砷胁迫下甘蓝型油菜苗期根、下胚轴和鲜重的全基因组关联分析

doi:10.3724/SP.J.1006.2019.84093

Abstract

Abstract:

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

Cun-Min QU,Guo-Qiang MA,Mei-Chen ZHU,Xiao-Hu HUANG,Le-Dong JIA,Shu-Xian WANG,Hui-Yan ZHAO,Xin-Fu XU,Kun LU,Jia-Na LI,Rui WANG. Genome-wide association of roots, hypocotyls and fresh weight at germination stage under as stress in Brassica napus L.[J].Acta Agronomica Sinica, 2019, 45(2): 175-187.

Figures/Tables 7

Table 1

Table 2

Fig. 1

Fig. 2

Table 3

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

性状 Trait	显著性SNP位点 Significant SNP	染色体 Chr.	SNP数目 No. of SNP	区间 Interval (bp)	等位基因 Allele	P值 P-value	贡献率 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 3

Table 4

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

关联性状 Associated trait	染色体 Chr.	油菜基因编号 B. napus code	位置 Position (bp)	拟南芥基因编号 Arabidopsis AGI No.	功能描述 Functional description
RHL	A01	BnaA01g01280D	662364	AT4G36430	过氧化物酶超家族蛋白 Peroxidase superfamily protein
RHL	A01	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)

Table 4

Fig. 3

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基因名 Gene name	基因号 Gene ID	引物序列 Sequences of primers (5'-3')
BnaABCG25	BnaA02g15690D	F: GTGGCACTCAGATTATCGAGACGTACA R: AGTCCGAGTCCTTGGGATGCTAAAA
BnaGSTU10	BnaA07g31660D	F: ATCGATGAAACCTGGAAGAACT R: GAATCTCTCTCTAGCCACTTCC
BnaGST16	BnaA02g20640D	F: GCAGGTATCAAAGTTTTCGGACACG R: GTGGGATATGTTCTTGGAGTCGGCT
BnaPHT3;3	BnaA06g25890D	F: GTGAAGCAACAGAAAGTAACGGTGGT R: CCGCCGCTGTTGTTGTTGTTAC
BnaPHT1;9	BnaA07g32730D, BnaA07g32740D, BnaA07g32750D	F: CTCCACGGCCGTGACCTCTTC R: AACCCCATTATCTGAATCTTGACTCG
BnaGSTU25	BnaA09g45070D, BnaA09g45080D, BnaA09g45090D	F: TCCTTCCTTCTGATCCTTACCA R: GGACACTCTGCTTCGATGCTAA
BnaGSTU12	BnaC06g31020D, BnaC06g31030D	F: TCAGATCCTTCCATCCTCCCCTCA R: CCACCATAGCCCCACAAGCGAT
BnaGSTU11	BnaC06g31040D	F: CCCCGTCCATAAACAGATCCCC R: CGCTATTGCCATCTTTCTTTCCTCC
BnaUBC21	BnaA06g27860D, BnaA09g04490D	F: CCTCTGCAGCCTCCTCAAGT R: CATATCTCCCCTGTCTTGAAATGC
BnaACTIN7	BnaA03g55890D, BnaC02g00690D, BnaA10g22340D	F: CCCTGGAATTGCTGACCGTA R: TGGAAAGTGCTGAGGGATGC

性状 Trait	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 Skewness	峰度 Kurtosis	变异系数 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

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

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