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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (02): 214-227.doi: 10.3724/SP.J.1006.2020.94067

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Candidate genes screening for plant height and the first branch height based on QTL mapping and genome-wide association study in rapessed (Brassica napus L.)

HUO Qiang1,2,YANG Hong1,2,CHEN Zhi-You1,2,JIAN Hong-Ju1,2,QU Cun-Min1,2,LU Kun1,2,LI Jia-Na1,2,*()   

  1. 1 College of Agronomy and Biotechnology, Southwest University / Chongqing Engineering Research Center for Rapeseed, Chongqing 400715, China
    2 Academy of Agricultural Sciences, Southwest University, Chongqing 400715, China
  • Received:2019-04-28 Accepted:2019-08-09 Online:2020-02-12 Published:2019-09-02
  • Contact: Jia-Na LI E-mail:ljn1950@swu.edu.cn
  • Supported by:
    This study was supported by the Special Project of Chongqing People’s Livelihood(cstc2016shms-ztzx80020);the National-Yunnan United Natural Science Foundation of China(U1302266);the National Key Research and Development Plan(2018YFD0100504-05)

Abstract:

Plant height (PH) and the first branch height (BH) are important agronomic traits closely related to thickness of pod canopy and harvest index of Brassica napus. There are many reports on quantitative trait locus (QTL) and genome-wide association study (GWAS) for PH, but few reports on QTL and GWAS localization and candidate gene screening for BH. In this study, QTLs for PH and BH using the 186 recombinant inbred lines (RIL) in the two environments of 2016 and 2017 were detected based on the high-density genetic linkage map. A total of eight PH QTLs located on chromosomes A03, A04, and A09 were detected in the two environments of 2016 and 2019, with the explained phenotypic variation of individual QTL range from 4.60% to 13.29%, among which overlapped QTLs (q-2017PH-A04-2 and q-BLUP-PH-A04-2) were detected both in 2017 and based on Best Linear Unbiased Prediction (BLUP). Nine BH QTLs located on chromosomes A01, A02, A05, A09, C01, and C05 were detected, in which a single QTL explained 5.12% to 19.10% of phenotypic variation. Among them, q-2017BH-A09-1, q-BLUP-BH-A09-2, and q-BLUP-BH-A09-3 were overlapped. GWAS for PH and BH was performed using 588 resequencing natural populations established by our previous study. A total of 50 SNPs associated with PH and 12 SNPs associated with BH were detected in two years. Thirteen PH candidate genes involved in cell proliferation, cell multiplication, cell cycle and cell wall activity and eleven BH candidate genes involved in the synthesis and metabolism of gibberellin and spermidine, ribosome composition, photosynthesis and germination were screened based on the physical locations of SNPs, and their expressions in extreme phenotypes by qRT-PCR. This result will provide a theoretical basis for improving plant architecture and subsequent functional studies of genes.

Key words: Brassica napus, plant height, first branch height, gene localization, candidate gene screening

Table 1

List of primer sequences for candidate genes"

基因名
Gene name
引物序列
Primer sequence (5°-3°)
BnaA03g47940D F: ATGGAGGCAATGAAGATGAAAC; R: GATAGACAAAGAAGCATCAGAG
BnaA07g28720D F: CAGCTTCTTCGCTTACAAGATC; R: ATGCTCGATGGCTTATACTCAA
BnaA07g28820D F: TTTTACTCGTCGTGCTTCTCTC; R: GACCTTCGAAAAACATGATGCT
BnaC06g30400D F: ACAAGAATAATCGTTCTGCTGC; R: CCAACAGTTTCACTCTTCAAGG
BnaC06g30410D F: TGGAAGCGTTACTGATTTGATG; R: TGAATATTGAGTGCAAGTAAGC
BnaA01g29630D F: ATAAAGACTCTATCGCGATCGG; R: ATCCAAGGAGCGATATTAGTGG
BnaA01g30830D F: ACTCTTTCGGTTCTTTTGTTGG; R: GTTTTGTTACGTCCGAAGAACA
BnaA02g31980D F: GACGATGTCAAGCTTATAAGCG; R: TAACCCCTAAACAAACCTCTCC
BnaA02g37010D F: TTCTTGAATTGGCAGAACGATC; R: CTTCCGTGACAACAACCTTTAG
BnaA09g48360D F: CAGTCAAAGCCATCCATGAAAA; R: CGAAGCTAATAGTGTGTTGGTG
BnaA09g49220D F: TTGCTTCTTTTGTCAACCTAGC; R: CAGAAACAGTGCATACAGCTAC
BnaC02g14570D F: GTGTTCTCAGGGAGATATCTCG; R: CACGAGGATCTTCAAATCCAAC

