Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (9): 1658-1673.doi: 10.3864/j.issn.0578-1752.2024.09.004

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• SPECIAL FOCUS: DROUGHT RESISTANCE IDENTIFICATION AND GENETIC RESOURCE MINING IN WHEAT • Previous Articles     Next Articles

Genome-Wide Association Study of Drought Tolerance at Seedling Stage in ICARDA-Introduced Wheat

ZHANG Ying1(), SHI TingRui1, CAO Rui1, PAN WenQiu1, SONG WeiNing1, WANG Li2(), NIE XiaoJun1()   

  1. 1 College of Agronomy, Northwest A&F University/State Key Laboratory for Crop Stress Resistance and High-Efficiency Production, Yangling 712100, Shaanxi
    2 Institute of Agricultural Resources and Environment, Shandong Academy of Agricultural Sciences/State Key Laboratory of Nutrient Use and Management, Ji’nan 250100
  • Received:2023-07-12 Accepted:2023-09-18 Online:2024-05-01 Published:2024-05-09
  • Contact: WANG Li, NIE XiaoJun

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Abstract:

【Objective】Drought is one of the most destructive environmental stresses limiting wheat production. The novel germplasm with excellent drought tolerance as well as their candidate loci were identified and characterized to enrich the genetic basis of drought tolerance and lay a material foundation for wheat genetic improvement in China. 【Method】In this study, the drought tolerance of 198 wheat accessions introduced from International Dry Area Agriculture Research (ICARDA) were investigated at seedling stage through hydroponic method with PEG6000 simulating drought. Drought tolerance index (DTI) was calculated using the shoot fresh weight, root fresh weight, total biomass and root-shoot ratio, respectively. Genome-wide association analysis was performed using 660K SNP array genotyping to obtain the SNP loci and chromosome regions associating with drought tolerance index. Combined with the expression patterns in root and other tissues, the potential candidate genes were identified, and then they were further verified by qRT-PCR approach with the most drought-tolerant accession IR214 and the most drought-sensitive accession IR36 as materials. Finally, the excellent haplotypes of key candidate genes were analyzed. 【Result】Compared to normal control condition, the growth and development of wheat were significantly impaired under drought treatment. There were also significant phenotypic variations among different accessions with all of the four traits displayed normal distribution. The coefficient of variation ranged from 0.363 to 0.760 with genetic diversity from 0.310 to 0.400. Using the weighted membership function value (D value), the drought tolerance of these accessions was evaluated. Results showed that accession IR214 had the highest D value with 0.851, followed by IR92, IR213, IR235, and IR218, which could be considered as the novel excellent drought-tolerance germplasm. Furthermore, through genome-wide association study (GWAS) analysis, a total of 102 loci were significantly associated with the DTI values based on these four traits, with the phenotypic variation explained value (PVE) from 1.07% to 38.70%, of which 60 loci were associated with above-ground fresh weight, 1 locus associated with underground fresh weight, 36 loci associated with biomass and the remaining 5 loci associated with root-shoot ratio. Then, 31 candidate genes were predicated based on genomic annotation information and LD block. Combined with the expression patterns of them in roots and other tissues, 4 candidates displaying differential expression between CK and drought conditions were obtained. Finally, the expression levels of these 4 candidates were further verified by qRT-PCR method with the most drought- tolerant accession IR214 and the most drought-sensitive accession IR36 as materials to obtain two key candidates associating with drought tolerance. Additionally, their haplotype effects were investigated. It was found that the different genotypes of AX-86174509 locus in TraesCS6A02G048600 gene showed significant differences in drought tolerance, which might be considered as a causal locus.【Conclusion】Totally, 102 loci and 2 key candidate genes (TraesCS5B02G053500 and TraesCS6A02G048600) underlying drought tolerance at seedling stage were detected in ICARDA-introduced wheat, and AX-86174509 in TraesCS6A02G048600 was a potential functional locus.

