Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Aug;161(4):1685–1696. doi: 10.1093/genetics/161.4.1685

Genetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana.

Daniel J Kliebenstein 1, Antje Figuth 1, Thomas Mitchell-Olds 1
PMCID: PMC1462221  PMID: 12196411

Abstract

The ability of a single genotype to generate different phenotypes in disparate environments is termed phenotypic plasticity, which reflects the interaction of genotype and environment on developmental processes. However, there is controversy over the definition of plasticity genes. The gene regulation model states that plasticity loci influence trait changes between environments without altering the means within a given environment. Alternatively, the allelic sensitivity model argues that plasticity evolves due to selection of phenotypic values expressed within particular environments; hence plasticity must be controlled by loci expressed within these environments. To identify genetic loci controlling phenotypic plasticity and address this controversy, we analyzed the plasticity of glucosinolate accumulation under methyl jasmonate (MeJa) treatment in Arabidopsis thaliana. We found genetic variation influencing multiple MeJa signal transduction pathways. Analysis of MeJa responses in the Landsberg erecta x Columbia recombinant inbred lines identified a number of quantitative trait loci (QTL) that regulate plastic MeJa responses. All significant plasticity QTL also impacted the mean trait value in at least one of the two "control" or "MeJa" environments, supporting the allelic sensitivity model. Additionally, we present an analysis of MeJa and salicylic acid cross-talk in glucosinolate regulation and describe the implications for glucosinolate physiology and functional understanding of Arabidopsis MeJa signal transduction.

Full Text

The Full Text of this article is available as a PDF (267.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alonso-Blanco C., El-Assal S. E., Coupland G., Koornneef M. Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. Genetics. 1998 Jun;149(2):749–764. doi: 10.1093/genetics/149.2.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bak S., Tax F. E., Feldmann K. A., Galbraith D. W., Feyereisen R. CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell. 2001 Jan;13(1):101–111. doi: 10.1105/tpc.13.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carroll S. B. Endless forms: the evolution of gene regulation and morphological diversity. Cell. 2000 Jun 9;101(6):577–580. doi: 10.1016/s0092-8674(00)80868-5. [DOI] [PubMed] [Google Scholar]
  4. Churchill G. A., Doerge R. W. Empirical threshold values for quantitative trait mapping. Genetics. 1994 Nov;138(3):963–971. doi: 10.1093/genetics/138.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clarke J. H., Mithen R., Brown J. K., Dean C. QTL analysis of flowering time in Arabidopsis thaliana. Mol Gen Genet. 1995 Aug 21;248(3):278–286. doi: 10.1007/BF02191594. [DOI] [PubMed] [Google Scholar]
  6. Doebley J., Stec A., Hubbard L. The evolution of apical dominance in maize. Nature. 1997 Apr 3;386(6624):485–488. doi: 10.1038/386485a0. [DOI] [PubMed] [Google Scholar]
  7. El-Din El-Assal S., Alonso-Blanco C., Peeters A. J., Raz V., Koornneef M. A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet. 2001 Dec;29(4):435–440. doi: 10.1038/ng767. [DOI] [PubMed] [Google Scholar]
  8. Grenier J. K., Carroll S. B. Functional evolution of the Ultrabithorax protein. Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):704–709. doi: 10.1073/pnas.97.2.704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gupta V., Willits M. G., Glazebrook J. Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol Plant Microbe Interact. 2000 May;13(5):503–511. doi: 10.1094/MPMI.2000.13.5.503. [DOI] [PubMed] [Google Scholar]
  10. Hansen C. H., Du L., Naur P., Olsen C. E., Axelsen K. B., Hick A. J., Pickett J. A., Halkier B. A. CYP83b1 is the oxime-metabolizing enzyme in the glucosinolate pathway in Arabidopsis. J Biol Chem. 2001 May 1;276(27):24790–24796. doi: 10.1074/jbc.M102637200. [DOI] [PubMed] [Google Scholar]
  11. Hermsmeier D., Schittko U., Baldwin I. T. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol. 2001 Feb;125(2):683–700. doi: 10.1104/pp.125.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kliebenstein D. J., Gershenzon J., Mitchell-Olds T. Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics. 2001 Sep;159(1):359–370. doi: 10.1093/genetics/159.1.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kliebenstein D. J., Kroymann J., Brown P., Figuth A., Pedersen D., Gershenzon J., Mitchell-Olds T. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 2001 Jun;126(2):811–825. doi: 10.1104/pp.126.2.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kliebenstein D. J., Lambrix V. M., Reichelt M., Gershenzon J., Mitchell-Olds T. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell. 2001 Mar;13(3):681–693. doi: 10.1105/tpc.13.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kliebenstein Daniel, Pedersen Deana, Barker Bridget, Mitchell-Olds Thomas. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics. 2002 May;161(1):325–332. doi: 10.1093/genetics/161.1.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maleck K., Levine A., Eulgem T., Morgan A., Schmid J., Lawton K. A., Dangl J. L., Dietrich R. A. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet. 2000 Dec;26(4):403–410. doi: 10.1038/82521. [DOI] [PubMed] [Google Scholar]
  17. Maloof J. N., Borevitz J. O., Dabi T., Lutes J., Nehring R. B., Redfern J. L., Trainer G. T., Wilson J. M., Asami T., Berry C. C. Natural variation in light sensitivity of Arabidopsis. Nat Genet. 2001 Dec;29(4):441–446. doi: 10.1038/ng777. [DOI] [PubMed] [Google Scholar]
  18. Rao M. V., Lee H., Creelman R. A., Mullet J. E., Davis K. R. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell. 2000 Sep;12(9):1633–1646. doi: 10.1105/tpc.12.9.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Reintanz B., Lehnen M., Reichelt M., Gershenzon J., Kowalczyk M., Sandberg G., Godde M., Uhl R., Palme K. Bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell. 2001 Feb;13(2):351–367. doi: 10.1105/tpc.13.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Reymond P., Weber H., Damond M., Farmer E. E. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell. 2000 May;12(5):707–720. doi: 10.1105/tpc.12.5.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Stotz H. U., Pittendrigh B. R., Kroymann J., Weniger K., Fritsche J., Bauke A., Mitchell-Olds T. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 2000 Nov;124(3):1007–1018. doi: 10.1104/pp.124.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sultan S. E. Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 2000 Dec;5(12):537–542. doi: 10.1016/s1360-1385(00)01797-0. [DOI] [PubMed] [Google Scholar]
  23. Tierens K. F., Thomma B. P., Brouwer M., Schmidt J., Kistner K., Porzel A., Mauch-Mani B., Cammue B. P., Broekaert W. F. Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol. 2001 Apr;125(4):1688–1699. doi: 10.1104/pp.125.4.1688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wittstock U., Halkier B. A. Cytochrome P450 CYP79A2 from Arabidopsis thaliana L. Catalyzes the conversion of L-phenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate. J Biol Chem. 2000 May 12;275(19):14659–14666. doi: 10.1074/jbc.275.19.14659. [DOI] [PubMed] [Google Scholar]
  25. Zeng Z. B. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. doi: 10.1093/genetics/136.4.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zeng Z. B. Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10972–10976. doi: 10.1073/pnas.90.23.10972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. van Der Schaar W., Alonso-Blanco C., Léon-Kloosterziel K. M., Jansen R. C., van Ooijen J. W., Koornneef M. QTL analysis of seed dormancy in Arabidopsis using recombinant inbred lines and MQM mapping. Heredity (Edinb) 1997 Aug;79(Pt 2):190–200. doi: 10.1038/hdy.1997.142. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES