Full paper

You have full text access to this OnlineOpen article

Characterization of metabolite quantitative trait loci and metabolic networks that control glucosinolate concentration in the seeds and leaves of Brassica napus

  1. Ji Feng1,
  2. Yan Long1,
  3. Lei Shi1,
  4. Jiaqin Shi1,
  5. Guy Barker2,
  6. Jinling Meng1

Article first published online: 4 OCT 2011

DOI: 10.1111/j.1469-8137.2011.03890.x

Issue

New Phytologist

New Phytologist

Volume 193, Issue 1, pages 96–108, January 2012

Additional Information

How to Cite

Feng, J., Long, Y., Shi, L., Shi, J., Barker, G. and Meng, J. (2012), Characterization of metabolite quantitative trait loci and metabolic networks that control glucosinolate concentration in the seeds and leaves of Brassica napus. New Phytologist, 193: 96–108. doi: 10.1111/j.1469-8137.2011.03890.x

Author Information

  1. 1

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

  2. 2

    Life Sciences, University of Warwick, Wellesbourne, Warwick CV35 9EF, UK

*Author for correspondence: Jinling Meng Tel: +86 27 87282457 Email: jmeng@mail.hzau.edu.cn

Publication History

  1. Issue published online: 2 DEC 2011
  2. Article first published online: 4 OCT 2011
  3. Received: 7 July 2011, Accepted: 15 August 2011

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (2647K)

