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Molecular Breeding

, 36:52 | Cite as

QTL analysis and the development of closely linked markers for days to flowering in spring oilseed rape (Brassica napus L.)

  • Haidong Liu
  • Dezhi Du
  • Shaomin Guo
  • Lu Xiao
  • Zhigang Zhao
  • Zhi Zhao
  • Xiaorong Xing
  • Guoyong Tang
  • Liang Xu
  • Zhong Fu
  • Yanmei Yao
  • Robert W. Duncan
Article

Abstract

Days to flowering (DTF) is an important trait impacting cultivar performance in oilseed rape (Brassica napus L.), but the interaction of all loci controlling this trait in spring-type oilseed rape is not fully understood. We identified quantitative trait loci (QTL) for variation in DTF in a doubled haploid (DH) population from the Qinghai–Tibet Plateau that includes 217 lines derived from a cross between spring-type oilseed rape (B. napus L.) line No. 5246 and line No. 4512, the latter of which is responsive to the effective accumulated temperature (EAT). A linkage map was constructed for the DH population, using 202 SSR and 293 AFLP markers. At least 22 DTF QTL were found in multiple environments. Four major QTL were located on linkage groups A7, C2, C8 and C8. Among these QTL, cqDTFA7a and cqDTFC2a were identified in five environments and individually explained 10.4 and 23.0 % of the trait variation, respectively. cqDTFC8, a major QTL observed in spring environments, and a unique winter environment QTL, qDTFC8-3, were identified; these QTL explained 10.0 and 46.5 % of the phenotypic variation, respectively. Minor QTL (for example, cqDTFC2c) and epistatic interactions seemed evident in this population. Two closely linked SSR markers for cqDTFA7a and cqDTFC8 were developed (G1803 and S034). BnAP1, a B. napus gene with homology to Arabidopsis thaliana that was identified as a cqDTFA7a candidate gene, played a major role in this study. The allelic effects of the major and minor QTL on DTF were further validated in the DH population and in 93 breeding genotypes.

Keywords

Spring Brassica napus L. Doubled haploid lines Days to flowering QTL analysis Molecular markers 

Notes

Acknowledgments

The authors thank Prof. Ruisheng Wang, Mr. Jianshe Qin and Mr. Jianrong Lin for providing help with field management. The authors also thank Dr. Jun Zou (HAU China) for assistance with data analysis. Financial support for this study was provided by the National System of Technology of the Rapeseed Industry (CARS-13), the “973” Program Early Research Project (2012CB723007), the “863” High-tech Program (2011AA10A104) and the National Science and Technology Support Program (2010BD01B03).

Compliance with ethical standards

Conflict of interest

We declare that we do not have any commercial or associative interests that represent a conflict of interest in connection with the work submitted.

Ethical approval

This article does not describe any studies involving human participants or animals.

