Advertisement

Theoretical and Applied Genetics

, Volume 124, Issue 2, pp 407–421 | Cite as

Molecular mapping of Arabidopsis thaliana lipid-related orthologous genes in Brassica napus

  • Jianyi ZhaoEmail author
  • Jixiang Huang
  • Fei Chen
  • Fei Xu
  • Xiyuan Ni
  • Haiming Xu
  • Yilong Wang
  • Chonchon Jiang
  • Hao Wang
  • Aixia Xu
  • Ruizhi Huang
  • Dianrong Li
  • Jinling Meng
Original Paper

Abstract

Quantitative Trait Loci (QTL) for oil content has been previously analyzed in a SG-DH population from a cross between a Chinese cultivar and a European cultivar of Brassica napus. Eight QTL with additive and epistatic effects, and with environmental interactions were evaluated. Here we present an integrated linkage map of this population predominantly based on informative markers derived from Brassica sequences, including 249 orthologous A. thaliana genes, where nearly half (112) are acyl lipid metabolism related genes. Comparative genomic analysis between B. napus and A. thaliana revealed 33 colinearity regions. Each of the conserved A. thaliana segments is present two to six times in the B. napus genome. Approximately half of the mapped lipid-related orthologous gene loci (76/137) were assigned in these conserved colinearity regions. QTL analysis for seed oil content was performed using the new map and phenotypic data from 11 different field trials. Nine significant QTL were identified on linkage groups A1, A5, A7, A9, C2, C3, C6 and C8, together explaining 57.79% of the total phenotypic variation. A total of 14 lipid related candidate gene loci were located in the confidence intervals of six of these QTL, of which ten were assigned in the conserved colinearity regions and felled in the most frequently overlapped QTL intervals. The information obtained from this study demonstrates the potential role of the suggested candidate genes in rapeseed kernel oil accumulation.

Keywords

Quantitative Trait Locus Cleave Amplify Polymorphic Sequence Significant Quantitative Trait Locus Sequence Characterize Amplify Region Marker Stable Quantitative Trait Locus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are grateful to Dr. Christian Moellers and Prof. Heiko Becker (University of Gottingen), and Dr Zhonghua Chen (University of Western Sydney) for their critical reading of the manuscript and to Dr. Wolfgang Ecke (University of Gottingen) for his providing the original SSR marker names from AAFC consortium. Thanks also to Drs. Liu Jing, Wang Lei and Shengyi Liu (CAAS) for offering marker primers, siRNAs precursor and BAC sequences. Prof. Weijun Zhou (Zhejiang University) for kindly providing the rapeseed line “Gaoyou”. This research was financially supported by National Basic Research Programs (2006CB101601), National High-tech R&D Program (2011AA10A104), National Natural Science Foundations of China (No. 30871543, 31171180) and Zhejiang Provincial Natural Science Foundation of China (Z3100592).

Supplementary material

122_2011_1716_MOESM1_ESM.xls (26 kb)
Supplementary material 1 (XLS 27 kb)
122_2011_1716_MOESM2_ESM.xls (340 kb)
Summary table of mapped markers (Table S2a, S2b, S2c and S2d) Table S2a. Summary table of all the reference SSR information, including marker prefixes, source of primers and the No. of markers from different resources. Table S2b. Summary table of all the mapped markers including names, types and primer sequences on 19 linkage groups in SG-DH population. Table S2c.Detailed information of the mapped functional gene markers in the updated SG map Table S2d. The list of reference SSR markers mapped in updated SG map (XLS 340 kb)
122_2011_1716_MOESM3_ESM.xls (120 kb)
Summary of the over genes annotations (Table S3a, S3b) Table S3a. Functional classification of mapped lipid-related candidate genes in the SG-population Table S3b. Functional classification of other mapped genes in the SG-population (XLS 120 kb)
122_2011_1716_MOESM4_ESM.xls (28 kb)
Table S4. (XLS) Phenotypic variation of seed oil content in the SG-DH population over 11 experiments (XLS 28 kb)
122_2011_1716_MOESM5_ESM.xls (32 kb)
Table S5. (XLS) Full QTL information for seed oil content over 11 experiments (XLS 32 kb)

