Skip to main content
SpringerLink
Log in

A quantitative genetics and ecological model system: understanding the aliphatic glucosinolate biosynthetic network via QTLs

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

Plants’ sessile nature has led them to develop chemical defenses, secondary metabolites, to directly cope with environmental changes rather than escape to more favorable sites. The diversity and fluctuation in biological stresses faced by a plant have generated extraordinary genetic diversity controlling the synthesis and regulation of secondary metabolites that is only now being explored. The glucosinolate secondary metabolites, amino acid derived thioglucosides specific to the order Capparales, is a model system for understanding the molecular basis of complex quantitative traits and their potential ecological role. This review focuses on the extensive progress being made towards understanding the complete molecular basis underlying the glucosinolate genetic diversity at both biosynthetic and regulatory loci. This has identified a highly interactive genetic network whereby biosynthetic loci have additional functions as regulatory loci and laid the foundation for glucosinolates to be a model system for understanding quantitative traits in a broader context.

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

Similar content being viewed by others

Abbreviations

QTL:

Quantitative trait locus

GSL-():

QTL for glucosinolates

GSL-OX:

QTL for conversion of methylthio to methylsulfinyl glucosinolate

GSL-Elong:

QTL for controlling side-chain length of glucosinolates

GSL-ALK:

QTL for production of alkenyl glucosinolates

GSL-OHP:

QTL for production of hydroxalkyl glucosinolates

GSL-AOP:

QTL for production of alkenyl or hydroxyalkyl glucosinolates

GSL-OH:

QTL for production of hydroxylalkenyl glucosinolates

FMO:

Flavin monooxygenase

BCAT:

Branched chain amino transferase

CYP:

Cytochromes P450

PMSR:

Peptide methionine sulfoxide reductase

MAM:

Methylthioalkylmalate synthase

UGT:

UDP-glucosyl transferase

ST:

Sulfotransferase

References

  • Barth C, Jander G (2006) Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glucosinolate breakdown and insect defense. Plant Journal 46:549–562

    Article  PubMed  CAS  Google Scholar 

  • Benderoth M, Textor S, Windsor AJ et al (2006) Positive selection driving diversification in plant secondary metabolism. Proc Natl Acad Sci USA 103:9118–9123

    Article  PubMed  CAS  Google Scholar 

  • Bones AM, Rossiter JT (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 97:194–208

    Article  CAS  Google Scholar 

  • Borevitz JO, Hazen SP, Michael TP et al (2007) Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:12057–12062

    Article  PubMed  CAS  Google Scholar 

  • Brem RB, Yvert G, Clinton R et al (2002) Genetic dissection of transcriptional regulation in budding yeast. Science 296:752–755

    Article  PubMed  CAS  Google Scholar 

  • Burow M, Wittstock U (this issue) Regulation and function of specifier proteins in plants. Phytochem Rev

  • Clark RM, Schweikert G, Toomajian C et al (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317:338–342

    Article  PubMed  CAS  Google Scholar 

  • Daubos P, Grumel V, Iori R et al (1998) Crambe abyssinica meal as starting material for the production of enantiomerically pure fine chemicals. Ind Crops Prod 7:187–193

    Article  CAS  Google Scholar 

  • Daxenbichler ME, Spencer GF, Carlson DG et al (1991) Glucosinolate composition of seeds from 297 species of wild plants. Phytochemistry 30:2623–2638

    Article  CAS  Google Scholar 

  • de Quiros HC, Magrath R, McCallum D et al (2000) α-Keto acid elongation and glucosinolate biosynthesis in Arabidopsis thaliana. Theor Appl Genet 101:429–437

    Article  Google Scholar 

  • Donkin SG, Eiteman MA, Williams PL (1995) Toxicity of glucosinolates and their enzymatic decomposition products to Caenorhabditis elegans. J Nematol 27:258–262

    CAS  PubMed  Google Scholar 

  • Ellner S, Hairston NG (1994) Role of overlapping generations in maintaining genetic-variation in a fluctuating environment. Am Nat 143:403–417

    Article  Google Scholar 

  • Faulkner K, Mithen R, Williamson G (1998) Selective increase of the potential anticarcinogen 4-methylsulphinylbutyl glucosinolate in broccoli. Carcinogenesis 19:605–609

    Article  PubMed  CAS  Google Scholar 

  • Gachon CMM, Langlois-Meurinne M, Henry Y et al (2005) Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications. Plant Mol Biol 58:229–245

    Article  PubMed  CAS  Google Scholar 

  • Gao MQ, Li GY, Yang B et al (2007) High-density Brassica oleracea linkage map: identification of useful new linkages. Theor Appl Genet 115:277–287

    Article  PubMed  CAS  Google Scholar 

  • Giamoustaris A, Mithen R (1995) The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus Ssp oleifera) on its interaction with specialist and generalist pests. Ann Appl Biol 126:347–363

    Article  CAS  Google Scholar 

  • Giamoustaris A, Mithen R (1996) Genetics of aliphatic glucosinolates. IV. Side-chain modification in Brassica oleracea. Theor Appl Genet 93:1006–1010

    Article  CAS  Google Scholar 

  • Gigolashvili T, Yatusevich R, Berger B et al (2007) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51:247–261

    Article  PubMed  CAS  Google Scholar 

  • Graser G, Schneider B, Oldham NJ et al (2000) The methionine chain elongation pathway in the biosynthesis of glucosinolates in Eruca sativa (Brassicaceae). Arch Biochem Biophys 378:411–419

    Article  PubMed  CAS  Google Scholar 

  • Grubb CD, Zipp BJ, Ludwig-Müller J et al (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40:893–908

    Article  PubMed  CAS  Google Scholar 

  • Hairston NG, Dillon TA (1990) Fluctuating selection and response in a population of fresh-water copepods. Evolution 44:1796–1805

    Article  Google Scholar 

  • Halkier BA, Du L (1997) The biosynthesis of glucosinolates. Trends Plant Sci 2:425–431

    Article  Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Ann Rev Plant Biol 57:303–333

    Article  CAS  Google Scholar 

  • Hansen BG, Halkier BA, Kliebenstein DJ (2008) Identifying the molecular basis of QTLs: eQTLs add a new dimension. Trends Plant Sci 13:72–77

    PubMed  CAS  Google Scholar 

  • Hansen BG, Kliebenstein DJ, Halkier BA (2007) Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 50:902–910

    Article  PubMed  CAS  Google Scholar 

  • Hill J, Lethenborg P, Li PW et al (2003) Inheritance of progoitrin and total aliphatic glucosinolates in oilseed rape (Brassica napus L). Euphytica 134:179–187

    Article  CAS  Google Scholar 

  • Hirai M, Sugiyama K, Sawada Y et al (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 104:6478–6483

    Article  PubMed  CAS  Google Scholar 

  • Hogge LR, Reed DW, Underhill EW et al (1988) HPLC separation of glucosinolates from leaves and seeds of Arabidopsis thaliana and their identification using thermospary liquid chromatography-mass spectometry. J Chrom Sci 26:551–556

    CAS  Google Scholar 

  • Kahn RA, Fahrendorf T, Halkier BA et al (1999) Substrate specificity of the cytochrome P450 enzymes CYP79A1 and CYP71E1 involved in the biosynthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor (L.) Moench. Arch Biochem Biophys 363:9–18

    Article  PubMed  CAS  Google Scholar 

  • Keurentjes JJB, Fu JY, Terpstra IR et al (2007) Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proc Natl Acad Sci USA 104:1708–1713

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein DJ (2008) A role for gene duplication and natural variation of gene expression in the evolution of metabolism. PLos ONE 3:e1838

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein D, Lambrix V, Reichelt M et al (2001a) Gene duplication and the diversification of secondary metabolism: side chain modification of glucosinolates in Arabidopsis thaliana. Plant Cell 13:681–693

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein DJ, Gershenzon J, Mitchell-Olds T (2001b) Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159:359–370

    PubMed  CAS  Google Scholar 

  • Kliebenstein DJ, Kroymann J, Brown P et al (2001c) Genetic control of natural variation in Arabidopsis thaliana glucosinolate accumulation. Plant Physiol 126:811–825

    Article  PubMed  CAS  Google Scholar 

  • Kliebenstein DJ, Figuth A, Mitchell-Olds T (2002a) Genetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana. Genetics 161:1685–1696

    PubMed  CAS  Google Scholar 

  • Kliebenstein DJ, Pedersen D, Mitchell-Olds T (2002b) Comparative analysis of insect resistance QTL and QTL controlling the myrosinase/glucosinolate system in Arabidopsis thaliana. Genetics 161:325–332

    PubMed  CAS  Google Scholar 

  • Kliebenstein DJ, West MAL, Van Leeuwen H et al (2006) Genomic survey of gene expression diversity in Arabidopsis thaliana. Genetics 172:1179–1189