Key words: wheat, drought stress, 660K SNP array, genome-wide association analysis, candidate genes

Fig. 1

Investigation and statistics of phenotypic data of the 198 wheat accessions under drought stress A-D: Shoot fresh weight (SFW), root fresh weight (RFW), biomass (BIO) and root-shoot ratio (RSR) of 198 wheat cultivars under normal conditions and drought stress, respectively; E: Inhibition effect of drought stress on these wheat varieties (lines); F: Frequency distribution and correlation matrix of weighted membership function values (D values) of the drought tolerance coefficient indexes based on shoot fresh weight, root fresh weight, biomass and root-shoot ratio. *** represents a very significant difference of P<0.001. The same as below"

Table 1

Distribution of SNP markers, length of physical maps and their polymorphism"

色体
Chromosome 		SNP数目
No. of markers		 长度
Length (Mb)		 SNP标记密度
Density of SNP		 遗传多样性
Genetic diversity		 多态信息含量
PIC
1A 20417 594.02 0.03 0.54 0.35
2A 22864 780.77 0.03 0.68 0.40
3A 13916 750.73 0.02 0.59 0.37
4A 13577 744.65 0.02 0.62 0.38
5A 18446 709.76 0.03 0.64 0.39
6A 13496 617.99 0.02 0.59 0.37
7A 19497 736.69 0.03 0.54 0.35
1B 17527 689.38 0.03 0.57 0.37
2B 23450 801.26 0.03 0.59 0.37
3B 40010 830.70 0.05 0.51 0.34
4B 10870 673.44 0.02 0.62 0.38
5B 28406 713.02 0.04 0.63 0.39
6B 18994 720.95 0.03 0.59 0.37
7B 12898 750.61 0.02 0.57 0.36
1D 7703 495.61 0.02 0.56 0.36
2D 7149 651.81 0.01 0.64 0.39
3D 4834 651.53 0.01 0.45 0.31
4D 1954 509.91 0.00 0.56 0.36
5D 4873 565.98 0.01 0.56 0.36
6D 4698 720.95 0.01 0.57 0.36
7D 6617 638.46 0.01 0.52 0.34
A基因组A genome 122213 704.94 0.02 0.60 0.374428571
B基因组B genome 152155 739.91 0.03 0.58 0.368
D基因组D genome 37828 604.89 0.01 0.55 0.354
总计Total 312196 683.25 0.02 0.58 0.36547619

Fig. 2

Population structure of these 198 wheat accessions A: Cross validation of K-values of these 198 wheat accessions; B: The ancestry relationship of these 198 wheat accessions"

Table 2

SNP loci significantly associated with drought tolerance index at seedling stage and their phenotypic variation explained values (PVEs)"

