Abstract
The inheritance of flowering time trait in spring-type rapeseed (Brassica napus L.) is poorly understood, and the investigations on mapping of quantitative trait loci (QTL) for the trait are only few. We identified QTL underlying variation for flowering time in a doubled haploid (DH) mapping population of nonvernalization-responsive canola (B. napus L.) cultivar 465 and line 86 containing introgressions from Houyou11, a Chinese early-flowering cultivar in Brassica rapa L. Significant genetic variation in flowering time and response to photoperiod were observed among the DH lines from 465/86. A molecular linkage map was generated comprising three types of markers loci. QTL analysis indicated that flowering time is a complex trait and is controlled by at least 4 major loci, localized on four different linkage groups A6, A7, C8 and C9. These loci each accounted for between 9.2 and 12.56 % of the total genotypic variation for first flowering. The published high-density maps for flowering time mapping used different marker systems, and the parents of our crosses have different genetic origins, with either spring-type B. napus or B. rapa. So we cannot determine whether the QTL on the same linkage groups were in the same region or not. There was evidence of additive × additive epistatic effects for flowering time in the DH population. Epistasis existed not only between main-effect QTLs, but also between QTLs with minor effects. Four pair of epistasis effects between minor QTLs explained about 20 % of the genetic variance observed in the DH population. The results indicated that minor QTLs for flowering time should not be ignored. Significant genotypes × environment interactions were also found for the quantitative traits, and with significant change in the ranking of the DH lines in different environments. The results implied that FQ3 was a non-environment-specific QTL and may control flowering time by autonomous pathway. FQ4 were winter-environment-specific QTL and may control flowering time by photoperiod-pathway. Identification of the chromosomal location and effect of the genes influencing flowering time may hasten the development of canola varieties having an optimal time for flowering in target environments such as for high altitude areas, via marker-assisted selection.
Similar content being viewed by others
References
Akbar MA (1989) Resynthesis of B. napus aiming for improved earliness and carried out by different approaches. Hereditas 111:239–246
Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664
Beavis WD, Grant D, Albertsen M, Fincher R (1991) Quantitative Trait Loci for plant height in four maize populations and their associations with quantitative genetic loci. Theor Appl Genet 83:141–145
Becker HC, Engqvist GM, Karlsson B (1995) Comparison of rapeseed cultivars and resynthesized lines based on allozyme and RFLP markers. Theor Appl Genet 91:62–67
Bell CJ, Ecker JR (1994) Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19:137–144
Bohuon EJR, Ramsay LD, Craft JA (1998) The association of flowering time QTL with duplicated regions and candidate loci in B. oleracea. Genetics 150:393–401
Brandle JE, McVetty PBE (1990) Geographical diversity, parental selection and heterosis in oilseed rape. Can J Plant Sci 70:935–940
Butruille DV, Guries RP, Osborn TC (1999) Increasing yield of spring oilseed rape hybrids through introgression of winter germplasm. Crop Sci 39:1491–1496
Camargo LEA, Osborn TC (1996) Mapping loci controlling flowering time in Brassica oleracea. Theor Appl Genet 92:610–616
Cao G, Zhu J, He C, Gao Y, Yan J, Wu P (2001) Impact of epistasis and QTL × environment interaction on the developmental behavior of plant height in rice (Oryza sativa L.). Theor Appl Genet 103:153–160
Diers BW, Osborn TC (1994) Genetic diversity of oilseed Brassica napus germplasm based on restriction fragment length polymorphism. Theor Appl Genet 88:662–668
Du DZ, Yao YM, Hu Q, Xu L (2009) Genetic diversity and hybrid vigor of new spring rapeseed varieties (B. napus L.) with extreme early maturity. Chin J Oil Crop Sci 31:114–121
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):180–186
Faris JD, Laddomada B, Gill BS (1998) Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics 149: 319–327
Fauré S, Noyer JL, Horry JP, Bakry F, Lanaud C, Gońzalez de León D (1993) A molecular marker-based linkage map of diploid bananas (Musa acuminata). Theor Appl Genet 87(4):517–526
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 90:727–732