    Article  PubMed  Google Scholar 

  • Kliebenstein DJ, D’Auria JC, Behere AS et al (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J 51:1062–1076

    Article  PubMed  CAS  Google Scholar 

  • Kroymann J, Benderoth M, Pfalz M (this issue) Methylthioalkylmalate synthases: genetics, ecology & evolution. Phytochem Rev

  • Kroymann J, Donnerhacke S, Schnabelrauch D et al (2003) Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc Natl Acad Sci USA 100:14587–14592

    Article  PubMed  CAS  Google Scholar 

  • Lambrix V, Reichelt M, Mitchell-Olds T et al (2001) The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13:2793–2807

    Article  PubMed  CAS  Google Scholar 

  • Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175:176–184

    Article  PubMed  Google Scholar 

  • Lankau RA, Strauss SY (2007) Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317:1561–1563

    Article  PubMed  CAS  Google Scholar 

  • Li G, Quiros CF (2003) In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSL-ALK. Theor Appl Genet 106:1116–1121

    PubMed  CAS  Google Scholar 

  • Li Q, Eigenbrode SD, Stringham GR et al (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J Chem Ecol 26:2401–2419

    Article  CAS  Google Scholar 

  • Lionneton E, Aubert G, Ochatt S et al (2004) Genetic analysis of agronomic and quality traits in mustard (Brassica juncea). Theor Appl Genet 109:792–799

    Article  PubMed  CAS  Google Scholar 

  • Mackay TFC (2001) The genetic architecture of quantitative traits. Ann Rev Genet 35:303–339

    Article  PubMed  CAS  Google Scholar 

  • Magrath R, Bano F, Morgner M et al (1994) Genetics of aliphatic glucosinolates. I. Side chain elongation in Brassica napus and Arabidopsis thaliana. Heredity 72:290–299

    Article  CAS  Google Scholar 

  • Magrath R, Herron C, Giamoustaris A et al (1993) The inheritance of aliphatic glucosinolates in Brassica napus. Plant Breeding 111:55–72

    Article  CAS  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Tohge T et al (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251

    Article  PubMed  CAS  Google Scholar 

  • Mauricio R, Rausher MD (1997) Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–1444

    Article  Google Scholar 

  • Mithen R (1992) Leaf glucosinolate profiles and their relationships to pest and disease resistance in oilseed rape. Euphytica 63:71–83

    Article  CAS  Google Scholar 

  • Mithen R, Campos H (1996) Genetic variation of aliphatic glucosinolates in Arabidopsis thaliana and prospects for map based gene cloning. Entomol Exp Appl 80:202–205

    Article  CAS  Google Scholar 

  • Mithen R, Clarke J, Lister C et al (1995) Genetics of aliphatic glucosinolates.III. Side-chain structure of aliphatic glucosinolates in Arabidopsis thaliana. Heredity 74:210–215

    Article  CAS  Google Scholar 

  • Mithen R, Faulkner K, Magrath R et al (2003) Development of isothiocyanate-enriched broccoli, and its enhanced ability to induce phase 2 detoxification enzymes in mammalian cells. Theor Appl Genet 106:727–734

    PubMed  CAS  Google Scholar 

  • Mithen R, Toroser D (1995) Biochemical genetics of aliphatic glucosinolates in Brassica and Arabidopsis. Soc Exp Biol Semin Ser 56:261–275

    CAS  Google Scholar 

  • Mithen RF, Lewis BG, Fenwick GR (1986) In vitro activity of glucosinolates and their products against Leptosphaeria maculans. Trans Br Mycol Soc 87:433–440

    Article  CAS  Google Scholar 

  • Parkin I, Magrath R, Keith D et al (1994a) Genetics of aliphatic glucosinolates. II. Hydroxylation of alkenyl glucosinolates in Brassica napus. Heredity 72:594–598

    Article  CAS  Google Scholar 

  • Parkin I, Magrath R, Keith D et al (1994b) Genetis of aliphatic glucosinolates. II. Hydroxylation of alkenyl glucosinolates in Brassica napus. Heredity 72:594–598

    Article  CAS  Google Scholar 

  • Pfalz M, Vogel H, Mitchell-Olds T et al (2007) Mapping of QTL for Resistance against the Crucifer Specialist Herbivore Pieris brassicae in a New Arabidopsis Inbred Line Population, Da(1)-12 × Ei-2. PLos ONE 2:e578