性状
Character		 标记
Markers		 染色体
Chr.		 位置
Position (bp)		 P值
P value		 表型解释率
PVE (%)
地上部鲜重SFW AX-108729035 Chr.5B 569808382 4.27E-09 3.93
地上部鲜重SFW AX-108733337 Chr.5B 572139012 1.00E-08 11.84
地上部鲜重SFW AX-108759766 Chr.4A 583701435 9.82E-09 7.02
生物量BIO AX-108778026 Chr.4A 621846334 2.86E-08 17.18
生物量BIO AX-108783190 Chr.3D 611110400 1.74E-08 11.36
地上部鲜重SFW AX-108808371 Chr.5B 175234549 1.21E-10 11.17
生物量BIO AX-108834910 Chr.7D 617295870 6.10E-13 1.07
生物量BIO AX-108845700 Chr.5B 6647056 6.79E-09 2.57
生物量BIO AX-108854943 Chr.1B 629035301 8.72E-09 13.20
地上部鲜重SFW AX-108869016 Chr.3B 587178086 2.51E-08 14.18
地上部鲜重SFW AX-108900105 Chr.6B 467267816 3.14E-09 8.40
生物量BIO AX-108906545 Chr.3B 278404009 6.33E-10 11.21
地上部鲜重SFW AX-108914639 Chr.4A 602892400 3.12E-08 2.78
生物量BIO AX-108941515 Chr.3B 469534193 8.58E-09 2.66
地上部鲜重SFW AX-108941538 Chr.6A 614489969 1.38E-08 3.54
根冠比RSR AX-109084187 Chr.7A 690626229 1.51E-10 2.23
生物量BIO AX-109102300 Chr.6B 198063929 4.59E-09 10.14
地上部鲜重SFW AX-109284173 Chr.4A 613541932 2.93E-08 11.23
地上部鲜重SFW AX-109317181 Chr.3B 764180952 8.90E-09 34.66
生物量BIO AX-109350000 Chr.3B 415937806 6.22E-09 11.95
生物量BIO AX-109370689 Chr.7B 607425328 6.10E-13 4.92
根冠比RSR AX-109384491 Chr.7A 690193717 2.69E-10 2.43
生物量BIO AX-109394823 Chr5A 570133660 1.95E-08 7.23
地上部鲜重SFW AX-109395329 Chr.3B 350426152 1.34E-08 8.84
地上部鲜重SFW AX-109406330 Chr.7B 66821933 7.39E-09 21.61
地上部鲜重SFW AX-109442599 Chr.1A 574190347 5.57E-10 1.46
生物量BIO AX-109464813 Chr.2B 178867730 1.49E-08 1.66
生物量BIO AX-109483959 Chr.3A 597826146 8.32E-09 7.98
生物量BIO AX-109489650 Chr.6B 146700467 8.58E-09 11.84
生物量BIO AX-109495431 Chr.5B 593442274 4.01E-10 13.78
生物量BIO AX-109533280 Chr.2B 756707494 2.16E-09 13.36
地上部鲜重SFW AX-109549207 Chr.4A 569474177 6.19E-10 4.03
地上部鲜重SFW AX-109569380 Chr.5B 593660955 4.21E-09 4.29
生物量BIO AX-109926501 Chr.5B 611478805 6.31E-13 5.95
生物量BIO AX-109932327 Chr.7A 590944141 1.95E-08 9.99
根冠比RSR AX-109951696 Chr.5B 690361180 3.37E-10 4.98
地上部鲜重SFW AX-110008321 Chr.1B 462797045 2.70E-09 24.66
地上部鲜重SFW AX-110013665 Chr.3B 544902602 1.96E-08 1.89
生物量BIO AX-110019023 Chr.5B 404539089 2.14E-08 3.31
生物量BIO AX-110025532 Chr.7A 582132117 1.95E-08 2.13
地上部鲜重SFW AX-110039998 Chr.5B 607474823 1.07E-08 6.17
地上部鲜重SFW AX-110068305 Chr.2A 445576038 1.63E-08 8.21
地上部鲜重SFW AX-110091667 Chr.6B 712350186 1.52E-09 11.71
地上部鲜重SFW AX-110363991 Chr.5B 57981237 9.95E-11 17.72
生物量BIO AX-110365890 Chr.7A 612378254 9.99E-10 4.61
地上部鲜重SFW AX-110377479 Chr.5A 468466491 1.95E-12 1.89
地上部鲜重SFW AX-110419650 Chr.7A 608395311 1.07E-08 5.21
地上部鲜重SFW AX-110430526 Chr.3B 144807718 3.14E-09 4.75
地上部鲜重SFW AX-110462825 Chr.1A 577478241 4.27E-09 13.33
地上部鲜重SFW AX-110476280 Chr.3B 580060753 4.27E-09 8.75