Table 2

Phenotypic variation of plant height and the first branch height in two populations"

性状
Trait
群体
Population
年份
Year
均值±标准差
Mean ± SD
范围
Range
变异系数
CV (%)
广义遗传力
h2 (%)
ZY821父本株高 RIL 2016 190.80±6.85
ZY821♂ PH 2017 184.33±11.74
GH06母本株高 RIL 2016 217.40±5.61
GH06♀ PH 2017 187.33±10.8
ZY821父本一次有效分枝高度 RIL 2016 86.25±5.35
ZY821♂ BH 2017 68.63±11.54
GH06母本一次有效分枝高度 RIL 2016 83.00±6.70
GH06♀ BH 2017 95.14±15.67
株高PH RIL 2016 213.82±11.20 187.0-241.6 5.24 75.45
2017 207.26±11.91 163.0-238.4 5.75
N 2016 211.84±18.15 162.2-259.0 8.57 87.42
2017 204.39±20.76 127.4-262.4 10.16
一次有效分枝高度BH RIL 2016 85.26±15.84 49.6-118.0 18.58 68.77
2017 82.85±14.69 50.1-123.6 17.73
N 2016 84.17±22.43 19.0-142.8 26.65 82.21
2017 82.90±23.09 11.0-141.1 27.86

Fig. 1

Frequency distribution of plant height and the first branch height in two populations PH: plant height; BH: the first branch height; RIL: recombinant inbred lines; N: natural population."

Fig. 2

Putative QTL locations of plant height and the first branch height on the SNP genetic map"

Table 3

Putative QTLs for plant height and the first branch height detected in two years"

位点
QTL
染色体
Chr.
阈值
LOD score
加性效应
Additive effect
贡献率
R2 (%)
标记区间
SNP interval
物理区间
Physical position (bp)
环境
Environment
株高 PH
q-2016PH-A03-1 A03 2.87 4.27 13.29 SNP6093-SNP6075 18421721-18543828 2016
q-2016PH-A09-1 A09 3.51 -3.81 11.28 KS30880-H112B21-1 2016
q-2017PH-A04-1 A04 2.79 2.71 4.92 SNP8751-SNP8781 14085289-14244618 2017
q-2017PH-A04-2 A04 3.26 2.93 5.75 SNP8596-SNP8650 13373664-13531885 2017
q-2017PH-A09-1 A09 5.20 -5.58 9.63 SNP46371-SNP20466 22590345-23259990 2017
q-2017PH-A09-2 A09 4.16 -5.81 7.55 SNP20486-SNP20487 23517031-23521212 2017
q-2017PH-A09-3 A09 4.72 -5.40 8.51 SNP20492-SNP20496 23603951-23642701 2017
q-2017PH-A09-4 A09 4.31 -4.55 7.86 KS10551-KS10551 2017
q-BLUP-PH-A04-1 A04 4.25 1.43 7.60 SNP8701-SNP8801 13798050-14401987 BLUP
q-BLUP-PH-A04-2 A04 3.45 1.31 6.27 SNP8596-SNP8650 13373664-13531885 BLUP
q-BLUP-PH-A09-1 A09 2.60 -1.36 4.60 ENA22-niab_ssr003 BLUP
一次有效分枝高度 BH
q-2016BH-A02-1 A02 4.14 6.24 13.56 SNP3957-SNP3759 22556597-23778808 2016
q-2016BH-C05-1 C05 5.26 7.49 19.10 SNP26887-SNP26897 4224409-4258940 2016
q-2017BH-A01-1 A01 4.78 -5.53 9.15 SNP1148-SNP1370 17881769-19687948 2017
q-2017BH-A01-2 A01 3.08 -4.64 6.03 SNP47359-SNP1693 20189127-21190484 2017
q-2017BH-A09-1 A09 2.69 -3.46 5.36 SNP21394-SNP46209 32375997-32618214 2017
q-2017BH-C01-1 C01 6.16 6.22 12.17 SNP38247-SNP38236 11120369-11162114 2017
q-BLUP-BH-A05-1 A05 2.76 1.25 5.12 SNP11708-SNP11713 20293807-20374178 BLUP
q-BLUP-BH-A09-1 A09 4.60 -1.66 9.32 SNP21425-SNP21477 32728408-33029776 BLUP
q-BLUP-BH-A09-2 A09 6.52 -1.95 13.09 SNP21413-SNP21402 32435925-32608817 BLUP
q-BLUP-BH-A09-3 A09 4.62 -1.64 9.48 SNP21405-SNP21415 32514368-32619386 BLUP
q-BLUP-BH-C05-1 C05 2.77 1.23 5.51 SNP44674-SNP47114 11206177-11417643 BLUP

