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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (2): 262-274.doi: 10.3724/SP.J.1006.2021.04037


Genome-wide association analysis reveals zinc-tolerant loci of rapeseed at germination stage

WEI Li-Juan(), SHEN Shu-Lin, HUANG Xiao-Hu, MA Guo-Qiang, WANG Xi-Tong, YANG Yi-Ling, LI Huan-Dong, WANG Shu-Xian, ZHU Mei-Chen, TANG Zhang-Lin, LU Kun, LI Jia-Na*(), QU Cun-Min*()   

  1. College of Agronomy and Biotechnology, Southwest University / Chongqing Engineering Research Center for Rapeseed / Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China
  • Received:2020-02-18 Accepted:2020-04-15 Online:2021-02-12 Published:2020-12-25
  • Contact: LI Jia-Na,QU Cun-Min E-mail:lijuan525888@163.com;ljn1950@swu.edu.cn;drqucunmin@swu.edu.cn
  • Supported by:
    National Natural Science Foundation of China(31701460);Fundamental Research Funds for the Central Universities(XDJK2019C041);Fundamental Research Funds for the Central Universities(XDJK2020D023);Chongqing Basic Scientific and Advanced Technology Research(cstc2016shms-ztzx80010);Chongqing Basic Scientific and Advanced Technology Research(cstc2017jcyjAX0321);China Agricultural Research System(CARS-12);Intellectual Base for Discipline Innovation in Colleges and Universities(B12006)


Zinc (Zn) is one of the important mircroelements, but the excessive amount application would affect plant growth and development. Genome-wide association analysis (GWAS) was performed on the relative hypocotyl length (RHL) using the 140 B. napus genotyped under zinc stress treatment (30 mg L-1) at germination stage by Illumina 60K SNP array, and then significant SNP locus and candidate genes were detected. In the study, the population structure analysis revealed that the 140 B. napus were classified into two subgroups, and the kinship coefficients of the 89% materials were less than 0.1, indicating the tested population had a distant relationship. GWAS analysis indicated that there were significantly 8 SNP locus correlated to RHL, and single SNP loci could give an explanation on the 22.0%-33.2% phenotype variation. The differential expressed gene (DEGs) were detected by RNA-Seq. GO enrichment analysis indicated that the up-regulated genes mainly participated in redox reaction, ion transport, stress response, defense response and sulfur compound transport. Nineteen candidate genes response to zinc stress were identified by GWAS analysis and RNA-seq, including the genes encoding zinc finger protein (B-box type and ZFP1), glutathione transferase GSTU21, peroxidase family protein, ABC and MFS transporters, cell wall-related kinase protein, and genes encoding transcription factors (TF), such as BnaA07g27330D (MYB), BnaA02g30270D (bHLH), BnaA07g27840D (WRKY57), BnaA07g31860D (ORA47), and BnaA07g28000 (NAC). This study laid the foundation for understanding the molecular mechanism of zinc stress in B. napus.

Key words: Brassica napus, heavy metal, zinc stress, GWAS, germination stage

Table S1

Detailed information of the 140 B. napus accessions"

