甘蓝型油菜湿害胁迫响应性状的全基因组关联分析及候选基因预测

doi:10.3724/SP.J.1006.2019.94027

Abstract

Abstract:

The yield and quality of rapeseed are significantly affected by waterlogging. Many researches on waterlogging of rapeseed mostly aimed at its mechanism and physiological response, but a few of them identified the genes related to waterlogging. In this study, 248 Brassica napus L. accessions were planted in flowerpots with treatments of waterlogging and well watering for four weeks when the plants had four true leaves in rain-proof installation, and eight waterlogging-responding traits were investigated. The genome-wide association analysis was carried out based on 60K Illumina Infinium SNP genotype data and the candidate genes associated with waterlogging responses were predicted. Under waterlogging, the number of green leaf, the shoot fresh weight and dry weight, the leaf soluble protein content were lower, and the leaf POD activity, the MDA content were higher than those under well watering. The root fresh weight and dry weight were lower in most accessions and higher in some accessions under waterlogging stress. A total of 36 SNPs were identified associated with waterlogging traits and explained the phenotypic variation of 8.28%-12.95%. There were significant (P < 0.05) or extremely significant (P < 0.01) differences in the waterlogging resistance index among genotypes of 17 SNPs. The Blocks containing 17 SNPs covered 71 candidate genes. Among them, 64 candidate genes were homologous to Arabidopsis genes by blast. They encoded transcription factors (e.g. transcription initiation factor IIF, bZIP68, myb-like HTH transcriptional regulator family protein), transport protein (e.g. SUC2), inhibitor of growth (e.g. ING2), protein phosphatase (e.g. protein phosphatase 2C family protein), DNA/RNA binding proteins [e.g. bHLH DNA-binding superfamily protein, RNA-binding (RRM/RBD/RNP motifs) family protein], hormone response proteins (e.g. ARF8, ADC2, ERD6, NF-YC9), oxidative/osmotic/cold stress or water deprivation response proteins (e.g. ERD6, NP1, TIR-NBS-LRR, CRT1b). These results would be benefit for revealing the waterlogging resistance mechanism and cultivating new varieties with waterlogging resistance in Brassica napus L.

Key words: Brassica napus L., waterlogging-responding traits, genome-wide association analysis, candidate genes

Yang-Yang LI,Rong-Rong JING,Rong-Rong LYU,Peng-Cheng SHI,Xin LI,Qin WANG,Dan WU,Qing-Yuan ZHOU,Jia-Na LI,Zhang-Lin TANG. Genome-wide association analysis and candidate genes prediction of waterlogging-responding traits in Brassica napus L.[J].Acta Agronomica Sinica, 2019, 45(12): 1806-1821.

Figures/Tables 13

Fig. 1

Table 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Table 2

Fig. 6

Fig. 7

Table 3

SNPs significantly associated with WLRI of waterlogging-responding traits in B. napus"

性状 Trait	标记 Marker	染色体 Chromosome	位置 Position	P值 P-value	贡献率 R²(%)
GLN	Bn-scaff_23954_1-p1045541	C03	10,880,567	1.61E-05	9.82
	Bn-scaff_20901_1-p1110262	C05	2,905,509	5.17E-06	10.69
	Bn-A03-p11122273	C07	41,947,271	5.09E-06	10.70
性状 Trait	标记 Marker	染色体 Chromosome	位置 Position	P值 P-value	贡献率 R²(%)
SFW	Bn-A02-p13803435	A02	10,432,008	1.36E-05	9.71
	Bn-A04-p6975646^a	A04	8,262,555	8.53E-06	10.06
	Bn-A04-p6978163^b	A04	8,265,085	8.53E-06	10.06
	Bn-A04-p6980459	A04	8,267,518	1.64E-05	9.57
	Bn-A10-p15740896^c	A10	15,809,264	1.46E-05	9.65
	Bn-scaff_16531_1-p428890^d	C04	21,584,887	7.76E-06	10.13
SDW	Bn-A04-p6975646^a	A04	8,262,555	1.71E-05	9.74
	Bn-A04-p6978163^b	A04	8,265,085	1.71E-05	9.74
	Bn-A10-p15740896^c	A10	15,809,264	1.94E-06	11.40
	Bn-scaff_21884_1-p644186	C01	37,469,955	7.66E-06	10.36
	Bn-scaff_16531_1-p428890^d	C04	21,584,887	4.67E-06	10.73
	Bn-scaff_17919_1-p94976	C09	34,508,780	2.82E-05	8.28
RFW	Bn-scaff_18062_1-p214669	C04	31,128,751	2.45E-05	9.47
	Bn-scaff_21124_1-p301252	C05	37,592,772	7.89E-06	10.35
RDW	Bn-A08-p15326882	A08	12,894,573	2.74E-06	12.39
	Bn-A09-p20263302	A09	17,272,800	1.95E-06	12.71
	Bn-scaff_18826_1-p776957	C05	36,457,927	1.02E-05	11.14
	Bn-scaff_17888_1-p170198	C09	15,826,668	1.74E-05	10.64
Protein	Bn-A01-p6538362	A01	6,002,545	2.06E-05	10.54
	Bn-A02-p12822311	A02	9,572,851	8.39E-06	11.47
	Bn-A03-p7079712	A03	6,365,301	2.87E-05	11.61
	Bn-A03-p20100490	A03	18967298	1.57E-05	10.83
	Bn-A07-p20887568	A07	22,470,590	7.18E-06	11.63
	Bn-A09-p21935602	A09	19,325,386	2.67E-06	12.65
	Bn-scaff_20675_1-p32364	C01	9,755,072	2.08E-05	11.96
	Bn-scaff_21188_1-p1142	C02	17,317,511	8.30E-06	12.95
	Bn-scaff_17067_1-p509745	C02	27,930,748	2.18E-05	11.91
	Bn-scaff_15585_1-p1047449	C04	44,459,141	2.45E-06	12.74
POD	Bn-A01-p637586	A01	228,343	4.62E-06	9.61
	Bn-A03-p12250401	A03	11,367,398	1.93E-05	9.62
	Bn-A09-p30788157	A09	28,540,524	7.44E-06	10.35
	Bn-A10-p2246688	A10	1,588,516	2.00E-05	9.59
MDA	Bn-A06-p3088460	C05	3,221,158	2.31E-05	9.38