Fig.3

Quantile-quantile plot for six models and Manhattan plots of association analysis using the optimal model for plant height and the first branch height in two years PH: plant height; BH: the first branch height; BLUP: best linear unbiased prediction."

Supplementary table 1

Summary of significant SNPs for plant height and the first branch height by using the best model"

性状
Trait
环境
Env.
模型
Model
位点
SNP
染色体
Chr.
位置
Position
域值
-lg (P)
贡献率
R2 (%)
PH 2016 K+PCA S3_24415510 A03 24415510 5.69 20.05
2017 K+PCA S2_4664084 A02 4664084 5.84 6.72
S7_19604035 A07 19604035 6.24 7.41
S7_19609237 A07 19609237 6.01 6.81
S7_19665408 A07 19665408 5.85 7.06
S7_19781536 A07 19781536 5.87 7.36
S7_19889261 A07 19889261 5.64 7.20
S7_19890772 A07 19890772 5.66 6.94
S7_19902486 A07 19902486 5.77 7.52
S7_19993228 A07 19993228 5.63 6.59
S7_19993448 A07 19993448 6.07 6.88
S7_19993458 A07 19993458 5.69 6.42
S7_19994131 A07 19994131 6.45 7.69
S7_19997901 A07 19997901 5.71 6.67
S7_19998470 A07 19998470 6.37 7.52
S7_19999615 A07 19999615 6.07 7.05
S7_19999649 A07 19999649 5.63 7.52
S7_20000927 A07 20000927 6.31 7.47
S7_20003694 A07 20003694 5.79 6.83
S7_20005472 A07 20005472 6.67 7.80
S7_20006012 A07 20006012 6.50 7.73
S7_20006528 A07 20006528 5.87 7.09
S7_20009397 A07 20009397 5.86 6.67
S7_20009417 A07 20009417 6.19 7.04
S7_20033861 A07 20033861 6.11 6.88
S7_20050137 A07 20050137 5.96 8.10
S7_20050232 A07 20050232 6.22 7.74
S7_20053742 A07 20053742 6.72 7.72
S7_20056543 A07 20056543 5.65 6.53
S7_20079034 A07 20079034 5.76 7.36
S7_20107214 A07 20107214 7.69 9.22
S7_20107455 A07 20107455 6.40 7.44
S7_20107531 A07 20107531 6.31 8.24
S7_20108117 A07 20108117 5.75 6.74
S7_20125834 A07 20125834 6.37 7.28
S7_20144336 A07 20144336 6.16 7.20
S7_20154451 A07 20154451 6.42 8.22
S7_20160199 A07 20160199 5.84 7.20
S7_20171415 A07 20171415 5.87 6.65
S7_20171839 A07 20171839 6.46 7.34
S7_20178594 A07 20178594 6.55 7.85
S7_20178844 A07 20178844 6.23 7.54
S7_20178851 A07 20178851 5.93 7.18
S7_20186093 A07 20186093 5.79 6.56
S7_20188262 A07 20188262 5.83 6.87
S7_20207662 A07 20207662 5.72 6.70
S7_20547520 A07 20547520 5.71 6.83
S16_30960716 C06 30960716 6.60 7.81
S16_30960741 C06 30960741 7.02 8.31
S16_31108747 C06 31108747 5.89 6.78
BLUP K+PCA S2_4664084 A02 4664084 6.36 7.07
S2_5390778 A02 5390778 5.90 7.03
S7_19604035 A07 19604035 6.64 7.71
S7_19607230 A07 19607230 6.02 6.75
S7_19609237 A07 19609237 5.96 6.47
S7_19665408 A07 19665408 6.05 6.92
S7_19749218 A07 19749218 6.29 7.29
S7_19781536 A07 19781536 6.10 7.37
S7_19856864 A07 19856864 5.73 6.34
S7_19889261 A07 19889261 5.75 7.08
S7_19902486 A07 19902486 5.92 7.19