1 中双3号Zhongshuang 3 半冬性Semi-winter 中国浙江Zhejiang, China
2 镇油5号Zhenyou 5 半冬性Semi-winter 中国江苏Jiangsu, China
3 SWU46 半冬性Semi-winter 中国重庆Chongqing, China
4 WH-127 半冬性Semi-winter 中国湖北Hubei, China
5 WH-41 半冬性Semi-winter 中国湖北Hubei, China
6 WX10329 半冬性Semi-winter 中国湖南Hunan, China
7 JY-16 半冬性Semi-winter 中国湖北Hubei, China
8 黔油331 Qianyou 331 半冬性Semi-winter 中国贵州Guizhou, China
9 SWU47 半冬性Semi-winter 中国重庆Chongqing, China
10 浙双72 Zheshuang 72 半冬性Semi-winter 中国浙江Zhejiang, China
11 沪油17 Huyou 17 半冬性Semi-winter 中国上海Shanghai, China
12 中双7号Zhongshuang 7 半冬性Semi-winter 中国武汉Wuhan, China
13 WH-26 半冬性Semi-winter 中国湖北Hubei, China
14 Taisetsu 冬性Winter 日本Japan
15 M114 半冬性 Semi-winter 中国China
16 中油589 Zhongyou 589 半冬性Semi-winter 中国武汉Wuhan, China
17 农林43 Nonglin 43 冬性Winter 日本Japan
18 广德8104 Guangde 8104 半冬性Semi-winter 中国江苏Jiangsu, China
19 至尊Zhizun 半冬性Semi-winter 中国湖北Hubei, China
20 中双2号Zhongshuang 2 半冬性Semi-winter 中国湖北Hubei, China
21 中双4号Zhongshuang 4 半冬性Semi-winter 中国湖北Hubei, China
22 华油3号Huayou 3 半冬性Semi-winter 中国湖北Hubei, China
23 宁油14 Ningyou 14 半冬性Semi-winter 中国江苏Jiangsu, China
24 华油12 Huayou 12 半冬性Semi-winter 中国湖北Hubei, China
25 湖北白花油菜Hubei white flower rape 半冬性Semi-winter 中国湖北Hubei, China
26 WH-58 半冬性Semi-winter 中国湖北Hubei, China
27 699 半冬性Semi-winter 中国湖北Hubei, China
28 SWU63 半冬性Semi-winter 中国重庆Chongqing, China
29 WH-57 半冬性Semi-winter 中国湖北Hubei, China
30 苏油1号Shuyou 1 半冬性Semi-winter 中国江苏Jiangsu, China
31 WH-19 半冬性Semi-winter 中国湖北Hubei, China
32 中双4号Zhongshuang 4 半冬性Semi-winter 中国湖北Hubei, China
33 Nakate Chousen 春性Spring 朝鲜DPRK
34 广德761 Gaungde 761 半冬性Semi-winter 中国江苏Jiangsu, China
35 SWU110 半冬性Semi-winter 中国重庆Chongqing, China
36 7094 半冬性Semi-winter 中国湖北Hubei, China
37 SWU71 半冬性Semi-winter 中国重庆Chongqing, China
38 1111 半冬性Semi-winter 中国湖北Hubei, China
39 Erake 半冬性Semi-winter 波兰Poland
40 Campino 春性Spring 德国Germany
41 宁油10号 Ningyou 10 半冬性Semi-winter 中国江苏Jiangsu, China
42 中双11DH Zhongshuang 11DH 半冬性Semi-winter 中国湖北Hubei, China
43 浙双8号 Zheshuang 8 半冬性Semi-winter 中国浙江Zhejiang, China
44 cresor 春性Spring 法国France
45 浙油17 Zheyou 17 半冬性Semi-winter 中国浙江Zhejiang, China
46 华航901 Huahang 901 半冬性Semi-winter 中国湖北Hubei, China
47 Wesreo 春性Spring 澳大利亚Australia
48 南川长角 Nanchuansiliqua 半冬性Semi-winter 中国重庆Chongqing, China
49 J-917 半冬性Semi-winter 中国湖北Hubei, China
50 浙双6号 Zheshuang 6 半冬性Semi-winter 中国浙江Zhejiang, China
51 荣选 Rongxuan 半冬性Semi-winter 中国江苏Jiangsu, China
52 SWU106 半冬性Semi-winter 中国重庆Chongqing, China
53 D2 春性Spring 丹麦Denmark
54 豫油1号 Yuyou 1 半冬性Semi-winter 中国重庆Chongqing, China
55 WH-37 半冬性Semi-winter 中国湖北Hubei, China
56 J-951 半冬性Semi-winter 中国湖北Hubei, China
57 全紫油菜 Quanzi rape 春性Spring 中国江苏Jiangsu, China
58 SWU69 半冬性Semi-winter 中国重庆Chongqing, China
59 SWU60 半冬性Semi-winter 中国重庆Chongqing, China
60 丰油9号 Fengyou 9 半冬性Semi-winter 中国河南Henan, China
61 宁油1号 Ningyou 1 半冬性Semi-winter 中国湖北Hubei, China
62 SWU80 半冬性Semi-winter 中国重庆Chongqing, China
63 10-C29 半冬性Semi-winter 中国湖北Hubei, China
64 秦油5号 Qinyou 5 半冬性Semi-winter 中国陕西Shaanxi, China
65 Sophia 春性Spring 德国Germany
66 WaseChousen 春性Spring 朝鲜DPRK
67 Korina 春性Spring 德国Germany
68 J-915 半冬性Semi-winter 中国湖北Hubei, China
69 Bienvenu 半冬性Semi-winter 法国France
70 SWU102 半冬性Semi-winter 中国重庆Chongqing, China
71 漕泾胜利 Caojingshengli 半冬性Semi-winter 中国上海Shanghai, China
72 563 半冬性Semi-winter 中国湖南Hunan, China