Foisset N, Delourme R, Barret P, Hubert N, Landry BS, Renard M (1996) Molecular-mapping analysis in Brassica napus using isozyme, RAPD and RFLP markers on a doubled-haploid progeny 93:1017-1025
Girke A, Schierholt A, Becher HC (2012a) Extending the rapeseed genepool with resynthesized Brassica napus I: Heterosis. Genet Resour Crop Evol 59:1441–1447
Girke A, Schierholt A, Becher HC (2012b) Extending the rapeseed gene pool with resynthesized Brassica napus II: heterosis. Theor Appl Genet 124:1017–1026
Gómez-Campo C (1999) Biology of Brassica coenospecies. Elsevier Press, Netherlands, pp 33–58
Gong YG, Wue CN, Xing QH, Zhao XZ, Zhu J, He L (2009) A two method meta analysis of Neuregulin 1 (NRG1) association and heterogeneity in schizophrenia. Schizophr Res 111:109–114
Grant I, Beversdorf WD, Zilka J (1983) Response of light- and dark-grown callus of atrazine-resistant and susceptible rapeseed (Brassica napus) to varying concentrations of atrizine. Plant Cell Tissue Organ Cult 2:185–189
Hou J, Long Y, Raman H, Zou XX, Wang J, Dai ST, Xiao QQ, Li C, Fan L, Liu B, Meng J (2012) A tourist-like MITE insertion in the upstream region of BnFLC.A10 gene is associated with vernalization requirement in rapeseed (Brassica napus L.). BMC Plant Biol 12:238
Iniguez-Luy FL, Federico ML (2011) The genetics of Brassica napus L. In: Bancroft I, Schmidt R (eds) Genetics and genomics of the Brassicaceae. Springer, New York, pp 291–322
Iniguez-Luy FL, Lukens L, Famham MW, Amasino R, Osborn TC (2009) Development of public immortal mapping populations, molecular markers and linkage maps for rapid cycling Brassica rapa and B. oleracea. Theor Appl Genet 120:31–43
Kennard WC, Slocum MK, Figdore SS, Osborn TC (1994) Genetic analysis of morphological variation in Brassica oleracea using molecular markers. Theor Appl Genet 87:721–732
Kole C, Quijada P, Michaels SD, Amasino RM, Osborn TC (2001) Evidence for homology of flowering-time genes VFR2 from Brassica rapa and FLC from Arabidopsis thaliana. Theor Appl Genet 102:2–3
Kole C, Thormann CE, Karlsson BH, Palta JP, Gaffney P, Yandell B, Osborn TC (2002) Comparative mapping of loci controlling winter survival and related traits in oilseed Brassica rapa and B. napus. Mol Breeding 9:201–210
Koornneef M, Hanhart CJ, Van der Veen JH (1991) A genetic and physiological analysis of late-flowering mutants in Arabidopsis. Mol Gen Genet 229:57–66
Koornneef M, Blankestijn-de Vries H, Hanhart C, Soppe W, Peeters T (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J 6:911–919
Kosambi DD (1944) The estimation of map distance from recombination values. Ann Hum Genet 12:172–175
Kowalski SP, Ln TH, Feldmann KA, Paterson AH (1994) QTL mapping of naturally-occurring variation in-flowering time in Arabidopsis thaliana. Mol Gen Genet 245:548–555
Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping of Arabidopsis and Brassica, fine scale collinearity and congruence of genes controlling flowering time. Plant J 9:13–20
Lee I, Amasino RM (1995) Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol 108:157–162
Li G, Quiros CF (2001) Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor Appl Genet 103:455–461
Li Z, Pinson SRM, Park WD, Paterson AH, Stansel JW (1997) Epistasis for three grain yield components in rice (Oryza sativa L.). Genetics 145:453–465
Li F, Kitashiba H, Innaba K, Nishio T (2009) A Brassica rapa linkage map of EST-based SNP marker for identification of candidate genes controlling flowering time and leaf morphological traits. DNA Res 16:311–323
Li Y, Zhang X, Ma C, Sheng J, Cheng Q, Wang T, Fu T, Tu J (2012) QTL and epistatic analyses of heterosis for seed yield and three yield component traits using molecular markers in rapeseed (Brassica napus L.). Russ J Genet 48:1001–1008
Lincoln S, Daly M, Lander E (1992) Constructing genetic maps with MAPMAKER/EXP 3.0, 3rd edn. Whitehead Institute Technical Report
Lombard V, Delourme R (2001) A consensus linkage map for rapeseed (Brassica napus L.): construction and integration of three individual maps from DH populations. Theor Appl Genet 103:491–507
Long Y, Shi J, Qiu D, Li R, Zhng C, Wang J, Hou J, Zhao J, Shi L, Park BS, Chio SR, Lin YP, Meng J (2007) Flowering time quantitative trait loci analysis of oilseed brassica in multiple environments and genome wide alignment with Arabidopsis. Genetics 177:2433–2444
Lorieux M, Goffinet B, Perrier X, Gonzalez De Leon D, Lanaud C (1995) Maximum likelihood models for mapping genetic markers showing segregation distortion. I. Backcross population. Theor Appl Genet 90:73–80