S7_19902495 A07 19902495 5.69 7.19
S7_19902618 A07 19902618 5.59 6.50
S7_19911177 A07 19911177 5.83 6.72
S7_19923829 A07 19923829 5.68 6.33
S7_19923850 A07 19923850 5.84 6.42
S7_19989673 A07 19989673 5.61 6.35
S7_19993448 A07 19993448 6.07 6.54
S7_19993458 A07 19993458 5.61 6.01
S7_19994131 A07 19994131 6.02 6.74
S7_19997901 A07 19997901 6.04 6.71
S7_19998042 A07 19998042 5.80 6.38
S7_19998470 A07 19998470 5.88 6.50
S7_19999615 A07 19999615 6.09 6.66
S7_20000927 A07 20000927 6.31 7.10
S7_20003694 A07 20003694 6.14 6.84
S7_20005472 A07 20005472 6.76 7.50
S7_20006012 A07 20006012 6.97 7.94
S7_20006186 A07 20006186 5.73 6.36
S7_20006210 A07 20006210 5.77 6.38
S7_20006234 A07 20006234 5.81 6.73
S7_20006528 A07 20006528 6.10 7.05
S7_20008610 A07 20008610 5.71 6.89
S7_20009397 A07 20009397 6.23 6.79
S7_20009417 A07 20009417 6.59 7.15
S7_20030774 A07 20030774 5.75 6.16
S7_20050137 A07 20050137 6.12 7.78
S7_20050232 A07 20050232 6.84 8.25
S7_20050979 A07 20050979 5.61 6.24
S7_20053742 A07 20053742 6.52 7.07
S7_20057981 A07 20057981 5.77 7.00
S7_20082865 A07 20082865 5.76 7.54
S7_20107214 A07 20107214 7.94 8.87
S7_20107455 A07 20107455 6.83 7.64
S7_20107531 A07 20107531 7.26 9.02
S7_20108117 A07 20108117 5.95 6.64
S7_20125834 A07 20125834 6.23 6.77
S7_20144336 A07 20144336 6.62 7.31
S7_20154451 A07 20154451 6.55 7.99
S7_20160199 A07 20160199 6.36 7.53
S7_20171415 A07 20171415 6.24 6.68
S7_20171839 A07 20171839 6.30 6.80
S7_20178594 A07 20178594 6.59 7.55
S7_20178844 A07 20178844 5.93 6.86
S7_20186093 A07 20186093 6.22 6.69
S7_20188262 A07 20188262 6.11 6.84
S7_20198799 A07 20198799 5.65 6.49
S7_20207662 A07 20207662 5.79 6.43
S7_20429083 A07 20429083 5.63 6.38
S7_20547520 A07 20547520 6.69 7.75
S7_20567053 A07 20567053 5.67 6.06
S12_38247607 C02 38247607 5.70 6.43
S16_30166343 C06 30166343 5.96 6.92
S16_30650628 C06 30650628 5.62 6.27
S16_30960716 C06 30960716 6.66 7.47
S16_30960741 C06 30960741 7.24 8.08
S16_31108747 C06 31108747 6.36 6.99
BH 2016 K S13_3400444 C03 3400444 5.67 16.87
S13_12620221 C03 12620221 5.70 16.89
S14_36535069 C04 36535069 5.76 18.36
S19_41983822 C09 41983822 5.75 17.28
2017 K+PCA S2_1549097 A02 1549097 5.80 7.63
S2_1553600 A02 1553600 6.39 7.73
S2_5424292 A02 5424292 6.14 7.01
S2_5503092 A02 5503092 6.19 7.32
S2_5827516 A02 5827516 6.66 7.95
S2_6130942 A02 6130942 5.76 7.02
S12_10249838 C02 10249838 6.06 6.23
S15_7059739 C05 7059739 5.92 6.80
BLUP K+PCA S2_1553600 A02 1553600 5.81 6.55
S2_5503092 A02 5503092 6.09 6.83
S2_5827516 A02 5827516 6.81 7.69
S2_9351215 A02 9351215 5.98 6.95
S2_9351221 A02 9351221 5.89 6.82
S12_10249838 C02 10249838 5.62 6.32
S15_7059739 C05 7059739 6.00 6.49

