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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (2): 175-187.doi: 10.3724/SP.J.1006.2019.84093


Genome-wide association of roots, hypocotyls and fresh weight at germination stage under as stress in Brassica napus L.

Cun-Min QU1,2,Guo-Qiang MA1,2,Mei-Chen ZHU1,2,Xiao-Hu HUANG1,2,Le-Dong JIA1,2,Shu-Xian WANG1,2,Hui-Yan ZHAO1,2,Xin-Fu XU1,2,Kun LU1,2,Jia-Na LI1,2,*(),Rui WANG1,2,*()   

  1. 1 College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China
    2 Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China
  • Received:2018-07-05 Accepted:2018-10-08 Online:2019-02-12 Published:2018-11-06
  • Contact: Jia-Na LI,Rui WANG E-mail:ljn1950@swu.edu.cn;ruiwang71@163.com
  • Supported by:
    This study was supported by the National Key Research and Development Plan(2018YFD0100505);the National Natural Science Foundation of China(31401412);the National Natural Science Foundation of China(31571701);Chongqing Basic Scientific and Advanced Technology Research(cstc2015jcyjBX0001);Chongqing Basic Scientific and Advanced Technology Research(cstc2016shms-ztzx80010);Chongqing Basic Scientific and Advanced Technology Research(cstc2017jcyjAX0321);the China Agriculture Research System(CARS-12);the 111 Project(B12006);and the Fundamental Research Funds for the Central Universities(XDJK2016A005);and the Fundamental Research Funds for the Central Universities(XDJK2016B030)


Brassica napus is an optimum crop for repairing the heavy metal pollution of soil. To identify the associated SNP locus and candidate genes with arsenic (As) stress tolerance in B. napus, we measured and performed genome-wide association studies (GWAS) on relative root length (RRL), relative hypocotyl length (RHL), and relative fresh weight (RFW) of 140 rapeseed accessions by the Brassica 60K Illumina Infinium SNP array. In total, 15 SNPs significantly associated with RRL, 20 loci with RHL, and 35 SNP with RFW were identified, and each of SNP explained 13.31%-24.39%, 18.04%-33.82%, and 20.19%-25.06% of observed phenotypic variation, respectively. The most notable significant SNPs were located on chromosomes A02, A07, and C02, which were repeatedly detected and associated with RRL, RHL, and RFW simultaneously. Based on the rapeseed genome annotation of the linkage disequilibrium (LD) regions, we predicted 61 As resistance of candidate genes, among them, PHT3;3, PHT1;9, GST, OTC5, NRAMP1, and ZIP12, were related to the heavy metal absorbing and transporting. With the results of qRT-PCR, the PHT3;3 and PHT1;9 were obviously induced by As stress treatment in roots, hypocotyls and leaves, indicating that they were the important candidate genes related to As absorption and transport in B. napus. These results provide a reference for elucidating the regulation mechanism of candidate genes and improving agronomic traits in B. napus under As stress.

Key words: Brassica napus L., As stress resistance, genome-wide association studies (GWAS), candidate genes

Table 1

Primers sequences of candidate genes for qRT-PCR"

Gene name
Gene ID
Sequences of primers (5'-3')
BnaPHT1;9 BnaA07g32730D, BnaA07g32740D,
BnaGSTU25 BnaA09g45070D, BnaA09g45080D,
BnaACTIN7 BnaA03g55890D, BnaC02g00690D,

Table 2

Statistical analysis of traits of B. napus seedlings at germination stage under As stress"

材料数Number of accessions 均值±标准差Mean±SD 最小值Minimum 中位数Median 最大值Maximum 偏度
CV (%)
相关系数Correlation coefficient
CRL 140 8.898±2.306 1.410 9.065 15.800 -0.135 0.958 25.91 0.986**
TRL 137 7.823±2.226 0.610 7.767 13.386 -0.571 1.053 28.91
RRL 137 0.903±0.280 0.061 0.876 1.686 0.409 0.950 31.09
CHL 140 5.735±0.968 2.680 5.695 7.990 -0.338 1.036 16.87 0.995**
THL 137 4.453±0.792 1.755 4.473 6.477 -0.155 1.060 17.79
RHL 137 0.793±0.163 0.257 0.779 1.437 0.816 3.165 20.62
CFW 140 0.056±0.012 0.026 0.055 0.093 0.382 0.379 21.93 0.996**
TFW 138 0.047±0.013 0.019 0.048 0.087 -0.409 2.227 26.68
RFW 138 0.863±0.174 0.160 0.867 1.326 -0.318 1.461 20.27