References

  1. 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 120:271–281PubMedCrossRefGoogle Scholar
  2. Baud S, Mendoza MS, To A, Harscoet E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50:825–838PubMedCrossRefGoogle Scholar
  3. Baud S, Wuilleme S, To A, Rochat C, Lepiniec L (2009) Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. Plant J 60:933–947PubMedCrossRefGoogle Scholar
  4. BeGora MD, Macleod MJR, McCarry BE, Summers PS, Weretilnyk EA (2010) Identification of phosphomethylethanolamine N-methyltransferase from Arabidopsis and its role in choline and phospholipid metabolism. J Biol Chem 285:29147–29155PubMedCrossRefGoogle Scholar
  5. Beisson F, Koo AJK, Ruuska S, Schwender J, Pollard M (2003) Arabidopsis genes involved in acyl lipid metabolism: a census of the candidates, a 2003 study of the distribution of expressed sequence tags in organs, and a Web-based database. Plant Physiol 132:681–697PubMedCrossRefGoogle Scholar
  6. Burns MJ, Barnes SR, Bowman JG, Clarke MHE, Werner CP, Kearsey MJ (2003) QTL analysis of an intervarietal set of substitution lines in Brassica napus: (i) seed oil content and fatty acid composition. Heredity 90:39–48PubMedCrossRefGoogle Scholar
  7. Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585PubMedCrossRefGoogle Scholar
  8. 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
  9. Cheng XM, Xu JS, Xia S, Guo J, 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 118:1121–1131PubMedCrossRefGoogle Scholar
  10. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedGoogle Scholar
  11. Delourme R, Falentin C, Huteau V, Clouet V, Horvais R, Gandon B, Specel S, Hanneton L, Dheu JE, Deschamps M et al (2006) Genetic control of oil content in oilseed rape (Brassica napus L.). Theor Appl Genet 113:1331–1345PubMedCrossRefGoogle Scholar
  12. Ecke W, Uzunova M, Wiessleder K (1995) Mapping the genome of rapeseed (Brassica napus L.). II. Localisation of genes controlling erucic acid synthesis and seed oil content. Theor Appl Genet 91:972–977CrossRefGoogle Scholar
  13. Frandsen GI, Mundy J, Tzen JTC (2001) Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plantarum 112:301–307CrossRefGoogle Scholar
  14. Glazebrook J, Drenkarci E, Preuss D, Ausubel FM (1998) Use of cleaved amplified polymorphic sequences (CAPS) as genetic markers in Arabidopsis thaliana. Meth Mol Biol 82:173–182Google Scholar
  15. He JP, Ke LP, Hong DF, Xie YZ, Wang GC, Liu PW, Yang GS (2008) Fine mapping of a recessive genic male sterility gene (Bnms3) in rapeseed (Brassica napus) with AFLP- and Arabidopsis-derived PCR markers. Theor Appl Genet 117:11–18PubMedCrossRefGoogle Scholar
  16. Hernandez-Pinzon I, Patel K, Murphy DJ (2001) The Brassica napus calcium-binding protein, caleosin, has distinct endoplasmic reticulum- and lipid body-associated isoforms. Plant Physiol Biochem 39:615–622CrossRefGoogle Scholar
  17. Hobbs DH, Flintham JE, Hills MJ (2004) Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiol 136:3341–3349PubMedCrossRefGoogle Scholar
  18. Kaur S, Cogan NOI, Ye G, Baillie RC, Hand ML, Ling AE, Mcgearey AK, Kaur J, Hopkins CJ, Todorovic M et al (2009) Genetic map construction and QTL mapping of resistance to blackleg (Leptosphaeria maculans) disease in Australian canola (Brassica napus L.) cultivars. Theor Appl Genet 120:71–83PubMedCrossRefGoogle Scholar
  19. Keurentjes JJ, Sulpice R, Gibon Y, Steinhauser MC, Fu J, Koornneef M, Stitt M, Vreugdenhil D (2008) Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biol 9:R129PubMedCrossRefGoogle Scholar
  20. Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498PubMedGoogle Scholar
  21. Li R, Yu K, Hildebrand DF (2010) DGAT1, DGAT2 and PDAT expression in seeds and other tissues of epoxy and hydroxy fatty acid accumulating plants. Lipids 45(2):145–157PubMedCrossRefGoogle Scholar
  22. 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 103:455–461CrossRefGoogle Scholar
  23. Li YY (2006) Localization of QTLs for yield-related traits and heterosis dissection using functional markers in Brassica napus L. PhD Dissertation, Hauzhong Agricultural University, Wuhan (in Chinese)Google Scholar