Lowe A, Moule C, Trich M, Edwards K (2004) Efficient large-scale development of microsatellites for marker and mapping applications in Brassica crop species. Theor Appl Genet 108:1103–1112
Luo YX, Du DZ (2007a) Study on Self-incompatibility and Pollinations of Brassica campestris L. Acta Agriculturae Boreali-Occidentalis Sinica 16:56–58
Luo YX, Du DZ (2007b) Studies on the Main Characters of Qinghai Dahuang Rape. Acta Agriculturae Boreali-Occidentalis Sinica 16:136–139
Luo YX, Du DZ (2008) Genetic analyses of self-incompatible character in Brassica rapa. J Qinghai Univ 26:7–10
Luo YX, Du DZ, Tang GY (2010) Studies on plantlet formation of microspore embryoid in spring Brassica napus L. J Northwest A & F Univ 38:84–88
Ma C, Kimura Y, Fujimoto H, Sakai T, Imamura J, Fu T (2000) Genetic diversity of Chinese and Japanese rapeseed (Brassica napus L.) varieties detected by RAPD markers. Breeding Sci 50:257–265
Mahmood T, Rahman MH, Stringam GR (2006) Identification of quantitative trait loci (QTL) for oil and protein contents and their relationships with other seed quality traits in Brassica juncea. Theor Appl Genet 113:1211–1220
Michaels SD, Amasino RM (1999) Flowering locus c encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956
Miguel A, Green R, Nilsson O, Michael R, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800
Mukhopadhyay, Arumugam N, Pental D, Pradhan AK (2007) Mapping of yield in Xuencing QTL in Brassica juncea: implications for breeding of a major oilseed crop of dryland areas. Theor Appl Genet 115:807–817
Murphy LA, Scarth R (1998) Inheritance of vernalization response determined by doubled haploids in spring oilseed rape. Crop Sci 38:1463–1467
Nilsson O, Lee I, Blazquez MA, Weigel D (1998) Flowering time genes modulate the response to LEAFY activity. Genetics 150:403–410
Okazaki K, Sakamoto K, Kikuchi R, Saito A, Togashi E, Kuginuld Y, Matsumoto S, Hirai M (2007) Mapping and characterization of FLC homologs and QTL analysis of flowering time in Brassica oleracea. Theor Appl Genet 114:595–608
Osborn T, Lukens L (2003) The molecular genetic basis of flowering time variation in Brassica species. In: Nagata T, Tabata S (eds) Brassicas and Legumes, from genome structure to breeding. Springer, Berlin, pp 69–86
Osborn TC, Kole C, Parkin IAP, Sharpe AG, Kuiper M, Lydiate DJ, Trick M (1997) Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146:1123–1129
Parkin IAP, Lydiate DJ, Trick M (2002) Assessing the level of collinearity between Arabidopsis thaliana and Brassica napus for A. thaliana chromosome 5. Genome 45:1–11
Périlleux C, Bernier G (2002) The control of flowering: do genetical and physiological approaches converge? In: O’Neill SD, Roberts JA (eds) Plant reproduction, annual plant reviews, vol 6. Sheffield Academic Press, Sheffield, pp 1–32
Pineiro M, Coupland CG (1998) The control of flowering time and floral identity in Arabidopsis. Plant Physiol 117:1–8
Piquemal J, Cinquin E, Couton F, Roudeau C, Seignoret E, Doucet I, Perret D, Villeger P, Blanchard P (2005) Construction of an oilseed rape (Brassica napus L.) genetic map with SSR markers. Theor Appl Genet 111:1514–1523
Primack D, Imbres C, Primack RB, Miller-Rushing AJ, Del Tredici P (2004) Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. Am J Bot 91:1260–1264
Putterill J, Robson F, Lee K, Coupland G (1993) Chromosome walking with YAC clones in Arabidopsis: isolation of 1700 kb of contiguous DNA on chromosome 5, including a 300 kb region containing the flowering time gene CO. Mol Gen Genet 239:145–157
Qian W, Sass O, Meng J, Li M, Frauen M, Jung C (2007) Heterotic patterns in rapeseed (Brassica napus L.): I. Crosses between spring and Chinese semi-winter lines. Theor Appl Genet 115:27–34
Quijada PA, Udall JA, Polewicz H, Vogelzang RD, Osborn TC (2004) Phenotypic effects of introgressing French winter germplasm into hybrid spring canola. Crop Sci 44:1982–1989
Raman H, Raman R, Nelson MN, Aslam MN, Rajasekaran R, Wratten N, Cowling WA, Kilian A, Sharpe AG, Schondelmaier J (2012) Diversity Array Technology markers: Genetic diversity analyses and linkage map construction in rapeseed (Brassica napus L.). DNA Res 19:51–65
Raman H, Raman R, Coombes N, Manoli S, Zou XX, Edwards D, Meng JL (2013) Genetic and physical mapping of flowering time loci in canola (Brassica napus L.). Theor Appl Genet 126:119–132
Ratcliffe O, Kumimoto RW, Wong BJ, Riechmann JL (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15:1159–1169