73 皖油15号 Wanyou 15 半冬性Semi-winter 中国安徽Anhui, China
74 阳光198 Yangguang 198 半冬性Semi-winter 中国湖北Hubei, China
75 湘油13号 Xiangyou 13 半冬性Semi-winter 中国湖南Hunan, China
76 皖油16号 Wanyou 16 半冬性Semi-winter 中国安徽Anhui, China
77 华油13号 Huayou 13 半冬性Semi-winter 中国湖北Hubei, China
78 湘油15号 Xiangyou 15 半冬性Semi-winter 中国湖南Hunan, China
79 Tapidor 冬性Winter 法国France
80 10-C24 半冬性Semi-winter 中国湖北Hubei, China
81 圣光77 Shengguang 77 半冬性Semi-winter 中国湖北Hubei, China
82 史力丰 Shilifeng 半冬性Semi-winter 中国江苏Jiangsu, China
83 沪油3号 Huyou 3 半冬性Semi-winter 中国上海Shanghai, China
84 Santana 半冬性Semi-winter 中国China
85 10-C34 半冬性Semi-winter 中国湖北Hubei, China
86 11-Y7-117 半冬性Semi-winter 中国湖北Hubei, China
87 SWU99 半冬性Semi-winter 中国重庆Chongqing, China
88 宁油12 Ningyou 12 半冬性Semi-winter 中国江苏Jiangsu, China
89 Comet 春性Spring 瑞典Sweden
90 WH-20 半冬性Semi-winter 中国湖北Hubei, China
91 扬J6711 Yang J6711 半冬性Semi-winter 中国江苏Jiangsu, China
92 7191 半冬性Semi-winter 中国湖北Hubei, China
93 中双9号 Zhongshuang 9 半冬性Semi-winter 中国湖北Hubei, China
94 Daechosen 半冬性Semi-winter 朝鲜DPRK
95 Monty 半冬性Semi-winter 澳大利亚Australia
96 纬隆88 Weilong 88 半冬性Semi-winter 中国陕西Shanxi, China
97 沪油14 Huyou 14 半冬性Semi-winter 中国上海Shanghai, China
98 A117 半冬性Semi-winter 中国陕西Shaanxi, China
99 WH-15 半冬性Semi-winter 中国湖北Hubei, China
100 2011-7103 半冬性Semi-winter 中国湖北Hubei, China
101 SWU68 半冬性Semi-winter 中国重庆Chongqing, China
102 浙油18 Zheyou 18 半冬性Semi-winter 中国四川Zhejiang, China
103 Yan 81-2 半冬性Semi-winter 中国重庆Chongqing, China
104 2012-K8053 半冬性Semi-winter 中国湖北Hubei, China
105 淮油6号 Huaiyou 6 半冬性Semi-winter 中国江苏Jiangsu, China
106 2012-3546 半冬性Semi-winter 中国湖北Hubei, China
107 wx 10296 半冬性Semi-winter 中国湖南Hunan, China
108 2012-8380 半冬性Semi-winter 中国湖北Hubei, China
109 SWU92 半冬性Semi-winter 中国重庆Chongqing, China
110 农林42 Nonglin 42 半冬性Semi-winter 日本Japan
111 大花球 Dahuaqiu 半冬性Semi-winter 中国江苏Jiangsu, China
112 华油6号 Huayou 6 半冬性Semi-winter 中国湖北Hubei, China
113 CY12Q95406 半冬性Semi-winter 中国四川Sichuan, China
114 SWU49 半冬性Semi-winter 中国重庆Chongqing, China
115 SWU70 半冬性Semi-winter 中国重庆Chongqing, China
116 华双128 Huashuang 128 半冬性Semi-winter 中国湖北Hubei, China
117 皖油早 Wanyouzao 半冬性Semi-winter 中国安徽Anhui, China
118 宁油12 Ningyou 12 半冬性Semi-winter 中国江苏Jiangsu, China
119 滁油1号 Chuyou 1 半冬性Semi-winter 中国安徽Anhui, China
120 10-JP3 半冬性Semi-winter 中国湖北Hubei, China
121 2359 半冬性Semi-winter 中国湖北Hubei, China
122 宁油8号 Ningyou 8 半冬性Semi-winter 中国江苏Jiangsu, China
123 CY21PXW-84 半冬性Semi-winter 中国四川Sichuan, China
124 SWU88 半冬性Semi-winter 中国重庆Chongqing, China
125 Sida 春性Spring 加拿大Canada
126 川油20 Chuanyou 20 半冬性Semi-winter 中国四川Sichuan, China
127 沪油19 Huyou 19 半冬性Semi-winter 中国上海Shanghai, China
128 WH-62 半冬性Semi-winter 中国湖北Hubei, China
129 华油14 Huayou 14 半冬性Semi-winter 中国湖北Hubei, China
130 CY12GJ-1 半冬性Semi-winter 中国四川Sichuan, China
131 湘油11号 Xiangyou 11 半冬性Semi-winter 中国湖南Hunan, China
132 浙油601 Zheyou 601 半冬性Semi-winter 中国浙江Zhejiang, China
133 SWU108 半冬性Semi-winter 中国重庆Chongqing, China
134 CY14PXW-18 半冬性Semi-winter 中国四川Sichuan, China
135 Nca 半冬性Semi-winter 中国湖北Hubei, China
136 甘油5号 Ganyou 5 半冬性Semi-winter 中国湖北Hubei, China
137 SWU94 半冬性Semi-winter 中国重庆Chongqing, China
138 中油821 Zhongyou 821 半冬性Semi-winter 中国湖北Hubei, China
139 川油18 Chuanyou 18 半冬性Semi-winter 中国四川Sichuan, China
140 wx 10213 半冬性Semi-winter 中国湖北Hunan, China

