Skip to main content
SpringerLink
Log in

A 24,482-bp deletion is associated with increased seed weight in Brassica napus L.

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

A major QTL for seed weight was fine-mapped in rapeseed, and a 24,482-bp deletion likely mediates the effect through multiple pathways.

Abstract

Exploration of the genes controlling seed weight is critical to the improvement of crop yield and elucidation of the mechanisms underlying seed formation in rapeseed (Brassica napus L.). We previously identified the quantitative trait locus (QTL) qSW.C9 for the thousand-seed weight (TSW) in a double haploid population constructed from F1 hybrids between the parental accessions HZ396 and Y106. Here, we confirmed the phenotypic effects associated with qSW.C9 in BC3F2 populations and fine-mapped the candidate causal locus to a 266-kb interval. Sequence and expression analyses revealed that a 24,482-bp deletion in HZ396 containing six predicted genes most likely underlies qSW.C9. Differential gene expression analysis and cytological observations suggested that qSW.C9 affects both cell proliferation and cell expansion through multiple signaling pathways. After genotyping of a rapeseed diversity panel to define the haplotype structure, it could be concluded that the selection of germplasm with two specific markers may be effective in improving the seed weight of rapeseed. This study provides a solid foundation for the identification of the causal gene of qSW.C9 and offers a promising target for the breeding of higher-yielding rapeseed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abe Y, Mieda K, Ando T, Kono I, Yano M, Kitano H, Iwasaki Y (2010) The SMALL AND ROUND SEED1 (SRS1/DEP2) gene is involved in the regulation of seed size in rice. Genes Genet Syst 85:327–339

    Article  CAS  PubMed  Google Scholar 

  • Ali MRM, Uemura T, Ramadan A, Adachi K, Nemoto K, Nozawa A, Hoshino R, Abe H, Sawasaki T, Arimura GI (2019) The ring-type E3 Ubiquitin Ligase JUL1 targets the VQ-Motif protein JAV1 to coordinate Jasmonate signaling. Plant Physiol 179:1273–1284

    Article  CAS  PubMed  Google Scholar 

  • Bashandy T, Meyer Y, Reichheld JP (2011) Redox regulation of auxin signaling and plant development in Arabidopsis. Plant Signal Behav 6:117–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basunanda P, Radoev M, Ecke W, Friedt W, Becker HC, Snowdon RJ (2010) Comparative mapping of quantitative trait loci involved in heterosis for seedling and yield traits in oilseed rape (Brassica napus L.). Theor Appl Genet 120:271–281

    Article  CAS  PubMed  Google Scholar 

  • Besnard J, Zhao C, Avice JC, Vitha S, Hyodo A, Pilot G, Okumoto S (2018) Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading. J Exp Bot 69:5221–5232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bencivenga S, Serrano-Mislata A, Bush M, Fox S, Sablowski R (2016) Control of oriented tissue growth through repression of organ boundary genes promotes stem morphogenesis. Dev Cell 39:198–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulankova P, Akimcheva S, Fellner N, Riha K (2013) Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes. PLoS Genet 9:e1003508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulankova P, Riehs-Kearnan N, Nowack MK, Schnittger A, Riha K (2010) Meiotic progression in Arabidopsis is governed by complex regulatory interactions between SMG7, TDM1, and the meiosis I-specific cyclin TAM. Plant Cell 22:3791–3803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai D, Xiao Y, Yang W, Ye W, Wang B, Younas M, Wu J, Liu K (2014) Association mapping of six yieldrelated traits in rapeseed (Brassica napus L.). Theor Appl Genet 127:85–96

    Article  CAS  PubMed  Google Scholar 

  • Carvalho SD, Chatterjee M, Coleman L, Clancy MA, Folta KM (2016) Analysis of Block of cell proliferation 1 (BOP1) activity in strawberry and Arabidopsis. Plant Sci 245:84–93

    Article  CAS  PubMed  Google Scholar 

  • Chalhoub B, Denoeud F, Liu S et al (2014) Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 345:950–953

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Dong F, Cai J, Xin Q, Fang C, Liu L, Wan L, Yang G, Hong D (2018a) A 2.833-kb insertion in BnFLC.A2 and its homeologous exchange with BnFLC.C2 during breeding selection generated early-flowering rapeseed. Mol Plant 11:222–225

