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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (01): 147-153.doi: 10.3724/SP.J.1006.2020.94060

• RESEARCH NOTES • Previous Articles    

Genome-wide association study of seed number per silique in rapeseed (Brassica napus L.)

SUN Cheng-Ming1,2,CHEN Feng1,CHEN Song1,PENG Qi1,ZHANG Wei1,YI Bin2,*(),ZHANG Jie-Fu1,*(),FU Ting-Dong2   

  1. 1 Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences/Key Laboratory of Cotton and Rapeseed (Nanjing), Ministry of Agriculture/Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing 210014, Jiangsu, China
    2 National Key Laboratory of Crop Genetic Improvement/College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China;
  • Received:2019-04-15 Accepted:2019-08-09 Online:2020-01-12 Published:2019-09-11
  • Contact: Bin YI,Jie-Fu ZHANG E-mail:yibin@mail.hzau.edu.cn;jiefu_z@163.com
  • Supported by:
    The study was supported by the National Key Research and Development Program of China(2018YFD0100602);Earmarked Fund for China Agriculture Research System(CARS-12);Jiangsu Agriculture Science and Technology Innovation Fund(CX(19)3055-12);Natural Fund Project of Jiangsu Basic Research Program(BK20190260);Fundamental Research Funds for the Central Universities(2662016PY063)

Abstract:

Seed number per silique (SSN) is a key component of seed yield in rapeseed, increasing SSN can improve the seed yield of plants. A collection of 496 representative rapeseed accessions was genotyped by the Illumina 60K SNP array and phenotyped for SSN in two environments. The genome-wide association study (GWAS) of SSN was performed via the MLM (Mixed linear model) and GLM (General linear model). The broad-sense heritability of SSN was 57.7%. Nine and twenty loci were detected with MLM and GLM, respectively, and all loci detected by MLM were included those by GLM. Six loci were overlapped with reported QTLs, and two of them were validated by two independent researches, and the rest 14 loci were new. We identified plausible candidate genes nearby seven loci, and the reported rapeseed SSN gene BnaC9.SMG7b was found near the locus Bn-scaff_15576_1-p74980 on C09 chromosome detected in this study. Besides, six candidates orthologous to documented Arabidopsis SSN genes, like GRDP1, SPATULA, HVA22D, and DA2, were found near our GWAS loci. The results provide an insight into the genetic basis of seed number per silique and lay a foundation for further mechanism exploration and breeding for this trait in B. napus.

Key words: Brassica napus L., yield, seed number per silique, GWAS, SNP

Table 1

Statistical analysis of seed number per silique of the association panel"

环境
Environment
最小值
Min.
最大值
Max.
平均值±标准差
Mean ± SD
变异系数
CV
2014/2015 Taizhou 8.83 27.73 21.45±2.36 0.11
2015/2016 Taizhou 11.00 26.24 20.56±1.99 0.10

Fig. 1

Distribution of seed number per silique of the association panel in two environments"

Table 2

Significant GWAS loci of seed number per silique in MLM"

标记
Marker
染色体
Chr.
位置
Position
-lg (P) 表型变异
R2 (%)
环境
Environment
已报道QTL
Reported QTL
Bn-A01-p3904495 A01 3,530,446 5.01 0.03832 16TZ [5]
Bn-A04-p10393460 A04 11,537,744 5.15 0.03946 15TZ
Bn-A07-p22251229 A07 23,650,401 4.78 0.03896 15TZ
Bn-A08-p14749618 A08 12,312,967 4.37 0.03265 15TZ [7]
Bn-scaff_15936_1-p270915 C01 36,405,870 4.66 0.03521 BLUP [5-6]
Bn-scaff_15712_6-p1336179 C02 38,045,422 4.33 0.04469 15TZ, 16TZ
Bn-scaff_23954_1-p220801 C03 11,576,750 4.49 0.03371 15TZ
Bn-scaff_16027_1-p367097 C04 1,254,637 4.52 0.03698 15TZ
Bn-scaff_23907_1-p3780 C04 7,268,977 5.09 0.04605 BLUP

Fig. 2

Genome-wide association study of rapeseed seed number per silique (MLM) A: Manhattan plot of MLM based on BLUP value; B: Manhattan plot of MLM in15TZ; C: Manhattan plot of MLM in 16TZ. The dashed horizontal line depicts the Bonferroni significance threshold."