Table 3

Table 4

WLRIs of water-logging responding traits in different significant SNP genotypes in B. napus"

性状 Trait	SNP标记 SNP marker	基因型 Loci	耐湿系数 WLRI	方差 Variance
GLN	Bn-scaff_23954_1-p1045541	(GG)5	0.793 Aa	0.005
		(TG)25	0.627 Bb	0.012
		(TT)168	0.589 Bb	0.008
	Bn-scaff_20901_1-p1110262	(AA)50	0.656 Aa	0.013
		(CC)155	0.593 Bb	0.007
		(AC)20	0.570 Bb	0.009
	Bn-A03-p11122273	(CC)25	0.681 Aa	0.010
		(TC)5	0.647 ABab	0.007
		(TT)202	0.586 Bb	0.008
性状 Trait	SNP标记 SNP marker	基因型 Loci	耐湿系数 WLRI	方差 Variance
SFW	Bn-A02-p13803435	(TT)210	0.361 Aa	0.022
		(TC)12	0.347 ABab	0.016
		(CC)16	0.296 Bb	0.006
	Bn-A04-p6975646	(AA)12	0.560 Aa	0.036
		(CC)220	0.355 Bb	0.020
		(AC)8	0.273 Bb	0.017
	Bn-A04-p6978163	(TT)12	0.560 Aa	0.036
		(GG)222	0.356 Bb	0.021
		(TG)8	0.273 Bb	0.017
	Bn-A04-p6980459	(GG)13	0.570 Aa	0.034
		AA)218	0.355 Bb	0.021
	Bn-A10-p15740896	(TT)14	0.546 Aa	0.039
		(TC)3	0.435 ABab	0.026
		(CC)216	0.357 Bb	0.021
	Bn-scaff_16531_1-p428890	(CC)4	0.767 Aa	0.022
		(TC)17	0.380 Bb	0.014
		(TT)200	0.358 Bb	0.023
SDW	Bn-A04-p6975646	(AA)12	0.862 Aa	0.178
		(CC)220	0.548 ABb	0.046
		(AC)8	0.416 Bc	0.016
	Bn-A04-p6978163	(TT)12	0.862 Aa	0.178
		(GG)222	0.550 ABb	0.047
		(TG)8	0.416 Bc	0.016
	Bn-A10-p15740896	TT)14	0.865 Aa	0.098
		(TC)3	0.756 ABab	0.170
		(CC)216	0.544 Bb	0.048
	Bn-scaff_21884_1-p644186	(GG)4	1.125 Aa	0.094
		(AA)174	0.566 Bb	0.053
		(AG)25	0.512 Bb	0.050
	Bn-scaff_16531_1-p428890	(CC)4	1.145 Aa	0.138
		(TC)17	0.618 Bb	0.061
		(TT)200	0.545 Bb	0.049
	Bn-scaff_17919_1-p94976	(AA)213	0.559 Aa	0.051
		(AC)23	0.455 Bb	0.020
RFW	Bn-scaff_18062_1-p214669	(AC)11	2.538 Aa	2.529
		(CC)67	1.222 Ab	0.347
		(AA)143	1.291 Ab	0.850
	Bn-scaff_21124_1-p301252	(TT)208	1.363 Aa	0.969
		(CC)28	1.317 Aa	0.697