Fig. 1

Frequency distribution of RRL, RHL, and RFW of B. napus under As stress treatment"

Fig. 2

Manhattan plots of GWAS for RRL, RHL, and RFW of rapeseed under As stress treatment"

Table 3

Significantly associated SNPs of related traits of B. napus stage under As stress treatment"

Significant SNP
No. of SNP
Interval (bp)
R2 (%)
RHL Bn-A01-p1145674 A01 1 649099-849099 A/G 2.98E-06 19.08
RFW Bn-A01-p24425211 A01 1 20123238-20323238 C/G 3.23E-06 20.72
RFW Bn-A02-p8277939 A02 2 5250663-5523057 T/C 3.51E-06 20.70
RFW Bn-A02-p9422112 A02 4 6241447-6919284 T/C 8.37E-06 20.77
RFW Bn-A02-p11041638 A02 2 7804288-7830004 A/G 1.55E-05 22.92
RFW Bn-A02-p11750740 A02 2 8461461-8497275 A/G 1.99E-05 20.19
RFW Bn-A02-p12278577 A02 3 8993675-9490338 T/C 2.47E-05 22.60
RFW, RHL Bn-A02-p13019236 A02 3 9728636-10424361 T/G 6.46E-09 21.60
RFW Bn-A05-p9116236 A02 2 12983734-13031064 T/C 6.46E-07 20.49
RRL, RHL, RW Bn-A02-p23842763 A02 7 19237258-22535850 T/C 2.22E-06 25.04
RHL Bn-A03-p8733974 A03 1 7923113-8123113 A/G 9.44E-06 24.37
RRL Bn-A03-p19129006 A03 2 18067901-19247585 A/G 1.76E-05 20.14
RRL Bn-A04-p13050240 A04 1 13637904-13837904 T/G 2.92E-05 24.23
RRL Bn-A05-p2711208 A05 1 2708636-2908636 A/G 2.98E-05 24.39
RDW Bn-A05-p15227777 A05 1 11606312-11806312 T/C 3.17E-05 19.00
RRL Bn-A06-p16406113 A06 2 17919297-18408096 T/G 2.74E-06 20.53
RFW, RHL, RRL Bn-A07-p17382019 A07 6 19282162-22517611 A/G 6.28E-06 21.22
RHL Bn-A07-p21643815 A07 4 23186702-23580640 A/G 8.69E-06 18.16
RRL Bn-A08-p17193797 A08 1 14579373-14779373 A/C 1.66E-05 18.82
RFW Bn-A09-p32954471 A09 5 30697653-31316771 A/G 1.75E-05 20.40
RFW Bn-A02-p10745711 C02 1 13769735-13969735 A/G 2.37E-05 23.40
RHL, RFW Bn-C13944312-p158 C02 1 15912037-16112037 T/C 2.39E-05 18.05
RRL Bn-scaff_16300_1-p870231 C02 1 22806371-23006371 T/C 2.45E-05 18.92
RHL Bn-scaff_17109_1-p557859 C02 1 41708473-41908473 A/G 2.46E-05 21.79
RRL Bn-scaff_16182_1-p319123 C03 1 51869206-52069206 T/C 2.47E-05 22.17
RHL Bn-scaff_16534_1-p1804261 C04 1 4356230-4556230 A/C 2.52E-05 22.65
RFW Bn-scaff_20567_1-p64644 C04 1 20723951-20923951 A/G 2.57E-05 23.27
RRL Bn-scaff_16770_1-p684639 C05 1 35142768-35342768 T/G 2.75E-05 17.31
RRL Bn-scaff_17454_1-p87022 C06 1 8199084-8399084 A/C 2.78E-05 20.28
RHL Bn-scaff_15743_1-p353143 C06 1 27442608-27642608 T/C 2.87E-05 20.77
RHL Bn-scaff_16874_1-p269409 C06 4 31639304-36835784 A/C 2.88E-05 26.28
RFW Bn-scaff_28403_1-p154436 C07 1 8625086-8825086 T/C 3.14E-05 23.05
RRL Bn-scaff_16110_1-p1058284 C07 1 43787584-43987584 C/G 3.21E-05 22.86
RRL Bn-scaff_18602_1-p278628 C08 1 16338368-16538368 T/G 2.34E-05 21.11

Table 4

Candidate genes of B. napus traits under As stress treatment"