Table 3

Significant GWAS loci of seed number per silique in GLM"

标记
Marker
染色体
Chr.
位置
Position
-lg (P) 表型变异
R2 (%)
环境
Environment
已报道QTL
Reported QTL
Bn-A01-p3904495 A01 3,530,446 5.05 0.0357 16TZ [5]
Bn-A04-p10393460 A04 11,537,744 5.79 0.0408 15TZ
Bn-A07-p9916502 A07 11,196,091 4.50 0.0404 BLUP
Bn-A07-p22251229 A07 23,650,401 4.41 0.0322 15TZ
Bn-A08-p14749618 A08 12,312,967 4.74 0.0327 15TZ [7]
Bn-scaff_15838_1-p1554155 C01 1,926,096 4.41 0.0437 16TZ [8]
Bn-scaff_15936_1-p270915 C01 36,405,870 5.13 0.0353 BLUP [5-6]
Bn-scaff_15712_6-p1336179 C02 38,045,422 4.66 0.0435 16TZ
Bn-scaff_23954_1-p635109 C03 11,205,203 4.78 0.0330 15TZ
Bn-scaff_16027_1-p367097 C04 1,254,637 4.62 0.0365 15TZ
Bn-scaff_23907_1-p3780 C04 7,268,977 5.59 0.0483 15TZ,BLUP
Bn-scaff_19253_1-p524524 C04 15,606,945 4.29 0.0290 BLUP
Bn-scaff_15936_1-p357665 C05 9,508,115 4.78 0.0453 BLUP
Bn-scaff_16064_1-p1144443 C06 24,511,029 4.74 0.0327 15TZ
Bn-scaff_17484_1-p132976 C07 5,857,563 4.60 0.0317 15TZ
Bn-scaff_20084_1-p104549 C07 9,638,283 5.36 0.0375 15TZ
Bn-scaff_16069_1-p1651456 C07 38,070,340 5.23 0.0365 15TZ
Bn-scaff_16069_1-p3780494 C07 40,184,749 4.35 0.0302 16TZ
Bn-scaff_15808_1-p420800 C09 37,129,614 5.15 0.0365 16TZ [5]
Bn-scaff_15576_1-p74980 C09 41,126,168 4.35 0.0303 16TZ [5,19]

Fig. 3

Genome-wide association study of rapeseed seed number per silique (GLM) A: Manhattan plot of GLM based on BLUP value; B: Manhattan plot of GLM in 15TZ; C: Manhattan plot of GLM in 16TZ. The dashed horizontal line depicts the Bonferroni significance threshold."

Table 4

Information of candidate genes of seed number per silique GWAS loci"