		(TC)6	0.988 Aa	0.132
RDW	Bn-A08-p15326882	(AA)215	1.464 Aa	0.365
		(AG)27	1.321 Aa	0.241
	Bn-A09-p20263302	(TT)198	1.471 Aa	0.349
		(TA)19	1.414 Aab	0.412
性状 Trait	SNP标记 SNP marker	基因型 Loci	耐湿系数 WLRI	方差 Variance
		(AA)24	1.195 Ab	0.217
	Bn-scaff_18826_1-p776957	(TC)26	1.546 Aa	0.318
		(CC)69	1.469 Aa	0.334
		(TT)136	1.367 Aa	0.317
	Bn-scaff_17888_1-p170198	(AC)30	1.534 Aa	0.321
		(CC)77	1.505 Aa	0.423
		(AA)124	1.343 Aa	0.232
Protein	Bn-A01-p6538362	(TT)117	0.293 Aa	0.025
		(TG)108	0.291 Aa	0.023
	Bn-A02-p12822311	(AA)174	0.302 Aa	0.028
		(AG)67	0.302 Aa	0.024
	Bn-A03-p7079712	(AG)7	0.681 Aa	0.122
		(AA)33	0.312 Ab	0.034
		(GG)197	0.295 Ab	0.024
	Bn-A03-p20100490	(TC)50	0.318 Aa	0.029
		(CC)189	0.296 Aa	0.025
	Bn-A07-p20887568	(TC)75	0.299 Aa	0.023
		(TT)162	0.298 Aa	0.027
	Bn-A09-p21935602	(GG)217	0.314 Aa	0.031
		(AG)26	0.230 Bb	0.008
	Bn-scaff_20675_1-p32364	(GG)9	0.358 Aa	0.039
		(TG)14	0.305 Aa	0.028
		(TT)208	0.291 Aa	0.023
	Bn-scaff_21188_1-p1142	(GG)3	0.350 Aa	0.046
		(TT)193	0.293 Aa	0.022
		(TG)33	0.282 Aa	0.033
	Bn-scaff_17067_1-p509745	(TG)16	0.330 Aa	0.054
		(TT)33	0.313 Aa	0.029
		(GG)191	0.297 Aa	0.024
	Bn-scaff_15585_1-p1047449	(GG)211	0.301 Aa	0.026
		(AG)28	0.286 Aa	0.030
POD	Bn-A01-p637586	(AA)212	1.195 Aa	0.089
		(AG)28	1.118 Aa	0.066
	Bn-A03-p12250401	(AA)40	1.188 Aa	0.086
		(GG)162	1.186 Aa	0.076
		(AG)34	1.150 Aa	0.121
	Bn-A09-p30788157	(TT)225	1.201 Aa	0.084
		(CC)13	0.980 Bb	0.059
	Bn-A10-p2246688	(CC)34	1.282 Aa	0.115
		(AA)182	1.168 Aa	0.081
		(AC)20	1.146 Aa	0.092
MDA	Bn-A06-p3088460	(GG)195	1.513 Aa	0.489
		(AG)47	1.294 Ab	0.403

Table 4

Fig. 8

Table 5

Information of candidate genes associated with WLRI of water-logging responding traits in B. napus"