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ, Lin IW, Qu XQ, Sosso D, McFarlane HE, Londono A, Samuels AL, Frommer WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018b) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen W, Zhang Y, Liu X, Chen B, Tu J, Fu TD (2007) Detection of QTL for six yield-related traits in oilseed rape (Brassica napus) using DH and immortalized F2 populations. Theor Appl Genet 115:849–858

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Sun S, Wang X (2020) The epidermis-specific cyclin CYCP3;1 is involved in the excess brassinosteroid signaling-inhibited root meristem cell division. J Integr Plant Biol 62:1674–1687

    Article  CAS  PubMed  Google Scholar 

  • Cipollini D (2007) Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana. New Phytol 173:146–153

    Article  CAS  PubMed  Google Scholar 

  • Cucinotta M, Cavalleri A, Guazzotti A, Astori C, Manrique S, Bombarely A, Oliveto S, Biffo S, Weijers D, Kater MM, Colombo L (2020) Alternative splicing generates a MONOPTEROS isoform required for ovule development. Curr Biol 31:1–8

    Google Scholar 

  • Darnet S, Martin LBB, Mercier P, Bracher F, Geoffroy P, Schaller H (2020) Inhibition of Phytosterol biosynthesis by Azasterols. Molecules 25:1111

    Article  CAS  PubMed Central  Google Scholar 

  • DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16

    Article  CAS  PubMed  Google Scholar 

  • Du L, Li N, Chen L, Xu Y, Li Y, Zhang Y, Li C, Li Y (2014) The ubiquitin receptor DA1 regulates seed and organ size by modulating the stability of the ubiquitin-specific protease UBP15/SOD2 in Arabidopsis. Plant Cell 26:665–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan P, Xu J, Zeng D, Zhang B, Geng M, Zhang G, Huang K, Huang L, Xu R, Ge S, Qian Q, Li Y (2017) natural variation in the promoter of GSE5 Contributes to grain size diversity in rice. Mol Plant 10:685–694

    Article  CAS  PubMed  Google Scholar 

  • Eriksson S, Stransfeld L, Adamski NM, Breuninger H, Lenhard M (2010) KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis. Curr Biol 20:527–532

    Article  CAS  PubMed  Google Scholar 

  • Etchells JP, Provost CM, Turner SR (2012) Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genet 8:e1002997

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fan C, Cai G, Qin J, Li Q, Yang M, Wu J, Fu T, Liu K, Zhou Y (2010) Mapping of quantitative trait loci and development of allele-specific markers for seed weight in Brassica napus. Theor Appl Genet 121:1289–1301

    Article  CAS  PubMed  Google Scholar 

  • Fang W, Wang Z, Cui R, Li J, Li Y (2012) Maternal control of seed size by EOD3/CYP78A6 in Arabidopsis thaliana. Plant J 70:929–939

    Article  CAS  PubMed  Google Scholar 

  • Fattahi F, Fakheri BA, Solouki M, Möllers C, Rezaizad A (2018) Mapping QTL controlling agronomic traits in a doubled haploid population of winter oilseed rape (Brassica napus L.). J Genet 97:1389–1406

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Wei D, Dong H, He Y, Cui Y, Mei J, Wan H, Li J, Snowdon R, Friedt W, Li X, Qian W (2015) Comparative quantitative trait loci for silique length and seed weight in Brassica napus. Sci Rep 5:14407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao T, Wu Y, Zhang Y, Liu L, Ning Y, Wang D, Tong H, Chen S, Chu C, Xie Q (2011) OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol Biol 76:145–156

    Article  CAS  PubMed  Google Scholar 

  • Huang K, Wang D, Duan P, Zhang B, Xu R, Li N, Li Y (2017) WIDE AND THICK GRAIN 1, which encodes an otubain-like protease with deubiquitination activity, influences grain size and shape in rice. Plant J 91:849–860

    Article  CAS  PubMed  Google Scholar 

  • Hussain Q, Shi J, Scheben A, Zhan J, Wang X, Liu G, Yan G, King GJ, Edwards D, Wang H (2020) Genetic and signalling pathways of dry fruit size: targets for genome editing-based crop improvement. Plant Biotechnol J 18:1124–1140