Table 4

Candidate genes for plant height and the first branch height"

基因
Gene
物理位置
Physical position
拟南芥同源基因
Homologs
in A. thaliana
功能注释
Functional annotation
株高PH
BnaA02g09200D A02:4555438-4557323 AT5G55180 O-Glycosyl hydrolases family 17 protein (MCO15.13)
BnaA02g09270D A02:4576434-4582446 AT5G55120 GDP-L-galactose phosphorylase VITAMIN C DEFECTIVE 5 (VTC5)
BnaA03g47940D A03:24664280-24664459 AT4G26320 Arabinogalactan protein 13 (AGP13)
BnaA04g17050D A04:13894646-13897338 AT5G65940 Beta-hydroxyisobutyryl-CoA hydrolase 1 (CHY1)
BnaA04g17120D A04:13961721-13963012 AT2G29350 Senescence-associated gene 13 (SAG13)
BnaA04g17490D A04:14227152-14227949 AT2G30370 Allergen-like protein (CHAL)
BnaA07g27280D A07:19859720-19860312 AT1G68590 Ribosomal protein PSRP-3/Ycf65
BnaA07g28720D A07:20705370-20707220 AT1G70210 CYCD1;1/CYCLIN D1;1
BnaA07g28820D A07:20767232-20773649 AT1G70710 Glycosyl hydrolase 9B1 (GH9B1)
BnaC02g35320D C02:38070292-38074778 AT2G04030 Chaperone protein htpG family protein (CR88)
BnaC06g30260D C06:31058017-31061313 AT1G68580 Agenet domain-containing protein / bromo-adjacent homology (BAH) domain-containing protein (F24J5.18)
BnaC06g30400D C06:31172511-31173663 AT1G69220 Protein kinase superfamily protein (SIK1)
BnaC06g30410D C06:31173893-31177895 AT1G69220 Protein kinase superfamily protein (SIK1)
一次有效分枝高度BH
BnaA01g25960D A01:18111689-18112090 AT3G47370 Ribosomal protein S10p/S20e family protein (RPS20B)
BnaA01g27550D A01:19232447-19236961 AT3G16840 P-loop containing nucleoside triphosphate hydrolases superfamily protein (RH13)
BnaA01g28120D A01:19629034-19630394 AT3G16240 Delta tonoplast integral protein (DELTA-TIP)
BnaA01g29630D A01:20485424-20487751 AT3G14067 Subtilase family protein (SASP)
BnaA01g30830D A01:21042542-21043677 AT3G12145 Leucine-rich repeat (LRR) family protein (FLOR1)
BnaA02g37010D A02:1536206-1537938 AT5G61780 TUDOR-SN protein 2 (Tudor2)
BnaA02g31980D A02:23032463-23034656 AT5G25460 Transmembrane protein, putative (Protein of unknown function, DUF642) (DGR2)
BnaA09g48360D A09:32409788-32410789 AT1G09580 Emp24/gp25L/p24 family/GOLD family protein (F14J9.28)
BnaA09g49220D A09:32795595-32796344 AT1G07830 Ribosomal protein L29 family protein (F24B9.7)
BnaC02g14570D C02:10095432-10098417 AT5G53120 Spermidine synthase 3 (SPDS3)
BnaC02g14600D C02:10119161-10122317 AT5G53090 NAD(P)-binding Rossmann-fold superfamily protein (MFH8.1)

Fig. 4

Relative expression of the candidate genes of plant height in stem apex The error bar shows the standard deviation of three biological replicates. * and ** indicate significantly different expression in stem apex to the control at P < 0.05 and P < 0.01, respectively."

Fig. 5

Relative expression of the candidate genes of the first branch height in stem apex The error bar shows the standard deviation of three biological replicates. * and ** indicate significantly different expression in stem apex to the control at P < 0.05 and P < 0.01, respectively."

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