References

  • Agerbirk N, Olsen CE, Nielsen JK. 2001. Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58: 91–100.
  • Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J. 2004. BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20: 2324–2326.
  • Barker GC, Larson TR, Graham IA, Lynn JR, King GJ. 2007. Novel insights into seed fatty acid synthesis and modification pathways from genetic diversity and quantitative trait loci analysis of the Brassica C genome. Plant Physiology 144: 1827–1842.
  • Bisht NC, Gupta V, Ramchiary N, Sodhi YS, Mukhopadhyay A, Arumugam N, Pental D, Pradhan AK. 2009. Fine mapping of loci involved with glucosinolate biosynthesis in oilseed mustard (Brassica juncea) using genomic information from allied species. Theoretical and Applied Genetics 118: 413–421.
  • Chen S, Andreasson E. 2001a. Update on glucosinolate metabolism and transport. Plant Physiology and Biochemistry 39: 743–758.
  • Chen S, Glawischnig E, Jorgensen K, Naur P, Jorgensen B, Olsen CE, Hansen CH, Rasmussen H, Pickett JA, Halkier BA. 2003. CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant Journal 33: 923–937.
    Direct Link:
  • Chen S, Halkier BA. 2000. Characterization of glucosinolate uptake by leaf protoplasts of Brassica napus. Journal of Biological Chemistry 275: 22955–22960.
  • Chen S, Petersen BL, Olsen CE, Schulz A, Halkier BA. 2001b. Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiology 127: 194–201.
  • Churchill GA, Doerge RW. 1994. Empirical threshold values for quantitative trait mapping. Genetics 138: 963–971.
  • Dixon DP, Skipsey M, Edwards R. 2010. Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71: 338–350.
  • Du L, Halkier BA. 1998. Biosynthesis of glucosinolates in the developing silique walls and seeds of Sinapis alba. Phytochemistry 48: 1145–1150.
  • Fahey JW, Zalcmann AT, Talalay P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56: 5–51.
  • Fenwick GR, Curtis RF. 1980. Rapeseed meal and its use in poultry diets: a review. Animal Feed Science and Technology 5: 255–259.
  • Fu J, Swertz MA, Keurentjes JJ, Jansen RC. 2007. MetaNetwork: a computational protocol for the genetic study of metabolic networks. Nature Protocols 2: 685–694.
  • Gigolashvili T, Yatusevich R, Rollwitz I, Humphry M, Gershenzon J, Flugge UI. 2009. The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21: 1813–1829.
  • Goffinet B, Gerber S. 2000. Quantitative trait loci: a meta-analysis. Genetics 155: 463–473.
  • Griffiths D, Birch ANE, Hillman J. 1998. Antinutritional compounds in the Brassicaceae: analysis, biosynthesis, chemistry and dietary effects. Journal of Horticultural Science and Biotechnology 73: 1–18.
  • Grubb CD, Abel S. 2006. Glucosinolate metabolism and its control. Trends in Plant Science 11: 89–100.
  • Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57: 303–333.
  • Hansen BG, Kerwin RE, Ober JA, Lambrix VM, Mitchell-Olds T, Gershenzon J, Halkier BA, Kliebenstein DJ. 2008. A novel 2-oxoacid-dependent dioxygenase involved in the formation of the goiterogenic 2-hydroxybut-3-enyl glucosinolate and generalist insect resistance in Arabidopsis. Plant Physiology 148: 2096–2108.
  • Hasan M, Friedt W, Pons-Kuhnemann J, Freitag NM, Link K, Snowdon RJ. 2008. Association of gene-linked SSR markers to seed glucosinolate content in oilseed rape (Brassica napus ssp. napus). Theoretical and Applied Genetics 116: 1035–1049.
  • Hemm MR, Ruegger MO, Chapple C. 2003. The Arabidopsis ref2 mutant is defective in the gene encoding CYP83A1 and shows both phenylpropanoid and glucosinolate phenotypes. Plant Cell 15: 179–194.
  • Howell PM, Sharpe AG, Lydiate DJ. 2003. Homoeologous loci control the accumulation of seed glucosinolates in oilseed rape (Brassica napus). Genome 46: 454–460.
  • Hull AK, Vij R, Celenza JL. 2000. Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proceedings of the National Academy of Sciences, USA 97: 2379–2384.
  • Husebye H, Chadchawan S, Winge P, Thangstad OP, Bones AM. 2002. Guard cell- and phloem idioblast-specific expression of thioglucoside glucohydrolase 1 (myrosinase) in Arabidopsis. Plant Physiology 128: 1180–1188.
  • Iqbal MCM, Robbelen G, Mollers C. 1995. Biosynthesis of glucosinolates by microspore derived embryoids and plantlets in vitro of Brassica napus L. Plant Science 112: 107–115.
  • ISO9167-1. 1992. Rapeseed-determination of glucosinolates content. Part 1: method using gradient elution high-performance liquid chromatography. Switzerland, Europe: International Organization for Standardization.
  • Keurentjes JJ, Fu J, de Vos CH, Lommen A, Hall RD, Bino RJ, van der Plas LH, Jansen RC, Vreugdenhil D, Koornneef M. 2006. The genetics of plant metabolism. Nature Genetics 38: 842–849.
  • Keurentjes JJ, Koornneef M, Vreugdenhil D. 2008. Quantitative genetics in the age of omics. Current Opinion in Plant Biology 11: 123–128.
  • Kliebenstein DJ, Gershenzon J, Mitchell-Olds T. 2001a. Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159: 359–370.
  • Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, Gershenzon J, Mitchell-Olds T. 2001b. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiology 126: 811–825.
  • Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T. 2001c. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13: 681–693.
  • Kliebenstein DJ, West MA, van Leeuwen H, Loudet O, Doerge RW, St Clair DA. 2006. Identification of QTLs controlling gene expression networks defined a priori. BMC Bioinformatics 7: 308.
  • Kondra ZP, Stefansson BR. 1970. Inheritance of the major glucosinolates of rapeseed (Brassica napus) meal. Canadian Journal of Plant Science 50: 643–647.
  • Li G, Gao M, Yang B, Quiros CF. 2003. Gene for gene alignment between the Brassica and Arabidopsis genomes by direct transcriptome mapping. Theoretical and Applied Genetics 107: 168–180.
  • 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. Theoretical and Applied Genetics 103: 455–461.