    Article  PubMed  PubMed Central  Google Scholar 

  • Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR, Kieber JJ (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huysmans M, Buono RA, Skorzinski N, Radio MC, De Winter F, Parizot B, Mertens J, Karimi M, Fendrych M, Nowack MK (2018) NAC transcription factors ANAC087 and ANAC046 control distinct aspects of programmed cell death in the Arabidopsis columella and lateral root cap. Plant Cell 30:2197–2213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jha AK, Wang Y, Hercyk BS, Shin HS, Chen R, Yang M (2014) The role for CYCLIN A1;2/TARDY ASYNCHRONOUS MEIOSIS in differentiated cells in Arabidopsis. Plant Mol Biol 85:81–94

    Article  CAS  PubMed  Google Scholar 

  • Kerenyi F, Wawer I, Sikorski PJ, Kufel J, Silhavy D (2013) Phosphorylation of the N- and C-terminal UPF1 domains plays a critical role in plant nonsense-mediated mRNA decay. Plant J 76:836–848

    Article  CAS  PubMed  Google Scholar 

  • Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T, Sano N, Koshiba T, Kamiya Y, Ueda M, Seo M (2016) AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat Commun 7:13245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kathare PK, Dharmasiri S, Dharmasiri N (2018) SAUR53 regulates organ elongation and apical hook development in Arabidopsis. Plant Signal Behav 13:e1514896

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan MHU, Hu L, Zhu M, Zhai Y, Khan SU, Ahmar S, Amoo O, Zhang K, Fan C, Zhou Y (2021) Targeted mutagenesis of EOD3 gene in Brassica napus L. regulates seed production. J Cell Physiol 236:1996–2007

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37:907–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim EH, Kim YS, Park SH, Koo YJ, Choi YD, Chung YY, Lee IJ, Kim JK (2009) Methyl jasmonate reduces grain yield by mediating stress signals to alter spikelet development in rice. Plant Physiol 149:1751–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knox AK, Dhillon T, Cheng H, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35

    Article  PubMed  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee BH, Kwon SH, Lee SJ, Park SK, Song JT, Lee S, Lee MM, Hwang YS, Kim JH (2015) The Arabidopsis thaliana NGATHA transcription factors negatively regulate cell proliferation of lateral organs. Plant Mol Biol 89:529–538

    Article  CAS  PubMed  Google Scholar 

  • Lee KH, Park SW, Kim YJ, Koo YJ, Song JT, Seo HS (2018) Grain width 2 (GW2) and its interacting proteins regulate seed development in rice (Oryza sativa L.). Bot Stud 59:23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee WC, Hou BH, Hou CY, Tsao SM, Kao P, Chen HM (2020) Widespread exon junction complex footprints in the RNA degradome mark mRNA degradation before steady state translation. Plant Cell 32:904–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Chen B, Xu K, Wu J, Song W, Bancroft I, Harper AL, Trick M, Liu S, Gao G, Wang N, Yan G, Qiao J, Li J, Li H, Xiao X, Zhang T, Wu X (2014) Genome-wide association study dissects the genetic architecture of seed weight and seed quality in rapeseed (Brassica napus L.). DNA Res 21:355–367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li N, Li Y (2014) Ubiquitin-mediated control of seed size in plants. Front Plant Sci 5:332

    Article  PubMed  PubMed Central  Google Scholar 

  • Li N, Song D, Peng W, Zhan J, Shi J, Wang X, Liu G, Wang H (2019a) Maternal control of seed weight in rapeseed (Brassica napus L.): the causal link between the size of pod (mother, source) and seed (offspring, sink). Plant Biotechnol J 17:736–749

    Article  CAS  PubMed  Google Scholar 

  • Li N, Xu R, Duan P, Li Y (2018) Control of grain size in rice. Plant Reprod 31:237–251

    Article  CAS  PubMed  Google Scholar 

  • Li N, Xu R, Li Y (2019b) Molecular networks of seed size control in plants. Annu Rev Plant Biol 70:435–463

