Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (11): 2249-2260.doi: 10.3864/j.issn.0578-1752.2021.11.001


Genome-Wide Association Analysis of Superoxide Dismutase (SOD) Activity in Wheat Grain

WANG JiQing1(),REN Yi1,SHI XiaoLei1,WANG LiLi1,ZHANG XinZhong2,SULITAN· GuZhaLiAYi1,XIE Lei1,GENG HongWei1()   

  1. 1College of Agriculture, Xinjiang Agricultural University/Key Laboratory of Agricultural Biological Technology, Urumqi 830052
    2Institute of Grain Crops, Xinjiang Academy of Agricultural Sciences, Urumqi 830091
  • Received:2020-10-31 Accepted:2020-12-28 Online:2021-06-01 Published:2021-06-09
  • Contact: HongWei GENG;


【Objective】The activity of superoxide dismutase (SOD) in wheat grains has a significant effect on the color and nutritional quality of wheat flour. Identification of associated loci and candidate genes for SOD activity in wheat grains is important for discovering the genetic mechanism of SOD activity in wheat grains and genetic improvement of wheat flour color. 【Method】The SOD activity of 212 common wheat varieties (lines) planted in 3 environments was detected by photoreduction method of nitro-blue tetrazolium (NBT), and the genome-wide association study (GWAS) of SOD activity in wheat grains was carried out by 16 705 high-quality SNP markers of 90K SNP chip, and candidate genes of significantly associated loci of stable inheritance were identified. 【Result】The phenotypic variation of SOD activity among wheat varieties (lines) was significant in different environments, with the coefficient of variation ranging from 4.34% to 5.23%, the correlation coefficient ranging from 0.60 to 0.90 (P<0.001). Polymorphic information content (PIC) ranging from 0.24 to 0.29 and the whole genome linkage disequilibrium (LD) attenuation distance of 7 Mb. The analysis of population structure showed that the tested materials could be divided into 3 subgroups. GWAS analysis showed that 29 loci (P≤0.001) were significantly associated with SOD activity, which were distributed on chromosomes 1A, 1B, 2A, 2B, 2D, 3B, 3D, 4B, 4D, 5A, 5B, 5D, 6A, 6B, 6D and 7B. A single locus can explain the phenotypic variation(R2) between 5.47% and 32.43%, of which 14 loci were detected in 2 or more environments. Nine significant associated loci were detected in three environments, distributed on chromosomes 1B, 2B, 4B, 5A, 5B, 6B and 6D, with a contribution rate of 6.21%-16.62%. SOD genes of TraesCS2B01G567600, TraesCS3D01G069900, TraesCS3D01G070200, TraesCS5B01G525700, TraesCS6A01G021400 and TraesCS6D01G431500, and SOD-activity-related candidate genes of TraesCS5A01G263500 and TraesCS6B01G707800 were used to identify the candidate genes of significantly associated loci of stable inheritance. The functions of the candidate genes were mainly related to the inhibition of cell reactive oxygen species accumulation and the participation in antioxidant regeneration. 【Conclusion】Twenty-nine SNP loci associated with SOD activity in wheat grains were detected, and 7 SOD genes and 2 candidate genes related to SOD activity were screened out.

Key words: wheat grain, SOD activity, genome-wide association study, SNP, candidate genes

Table 1

Statistical analysis of SOD activity of 212 winter wheat grains in different environments"

相关系数Correlation coefficient 遗传力
2016—2017 2017—2018 2018—2019
2016—2017 1784.14±73.31 1348.71—2025.14 4.34 0.79
2017—2018 1798.26±97.28 1316.83—2016.18 5.23 0.60***
2018—2019 1774.25±78.14 1348.26—2021.86 4.85 0.64*** 0.62***
均值Mean 1781.28±73.40 1407.32—1988.93 4.72 0.86*** 0.90*** 0.87***

Fig. 1

SOD activity distribution frequency of 212 winter wheat in different environments"

Table 2

SOD activity of winter wheat grains in different wheat regions"

来源 Origin
Northern winter
wheat region
Southwest winter wheat region
Huanghuai winter wheat region
Middle/lower reaches of the Yangtze River winter wheat region
Foreign varieties
2016—2017 1795.17 1782.41 1769.27 1733.88 1789.64
2017—2018 1804.36 1772.71 1790.38 1800.16 1800.91
2018—2019 1806.25 1799.82 1761.35 1747.94 1779.12
总计Total 1801.74 1787.21 1771.19 1759.67 1788.26

Table 3

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

No. of markers
Length (Mb)
Density of marker
Genetic diversity
1A 1262 592.38 0.47 0.32 0.26
1B 1293 688.60 0.53 0.34 0.27
1D 573 495.14 0.86 0.31 0.26
2A 1151 780.46 0.68 0.29 0.24
2B 1293 799.62 0.62 0.32 0.26
2D 481 650.94 1.35 0.31 0.25
3A 894 749.46 0.84 0.31 0.26
3B 1090 829.32 0.76 0.33 0.27
3D 234 613.92 2.62 0.29 0.24
4A 705 741.73 1.05 0.30 0.25
4B 571 672.56 1.18 0.32 0.26
4D 99 508.58 5.14 0.31 0.26
5A 960 709.43 0.74 0.36 0.29
5B 1157 712.82 0.62 0.35 0.28
5D 240 563.41 2.35 0.31 0.25
6A 1007 617.40 0.61 0.34 0.27
6B 1081 720.82 0.67 0.31 0.26
6D 319 472.61 1.48 0.31 0.25
7A 1174 736.44 0.63 0.30 0.25
7B 861 750.49 0.87 0.31 0.25
7D 260 637.17 2.45 0.29 0.24
A基因组 A genome 7153 4927.29 0.69 0.32 0.26
B基因组 B genome 7346 5174.23 0.70 0.33 0.27
D基因组 D genome 2206 3941.77 1.79 0.31 0.24
总计Total 16705 14043.30 0.84 0.32 0.26


