48254×10-5 LOC_Os06g45030 Transposon protein putative unclassified expressed
PXO99 6_27238426_A_G 6 27238426 4.48254×10-5 LOC_Os06g45030 Transposon protein putative unclassified expressed
PXO99 11_16720749_G_A 11 16720749 5.24152×10-5 LOC_Os11g28890 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 3_28507186_C_T 3 28507186 5.35983×10-5 LOC_Os03g49980 Retrotransposon protein putative unclassified expressed
PXO99 9_8088480_G_C 9 8088480 5.59333×10-5 LOC_Os09g13800 Retrotransposon protein putative Ty1-copia subclass expressed
PXO99 8_15034247_T_G 8 15034247 6.82446×10-5 LOC_Os08g24850 Retrotransposon putative centromere-specific expressed
PXO99 1_40956241_G_A 1 40956241 7.49332×10-5 LOC_Os01g70760 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 1_40956243_C_T 1 40956243 7.49332×10-5
PXO99 1_40956268_A_G 1 40956268 7.49332×10-5
PXO99 8_10707195_C_A 8 10707195 9.39077×10-5 LOC_Os08g17480 Retrotransposon protein putative Ty3-gypsy subclass expressed
PXO99 12_23610183_G_A 12 23610183 9.70588×10-5 LOC_Os12g38460 RNA recognition motif family protein expressed

Fig. 6

Relative expression profile of candidate genes A-D indicate the qRT-PCR results of four genes including SNP_11_ 26220673_C_T (P=5.00378×10-5), SNP_11_27792921_A_G (P=2.70257×10-5), SNP_ 6_25611297_T_C (P=8.66×10-7), and Xa21 respectively. The horizontal axis of each bar chart is the days post inoculation of Xoo strains “0” means the samples have not been inoculated; “1” means the samples have been inoculated for one day; “4” means the samples have been inoculated for four days. The inoculated leaves were collected from the same group at three different days with at least three biological repeats. The vertical axis is the relative expression level (folds) with actin as the internal reference gene. E indicates SNP polymorphism of three candidate genes (LOC_Os11g43420, LOC_Os11g45930, and LOC_Os06g42590) in coding sequence or promoter region. *: P ≤ 0.05 **: P ≤ 0.01 (Student’s t-test)."

Table 3

Cloned rice bacterial blight disease resistance genes"

R基因
R gene		 位点
Loci (MSU format)		 染色体
Chr.		 物理位置
Position		 参考文献
Reference
Xa1 LOC_Os04g53120 4 31638099-31644795 Yoshimura et al. [9]
Xa3/Xa26 LOC_Os11g47210 11 28399360-28402773 Sun et al. [13]
Xa4 LOC_Os11g46870 11 28142192-28148337 Sun et al. [14]
xa5 LOC_Os05g01710 5 437013-443270 Blair et al. [11];
Xa10 LOC_Os11g37570 11 22181556-22181152 Tian et al. [16]
xa13 LOC_Os08g42350 8 26728795-26725898 Chu et al. [10]
Xa21 LOC_Os11g35500 11 20802924-20806518 Song et al. [17 ];
Xa23 LOC_Os11g37620 11 22204676-22203734 Wang et al. [15 ]
Xa25 LOC_Os12g29220 12 17305326-17302073 Triplettl et al [55].
Xa27 LOC_Os06g39810 6 23654303-23653851 Gu et al. [12]
xa41(t) LOC_Os11g31190 11 18171678-18174478 Hutin et al. [6]

Fig. 7

Phylogenetic tree of bacterial blight candidate resistance genes in rice Neighbor-joining tree are constructed using MEGA based on multiple sequence alignments made by Clastal X. Selected protein names and MSU loci are as follows: LOC_Os11g43420, LOC_Os11g45930, LOC_Os11g32980, LOC_Os12g17880, Xa1, Xa3/Xa26, Xa4, xa5, Xa10, xa13, Xa21, Xa23, Xa25, Xa27, and xa41(t)."

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