    Article  CAS  PubMed  Google Scholar 

  • Li S, Chen L, Zhang L, Li X, Liu Y, Wu Z, Dong F, Wan L, Liu K, Hong D, Yang G (2015) BnaC9.SMG7b functions as a positive regulator of number of seeds per silique in rapeseed (Brassica napus L.) by regulating the formation of functional female gametophytes. Plant Physiol 169:2744–2760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, He Y, Zhang Q (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Xiao J, Wu J, Duan J, Liu Y, Ye X, Zhang X, Guo X, Gu Y, Zhang L, Jia J, Kong X (2012) A tandem segmental duplication (TSD) in green revolution gene Rht-D1b region underlies plant height variation. New Phytol 196:282–291

    Article  CAS  PubMed  Google Scholar 

  • Liao S, Wang L, Li J, Ruan YL (2020) Cell wall invertase is essential for ovule development through sugar signaling rather than provision of carbon nutrients. Plant Physiol 183:1126–1144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Hua W, Hu Z, Yang H, Zhang L, Li R, Deng L, Sun X, Wang X, Wang H (2015) Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed. Proc Natl Acad Sci 112:E5123–E5132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Xia Z, Wang M, Zhang X, Yang T, Wu J (2013) Overexpression of a maize E3 ubiquitin ligase gene enhances drought tolerance through regulating stomatal aperture and antioxidant system in transgenic tobacco. Plant Physiol Biochem 73:114–120

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhou X, Yan M, Wang P, Wang H, Xin Q, Yang L, Hong D, Yang G (2020a) Fine mapping and candidate gene analysis of a seed glucosinolate content QTL, qGSL-C2, in rapeseed (Brassica napus L.). Theor Appl Genet 133:479–490

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Li N, Zhang Y, Li Y (2020b) Transcriptional repression of GIF1 by the KIX-PPD-MYC repressor complex controls seed size in Arabidopsis. Nat Commun 11:1846

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu K, Peng L, Zhang C, Lu J, Yang B, Xiao Z, Liang Y, Xu X, Qu C, Zhang K, Liu L, Zhu Q, Fu M, Yuan X, Li J (2017) Genome-wide association and transcriptome analyses reveal candidate genes underlying yield-determining traits in Brassica napus. Front Plant Sci 8:206

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyu J, Wang D, Duan P, Liu Y, Huang K, Zeng D, Zhang L, Dong G, Li Y, Xu R, Zhang B, Huang X, Li N, Wang Y, Qian Q, Li Y (2020) Control of grain size and weight by the GSK2-LARGE1/OML4 pathway in rice. Plant Cell 32:1905–1918

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma M, Zhao H, Li Z, Hu S, Song W, Liu X (2016) TaCYP78A5 regulates seed size in wheat (Triticum aestivum). J Exp Bot 67:1397–1410

    Article  CAS  PubMed  Google Scholar 

  • Mao P, Duan M, Wei C, Li Y (2007) WRKY62 transcription factor acts downstream of cytosolic NPR1 and negatively regulates jasmonate-responsive gene expression. Plant Cell Physiol 48:833–842

    Article  CAS  PubMed  Google Scholar 

  • Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Pineros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci U S A 110:5241–5246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet 17(1):10–12

    Article  Google Scholar 

  • Miller C, Wells R, McKenzie N, Trick M, Ball J, Fatihi A, Dubreucq B, Chardot T, Lepiniec L, Bevan MW (2019) Variation in expression of the HECT E3 Ligase UPL3 modulates LEC2 levels, seed size, and crop yields in Brassica napus. Plant Cell 31:2370–2385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran CN, Halliday KJ (2010) Fruit development: new directions for an old pathway. Curr Biol 20:R1081-1083

    Article  CAS  PubMed  Google Scholar 

  • Müller B, Fastner A, Karmann J, Mansch V, Hoffmann T, Schwab W, Suter-Grotemeyer M, Rentsch D, Truernit E, Ladwig F, Bleckmann A, Dresselhaus T, Hammes Ulrich Z (2015) Amino acid export in developing Arabidopsis seeds depends on UmamiT facilitators. Curr Biol 25:3126–3131

    Article  PubMed  CAS  Google Scholar 

  • Nguyen NH, Nguyen CTT, Jung C, Cheong JJ (2019) AtMYB44 suppresses transcription of the late embryogenesis abundant protein gene AtLEA4-5. Biochem Biophys Res Commun 511:931–934