Population structure analysis of 212 wheat varieties (lines) A: Estimation of ?K value in population; B: Group structure diagram"

Fig. 3

Manhattan plot and Q-Q plot of SOD activity in different environments E1: 2016-2017 environmental point; E2: 2017-2018 environmental point; E3: 2018-2019 environmental point; A: Average environment"

Table 4

SOD activity related loci detected by SNP-GWAS"

Position (bp)
P value
R2 (%)
Ex_c12584_2014 1A 435061794 A 5.77E-04 5.94
BS00109991_51 1A 536439240—536614333 A 7.90E-04—8.82E-04 7.02—7.07
Ra_c5683_2584 1A 551460924 A 9.44E-04 5.38
Kukri_c8533_1398 1B 49886407 E2 9.60E-04 8.43
Ra_c11303_359 1B 379383435 E2 9.78E-04 8.46
BS00022411_51 1B 629159210 E1/E3/A 2.88E-05—2.97E-04 8.93—11.10
Tdurum_contig92425_1574 2A 779977420 E2/A 6.80E-06—2.13E-04 8.52—16.45
BS00038217_51 2B 99961034 E1 6.35E-04 8.66
RFL_Contig1987_3440 2B 555840884 E1/E3/A 7.00E-05—3.92E-04 8.83—11.28
BS00026037_51 2B 793151228 E1/E3/A 1.24E-04—5.25E-04 14.23—16.62
BS00049876_51 2D 12891888 A 7.40E-04 7.36
Kukri_c40882_76 3B 19250811—19390877 E1 4.50E-04—6.44E-04 6.04—6.38
CAP8_c9373_277 3D 21005688 E1/A 3.13E-04—5.86E-04 5.81—6.81
Tdurum_contig12116_297 4B 60543887 E1/E3/A 4.52E-05—3.71E-04 8.40—10.97
Excalibur_c29496_799 4D 475027917 E1 3.96E-04 7.68
BS00022191_51 5A 476402782 E1/E3/A 6.11E-05—3.21E-04 8.57—10.77
BS00024602_51 5A 499660243 E3/A 2.64E-04—4.51E-04 26.29—32.43
Kukri_c14889_1086 5A 540052370—540611794 E1 3.04E-04—9.20E-04 6.22—9.17
tplb0061l23_1365 5B 506768500 A 6.90E-04 7.18
BobWhite_rep_c62475_70 5B 531199416 E1/E3/A 6.96E-05—5.30E-04 7.93—11.03
RAC875_c33791_320 5B 679804074 E1/E3/A 8.46E-06—7.05E-04 6.91—10.13
RAC875_c49940_385 5D 399290149 E1/A 3.21E-04—9.48E-04 5.37—6.69
RAC875_c13610_1239 6A 1497847—2402603 E2/A 8.61E-06—6.32E-04 6.29—17.00
BS00037162_51 6A 617689729 A 8.99E-04 7.93
BS00082893_51 6B 166226—169518 E2 2.24E-04—5.29E-04 13.18—13.22
Kukri_c49331_77 6B 664266146—667884621 E1/E3/A 4.25E-05—7.81E-04 6.21—11.61
Kukri_c338_109 6B 708660893 E3 7.10E-04 9.40%
Excalibur_c57840_227 6D 456465650 E1/E3/A 7.43E-05—4.78E-04 8.21—10.83
Kukri_c16814_103 7B 700830992 E1 9.32E-04 5.69

Table 5

Screening for candidate gene information"

Position (bp)
Gene annotation or coding protein
BS00026037_51 Chr.2B 758592689 TraesCS2B01G567600 超氧化物歧化酶Superoxide dismutase
CAP8_c9373_277 Chr.3D 30983003 TraesCS3D01G069900 铜、锌超氧化物歧化酶Superoxide dismutase [Cu-Zn]
31432328 TraesCS3D01G070200 铜、锌超氧化物歧化酶 Superoxide dismutase [Cu-Zn]
BS00022191_51 Chr.5A 476402782 TraesCS5A01G263500 锌指应激蛋白Zinc finger stress protein
BobWhite_rep_c62475_70 Chr.5B 531620481 TraesCS5B01G525700 铜、锌超氧化物歧化酶Superoxide dismutase [Cu-Zn]
551408544 TraesCS5B01G373700 铜、锌超氧化物歧化酶Superoxide dismutase [Cu-Zn]
RAC875_c13610_1239 Chr.6A 8971283 TraesCS6A01G021400 超氧化物歧化酶Superoxide dismutase
Kukri_c49331_77 Chr.6B 664393248 TraesCS6B01G707800 谷胱甘肽转移酶Glutathione transferase
Excalibur_c57840_227 Chr.6D 430047351 TraesCS6D01G431500 铜、锌超氧化物歧化酶Superoxide dismutase [Cu-Zn]
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