Table 1

Hypocotyl length with different Zn(NO3)2 concentration solutions in B. napus "

Zn(NO3)2溶液浓度 Concentration of Zn(NO3)2 solutions (mg L-1)
0 5 10 15 20 30 50 70
1 5.76 4.46 4.74 5.82 3.78 2.54 2.54 1.68
2 4.38 4.38 4.02 3.16 2.38 2.54 2.52 2.08
3 6.80 6.64 5.02 6.02 4.34 2.62 2.24 2.34
4 7.60 7.66 6.64 5.20 4.20 3.14 2.76 2.14
5 6.70 6.28 5.24 4.32 3.24 3.20 2.84 1.80
6 6.25 5.88 5.13 4.90 3.59 2.81 2.58 2.01
7 7.90 6.30 8.40 6.52 5.88 5.46 4.84 2.60
8 5.90 7.98 8.64 4.50 4.08 4.58 4.64 2.40
9 6.30 7.90 7.10 5.60 6.54 4.50 3.74 2.40
10 6.96 7.08 8.06 5.73 6.01 4.86 4.94 2.91
平均值 Mean (cm) 6.45 6.46 6.30 3.78 3.58 2.48 3.36 2.24
标准差SD (cm) 1.00 1.29 1.68 1.17 1.25 0.87 1.07 0.37
变异系数 CV (%) 0.155 0.200 0.267 0.309 0.349 0.352 0.319 0.166

Table 2

Statistical analysis of the traits at germination stage under zinc stress"

性状 最小值 最大值 均值±标准差 变异系数 偏度 峰度
Trait Min.(cm) Max.(cm) Mean±SD CV (%) Skewness Kurtosis
CHL 3.66 7.99 5.77±0.92 15.85 -0.13 0.83
THL 2.28 6.47 4.24±0.80 18.84 0.41 0.02
RHL 0.38 1.08 0.73±0.13 17.57 0.28 0.15

Fig. 1

Frequency distribution of RHL under zinc stress in B. napus"

Fig. 2

Population structure and relative kinship diagram based on SNP markers A: plot of lnP(D) and ΔK; B: population structure profile (K = 2), the areas of the two colors (green and red) indicate the proportion of each subgroup, respectively; C: relative kinship diagram of 140 B. napus."