    Article  CAS  PubMed  Google Scholar 

  • Oh K, Matsumoto T, Yamagami A, Hoshi T, Nakano T, Yoshizawa Y (2015) Fenarimol, a Pyrimidine-Type fungicide, inhibits Brassinosteroid biosynthesis. Int J Mol Sci 16:17273–17288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohashi-Ito K, Iwamoto K, Nagashima Y, Kojima M, Sakakibara H, Fukuda H (2019) A positive feedback loop comprising LHW–TMO5 and local Auxin biosynthesis regulates initial vascular development in Arabidopsis roots. Plant Cell Physiol 60:2684–2691

    Article  CAS  PubMed  Google Scholar 

  • Oshima Y, Mitsuda N (2013) The MIXTA-like transcription factor MYB16 is a major regulator of cuticle formation in vegetative organs. Plant Signal Behav 8:e26826

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Raboanatahiry N, Chao H, Dalin H, Pu S, Yan W, Yu L, Wang B, Li M (2018) QTL Alignment for seed yield and yield related traits in Brassica napus. Front Plant Sci 9:1127

    Article  PubMed  PubMed Central  Google Scholar 

  • Raxwal VK, Simpson CG, Gloggnitzer J, Entinze JC, Guo W, Zhang R, Brown JWS, Riha K (2020) Nonsense-mediated RNA decay factor UPF1 is critical for Posttranscriptional and translational gene regulation in Arabidopsis. Plant Cell 32:2725–2741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riehs-Kearnan N, Gloggnitzer J, Dekrout B, Jonak C, Riha K (2012) Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response. Nucleic Acids Res 40:5615–5624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampedro J, Gianzo C, Iglesias N, Guitian E, Revilla G, Zarra I (2012) AtBGAL10 is the main xyloglucan β-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158:1146–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schommer C, Debernardi JM, Bresso EG, Rodriguez RE, Palatnik JF (2014) Repression of cell proliferation by miR319-regulated TCP4. Mol Plant 7:1533–1544

    Article  CAS  PubMed  Google Scholar 

  • Sestili F, Pagliarello R, Zega A, Saletti R, Pucci A, Botticella E, Masci S, Tundo S, Moscetti I, Foti S, Lafiandra D (2019) Enhancing grain size in durum wheat using RNAi to knockdown GW2 genes. Theor Appl Genet 132:419–429

    Article  CAS  PubMed  Google Scholar 

  • Shi L, Song J, Guo C, Wang B, Guan Z, Yang P, Chen X, Zhang Q, King GJ, Wang J, Liu K (2019) A CACTA-like transposable element in the upstream region of BnaA9.CYP78A9 acts as an enhancer to increase silique length and seed weight in rapeseed. Plant J 98:524–539

    Article  CAS  PubMed  Google Scholar 

  • Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmonds J, Scott P, Brinton J, Mestre TC, Bush M, Del Blanco A, Dubcovsky J, Uauy C (2016) A splice acceptor site mutation in TaGW2-A1 increases thousand grain weight in tetraploid and hexaploid wheat through wider and longer grains. Theor Appl Genet 129:1099–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song JM, Guan Z, Hu J, Guo C, Yang Z, Wang S, Liu D, Wang B, Lu S, Zhou R, Xie WZ, Cheng Y, Zhang Y, Liu K, Yang QY, Chen LL, Guo L (2020) Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat Plants 6:34–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song W-m, Cheng Z-h, Guo X-t, Yu C-y, Wang H-h, Wang J, Li B, Zhang H-x, Bao Y (2019) Overexpression of NHL6 affects seed production in transgenic Arabidopsis plants. Plant Growth Regul 88:41–47

    Article  CAS  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Wang X, Yu K, Li W, Peng Q, Chen F, Zhang W, Fu S, Xiong D, Chu P, Guan R, Zhang J (2018) Mapping of QTLs controlling seed weight and seed-shape traits in Brassica napus L. using a high-density SNP map. Euphytica 214:228