标记
Marker
油菜基因
Rapeseed gene
染色体
Chr.
位置
Position
拟南芥同源基因
Ar. homolog
Bn-A04-p10393460 BnaA04g13080 A04 11,015,882 GRDP1
Bn-A07-p9916502 BnaA07g13170 A07 11,744,966 GLE1
Bn-A08-p14749618 BnaA08g15580 A08 12,923,783 SPATULA
Bn-scaff_23954_1-p635109 BnaC03g21140 C03 11,367,292 DA2
Bn-scaff_16069_1-p3780494 BnaC07g39210 C07 40,210,953 HVA22D
Bn-scaff_15808_1-p420800 BnaC09g33680 C09 36,922,347 MSI1
Bn-scaff_15576_1-p74980 BnaC09g38310 C09 41,208,383 SMG7b
[1] 王汉中 . 我国油菜产业发展的历史回顾与展望. 中国油料作物学报, 2010,32:300-302.
Wang H Z . Review and future development of rapeseed industry in China. Chin J Oil Crop Sci, 2010,32:300-302 (in Chinese with English abstract).
[2] 李永鹏, 程焱, 蔡光勤, 范楚川, 周永明 . 油菜每角果粒数差异的细胞学基础和分子机理. 中国科学: 生命科学, 2014,44:822-831.
Li Y P, Cheng Y, Cai G Q, Fan C C, Zhou Y M . Cytological basis and molecular mechanism of variation in number of seeds per pod in Brassica napus. Sci Sin Vitae, 2014,44:822-831 (in Chinese with English abstract).
[3] Yang Y, Wang Y, Zhan J, Shi J, Wang X, Liu G, Wang H . Genetic and cytological analyses of the natural variation of seed number per pod in rapeseed (Brassica napus L.). Front Plant Sci, 2017,8:1890. doi: 10.3389/fpls.2017.01890.
doi: 10.3389/fpls.2017.01890 pmid: 29163611
[4] Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J . Unraveling the complex trait of crop yield with quantitative trait loci mapping inBrassica napus. Genetics, 2009,182:851-861.
doi: 10.1534/genetics.109.101642 pmid: 19414564
[5] Luo Z, Wang M, Long Y, Huang Y, Shi L, Zhang C, Liu X, Fitt B D, Xiang J, Mason A S . Incorporating pleiotropic quantitative trait loci in dissection of complex traits: seed yield in rapeseed as an example. Theor Appl Genet, 2017,130:1569-1585.
doi: 10.1007/s00122-017-2911-7 pmid: 28455767
[6] 漆丽萍 . 甘蓝型油菜株型与角果相关性状的QTL分析. 华中农业大学博士学位论文, 湖北武汉, 2014.
Qi L P . QTL Analysis for the Traits Associated with Plant Architecture and Silique in Brassica napus L. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hubei, China, 2014 (in Chinese with English abstract).
[7] Cai G, Yang Q, Chen H, Yang Q, Zhang C, Fan C, Zhou Y . Genetic dissection of plant architecture and yield-related traits in Brassica napus. Sci Rep, 2016,6:21625. doi: 10.1038/srep 21625.
doi: 10.1038/srep21625 pmid: 26880301
[8] Yang Y, Shi J, Wang X, Liu G, Wang H . Genetic architecture and mechanism of seed number per pod in rapeseed: elucidated through linkage and near-isogenic line analysis. Sci Rep, 2016,6:24124. doi: 10.1038/srep24124.
doi: 10.1038/srep24124 pmid: 27067010
[9] Sun C, Wang B, Yan L, Hu K, Liu S, Zhou Y, Guan C, Zhang Z, Li J, Zhang J, Chen S, Wen J, Ma C, Tu J, Shen J, Fu T, Yi B . Genome-wide association study provides insight into the genetic control of plant height in rapeseed (Brassica napus L.). Front Plant Sci, 2016,7:1102. doi: 10.3389/fpls.2016.01102.
doi: 10.3389/fpls.2016.01102 pmid: 27512396
[10] Lu K, Wei L, Li X, Wang Y, Wu J, Liu M, Zhang C, Chen Z, Xiao Z, Jian H . Whole-genome resequencing revealsBrassica napus origin and genetic loci involved in its improvement. Nat Commun, 2019,10:1154. doi: 10.1038/s41467-019-09134-9.
doi: 10.1038/s41467-019-09134-9 pmid: 30858362
[11] Chen L, Wan H, Qian J, Guo J, Sun C, Wen J, Yi B, Ma C, Tu J, Song L . Genome-wide association study of cadmium accumulation at the seedling stage in rapeseed (Brassica napus L.). Front Plant Sci, 2018,9:375. doi: 10.3389/fpls.2018.00375.
doi: 10.3389/fpls.2018.00375 pmid: 29725340