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References

  1. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2:e106CrossRefPubMedPubMedCentralGoogle Scholar
  2. Blanc G, Charcosset A, Mangin B, Gallais A, Moreau L (2006) Connected populations for detecting quantitative trait loci and testing for epistasis: an application in maize. Theor Appl Genet 113:206–224CrossRefPubMedGoogle Scholar
  3. Blazquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171CrossRefPubMedGoogle Scholar
  4. Butruille DV, Guries RP, Osborn TC (1999) Linkage analysis of molecular markers and quantitative trait loci in populations of inbred backcross lines of Brassica napus L. Genetics 153:949–964PubMedPubMedCentralGoogle Scholar
  5. Cai GQ, Yang QY, Yang Q, Zhao ZX, Chen H, Wu J, Fan CC, Zhou YM (2012) Identification of candidate genes of QTL for seed weight in Brassica napus through comparative mapping among Arabidopsis and Brassica species. BMC Genet 13:105–122CrossRefPubMedPubMedCentralGoogle Scholar
  6. Camargo LEA, Osborn TC (1996) Mapping loci controlling flowering time in Brassica oleracea. Theor Appl Genet 92:610–616CrossRefPubMedGoogle Scholar
  7. Chen G, Geng JF, Rahman M, Liu XP, Tu JX, Fu TD, Li GY, McVetty PBE, Tahir M (2010) Identification of QTL for oil content, seed yield, and flowering time in oilseed rape (Brassica napus). Euphytica 175:161–174CrossRefGoogle Scholar
  8. Cheng XM, Xu JS, Xia S, Gu JX, Yang Y, Fu J, Qian XJ, Zhang SC, Wu JS, Liu KD (2009) Development and genetic mapping of microsatellite markers from genome survey sequences in Brassica napus. Theor Appl Genet 118:1121–1131CrossRefPubMedGoogle Scholar
  9. Delourme R, Falentin C, Huteau V, Clouet V, Horvais R, Gandon B, Specel S, Hanneton L, Dheu JE, Deschamps M, Margale E, Vincourt P, Renard M (2006) Genetic control of oil content in oilseed rape (Brassica napus L.). Theor Appl Genet 113:1331–1345CrossRefPubMedGoogle Scholar
  10. Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294PubMedPubMedCentralGoogle Scholar
  11. Du DZ, Liu QY, Li XP, Yu QL, Fu Z, Wang RS, Zhao HC, Tang GY, An FY, Wang NH (2004) Breeding for a hybrid variety Qingza No.3 with very early maturity and double-low quality in Brassica napus L. Chin J Oil Crop Sci 26(1):66–68Google Scholar
  12. Du DZ, Nie P, Xu L, Luo YX, Yao YM, Zhou HW, Zhang XM (2010) Rapeseed heterosis of different ecotypes in Qinghai province. Chin J Oil Crop Sci 32(2):180–186Google Scholar
  13. Fan CC, Cai GQ, Qin J, Li QY, Yang MG, Wu JZ, Fu TD, Liu KD, Zhou YM (2010) Mapping of quantitative trait loci and development of allele-specific markers for seed weight in Brassica napus. Theor Appl Genet 121:1289–1301CrossRefPubMedGoogle Scholar
  14. Ferreira ME, Satagopan J, Yandell BS, Williams PH, Osborn TC (1995) Mapping loci controlling vernalization requirement and flowering time in Brassica napus. Theor Appl Genet 90:727–732CrossRefPubMedGoogle Scholar
  15. Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141(3):550–550.e2CrossRefPubMedGoogle Scholar
  16. Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473PubMedPubMedCentralGoogle Scholar
  17. Javed N, Geng JF, Muhammad T, McVetty PBE, Li GY, Duncan Robert W (2015) Identification of QTL influencing seed oil content, fatty acid profile and days to flowering in Brassica napus L. Euphytica 207:191–211CrossRefGoogle Scholar
  18. Juenger TE, Sen Su, Stowe KA, Simms EL (2005) Epistasis and genotype–environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica 123:87–105CrossRefPubMedGoogle Scholar
  19. Kennard WC, Slocum MK, Figdore SS, Osborn TC (1994) Genetic analysis of morphological variation in Brassica oleracea using molecular markers. Theor Appl Genet 87:721–732CrossRefPubMedGoogle Scholar
  20. Kim SY, Park BS, Kwon SJ, Kim J, Lim MH, Park YD, Kim DY, Suh SC, Jin YM, Ahn JH, Lee YH (2007) Delayed flowering time in Arabidopsis and Brassica rapa by the overexpression of FLOWERING LOCUS C (FLC) homologs isolated from Chinese cabbage (Brassica rapa L.: ssp. pekinensis). Plant Cell Rep 26:327–336CrossRefPubMedGoogle Scholar