Associated trait
B. napus code
Position (bp)
Arabidopsis AGI No.
Functional description
RHL A01 BnaA01g01280D 662364 AT4G36430 过氧化物酶超家族蛋白 Peroxidase superfamily protein
BnaA01g01600D 848378 AT4G35970 抗坏血酸过氧化物酶(APX5) ascorbate peroxidase 5 (APX5)
RFW, RHW, RRL A02 BnaA02g10160D 5151058 AT5G53650 未知功能蛋白 unknown protein
BnaA02g10840D 5596986 AT4G25630 纤维蛋白(FIB2) fibrillarin 2 (FIB2)
BnaA02g11800D 6188790 AT5G49890 氯离子通道C (CLC-C) chloride channel C (CLC-C)
BnaA02g12080D 6320966 AT1G65410 NAP蛋白(NAP11) non-intrinsic ABC protein 11 (NAP11)
BnaA02g12270D 6486908 AT1G65820 谷胱甘肽s-转移酶 microsomal glutathione s-transferase
BnaA02g12430D 6638194 AT1G66200 谷氨酰胺合成酶(GSR2) glutamine synthase clone F11 (GSR2)
BnaA02g14910D 8543407 AT3G29670 HXXXD 型酰基转移酶 HXXXD-type acyl-transferase family protein
BnaA02g15690D 9144596 AT1G71960 ATP绑定蛋白类(ABCG25) ATP-binding casette family G25 (ABCG25)
BnaA02g16380D 9732696 AT1G73190 α-内在蛋白(TIP3) TIP3
BnaA02g20570D 12940679 AT4G02480 AAA型ATP酶蛋白 AAA-type ATPase family protein
BnaA02g20640D 13009933 AT2G02930 谷胱甘肽s-转移酶(GSTF3) glutathione S-transferase F3 (GSTF3)
BnaA02g31250D 22577390 AT5G27690 重金属运输 解毒超家族蛋白 Heavy metal transport detoxification superfamily protein
BnaA02g31310D 22604742 AT3G05580 钙调磷酸酶家族蛋白 Calcineurin-like metallo-phosphoesterase superfamily protein
RHL, RRL A03 BnaA03g17000D 7971502 AT2G37130 过氧化物酶超家族蛋白 Peroxidase superfamily protein
BnaA03g17020D 7983649 AT2G37170 质膜内在蛋白(PIP2B) plasma membrane intrinsic protein 2 (PIP2B)
BnaA03g17030D 7987203 AT2G37170 质膜内在蛋白(PIP2B) plasma membrane intrinsic protein 2 (PIP2B)
BnaA03g17160D 8044155 AT2G37300 未知功能蛋白 unknown protein
BnaA03g38620D 19192627 AT2G14580 基本抗病相关蛋白(PRB1) basic pathogenesis-related protein 1 (PRB1)
RRL A05 BnaA05g05230D 2731629 AT4G00430 跨膜蛋白(TMP-C) TRANSMEMBRANE PROTEIN C (TMP-C)
RRL A06 BnaA06g25890D 17916831 AT2G17270 磷酸盐转运蛋白 phosphate transporter 3
BnaA06g25960D 17949890 AT5G66110 重金属运输 解毒超家族蛋白 Heavy metal transport detoxification superfamily protein
BnaA06g26040D 17979799 AT5G23310 铁超氧化物歧化酶 Fe superoxide dismutase 3 (FSD3)
RFW, RHL, RRL A07 BnaA07g26010D 19187837 AT1G64820 伴侣排出的家族蛋白 MATE efflux family protein
BnaA07g26020D 19193050 AT1G64820 伴侣排出的家族蛋白 MATE efflux family protein
BnaA07g26030D 19199115 AT1G64820 伴侣排出的家族蛋白 MATE efflux family protein
BnaA07g26040D 19203891 AT1G66760 伴侣排出的家族蛋白 MATE efflux family protein
BnaA07g26290D 19358162 AT1G67280 乙二醛酶 博来霉素抗性蛋白 加双氧酶蛋白
Glyoxalase Bleomycin resistance protein Dioxygenase superfamily protein
BnaA07g26330D 19381145 AT2G18330 AAA型ATP酶蛋白 AAA-type ATPase family protein
BnaA07g27500D 19996403 AT1G68850 过氧化物酶超级家族蛋白 Peroxidase superfamily protein
BnaA07g31660D 22053195 AT1G74590 谷胱甘肽s-转移酶(GSTU10) glutathione S-transferase TAU 10 (GSTU10)
BnaA07g32730D 22592486 AT1G76430 磷酸盐转运蛋白 phosphate transporter 1