  • Li G, Quiros CF. 2002. Genetic analysis, expression and molecular characterization of BoGSL-ELONG, a major gene involved in the aliphatic glucosinolate pathway of Brassica species. Genetics 162: 1937–1943.
  • Li G, Quiros CF. 2003. In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSL-ALK. Theoretical and Applied Genetics 106: 1116–1121.
  • Li Y, Kiddle G, Bennett R, Doughty K, Wallsgrove R. 1999. Variation in the glucosinolate content of vegetative tissues of Chinese lines of Brassica napus L. Annals of Applied Biology 134: 131–136.
    Direct Link:
  • Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Park BS et al. 2007. Flowering time quantitative trait loci analysis of oilseed brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177: 2433–2444.
  • Lou P, Zhao J, He H, Hanhart C, Del Carpio DP, Verkerk R, Custers J, Koornneef M, Bonnema G. 2008. Quantitative trait loci for glucosinolate accumulation in Brassica rapa leaves. New Phytologist 179: 1017–1032.
    Direct Link:
  • Mikkelsen MD, Petersen BL, Glawischnig E, Jensen AB, Andreasson E, Halkier BA. 2003. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiology 131: 298–308.
  • Mikkelsen MD, Petersen BL, Olsen CE, Halkier BA. 2002. Biosynthesis and metabolic engineering of glucosinolates. Amino Acids 22: 279–295.
  • Mithen R. 1992. Leaf glucosinolate profiles and their relationship to pest and disease resistance in oilseed rape. Euphytica 63: 71–83.
  • Mugford SG, Yoshimoto N, Reichelt M, Wirtz M, Hill L, Mugford ST, Nakazato Y, Noji M, Takahashi H, Kramell R et al. 2009. Disruption of adenosine-5′-phosphosulfate kinase in Arabidopsis reduces levels of sulfated secondary metabolites. Plant Cell 21: 910–927.
  • Padilla G, Cartea ME, Velasco P, de Haro A, Ordas A. 2007. Variation of glucosinolates in vegetable crops of Brassica rapa. Phytochemistry 68: 536–545.
  • 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. Theoretical and Applied Genetics 114: 67–80.
  • 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. Theoretical and Applied Genetics 113: 549–561.
  • Ramchiary N, Bisht NC, Gupta V, Mukhopadhyay A, Arumugam N, Sodhi YS, Pental D, Pradhan AK. 2007. QTL analysis reveals context-dependent loci for seed glucosinolate trait in the oilseed Brassica juncea: importance of recurrent selection backcross scheme for the identification of ‘true’ QTL. Theoretical and Applied Genetics 116: 77–85.
  • Reintanz B, Lehnen M, Reichelt M, Gershenzon J, Kowalczyk M, Sandberg G, Godde M, Uhl R, Palme K. 2001. Bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13: 351–367.
  • Sawada Y, Kuwahara A, Nagano M, Narisawa T, Sakata A, Saito K, Hirai MY. 2009. Omics-based approaches to methionine side chain elongation in Arabidopsis: characterization of the genes encoding methylthioalkylmalate isomerase and methylthioalkylmalate dehydrogenase. Plant and Cell Physiology 50: 1181–1190.
  • Sharpe AG, Lydiate DJ. 2003. Mapping the mosaic of ancestral genotypes in a cultivar of oilseed rape (Brassica napus) selected via pedigree breeding. Genome 46: 461–468.
  • Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J. 2009. Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182: 851–861.
  • Sonderby IE, Geu-Flores F, Halkier BA. 2010. Biosynthesis of glucosinolates--gene discovery and beyond. Trends in Plant Science 15: 283–290.
  • Talalay P, Fahey JW. 2001. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. Journal of Nutrition 131: 3027–3033.
  • Tierens KF, Thomma BP, Brouwer M, Schmidt J, Kistner K, Porzel A, Mauch-Mani B, Cammue BP, Broekaert WF. 2001. Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiology 125: 1688–1699.
  • Toroser D, Thormann CE, Osborn TC, Mithen R. 1995. RFLP mapping of quantitative trait loci controlling seed aliphatic glucosinolate content in oilseed rape (Brassica napus L.). Theoretical and Applied Genetics 91: 802–808.
  • Uzunova M, Ecke W, Weissleder K, Röbbelen 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. Theoretical and Applied Genetics 90: 194–204.
  • Vaughn SF, Isbell TA, Weisleder D, Berhow MA. 2005. Biofumigant compounds released by field pennycress (Thlaspi arvense) seedmeal. Journal of Chemical Ecology 31: 167–177.
  • Wang DL, Zhu J, Li ZK, Paterson AH. 1999. Mapping QTLs with epistatic effects and QTL X environment interactions by mixed linear model approaches. Theoretical and Applied Genetics 99: 1255–1264.
  • Wathelet J-P, Iori R, Leoni O, Rollin P, Quinsac A, Palmieri S. 2004. Guidelines for glucosinolate analysis in green tissues used for biofumigation. Agroindustria 3: 257–266.
  • Wentzell AM, Rowe HC, Hansen BG, Ticconi C, Halkier BA, Kliebenstein DJ. 2007. Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways. PLoS Genetics 3: 1687–1701.
  • Windsor AJ, Reichelt M, Figuth A, Svatos A, Kroymann J, Kliebenstein DJ, Gershenzon J, Mitchell-Olds T. 2005. Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66: 1321–1333.
  • Wittkop B, Snowdon RJ, Friedt W. 2009. Status and perspectives of breeding for enhanced yield and quality of oilseed crops for Europe. Euphytica 170: 131–140.
  • Yatusevich R, Mugford SG, Matthewman C, Gigolashvili T, Frerigmann H, Delaney S, Koprivova A, Flugge UI, Kopriva S. 2010. Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant Journal 62: 1–11.
    Direct Link:
  • Zeng ZB. 1994. Precision mapping of quantitative trait loci. Genetics 136: 1457–1468.
  • Zhao J, Dimov Z, Becker HC, Ecke W, Möllers C. 2008. Mapping QTL controlling fatty acid composition in a doubled haploid rapeseed population segregating for oil content. Molecular Breeding 21: 115–125.
  • Zhao J, Meng J. 2003. Detection of loci controlling seed glucosinolate content and their association with Sclerotinia resistance in Brassica napus. Plant Breeding 122: 19–23.
    Direct Link:
  • Zukalová H, Vašák J. 2002. The role and effects of glucosinolates of Brassica species- a review. Rostlinna Vyroba – UZPI 48: 175–180.
View Full Article with Supporting Information (HTML) Get PDF (2647K)