    Article  PubMed  CAS  Google Scholar 

  • Potokina E, Druka A, Luo Z et al (2008) Gene expression quantitative trait locus analysis of 16 000 barley genes reveals a complex pattern of genome-wide transcriptional regulation. Plant J 53:90–101

    Article  PubMed  CAS  Google Scholar 

  • Raybould AF, Moyes CL (2001) The ecological genetics of aliphatic glucosinolates. Heredity 87:383–391

    Article  PubMed  CAS  Google Scholar 

  • Rodman J (1980) Population variation and hybridization in sea-rockets (Cakile, Cruciferae): Seed glucosinolate characters. Am J Bot 67:1145–1159

    Article  CAS  Google Scholar 

  • Rodman JE, Kruckeberg AR, Alshehbaz IA (1981) Chemotaxonomic diversity and complexity in seed glucosinolates of Caulanthus and Streptanthus (Cruciferae). Syst Bot 6:197–222

    Article  Google Scholar 

  • Sønderby IE, Hansen BG, Bjarnholt N et al (2007) A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLos ONE 2:e1322

    Article  PubMed  CAS  Google Scholar 

  • Textor S, Bartram S, Kroymann J et al (2004) Biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana: recombinant expression and characterization of methylthioalkylmalate synthase, the condensing enzyme of the chain-elongation cycle. Planta 218:1026–1035

    Article  PubMed  CAS  Google Scholar 

  • Textor S, de Kraker JW, Hause B et al (2007) MAM3 catalyzes the formation of all aliphatic glucosinolate chain lengths in Arabidopsis. Plant Physiol 144:60–71

    Article  PubMed  CAS  Google Scholar 

  • Tierens K-J, Thomma B, Brower M et al (2001) Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol 125:1688–1699

    Article  PubMed  CAS  Google Scholar 

  • Tiffin P, Rausher MD (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154:700–716

    Article  PubMed  Google Scholar 

  • Toroser D, Thormann C, Osborn T et al (1995) RFLP mapping of quantitative trait loci controlling seed aliphatic glucosinolate content in oilseed rape (Brassica napus L.). Theor Appl Genet 91:802–808

    Article  CAS  Google Scholar 

  • Uzunova M, Ecke W, Weissleder K et al (1995) Mapping the genome of rapeseed (Brassica napus L).1. Construction of an RFLP linkage map and localization of QTLs for seed glucosinolate content. Theor Appl Genet 90:194–204

    Article  CAS  Google Scholar 

  • Wentzell AM, Rowe HC, Hansen BG et al (2007) Linking metabolic QTL with network and cis-eQTL controlling biosynthetic pathways. PLOS Genet 3:e162

    Article  CAS  Google Scholar 

  • West MAL, van Leeuwen H, Kozik A et al (2006) High-density haplotyping with microarray-based expression and single feature polymorphism markers in Arabidopsis. Genom Res 16:787–795

    Article  CAS  Google Scholar 

  • West MAL, Kim K, Kliebenstein DJ et al (2007) Global eQTL mapping reveals the complex genetic architecture of transcript level variation in Arabidopsis. Genetics 175:1441–1450

    Article  PubMed  CAS  Google Scholar 

  • Windsor AJ, Reichelt M, Figuth A et al (2005) Geographic and evolutionary diversification of glucosinolates among near relatives of Arabidopsis thaliana (Brassicaceae). Phytochemistry 66:1321–1333

    Article  PubMed  CAS  Google Scholar 

  • Wink M (1988) Plant Breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233

    Article  CAS  Google Scholar 

  • Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79A2 from Arabidopsis thaliana L. catalyzes the conversion of L-phenylalanine to phenylacetaldoxime in the biosynthesis of the benzylglucosinolate. J Biol Chem 275:14659–14666

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z-Y, Ober JA, Kliebenstein DJ (2006) The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. Plant Cell 18:1524–1536

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

Funding for metabolite QTL analysis was obtained by a National Science Foundation grants DBI 0642481 to DJK.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, University of California, Davis, One Shields Avenue, Davis, CA, 95616, USA

    Daniel J. Kliebenstein

Authors
  1. Daniel J. Kliebenstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel J. Kliebenstein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kliebenstein, D.J. A quantitative genetics and ecological model system: understanding the aliphatic glucosinolate biosynthetic network via QTLs. Phytochem Rev 8, 243–254 (2009). https://doi.org/10.1007/s11101-008-9102-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-008-9102-8

Keywords

Search

Navigation