BnaA07g32740D 22596590 AT1G76430 磷酸盐转运蛋白 phosphate transporter 1
BnaA07g32750D 22608377 AT1G76430 磷酸盐转运蛋白 phosphate transporter 1
BnaA07g34210D 23311592 AT1G78360 谷胱甘肽s-转移酶(GSTU21) glutathione S-transferase TAU 21 (GSTU21)
BnaA07g34260D 23358782 AT1G78610 电导率敏感通道蛋白(MSL6) mechanosensitive channel of small conductance-like 6 (MSL6)
BnaA07g34490D 23426237 AT1G78900 液泡ATP酶(VHA-A) vacuolar ATP synthase subunit A (VHA-A)
BnaA07g34850D 23620541 AT1G79360 阳离子转运蛋白(2-Oct) organic cation carnitine transporter 2 (2-Oct)
BnaA07g34890D 23632496 AT1G79410 阳离子转运蛋白(5-Oct) organic cation carnitine transporter5 (5-Oct)
RFW A09 BnaA09g44820D 30722833 AT1G17810 β-脂质体内在蛋白(BETA-TIP) beta-tonoplast intrinsic protein (BETA-TIP)
BnaA09g44870D 30765654 AT2G04040 解毒蛋白 TX1
BnaA09g44980D 30813852 AT1G17500 ATPase E1-E2型家族蛋白 ATPase
E1-E2 type family protein haloacid dehalogenase-like hydrolase family protein
BnaA09g45070D 30894204 AT1G17180 谷胱甘肽s-转移酶(GSTU25) glutathione S-transferase TAU 25 (GSTU25)
BnaA09g45080D 30902768 AT1G17180 谷胱甘肽s-转移酶(GSTU25) glutathione S-transferase TAU 25 (GSTU25)
BnaA09g45090D 30909957 AT1G17180 谷胱甘肽s-转移酶(GSTU25) glutathione S-transferase TAU 25 (GSTU25)
BnaA09g45650D 31200643 AT4G18593 双特异性抗病蛋白 dual specificity protein phosphatase-related
BnaA09g45870D 31257749 AT1G14040 维持磷锌平衡基因 PHO1;H3
BnaA09g45890D 31281439 AT1G14040 维持磷锌平衡基因 PHO1;H3
RRL C03 BnaC03g62740D 51991951 AT4G18593 双特异性抗病蛋白 dual specificity protein phosphatase-related
RHL C04 BnaC04g06200D 4438087 AT2G39350 ABC-2型转运蛋白 ABC-2 type transporter family protein
BnaC04g06210D 4439047 AT3G55090 ABC-2型转运蛋白 ABC-2 type transporter family protein
RHL C06 BnaC06g31020D 31680823 AT1G69920 谷胱甘肽s-转移酶(GSTU12) glutathione S-transferase TAU 12 (GSTU12)
BnaC06g31030D 31683577 AT1G69920 谷胱甘肽s-转移酶(GSTU12) glutathione S-transferase TAU 12 (GSTU12)
BnaC06g31040D 31689290 AT1G69930 谷胱甘肽s-转移酶(GSTU11) glutathione S-transferase TAU 11 (GSTU11)
BnaC06g32880D 32943807 AT1G71880 糖基转运蛋白(SUC1) sucrose-proton symporter 1 (SUC1)
BnaC06g39760D 36750159 AT1G79360 阳离子转运蛋白(2-Oct) organic cation carnitine transporter 2 (2-Oct)
BnaC06g39810D 36768217 AT1G79410 阳离子转运蛋白(5-Oct) organic cation carnitine transporter5 (5-Oct)
BnaC06g39820D 36770807 AT1G79410 阳离子转运蛋白(5-Oct) organic cation carnitine transporter5 (5-Oct)
BnaC06g40180D 36932959 AT1G80830 吞噬细胞抗性蛋白(NRAMP1) natural resistance-associated macrophage protein 1 (NRAMP1)
RRL C08 BnaC08g10950D 16367664 AT5G62160 锌转运蛋白(ZIP12) zinc transporter 12 precursor (ZIP12)

Fig. 3

Expression patterns of candidate genes in B. napus under As stress Error bar represents the standard error of the mean (n=3); * and ** indicate significant difference at the 0.05 and 0.01 probability levels, respectively."

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