  21. Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  22. Kubo T, Yoshimura A (2005) Epistasis underlying female sterility detected in hybrid breakdown in a Japonica-Indica cross of rice (Oryza sativa L.). Theor Appl Genet 110:346–355CrossRefPubMedGoogle Scholar
  23. Li KX, Wang YN, Han CY, Zhang WS, Jia HZ, Li X (2007) GA signaling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana. Plant Growth Regul 53:195–206CrossRefGoogle Scholar
  24. Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Park BS, Choi SR, Lim YP, Meng J (2007) Flowering time quantitative trait loci analysis of oilseed Brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177:2433–2444PubMedPubMedCentralGoogle Scholar
  25. Lowe AJ, Moule C, Trick M, Edwards KJ (2004) Efficient large-scale development of microsatellites for marker and mapping applications in Brassica crop species. Theor Appl Genet 108:1103–1112CrossRefPubMedGoogle Scholar
  26. Mathews A, Carroll BJ, Gresshoff PM (1990) The genetic interaction between non-nodulation and supernodulation in soybean: an example of developmental epistasis. Theor Appl Genet 79:125–130CrossRefPubMedGoogle Scholar
  27. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14(Suppl):S111–S130PubMedPubMedCentralGoogle Scholar
  28. Narita A, Sasaki Y (2004) Detection of multiple QTL with epistatic effects under a mixed inheritance model in an outbred population. Genet Sel Evol 36:415–432CrossRefPubMedPubMedCentralGoogle Scholar
  29. Okazaki K, Sakamoto K, Kikuchi R, Saito A, Togashi E, Kuginuki Y, Matsumoto S, Hirai M (2007) Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea. Theor Appl Genet 114:595–608CrossRefPubMedGoogle Scholar
  30. Osborn TC, Kole C, Parkin IAP, Sharpe AG, Kuiper M, Lydiatet DJ, Trickt M (1997) Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146:1123–1129PubMedPubMedCentralGoogle Scholar
  31. Panjabi P, Jagannath A, Bisht NC, Padmaja KL, Sharma S, Gupta V, Pradhan AK, Pental D (2008) Comparative mapping of Brassica juncea and Arabidopsis thaliana using Intron Polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genom 9:113–132CrossRefGoogle Scholar
  32. Piquemal J, Cinquin E, Couton F, Rondeau C, Seignoret E, Doucet I, Perret D, Villeger M-J, Vincourt P, Blanchard P (2005) Construction of an oilseed rape (Brassica napus L.) genetic map with SSR markers. Theor Appl Genet 111:1514–1523CrossRefPubMedGoogle Scholar
  33. Quijada PA, Udall JA, Lambert B, Osborn TC (2006) Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 1. Identification of genomic regions from winter germplasm. Theor Appl Genet 113:549–561CrossRefPubMedGoogle Scholar
  34. Raman H, Raman R, Eckermann P, Coombes N, Manoli S, Zou X, Edwards D, Meng J, Prangnell R, Stiller J, Batley J, Luckett D, Wratten N, Dennis E (2013) Genetic and physical mapping of flowering time loci in canola (Brassica napus L.). Theor Appl Genet 126:119–132CrossRefPubMedGoogle Scholar
  35. Raman H, Raman R, Kilian A, Detering F, Carling J, Coombes N et al (2014) Genome-wide delineation of natural variation for pod shatter resistance in Brassica napus. PLoS One 9(7):e101673. doi: 10.1371/journal.pone.0101673 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Raman H, Raman R, Coombes N, Song J, Prangnell R, Bandaranayake C, Tahira R, Sundaramoorthi V, Killian A, Meng J, Dennis ES, Balasubramanian S (2015) Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola. Plant Cell Environ. doi: 10.1111/pce.12644 Google Scholar
  37. Sachan JN, Singh B (1987) Generation mean analyses for flowering and maturity in Indian mustard (Brassica junces (L.) Czern and Coss). Theor Appl Genet 73:571–574CrossRefPubMedGoogle Scholar
  38. Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468PubMedPubMedCentralGoogle Scholar
  39. Shao YL, Gao YN, Kong YQ, Wang YP (2013) Study on anti-nutritional compounds in seeds of Brassica napus. Bot Res 2:56–61Google Scholar
  40. Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037CrossRefPubMedGoogle Scholar