油菜基因 B. napus gene	染色体 Chr.	物理位置 Position (bp)	拟南芥基因 AT gene	功能 Function
BnaA02g17270D	A02	10,385,018-10,386,352	AT1G75510	Transcription initiation factor IIF
BnaA02g17280D	A02	10,389,281-10,390,641	AT1G75520	SHI-related sequence 5 (SRS5)
BnaA02g17290D	A02	10,428,468-10,429,854	AT1G75540	Salt tolerance homolog 2 (STH2)
BnaA02g17300D	A02	10,461,565-10,461,997	AT1G75580	SAUR-like auxin-responsive protein family
BnaA03g13900D	A03	6,364,664-6,366,026	AT2G30360	SOS3-interacting protein 4 (SIP4)
BnaA04g09140D	A04	8,212,219-8,213,486	AT5G39320	UDP-glucose 6-dehydrogenase family protein
BnaA04g09150D	A04	8,215,808-8,217,193	AT5G39050	HXXXD-type acyl-transferase family protein
BnaA04g09160D	A04	8,231,509-8,231,884	AT1G22710	ARABIDOPSIS THALIANA SUCROSE-PROTON SYMPORTER 2 (SUC2)
BnaA04g09170D	A04	8,231,950-8,233,460	AT5G39340	Histidine-containing phosphotransmitter 3 (AHP3)
BnaA04g09180D	A04	8,233,647-8,235,665	AT5G39350	Tetratricopeptide repeat (TPR)-like superfamily protein
BnaA04g09190D	A04	8,235,944-8,237,287	AT5G39360	EID1-like 2 (EDL2)
BnaA04g09200D	A04	8,238,128-8,241,036	AT5G39380	Plant calmodulin-binding protein-related
BnaA04g09210D	A04	8,261,813-8,262,055	—
BnaA04g09220D	A04	8,280,136-8,282,045	AT5G39400	PTEN1
BnaA04g09230D	A04	8,282,166-8,284,176	AT5G39410	Saccharopine dehydrogenase
BnaA09g24570D	A09	17,276,994-17,280,062	AT1G32190	Alpha/beta-Hydrolases superfamily protein
BnaA09g24580D	A09	17,282,321-17,283,676	—
BnaA09g24590D	A09	17,303,368-17,305,678	AT1G46984	F-box family protein
BnaA09g24600D	A09	17,320,367-17,322,665	AT1G46984	F-box family protein
BnaA09g24610D	A09	17,360,901-17,363,794	AT1G32150	Basic region/leucine zipper transcription factor 68 (bZIP68)
BnaA09g26170D	A09	19,351,820-19,355,843	AT5G37020	Auxin response factor 8 (ARF8)
BnaA09g40620D	A09	28,538,438-28,542,878	AT2G26260	3 beta-hydroxysteroid-dehydrogenase/decarboxylase isoform 2 (3BETAHSD/D2)
BnaA10g24140D	A10	15,809,477-15,810,280	AT4G34710	Arginine decarboxylase 2 (ADC2)
BnaA10g24150D	A10	15,810,902-15,813,379	AT5G06800	Myb-like HTH transcriptional regulator family protein
BnaC03g20520D	C03	10,879,272-10,881,026	AT2G37110	PLAC8 family protein
BnaC04g20480D	C04	21,584,060-21,585,266	AT1G63740	Disease resistance protein (TIR-NBS-LRR class) family
BnaC04g29520D	C04	31,077,933-31,080,151	AT4G12790	P-loop containing nucleoside triphosphate hydrolases superfamily protein
BnaC04g29530D	C04	31,085,683-31,088,293	AT4G12740	HhH-GPD base excision DNA repair family protein
油菜基因 B. napus gene	染色体 Chr.	物理位置 Position (bp)	拟南芥基因 AT gene	功能 Function
BnaC04g29540D	C04	31,096,099-31,098,880	AT4G12650	Endomembrane protein 70 protein family
BnaC04g29550D	C04	31,113,638-31,113,859	—
BnaC04g29560D	C04	31,116,424-31,116,591	—
BnaC04g29570D	C04	31,121,991-31,124,968	AT4G12680	Unknown protein
BnaC04g29580D	C04	31,130,755-31,131,747	AT1G54390	INHIBITOR OF GROWTH 2 (ING2)
BnaC04g29590D	C04	31,133,548-31,136,282	AT5G35380	Protein kinase protein with adenine nucleotide alpha hydrolases-like domain
BnaC04g29600D	C04	31,158,769-31,162,504	AT5G35430	Tetratricopeptide repeat (TPR)-like superfamily protein
BnaC04g29610D	C04	31,170,772-31,172,233	AT5G35520	MINICHROMOSOME INSTABILITY 12 (MIS12)-LIKE (MIS12)
BnaC05g05880D	C05	2,904,698-2,910,332	AT1G08190	Vacuolar protein sorting 41 (VPS41)
BnaC05g06500D	C05	3,218,324-3,221,856	AT1G08930	EARLY RESPONSE TO DEHYDRATION 6 (ERD6)
BnaC05g06510D	C05	3,222,332-3,224,004	AT1G08940	Phosphoglycerate mutase family protein