Fig. 3

QQ and Manhattan plots on RHL under zinc stress treatment in B. napus"

Table 3

Significant SNP locus associated with the relative hypocotyl length at germination stage under zinc stress in B. napus"

Position (bp)
-log10 (P)
R2 (%)
A02 22,075,111 2.97E-06 5.53 24.62
A07 20,094,111 3.97E-06 5.40 22.11
A07 22,001,673 3.49E-06 5.46 21.99
A07 23,402,490 7.70E-06 5.11 19.90
A07 23,555,825 2.92E-06 5.53 22.06
A07 23,580,640 7.50E-08 7.13 33.18
C04 4,456,230 3.12E-06 5.51 24.66
C06 36,835,784 2.55E-06 5.59 24.45

Fig. 4

LD distribution (A) and synteny analysis (B) in different distances in B. napus"

Fig. 5

Number of up-regulated and down-regulated transcription factors under zinc stress treatment in B. napus"

Fig. 6

Differentially up-regulated (A) and down-regulated (B) genes by GO enrichment analysis under zinc stress treatment in B. napus"

Table 4

Candidate genes of the traits correlated with zinc stress treatment in B. napus "

Candidate genes
Physical position
Homologs in Arabidopsis
Gene annotation
log2 (Fold change)
BnaA02g30040D Chr.A02: 21813781-21815282 AT5G48250 B-box型锌指蛋白
B-box type zinc finger protein with CCT domain
BnaA02g30270D Chr.A02: 21934212-21936672 AT5G48560 bHLH转录因子
Basic helix-loop-helix (bHLH) DNA-binding protein
BnaA07g27330D ChrA07: 19877781-19879164 AT1G68670 MYB转录因子
MYB-like transcription factor family protein
BnaA07g27340D Chr.A07: 19884616-19887579 AT1G68690 蛋白激酶家族
Protein kinase superfamily protein
BnaA07g27500D Chr.A07: 19996402-19997781 AT1G68850 过氧化物酶家族蛋白
Peroxidase superfamily protein
BnaA07g27840D Chr.A07: 20196357-20198149 AT1G69310 WRKY57转录因子
WRKY DNA-binding protein 57
BnaA07g28000D Chr.A07: 20266703-20267687 AT1G69490 NAC转录因子
NAC-like, activated by AP3/PI (NAP)
BnaA07g31860D Chr.A07: 22136736-22137327 AT1G74930 ERF转录因子 ORA47 3.71
BnaA07g34210D Chr.A07: 23311591-23312410 AT1G78360 谷胱甘肽转移酶 (GSTU21)
Glutathione S-transferase TAU 21 (GSTU21)
BnaA07g35030D Chr.A07: 23695006-23698790 AT1G79610 Na+/H+逆向转运蛋白 Na+/H+ antiporter 6 (NHX6) 2.29
BnaA07g35090D Chr.A07: 23714116-23714860 AT1G79680 类细胞壁相关激酶WALL
BnaA07g35350D Chr.A07: 23800896-23801571 AT1G80730 锌指蛋白
Zinc-finger protein 1 (ZFP1)
BnaC04g06210D Chr.C04: 4439046-4439940 AT3G55090 ABC转运蛋白
ABC-2 type transporter family protein
BnaC04g06300D Chr.C04: 4503767-4505873 AT2G39210 主要协助转运蛋白超家族
Major facilitator superfamily protein (MFS)
BnaC06g38840D Chr.C06: 36254140-36254958 AT1G78360 谷胱甘肽转移酶(GSTU21)
Glutathione S-transferase TAU 21 (GSTU21)
BnaC06g38850D Chr.C06: 36255467-36256984 AT1G78360 谷胱甘肽转移酶(GSTU21)
Glutathione S-transferase TAU 21 (GSTU21)
BnaC06g39970D Chr.C06: 36849441-36853390 AT1G79610 Na+/H+逆向转运蛋白 Na+/H+ antiporter 6 (NHX6) 4.01
BnaC06g40020D Chr.C06: 36867031-36869575 AT1G69730 细胞壁相关激酶蛋白
Wall-associated kinase family protein
BnaC06g40250D Chr.C06: 36958965-36959628 AT1G80730 锌指蛋白
Zinc-finger protein 1 (ZFP1)
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