[12] Xu L, Hu K, Zhang Z, Guan C, Chen S, Hua W, Li J, Wen J, Yi B, Shen J . Genome-wide association study reveals the genetic architecture of flowering time in rapeseed (Brassica napus L.). DNA Res, 2015,23:43-52.
doi: 10.1093/dnares/dsv035 pmid: 26659471
[13] Merk H L, Yarnes S C, Van Deynze A, Tong N, Menda N, Mueller L A, Mutschler M A, Loewen S A, Myers J R, Francis D M . Trait diversity and potential for selection indices based on variation among regionally adapted processing tomato germplasm. J Am Soc Hortic Sci, 2012,137:427-437.
[14] Ihaka R, Gentleman R . R: a language for data analysis and graphics. J Comput Graph Stat, 1996,5:299-314.
doi: 10.1002/rcm.8315 pmid: 30366355
[15] Evanno G, Regnaut S, Goudet J . Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol, 2005,14:2611-2620.
doi: 10.1111/j.1365-294X.2005.02553.x pmid: 15969739
[16] Hardy O J, Vekemans X . SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes, 2002,2:618-620.
doi: 10.1016/j.yebeh.2019.106687 pmid: 31816478
[17] Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S . TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics, 2007,23:2633-2635.
doi: 10.1093/bioinformatics/btm308 pmid: 17586829
[18] Turner S D . qqman: an R package for visualizing GWAS results using QQ and manhattan plots. BioRxiv, 2014, 1: 005165. doi: http://dx.doi.org/10.1101/005165.
[19] Li S, Chen L, Zhang L, Li X, Liu Y, Wu Z, Dong F, Wan L, Liu K, Hong D . BnaC9. SMG7b functions as a positive regulator of the number of seeds per silique in Brassica napus by regulating the formation of functional female gametophytes. Plant Physiol, 2015,169:2744-2760.
doi: 10.1104/pp.15.01040 pmid: 26494121
[20] Rodríguez-Hernández A A, Muro-Medina C V, Ramírez-Alonso J I, Jiménez-Bremont J F . Modification of AtGRDP1 gene expression affects silique and seed development inArabidopsis thaliana. Biochem Biophys Res Common, 2017,486:252-256.
doi: 10.1016/j.bbrc.2017.03.015 pmid: 28285133
[21] Xia T, Li N, Dumenil J, Li J, Kamenski A, Bevan M W, Gao F, Li Y . The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell, 2013,25:3347-3359.
doi: 10.1105/tpc.113.115063
[22] Braud C, Zheng W, Xiao W . LONO1 encoding a nucleoporin is required for embryogenesis and seed viability in Arabidopsis. Plant Physiol, 2012,160:823-836.
doi: 10.1104/pp.112.202192 pmid: 22898497
[23] Groszmann M, Paicu T, Smyth D R . Functional domains of SPATULA, a bHLH transcription factor involved in carpel and fruit development in Arabidopsis. Plant J, 2008,55:40-52.
doi: 10.1111/j.1365-313X.2008.03469.x pmid: 18315540
[24] Chen N N, Chen H R, Yeh S Y, Vittore G, Ho H D . Autophagy is enhanced and floral development is impaired in AtHVA22d RNA interference Arabidopsis. Plant Physiol, 2009,149:1679-1689.
doi: 10.1104/pp.108.131490 pmid: 19151132
[25] Leroy O, Hennig L, Breuninger H, Laux T, Köhler C . Polycomb group proteins function in the female gametophyte to determine seed development in plants. Development, 2007,134:3639-3648.
doi: 10.1242/dev.009027 pmid: 17855429
[26] Yang Y, Zhu K, Li H, Han S, Meng Q, Khan S U, Fan C, Xie K, Zhou Y . Precise editing of CLAVATA genes in Brassica napus L. regulates multilocular silique development. Plant Biotechnol J, 2018,16:1322-1335.
doi: 10.1111/pbi.12872 pmid: 29250878
[27] Shah S, Karunarathna N L, Jung C, Emrani N . An APETALA1 ortholog affects plant architecture and seed yield component in oilseed rape (Brassica napus L.). BMC Plant Biol, 2018,18:380. doi: 10.1186/s12870-018-1606-9.
doi: 10.1186/s12870-018-1606-9 pmid: 30594150
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