BnaC05g06520D	C05	3,224,198-3,228,539	AT1G08970	Nuclear factor Y
BnaC05g06530D	C05	3,228,942-3,233,245	AT1G09000	NPK1-related protein kinase 1 (NP1)
BnaC05g06540D	C05	3,233,325-3,237,550	AT1G09010	Glycoside hydrolase family 2 protein
BnaC05g06550D	C05	3,239,409-3,244,162	AT1G09020	Homolog of yeast sucrose nonfermenting 4 (SNF4)
BnaC05g06560D	C05	3,246,008-3,247,080	—
BnaC05g06570D	C05	3,248,229-3,248,627	AT1G09030	Nuclear factor Y
BnaC05g06580D	C05	3,258,505-3,259,753	AT2G19610	RING/U-box superfamily protein
BnaC05g06590D	C05	3,261,801-3,265,778	AT1G09050	Unknown protein
BnaC05g06600D	C05	3,266,250-3,266,895	AT1G09060	Zinc finger protein
BnaC05g06610D	C05	3,267,487-3,268,443	AT1G09070	Soybean gene regulated by cold-2 (SRC2)
BnaC05g06620D	C05	3,269,846-3,271,741	AT1G09130	ATP-dependent caseinolytic (Clp) protease/crotonase family protein
BnaC05g06630D	C05	3,275,956-3,279,260	AT1G09140	SERINE-ARGININE PROTEIN 30 (ATSRP30)
BnaC05g06640D	C05	3,279,332-3,280,873	AT1G09150	Containing protein
BnaC05g06650D	C05	3,281,248-3,282,283	AT1G09155	Phloem protein 2-B15 (PP2-B15)
BnaC05g06660D	C05	3,298,672-3,298,972	AT1G09155	Phloem protein 2-B15 (PP2-B15)
BnaC05g06670D	C05	3,299,052-3,303,054	AT1G09155	Phloem protein 2-B15 (PP2-B15)
BnaC05g06680D	C05	3,303,126-3,306,459	AT2G43445	F-box and associated interaction domains-containing protein
BnaC05g06690D	C05	3,308,135-3,309,772	AT1G09160	Protein phosphatase 2C family protein
BnaC05g06700D	C05	3,311,000-3,312,454	AT1G09190	Tetratricopeptide repeat (TPR)-like superfamily protein
BnaC05g06710D	C05	3,312,506-3,313,708	AT1G56330	Secretion-associated RAS 1B (SAR1B)
BnaC05g06720D	C05	3,316,670-3,319,893	AT5G08020	RPA70-kDa subunit B (RPA70B)
BnaC05g06730D	C05	3,321,779-3,322,096	—
BnaC05g06740D	C05	3,324,873-3,325,493	AT5G09390	CD2-binding protein-related
BnaC05g06750D	C05	3,329,829-3,330,444	AT1G09250	Basic helix-loop-helix (bHLH) DNA-binding superfamily protein
BnaC05g06760D	C05	3,330,666-3,331,280	AT1G09250	Basic helix-loop-helix (bHLH) DNA-binding superfamily protein
BnaC05g06770D	C05	3,349,687-3,350,292	—
BnaC05g06780D	C05	3,356,126-3,359,392	AT1G09210	Calreticulin 1b (CRT1b)
BnaC05g06790D	C05	3,360,115-3,363,017	AT1G09230	RNA-binding (RRM/RBD/RNP motifs) family protein
BnaC05g06800D	C05	3,370,500-3,371,711	AT1G09240	Nicotianamine synthase 3 (NAS3)
BnaC05g06810D	C05	3,372,700-3,373,315	AT1G09250	Basic helix-loop-helix (bHLH) DNA-binding superfamily protein
BnaC05g06820D	C05	3,378,631-3,379,149	AT1G09260	Chaperone DnaJ-domain superfamily protein
BnaC05g06830D	C05	3,379,950-3,383,047	AT1G09270	Importin alpha isoform 4 (IMPA-4)

Table 5

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变异来源 Source of variation	自由度 df	F-value
变异来源 Source of variation	自由度 df	GLN	SFW	SDW	RFW	RDW	POD	MDA	Protein
水分间Water	1	4840.51^**	29,719.19^**	6028.69^**	67.37^**	1113.40^**	1167.63^**	2314.55^**	17,856.96^**
材料间Variety	245	7.89^**	38.19^**	17.30^**	11.25^**	13.21^**	12.81^**	34.72^**	20.95^**
水分×材料Water × Variety	245	1.95^**	20.63^**	8.97^**	8.08^**	7.62^**	13.27^**	31.70^**	17.80^**
误差Error	984

Genome-wide association analysis and candidate genes prediction of waterlogging-responding traits in Brassica napus L.

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染色体Chromosome	衰减距离 LD decay (kb)	染色体Chromosome	衰减距离 LD decay (kb)
A01	180	C01	750
A02	180	C02	1200
A03	180	C03	400
A04	180	C04	590
A05	180	C05	290
A06	180	C06	400
A07	180	C07	380
A08	500	C08	620
A09	380	C09	710
A10	210

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