  24. Lincoln SE, Daly MJ, Lander ES (1993) Constructing genetic linkage maps with MAPMARKER/EXP 3.0. A tutorial and reference manual. Whitehead Institute for Biomedical Research, CambridgeGoogle Scholar
  25. Liu J, Hua W, Zhan GM, Wei F, Wang XF, Liu GH, Wang HZ (2009) Increasing seed mass and oil content in transgenic Arabidopsis by the overexpression of wri1-like gene from Brassica napus. Plant Physiol Biochem 48:9–15PubMedCrossRefGoogle Scholar
  26. Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Beom-Seok P (2007) Flowering time quantitative trait loci analysis of oilseed Brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177:2433–2444PubMedGoogle Scholar
  27. Lung SC, Weselake RJ (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41:1073–1088PubMedCrossRefGoogle Scholar
  28. Maisonneuve S, Bessoule JJ, Lessire R, Delseny M, Roscoe TJ (2010) Expression of rapeseed microsomal lysophosphatidic acid acyltransferase isozymes enhances seed oil content in Arabidopsis. Plant Physiol 152:670–684PubMedCrossRefGoogle Scholar
  29. Mayerhofer R, Wilde K, Mayerhofer M, Lydiate D, Bansal VK, Good AG, Parkin IAP (2005) Complexities of chromosome landing in a highly duplicated genome: toward map-based cloning of a gene controlling blackleg resistance in Brassica napus. Genetics 171:1977–1988PubMedCrossRefGoogle Scholar
  30. Meyerowitz E (1992) Introduction to the Arabidopsis genome. In: Koncz C, Chua N, Schell J (eds) Methods in Arabidopsis research. World Scientific, Singapore, pp 102–118Google Scholar
  31. Mika V, Tillmann P, Koprna R, Nerusil P, Kucera V (2003) Fast prediction of quality parameters in whole seeds of oilseed rape (Brassica napus L.). Plant Soil Environ 49:141–145Google Scholar
  32. Mu JY, Tan HL, Zheng Q, Fu FY, Liang Y, Zhang J, Yang XH, Wang T, Chong K, Wang XJ, Zuo JR (2008) LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol 148:1042–1054PubMedCrossRefGoogle Scholar
  33. Niu Y, Wu GZ, Ye R, Lin WH, Shi QM, Xue LJ, Xu XD, Li Y, Du YG, Xu HW (2009) Global analysis of gene expression profiles in Brassica napus developing seeds reveals a conserved lipid metabolism regulation with Arabidopsis thaliana. Mol Plant 2:1107–1122PubMedCrossRefGoogle Scholar
  34. Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970PubMedCrossRefGoogle Scholar
  35. Parkin IAP, Sharpe AG, Keith DJ, Lydiate DJ (1995) Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38:1122–1131PubMedCrossRefGoogle Scholar
  36. Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781PubMedCrossRefGoogle Scholar
  37. Qiu D, Morgan C, Shi J, Long Y, Liu J, Li R, Zhuang X, Wang Y, Tan X, Dietrich E et al (2006) A comparative linkage map of oilseed rape and its use for QTL analysis of seed oil and erucic acid content. Theor Appl Genet 114:67–80PubMedCrossRefGoogle Scholar
  38. Sanguinetti C, Simpson NE (1994) Arapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:915–919Google Scholar
  39. Schmidt R, Acarkan A, Boivin K (2001) Comparative structural genomics in the Brassicaceae family. Plant Physiol Biochem 39:253–262CrossRefGoogle Scholar
  40. Schuler GD (1997) Sequence mapping by electronic PCR. Genome Res 7:541–550PubMedGoogle Scholar
  41. Shen B, Allen WB, Zheng PZ, Li CJ, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987PubMedCrossRefGoogle Scholar
  42. Smooker AM, Wells R, Morgan C, Beaudoin F, Cho K, Fraser F, Bancroft I (2011) The identification and mapping of candidate genes and QTL involved in the fatty acid desaturation pathway in Brassica napus. Theor Appl Genet 122:1075–1090PubMedCrossRefGoogle Scholar
  43. Snowdon RJ, Friedt W (2004) Molecular markers in Brassica oilseed breeding: current status and future possibilities. Plant Breed 123:1–8CrossRefGoogle Scholar
  44. Suwabe K, Tsukazaki H, Iketani H, Hatakeyama K, Kondo M, Fujimura M, Nunome T, Fukuoka H, Hirai M, Matsumoto S (2006) Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 173:309–319PubMedCrossRefGoogle Scholar