  41. Sun YN, Pan JB, Shi XL, Du XY, Wu Q, Qi ZM, Jiang HW, Xin DW, Liu CY, Hu GH, Chen QS (2012) Multi-environment mapping and meta-analysis of 100-seed weight in soybean. Mol Biol Rep 39:9435–9443CrossRefPubMedGoogle Scholar
  42. Tan ZM, Li YC, Hu Q, Mei DS, Li YD, Xu YS (2007) Heterosis prediction based on genetic distance estimated by molecular markers in rapeseed. Chin J Oil Crop Sci 29(2):20–26Google Scholar
  43. Tang QY, Zhang CX (2013) Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci 20(2):254–260CrossRefPubMedGoogle Scholar
  44. Teutonico RA, Osborn TC (1995) Mapping loci controlling vernalization requirement in Brassica rapa. Theor Appl Genet 91:1279–1283CrossRefPubMedGoogle Scholar
  45. Uptmoor R, Schrag T, Stützel H, Esch E (2007) Crop model based QTL analysis across environments and QTL based estimation of time to floral induction and flowering in Brassica oleracea. Mol Breed 21:205–216CrossRefGoogle Scholar
  46. Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  47. Vos P, Hogers R, Bleeker M, Reijans M, Tvd Lee, Miranda Hornes, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wang S, Bastern JC, Zeng ZB (2006) Windows QTL Cartographer 2.5. North Carolina State University, Raleigh. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
  49. Wang J, Lydiate DJ, Parkin IA, Falentin C, Delourme R, Carion PW, King GJ (2011a) Integration of linkage maps for the Amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Genom 12:101–121CrossRefGoogle Scholar
  50. Wang Y, Sun SL, Liu B, Wang H, Deng J, Liao YC, Wang Q, Cheng F, Wang XW, Wu J (2011b) A sequence-based genetic linkage map as a reference for Brassica rapa pseudochromosome assembly. BMC Genom 12:239–248CrossRefGoogle Scholar
  51. Wei DY, Mei JQ, Fu Y, Disi JO, Li JN, Qian W (2014) Quantitative trait loci analyses for resistance to Sclerotinia sclerotiorum and flowering time in Brassica napus. Mol Breed 34:1797–1804CrossRefGoogle Scholar
  52. Xiao L, Zhao Z, Du DZ, Yao YM, Xu L, Tang GY (2012) Genetic characterization and fine mapping of a yellow-seeded gene in Dahuang (a Brassica rapa landrace). Theor Appl Genet 124:903–909CrossRefPubMedGoogle Scholar
  53. Xu JX, Qian XJ, Wang XF, Li RY, Cheng XM, Yang YY, Fu J, Zhang SC, King JG, Wu JS, Liu KD (2010) Construction of an integrated genetic linkage map for the A genome of Brassica napus using SSR markers derived from sequenced BACs in B. rapa. BMC Genom 11:594–609CrossRefGoogle Scholar
  54. Xu YF, An DG, Liu DC, Zhang AM, Xu HX, Li B (2012) Mapping QTL with epistatic effects and QTL × treatment interactions for salt tolerance at seedling stage of wheat. Euphytica 186:233–245CrossRefGoogle Scholar
  55. Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536CrossRefPubMedGoogle Scholar
  56. Yao YM, Xu L, Hu Q, Du DZ (2008) Genetic diversity on spring-planted varieties of B. napus L. and their parents. Acta Agron Sin 17(4):114–118Google Scholar
  57. Yao YM, Liu HD, Xu L, Du DZ (2013) Enhancing the heterosis of spring rapeseed varieties (Brassica napus L.) by using semi-winter rapeseed varieties as parents. Acta Agron Sin 39:118–125CrossRefGoogle Scholar
  58. Yong WD, Chong K, Xu ZH, Tan KH, Zhu ZQ (2000) Gene control of flowering time in higher plants. Chin Sci Bull 45(18):1633–1642CrossRefGoogle Scholar
  59. Zhou QH, Fu DH, Mason AS, Zeng YJ, Zhao CX, Huang YJ (2014) In silico integration of quantitative trait loci for seed yield and yield-related traits in Brassica napus. Mol Breed 33:881–894CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Haidong Liu
    • 1
  • Dezhi Du
    • 1
  • Shaomin Guo
    • 1
  • Lu Xiao
    • 1
  • Zhigang Zhao
    • 1
  • Zhi Zhao
    • 1
  • Xiaorong Xing
    • 1
  • Guoyong Tang
    • 1
  • Liang Xu
    • 1
  • Zhong Fu
    • 1
  • Yanmei Yao
    • 1
  • Robert W. Duncan
    • 2
  1. 1.Key Laboratory of Spring Rapeseed Genetic Improvement, National Key Laboratory Breeding Base for Innovation and Utilization of Plateau Crop Germplasm, Qinghai Academy of Agricultural and Forestry SciencesQinghai UniversityXiningChina
  2. 2.Department of Plant ScienceUniversity of ManitobaWinnipegCanada

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