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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (12): 1806-1821.doi: 10.3724/SP.J.1006.2019.94027


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

Yang-Yang LI1,2,3,Rong-Rong JING1,3,Rong-Rong LYU1,2,3,Peng-Cheng SHI1,2,3,Xin LI1,2,3,Qin WANG1,2,3,Dan WU1,2,3,Qing-Yuan ZHOU1,3,Jia-Na LI1,2,3,Zhang-Lin TANG1,2,3,*()   

  1. 1 College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China
    2 Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China
    3 Chongqing Engineering Research Center for Rapeseed, Chongqing 400715, China
  • Received:2019-02-25 Accepted:2019-06-24 Online:2019-12-12 Published:2019-07-16
  • Contact: Zhang-Lin TANG E-mail:tangzhlin@swu.edu.cn
  • Supported by:
    This study was supported by the Science and Technology Innovation Project of Chongqing Social Undertakings & Livelihood Security(cstc2016shms-ztzx80010);the National Key R&D Program of China(2018YFD0100504);the Fundamental Research Funds for the Central Universities(XDJK2019D021)


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

Fig. 1

Frequency distribution for WLRI (waterlogging resistance index) of each waterlogging-responding trait at seedling stage in B. napus Abbreviations are the same as those given in Table 1."

Table 1

Variance analysis of waterlogging-responding traits in B. napus"

Source of variation
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

Fig. 2

Frequency distribution of relative kinship coefficient in 248 B. napus accessions"

Fig. 3

Estimation of ΔK based on change rate of ln P(D) between successive K value"

Fig. 4

Population structure of 248 B. napus accessions"

Fig. 5

LD decay of chromosomes in B. napus"

Table 2

Decay distance of each chromosome in B. napus"

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

Fig. 6

QQ plots of GWAS for WLRI of waterlogging-responding traits based on six models in B. napus"

Fig. 7

Manhattan plots of GWAS for WLRI of waterlogging-responding traits based on the best model in B. napus"

Table 3

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

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
R2 (%)
SFW Bn-A02-p13803435 A02 10,432,008 1.36E-05 9.71
Bn-A04-p6975646a A04 8,262,555 8.53E-06 10.06
Bn-A04-p6978163b A04 8,265,085 8.53E-06 10.06
Bn-A04-p6980459 A04 8,267,518 1.64E-05 9.57
Bn-A10-p15740896c A10 15,809,264 1.46E-05 9.65
Bn-scaff_16531_1-p428890d C04 21,584,887 7.76E-06 10.13
SDW Bn-A04-p6975646a A04 8,262,555 1.71E-05 9.74
Bn-A04-p6978163b A04 8,265,085 1.71E-05 9.74
Bn-A10-p15740896c 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-p428890d 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 4

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

SNP marker
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
SNP marker
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
SNP marker
(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

Fig. 8

Blocks including significant SNP markers and candidate genes Significant markers are marked with black border and the candidate genes are underlined."

Table 5

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

B. napus gene
Position (bp)
AT gene
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
B. napus gene
Position (bp)
AT gene
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)
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