    Article  CAS  Google Scholar 

  • Takahashi I, Kojima S, Sakaguchi N, Umeda-Hara C, Umeda M (2010) Two Arabidopsis cyclin A3s possess G1 cyclin-like features. Plant Cell Rep 29:307–315

    Article  CAS  PubMed  Google Scholar 

  • Takubo E, Kobayashi M, Hirai S, Aoi Y, Ge C, Dai X, Fukui K, Hayashi KI, Zhao Y, Kasahara H (2020) Role of Arabidopsis INDOLE-3-ACETIC ACID CARBOXYL METHYLTRANSFERASE 1 in auxin metabolism. Biochem Biophys Res Commun 527:1033–1038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taleski M, Chapman K, Imin N, Djordjevic MA, Groszmann M (2020) The peptide hormone receptor CEPR1 functions in the reproductive tissue to control seed size and yield. Plant Physiol 183:620–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang S, Zhao H, Lu S, Yu L, Zhang G, Zhang Y, Yang QY, Zhou Y, Wang X, Ma W, Xie W, Guo L (2020) Genome- and transcriptome-wide association studies provide insights into the genetic basis of natural variation of seed oil content in Brassica napus. Mol Plant 14:470

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Zhao X, Mace E, Henry R, Jordan D (2019) Exploring and exploiting pan-genomics for crop improvement. Mol Plant 12:156–169

    Article  CAS  PubMed  Google Scholar 

  • Thorvaldsdottir H, Robinson JT, Mesirov JP (2012) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • USDA ERS (2020) https://www.ers.usda.gov/data-products/oil-cropsyearbook/

  • Wang H, Yan M, Xiong M, Wang P, Liu Y, Xin Q, Wan L, Yang G, Hong D (2020a) Genetic dissection of thousand-seed weight and fine mapping of cqSW.A03-2 via linkage and association analysis in rapeseed (Brassica napus L.). Theor Appl Genet 133:1321–1335

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Wang R, Mao X, Zhang J, Liu Y, Xie Q, Yang X, Chang X, Li C, Zhang X, Jing R (2020b) RING finger ubiquitin E3 ligase gene TaSDIR1–4A contributes to grain size in common wheat. J Exp Bot 71:5377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JL, Tang MQ, Chen S, Zheng XF, Mo HX, Li SJ, Wang Z, Zhu KM, Ding LN, Liu SY, Li YH, Tan XL (2017) Down-regulation of BnDA1, whose gene locus is associated with the seeds weight, improves the seeds weight and organ size in Brassica napus. Plant Biotechnol J 15:1024–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Lu Q, Wen X, Lu C (2015a) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Simmonds J, Pan Q, Davidson D, He F, Battal A, Akhunova A, Trick HN, Uauy C, Akhunov E (2018) Gene editing and mutagenesis reveal inter-cultivar differences and additivity in the contribution of TaGW2 homoeologues to grain size and weight in wheat. Theor Appl Genet 131:2463–2475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XC, Wu J, Guan ML, Zhao CH, Geng P, Zhao Q (2020c) Arabidopsis MYB4 plays dual roles in flavonoid biosynthesis. Plant J 101:637–652

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xiong G, Hu J, Jiang L, Yu H, Xu J, Fang Y, Zeng L, Xu E, Xu J, Ye W, Meng X, Liu R, Chen H, Jing Y, Wang Y, Zhu X, Li J, Qian Q (2015b) Copy number variation at the GL7 locus contributes to grain size diversity in rice. Nat Genet 47:944–948

    Article  CAS  PubMed  Google Scholar 

  • Wurschum T, Boeven PH, Langer SM, Longin CF, Leiser WL (2015) Multiply to conquer: Copy number variations at Ppd-B1 and Vrn-A1 facilitate global adaptation in wheat. BMC Genet 16:96

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xia T, Li N, Dumenil J, Li J, Kamenski A, Bevan MW, Gao F, Li Y (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25:3347–3359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie G, Li Z, Ran Q, Wang H, Zhang J (2018) Over-expression of mutated ZmDA1 or ZmDAR1 gene improves maize kernel yield by enhancing starch synthesis. Plant Biotechnol J 16:234–244

    Article  CAS  PubMed  Google Scholar 

  • Xu FQ, Xue HW (2019) The ubiquitin-proteasome system in plant responses to environments. Plant Cell Environ 42:2931–2944