地上部鲜重SFW AX-110483678 Chr.7B 159513174 1.72E-09 31.58
地上部鲜重SFW AX-110498186 Chr.4B 605731378 3.12E-08 13.40
地上部鲜重SFW AX-110500421 Chr.7A 588877976 4.27E-09 28.18
地上部鲜重SFW AX-110503277 Chr.4B 611433171 1.71E-10 9.61
地上部鲜重SFW AX-110535744 Chr.7B 568487694 4.27E-09 18.48
地上部鲜重SFW AX-110558355 Chr.2A 589689131 9.82E-09 1.36
生物量BIO AX-110652899 Chr.5B 58567089 1.43E-10 5.45
生物量BIO AX-110889119 Chr.3D 604125290 6.10E-13 5.87
地上部鲜重SFW AX-110919290 Chr.3B 414371305 1.93E-10 6.58
地上部鲜重SFW AX-110924463 Chr.1B 512424681 3.78E-09 38.70
地上部鲜重SFW AX-110973125 Chr.4A 725499434 4.73E-12 13.76
地上部鲜重SFW AX-110995410 Chr.2A 751057672 8.68E-11 4.21
生物量BIO AX-110999606 Chr.5B 578826261 1.95E-08 6.86
地上部鲜重SFW AX-111010056 Chr.7A 66985517 2.96E-08 3.028
生物量BIO AX-111022500 Chr.7B 728831779 7.53E-10 17.96
生物量BIO AX-111050362 Chr.7D 58626667 1.81E-09 36.01
生物量BIO AX-111058445 Chr.6A 570916695 1.51E-10 10.25
生物量BIO AX-111073918 Chr.7A 470125650 5.30E-09 27.74
生物量BIO AX-111092822 Chr.2B 576053662 1.41E-08 4.79
生物量BIO AX-111132848 Chr.5D 405255511 6.15E-10 13.92
地上部鲜重SFW AX-111160674 Chr.7D 615485527 2.23E-09 21.86
地上部鲜重SFW AX-111190021 Chr.3B 760130726 3.14E-09 6.19
地下部鲜重RFW AX-111192688 Chr.4A 468154775 1.04E-08 15.83
生物量BIO AX-111208168 Chr.5B 463995322 8.58E-09 9.026
地上部鲜重SFW AX-111212815 Chr.5A 582970887 9.82E-09 4.34
地上部鲜重SFW AX-111359770 Chr.7D 615445739 6.66E-09 4.61
生物量BIO AX-111464456 Chr.1A 48980552 2.11E-08 1.41
地上部鲜重SFW AX-111534081 Chr.4A 610334173 3.24E-08 22.12
地上部鲜重SFW AX-111564049 Chr.7B 224728151 3.17E-08 3.42
根冠比RSR AX-111590236 Chr.7A 690440732 1.39E-09 10.59
地上部鲜重SFW AX-111598552 Chr.3B 116099069 1.35E-08 32.51
地上部鲜重SFW AX-111629228 Chr.7A 572186228 2.62E-08 10.99
地上部鲜重SFW AX-111638609 Chr.5B 275345486 4.47E-09 1.79
地上部鲜重SFW AX-111652946 Chr.6A 615722618 3.12E-08 12.64
地上部鲜重SFW AX-111694379 Chr.2A 580854646 1.35E-08 34.63
地上部鲜重SFW AX-111730956 Chr.4A 664219507 6.37E-09 3.17
生物量BIO AX-111831025 Chr.2B 781926736 4.61E-09 1.13
地上部鲜重SFW AX-111903622 Chr.7D 58049133 3.86E-09 1.07
地上部鲜重SFW AX-86174509 Chr.6A 24829724 2.82E-09 6.40
地上部鲜重SFW AX-89491115 Chr.3B 564771130 8.34E-09 6.11
地上部鲜重SFW AX-89706493 Chr.3A 25500453 4.62E-09 11.81
根冠比RSR AX-94454511 Chr.5B 678515559 3.29E-08 4.01
地上部鲜重SFW AX-94654260 Chr.1D 462487722 3.14E-09 7.86
生物量BIO AX-94687724 Chr.2D 577152448 1.95E-08 13.82
地上部鲜重SFW AX-94757082 Chr.7A 436070614 4.62E-10 3.80
地上部鲜重SFW AX-94768083 Chr.5B 563121347 1.27E-08 23.89
地上部鲜重SFW AX-94784142 Chr.2A 194538621 2.01E-09 5.28
生物量BIO AX-94863274 Chr.2D 571058114 1.95E-08 6.86
地上部鲜重SFW AX-95149581 Chr.2D 590410753 1.09E-08 1.17
生物量BIO AX-108921937 Chr.1A 583127676 2.53E-08 7.37
地上部鲜重SFW AX-95244677 Chr.7A 575268359 4.27E-09 1.39
地上部鲜重SFW AX-95659704 Chr.6D 453012504 1.65E-08 7.25