  45. Taylor DC, Katavic V, Zou JT, MacKenzie SL, Keller WA, An J, Friesen W, Barton DL, Pedersen KK, Giblin EM et al (2002) Field testing of transgenic rapeseed cv. Hero transformed with a yeast sn-2 acyltransferase results in increased oil content, erucic acid content and seed yield. Mol Breed 8:317–322CrossRefGoogle Scholar
  46. Thelen JJ, Ohlrogge JB (2002) Metabolic engineering of fatty acid biosynthesis in plants. Metab Eng 4:12–21PubMedCrossRefGoogle Scholar
  47. Uzunova MI, Ecke W, Weissleder K, Rübbelen G (1995) Mapping the genome of rapeseed (Brassica napus L.) I. Construction of an RFLP linkage map and localization of QTLs for seed glucosinolate content. Theor Appl Genet 90:194–204CrossRefGoogle Scholar
  48. Van Erp H, Bates PD, Burgal J, Shockey J, Browse J (2011) Castor phospholipid: diacylglycerol acyltransferase facilitates efficient metabolism of hydroxy fatty acids in transgenic Arabidopsis. Plant Physiol 155:683–693PubMedCrossRefGoogle Scholar
  49. Vigeolas H, Waldeck P, Zank T, Geigenberger P (2007) Increasing seed oil content in oil-seed rape (Brassica napus L.) by overexpression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter. Plant Biotechnol J 5:431–441PubMedCrossRefGoogle Scholar
  50. Wang SC, Bastern J, Zeng Z B (2006) Windows QTL Cartographer 2.5. North Carolina State University, Raleigh, NC (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)
  51. Wang L, Wang MB, Tu JX, Helliwell CA, Waterhouse PM, Dennis ES, Fu TD, Fan YL (2007) Cloning and characterization of microRNAs from Brassica napus. FEBS Lett 581:3848–3856PubMedCrossRefGoogle Scholar
  52. Wang J, Lydiate DJ, Parkin IAP, Falentin C, Delourme R, Carionl PWC, King GJ (2011) Integration of linkage maps for the amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Genomics 12:101PubMedCrossRefGoogle Scholar
  53. Xie YZ, Hong DF, Xu ZH, Liu PW, Yang GS (2008) Identification of AFLP markers linked to the epistatic suppressor gene of a recessive genic male sterility in rapeseed and conversion to SCAR markers. Plant Breed 127:145–149CrossRefGoogle Scholar
  54. Yan XY, Li JN, Fu FY, Jin MY, Chen L, Liu LZ (2009) Co-location of seed oil content, seed hull content and seed coat color QTL in three different environments in Brassica napus L. Euphytica 170:355–364CrossRefGoogle Scholar
  55. Yang YW, Lai KN, Tai PY, Li WH (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J Mol Evol 48:597–604PubMedCrossRefGoogle Scholar
  56. Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468PubMedGoogle Scholar
  57. Zhao JY, Becker HC, Zhang DQ, Zhang YF, Ecke W (2005) Oil content in a European-Chinese rapeseed population: QTL with additive and epistatic effects and their genotype-environment interactions. Crop Sci 45:51–59CrossRefGoogle Scholar
  58. Zhao JY, Becker HC, Zhang DQ, Zhang YF, Ecke W (2006) Conditional QTL mapping of oil content in rapeseed with respect to protein content and traits related to plant development and grain yield. Theor Appl Genet 113:33–38PubMedCrossRefGoogle Scholar
  59. Zou JT, Katavic V, Giblin EM, Barton DL, MacKenzie SL, Keller WA, Hu X, Taylor DC (1997) Modification of seed oil content and acyl composition in the Brassicaceae by expression of a yeast sn-2 acyltransferase gene. Plant Cell 9:909–923PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jianyi Zhao
    • 1
    Email author
  • Jixiang Huang
    • 1
  • Fei Chen
    • 1
  • Fei Xu
    • 2
  • Xiyuan Ni
    • 1
  • Haiming Xu
    • 2
  • Yilong Wang
    • 3
  • Chonchon Jiang
    • 4
  • Hao Wang
    • 5
  • Aixia Xu
    • 6
  • Ruizhi Huang
    • 7
  • Dianrong Li
    • 5
  • Jinling Meng
    • 4
  1. 1.Institute of Crop and Nuclear Technology UtilizationZhejiang Academy of Agricultural SciencesHangzhouChina
  2. 2.College of Agricultural and BiotechnologyZhejiang UniversityHangzhouChina
  3. 3.College of Bioscience and BiotechnologyYangzhou UniversityYangzhouChina
  4. 4.National Key Laboratory of Crop Genetic ImprovementHuazhong Agricultural UniversityWuhanChina
  5. 5.Hybrid Rapeseed Research Center of ShaanxiDaliChina
  6. 6.College of AgronomyNorthwest Agricultural and forestry UniversityYanglinChina
  7. 7.Institute of Virology and BiotechnologyZhejiang Academy of Agricultural SciencesHangzhouChina

Personalised recommendations