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Duan P, Yu H, Zhou Z, Zhang B, Wang R, Li J, Zhang G, Zhuang S, Lyu J, Li N, Chai T, Tian Z, Yao S, Li Y (2018) Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant 11:860–873

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Wendrich JR, De Rybel B, Weijers D, Xue HW (2019) Rice microtubule-associated protein IQ67-DOMAIN14 regulates grain shape by modulating microtubule cytoskeleton dynamics. Plant Biotechnol J 18:1141–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang F, Song Y, Yang H, Liu Z, Zhu G, Yang Y (2014) An auxin-responsive endogenous peptide regulates root development in Arabidopsis. J Integr Plant Biol 56:635–647

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Sun Q, Wang Y, Chan Z (2021) Global transcriptomic network of melatonin regulated root growth in Arabidopsis. Gene 764:145082

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Zhang L, Chen P, Liang T, Li X, Liu H (2020) UV-B photoreceptor UVR8 interacts with MYB73/MYB77 to regulate auxin responses and lateral root development. EMBO J 39:e101928

    Article  CAS  PubMed  Google Scholar 

  • Yu SG, Kim JH, Cho NH, Oh TR, Kim WT (2020a) Arabidopsis RING E3 ubiquitin ligase JUL1 participates in ABA-mediated microtubule depolymerization, stomatal closure, and tolerance response to drought stress. Plant J 103:824–842

    Article  CAS  PubMed  Google Scholar 

  • Yu SX, Zhou LW, Hu LQ, Jiang YT, Zhang YJ, Feng SL, Jiao Y, Xu L, Lin WH (2020b) Asynchrony of ovule primordia initiation in Arabidopsis. Development 147

  • Zhang L, Li S, Chen L, Yang G (2012) Identification and mapping of a major dominant quantitative trait locus controlling seeds per silique as a single Mendelian factor in Brassica napus L. Theor Appl Genet 125:695–705

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Yang G, Liu P, Hong D, Li S, He Q (2011) Genetic and correlation analysis of silique-traits in Brassica napus L. by quantitative trait locus mapping. Theor Appl Genet 122:21–31

    Article  PubMed  Google Scholar 

  • Zhang Y, Li D, Zhang D, Zhao X, Cao X, Dong L, Liu J, Chen K, Zhang H, Gao C, Wang D (2018) Analysis of the functions of TaGW2 homoeologs in wheat grain weight and protein content traits. Plant J 94:857–866

    Article  CAS  PubMed  Google Scholar 

  • Zhang YY, Li Y, Gao T, Zhu H, Wang DJ, Zhang HW, Ning YS, Liu LJ, Wu YR, Chu CC, Guo HS, Xie Q (2008) Arabidopsis SDIR1 enhances drought tolerance in crop plants. Biosci Biotechnol Biochem 72:2251–2254

    Article  CAS  PubMed  Google Scholar 

  • Zhao M, Gu Y, He L, Chen Q, He C (2015) Sequence and expression variations suggest an adaptive role for the DA1-like gene family in the evolution of soybeans. BMC Plant Biol 15:12

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by National Natural Science Foundation of China (32072099), Natural Science Foundation of Hubei (2019CFA090) and Wuhan Applied Foundational Frontier Project (2019020701011446). We thank Prof. Dr. Liang Guo for providing the thousand-seed weight phenotype of a rapeseed diversity panel. We declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Xiaohui Zhang, Qiyang Huang, Pengfei Wang, Feiyang Liu, Mudan Luo, Xiang Li, Guangsheng Yang & Dengfeng Hong

  2. Institute of Crops, Wuhan Academy of Agricultural Sciences, Wuhan, 430065, Hubei, China

    Zhuanrong Wang & Lili Wan

Authors
  1. Xiaohui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiyang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pengfei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Feiyang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mudan Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhuanrong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lili Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guangsheng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dengfeng Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XZ conducted most experiments, including fine-mapping, sequence analysis, cytological observations and haplotype analysis. QH and FL participated in phenotypic and genotypic analyses of BC3F2 populations and recombinant lines. ML and XL participated in sequence analysis. PW participated in RNA-seq data analysis. XZ wrote the original draft. ZW, LW and DH were involved in reviewing and editing the manuscript. DH and GY designed and supervised the project. All authors read and contributed to the revision of manuscript.