Fig. 3

GWAS of the drought tolerance index (DTI) at seedling stage in 198 wheat accessions from ICARDA A: Manhattan map of the GWAS results of the shoot fresh weight (SFW), root fresh weight (RFW), biomass (BIO) and root-shoot ratio (RSR); Un: Unknown chromosome; B: QQ maps of the GWAS results of shoot fresh weight (SFW), root fresh weight (RFW), biomass (BIO) and root-shoot ratio (RSR)"

Table 3

Prediction of the candidate gene underlying drought tolerance"

位点
Marker		 物理位置
Position (bp)		 基因
Gene		 染色体
Chr.		 性状
Trait		 基因注释或编码蛋白
Gene annotation or coding proteins
AX-111464456 48980552 TraesCS1A02G066400 Chr.1A 生物量BIO 氧化还原酶Oxidoreductase activity
AX-94784142 194538621 TraesCS2A02G210600 Chr.2A 地上部鲜重SFW 锌离子结合蛋白Zinc ion binding
AX-111694379 580854646 TraesCS2A02G344200 Chr.2A 地上部鲜重SFW 果胶酯酶Pectinesterase activity
AX-110558355 589689131 TraesCS2A02G349800 Chr.2A 地上部鲜重SFW 跨膜转运蛋白Transmembrane transport
AX-109533280 756707494 TraesCS2B02G565400 Chr.2B 生物量BIO DUF952
AX-95149581 590410753 TraesCS2D02G493000 Chr.2D 地上部鲜重SFW 质子跨膜转运蛋白Proton transmembrane transport
AX-94863274 571058114 TraesCS2D02G464900 Chr.2D 生物量BIO Remorin_C
AX-94687724 577152448 TraesCS2D02G473700 Chr.2D 生物量BIO 转录调控酶Regulation of DNA-templated transcription
AX-89706493 25500453 TraesCS3A02G048000 Chr.3A 地上部鲜重SFW 含重金属转运/解毒蛋白结构域的蛋白Heavy metal
transport/detoxification protein domain containing protein
AX-109395329 350426152 TraesCS3B02G231600 Chr.3B 地上部鲜重SFW DUF632/DUF630
AX-89491115 564771130 TraesCS3B02G354300 Chr.3B 地上部鲜重SFW 果胶酯酶Pectinesterase activity
AX-111192688 468154775 TraesCS4A02G189100 Chr.4A 地下部鲜重RFW 水解酶Alpha/beta hydrolase fold
AX-108778026 621846334 TraesCS4A02G341700 Chr.4A 生物量BIO 蛋白激酶Protein kinase
AX-110377479 468466491 TraesCS5A02G252300 Chr.5A 地上部鲜重SFW 结合蛋白Nucleic acid binding
AX-110363991 57981237 TraesCS5B02G053200 Chr.5B 地上部鲜重SFW 分生组织发育相关Meristem maintenance
AX-94768083 563121347 TraesCS5B02G384300 Chr.5B 地上部鲜重SFW 防御响应Defense response
AX-109569380 593660955 TraesCS5B02G418100 Chr.5B 地上部鲜重SFW 翻译延长因子Translational elongation
AX-110039998 607474823 TraesCS5B02G432900 Chr.5B 地上部鲜重SFW 结合蛋白RNA binding
AX-94454511 678515559 TraesCS5B02G513600 Chr.5B RSR HAD家族Haloacid dehalogenase-like hydrolase
AX-109951696 690361180 TraesCS5B02G533900 Chr.5B 根冠比RSR 膜组成蛋白Integral component of membrane
AX-108845700 6647056 TraesCS5B02G005000 Chr.5B 生物量BIO GTP结合蛋白GTP binding
AX-110652899 58567089 TraesCS5B02G053500 Chr.5B 生物量BIO 气孔运动调节Regulation of stomatal movement
AX-86174509 24829724 TraesCS6A02G048600 Chr.6A 地上部鲜重SFW Crr6蛋白Crr6 protein
AX-110091667 712350186 TraesCS6B02G456000 Chr.6B 地上部鲜重SFW ATP结合蛋白ATP hydrolysis activity
AX-95659704 453012504 TraesCS6D02G362600 Chr.6D 地上部鲜重SFW AANH
AX-94757082 436070614 TraesCS7A02G308300 Chr.7A 地上部鲜重SFW 组蛋白甲基化修饰酶Histone methylation
AX-95244677 575268359 TraesCS7A02G396700 Chr.7A 地上部鲜重SFW 结合蛋白Protein binding
AX-110419650 608395311 TraesCS7A02G416300 Chr.7A 地上部鲜重SFW GGATC
AX-110365890 612378254 TraesCS7A02G421300 Chr.7A 生物量BIO 结合蛋白Protein binding
AX-110483678 159513174 TraesCS7B02G131900 Chr.7B 地上部鲜重SFW 催化酶Catalytic activity
AX-111160674 615485527 TraesCS7D02G514700 Chr.7D 地上部鲜重SFW 锌指蛋白Zinc finger protein

Fig. 4

The expression level and conserved domain analysis of the candidate drought-responsive genes A: The expression level of candidate genes; DR: The root tissue under drought stress; CR: The root tissue under control; DL: The leave tissue under drought stress; CL: The leave tissue under control; DC: The crown tissue under drought stress; CC: The crown tissue under control. B: Protein domains in the key genes"

Fig. 5

The expression patterns of the key drought-tolerant candidate genes by qRT-PCR analysis"

Fig. 6

Phenotypic differences in drought tolerance between two genotypes of the key candidate TraesCS6A02G048600 * represents a significant difference of P<0.05"

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