Robert LS, Robson F, Sharpe A, Lydiate D, Coupland G (1998) Conserved structure and function of the Arabidopsis flowering time geneCONSTANS in Brassica napus. Plant mol Biol 37: 763–772
Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated fowering time gene FLC in Brassica rapa. Genetics 162:1457–1468
Searle I, He Y, Turck F, Vincent C, Fornara F, Krober S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Gens Dev 20:898–912
Sharma R, Mahla RH, Mohapatra T, Bhargava CS, Shama MM (2003) Isolating plant genomic DNA without liquid nitrogen. Plant Mol Biol Rep 21:43–50
Sheng JX, Fu TD, Tu JX, Ma CZ (2006) Prediction of heterosis using QTLs for yield traits in rapeseed (Brassica napus L.). Euphytica 151:165–171
Smith LB, King GJ (2000) The distribution of BoCAL-a alleles in Brassica oleracea is consistent with a genetic model for curd development and domestication of the cauliflower. Mol Breeding 6:603–613
Song KM, Osborn TC, Williams PH (1988a) Brassica taxonomy based on nuclear restriction fragment length polymorphism (RFLP) 2. Preliminary analysis of subspecies within B. rapa. Theor Appl Genet 76:593–600
Song KM, Osborn TC, Williams PH (1988b) Brassica taxonomy based on nuclear restriction fragment length polymorphism (RFLP) 1. Genome evolution of diploid and amphidiploid species. Theor Appl Genet 75:784–794
Sun ZD, Wang ZN, Tu JX et al (2007) An ultradense genetic recombination map for Brassica napus, consisting of 13551 SRAP markers. Theor Appl Genet 114:1305–1317
Thurling N, Vijendra Das LD (1979) Genetic control of the parenthesis development of spring rape (Brassica napus L.). II. Identification of individual genes controlling developmental pattern. Aust J Agric Res 30:261–271
UN (1935) Genomic analysis in Brassica with specific reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389–452
Udall JA, Quijada PA, Lambert B, Osborn TC (2006) Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 2. Identification of alleles from unadapted germplasm. Theor Appl Genet 113:597–609
Voorrips RE (2002) MapChart, software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP : a new technique for DNA fingerprinting. Nucleic Acids Res 23(21) :4407–4414
Wang J, Long Y, Wu BD, Liu J, Jiang CC, Shi L, Zhao JW, King GJ, Meng JL (2009) The evolution of Brassica napus FLOWERING LOCUS T paralogues in the context of inverted chromosomal duplication blocks. BMC Evol Biol 9:271
Wang J, Lydiate D, Parkin I, Falentin C, Delourme R, Carion P, King G (2011a) Integration of linkage maps for the amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Genom 12:101
Wang N, Qian W, Suppanz I, Wei L, Mao B, Long Y, Meng J, Müller AE, Jung C (2011b) Flowering time variation in oilseed rape (Brassica napus L) is associated with allelic variation in the FRIGIDA Homologue BnaA.FRI.a. J Exp Bot 62:5641–5658
Wang SC, Basten J, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
Yang J, Hu CC, Hu H, Yu RD, Xia Z, Ye XZ, Zhu J (2008) QTL network: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24:721–723
Yao YM, Xu L, Hu Q, Du DZ (2008) Genetic diversity on spring-planted varieties of B. napus L. and their parents. Acta Agriculturae Boreali-Occidentalis Sinica 4:114–118
Zhang LY, Wang SQ, Li HH, Deng QM, Zheng AP, Li SC, Li P, Li ZL, Wang JK (2010) Effects of missing marker and segregation distortion on QTL mapping in F2 populations. Theor Appl Genet 121:1071–1082
Zhao J, Wang X, Deng B, Lou P, Wu J, Sun R, Xu Z, Vromans J, Koornneef M, Bonnema G (2005) Genetic relationship within Brassica rapa as inferred from AFLP fingerprints. Theor Appl Genet 110:1301–1314
Zhu C, Wang C, Zhang Y (2007) Modeling segregation distortion for viability selection. Reconstruction of linkage maps with distorted markers. Theor Appl Genet 114:295–305
Zou X, Suppanz I, Raman H, Hou J, Wang J, Long Y, Jung C, Meng J (2012) Comparative analysis of FLC homologues in Brassicaceae provides insight into their role in the evolution of oilseed rape. PLoS ONE 7:e45751. doi:10.1371/journal.pone,0045751
Acknowledgments
The research was supported by the National Natural Science Foundation Grant (No. 31360345), Major State Basic Research Development Program (2012CB723007), and the Program from Science and Technology Department of Qinghai Province (2013-Z-716).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Luo, Y.X., Luo, C.Y., Du, D.Z. et al. Quantitative trait analysis of flowering time in spring rapeseed (B. napus L.). Euphytica 200, 321–335 (2014). https://doi.org/10.1007/s10681-014-1140-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-014-1140-2