Corresponding author

Correspondence to Dengfeng Hong.

Additional information

Communicated by Rod Snowdon.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

122_2021_3850_MOESM1_ESM.tif

Fig S1. Variation in TSW across the BC3F2 population. a, b Distribution of TSW in group haplotype B. Different colors represent different genotypes, as determined by the markers SCC9-136 (a) and STC9-164 (b). c, d Distribution of number of seeds per silique (NSS) in haplotype group A. Different colors represent different genotypes, as determined by the markers SCC9-136 (c) and STC9-164 (d). e, f Distribution of NSS in haplotype group B. Different colors represent different genotypes, as determined by the markers SCC9-136 (e) and STC9-164 (f). (TIF 5626 KB)

122_2021_3850_MOESM2_ESM.tif

Fig S2. TSW and NSS of recombinants isolated from the BC3F2 population. Left, “0” represents lines homozygous for the HZ396 genotype and “2” represents heterozygous lines. Phenotypic values are shown as ranges. Middle, lower TSW (range 2.7–3.5) phenotypic values are shown in black and higher TSW values (range 4.0–4.8) in light gray. Right, lower NSS phenotypic values (range 12–21) are shown in beige and higher NSS values (range 23–29) in darker brown.. (TIF 4979 KB)

122_2021_3850_MOESM3_ESM.tif

Fig S3. Analysis of the genomic structure of the parental lines. a Summary of DNA sequence alignment between the BAC clone HBnB016G24 and the corresponding ZS11 reference sequence. b Summary of DNA sequence alignment among HZ396, Y106 and the ZS11 reference sequence. c The PCR fragment amplified from HZ396 is not a perfect match to the reference sequence. d After adjustment of alignment parameters, the fragment amplified from HZ396 matches the reference sequence perfectly but also reveals a deletion. The approximate positions of the nine specific markers spanning the deletion interval are indicated. e PCR amplification results of the nine specific markers in HZ396, Y106, ZS11 and the BAC clone. The white arrow indicates the size of the specific band, and the white box indicates the markers that failed to be amplified in HZ396. M is DNA ladder, and the size of the stripe is shown to the right of the gel. (TIF 10616 KB)

122_2021_3850_MOESM4_ESM.tif

Fig S4. Sequence variation at SNP5479 across various germplasm.Portion of the sequence chromatograms for the genotypes at left, centered on SNP5479. The reference sequence from ZS11 is shown on line 11. (TIF 20239 KB)

122_2021_3850_MOESM5_ESM.tif

Fig S5. Expression patterns of genes within and outside the deletion interval in the ZS11 reference during seed development. (TIF 4547 KB)

Fig S6. Analysis of DEGs. a Volcano plot of DEGs. b RT-qPCR validation of 15 randomly selected DEGs. (TIF 15897 KB)

122_2021_3850_MOESM7_ESM.tif

Fig S7. Comparison of reads from resequencing and RNA-seq. a, b Comparison of reads from resequencing at BnaC09G0550900ZS (a) and BnaC09G0551500ZS (b). c, d Comparison of reads from RNA-seq at BnaC09G0550900ZS (c) and BnaC09G0551500ZS (d). (TIF 33453 KB)

122_2021_3850_MOESM8_ESM.tif

Fig S8. Images of genotyping agarose gels for the XH14 and STC9-164 markers.Analysis of some natural population materials. (TIF 5944 KB)

Table S1. Chi-squared test of segregation in the BC3F2 population. (DOCX 15 KB)

Table S2. Gene ontology (GO) analysis results. (XLSX 19 KB)

Table S3 Morphological and cytological traits in HZ396 and NIL(Y106). (DOCX 13 KB)

Table S4 Primers used in the study (DOCX 20 KB)

Table S5 List of 505 inbred lines. (DOCX 73 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, X., Huang, Q., Wang, P. et al. A 24,482-bp deletion is associated with increased seed weight in Brassica napus L.. Theor Appl Genet 134, 2653–2669 (2021). https://doi.org/10.1007/s00122-021-03850-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-021-03850-x

Search

Navigation