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PMID: 20026477 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition.

Molecular plant ·Vol. 3 ·No. 1 ·2010-01-00 ·Pages 224-35

Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK

Abstract

Heterosis, or hybrid vigor, is one of the most important tools in plant breeding and has previously been demonstrated for plant freezing tolerance. Freezing tolerance is an important trait because it can limit the geographical distribution of plants and their agricultural yield. Plants from temperate climates increase in freezing tolerance during exposure to low, non-freezing temperatures in a process termed 'cold acclimation'. Metabolite profiling has indicated a major reprogramming of plant metabolism in the cold, but it has remained unclear in previous studies which of these changes are related to freezing tolerance. In the present study, we have used metabolic profiling to discover combinations of metabolites that predict freezing tolerance and its heterosis in Arabidopsis thaliana. We identified compatible solutes and, in particular, the pathway leading to raffinose as crucial statistical predictors for freezing tolerance and its heterosis, while some TCA cycle intermediates contribute only to predicting the heterotic phenotype. This indicates coordinate links between heterosis and metabolic pathways, suggesting that a limited number of regulatory genes may determine the extent of heterosis in this complex trait. In addition, several unidentified metabolites strongly contributed to the prediction of both freezing tolerance and its heterosis and we present an exemplary analysis of one of these, identifying it as a hexose conjugate.

MeSH Terms
Arabidopsis/genetics,metabolism,physiology Computational Biology Freezing Gas Chromatography-Mass Spectrometry Gene Expression Regulation, Plant/genetics,physiology Models, Biological
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Korn Marina
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, Potsdam, Germany.
Gärtner Tanja
Erban Alexander
Kopka Joachim
Selbig Joachim
Hincha Dirk K
References (47)
47 references, click to expand
  1. TagFinder for the quantitative analysis of gas chromatography--mass spectrometry (GC-MS)-based metabolite profiling experiments.
    Bioinformatics. 2008 Mar 1;24(5):732-7 PMID: 18204057
  2. PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:571-599 PMID: 15012220
  3. The metabolic response of heterotrophic Arabidopsis cells to oxidative stress.
    Plant Physiol. 2007 Jan;143(1):312-25 PMID: 17122072
  4. GC-EI-TOF-MS analysis of in vivo carbon-partitioning into soluble metabolite pools of higher plants by monitoring isotope dilution after 13CO2 labelling.
    Phytochemistry. 2007 Aug-Sep;68(16-18):2258-72 PMID: 17475294
  5. Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content.
    Plant J. 2007 Jun;50(6):967-81 PMID: 17461790
  6. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis.
    Proc Natl Acad Sci U S A. 2004 Oct 19;101(42):15243-8 PMID: 15383661
  7. Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana.
    New Phytol. 2008;177(2):419-427 PMID: 17995917
  8. Natural genetic variation of freezing tolerance in Arabidopsis.
    Plant Physiol. 2006 Sep;142(1):98-112 PMID: 16844837
  9. Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses.
    J Biol Chem. 2001 Oct 26;276(43):39586-91 PMID: 11517217
  10. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance.
    Plant Cell Environ. 2008 Jun;31(6):813-27 PMID: 18284584
  11. Evidence for a large-scale population structure of Arabidopsis thaliana from genome-wide single nucleotide polymorphism markers.
    Theor Appl Genet. 2006 Apr;112(6):1104-14 PMID: 16453134
  12. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis.
    Plant J. 2005 Jan;41(2):195-211 PMID: 15634197
  13. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana.
    PLoS Genet. 2005 Aug;1(2):e26 PMID: 16121258
  14. In search of the molecular basis of heterosis.
    Plant Cell. 2003 Oct;15(10):2236-9 PMID: 14523245
  15. Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A.
    Plant Physiol. 2009 Aug;150(4):1972-80 PMID: 19502356
  16. Towards the molecular basis of heterosis.
    Trends Plant Sci. 2007 Sep;12(9):427-32 PMID: 17720610
  17. The role of raffinose in the cold acclimation response of Arabidopsis thaliana.
    FEBS Lett. 2004 Oct 8;576(1-2):169-73 PMID: 15474032
  18. Unraveling the genetic basis of hybrid vigor.
    Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):12957-8 PMID: 16938847
  19. The metabolic signature related to high plant growth rate in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4759-64 PMID: 17360597
  20. Exploring the temperature-stress metabolome of Arabidopsis.
    Plant Physiol. 2004 Dec;136(4):4159-68 PMID: 15557093
  21. Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement.
    Nat Biotechnol. 2006 Apr;24(4):447-54 PMID: 16531992
  22. Natural variation in CBF gene sequence, gene expression and freezing tolerance in the Versailles core collection of Arabidopsis thaliana.
    BMC Plant Biol. 2008 Oct 15;8:105 PMID: 18922165
  23. Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles.
    Phytochemistry. 2003 Mar;62(6):887-900 PMID: 12590116
  24. The control of protein stability and association by weak interactions with water: how do solvents affect these processes?
    Annu Rev Biophys Biomol Struct. 1993;22:67-97 PMID: 8347999
  25. Retention index thresholds for compound matching in GC-MS metabolite profiling.
    J Chromatogr B Analyt Technol Biomed Life Sci. 2008 Aug 15;871(2):182-90 PMID: 18501684
  26. Zooming in on a quantitative trait for tomato yield using interspecific introgressions.
    Science. 2004 Sep 17;305(5691):1786-9 PMID: 15375271
  27. Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome.
    Plant Cell. 2008 May;20(5):1199-216 PMID: 18515501
  28. [email protected]: the Golm Metabolome Database.
    Bioinformatics. 2005 Apr 15;21(8):1635-8 PMID: 15613389
  29. Plants in a cold climate.
    Philos Trans R Soc Lond B Biol Sci. 2002 Jul 29;357(1423):831-47 PMID: 12171647
  30. Establishment of a high-efficiency SNP-based framework marker set for Arabidopsis.
    Plant J. 2003 Oct;36(1):122-40 PMID: 12974817
  31. Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance.
    Plant J. 2004 Jun;38(5):790-9 PMID: 15144380
  32. The cause and consequences of natural variation: the genome era takes off!
    Curr Opin Plant Biol. 2008 Apr;11(2):99-102 PMID: 18337159
  33. Heterosis for biomass yield and related traits in five hybrids of Arabidopsis thaliana L. Heynh.
    Heredity (Edinb). 2003 Jul;91(1):36-42 PMID: 12815451
  34. Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis.
    Nature. 2006 Jun 22;441(7096):947-52 PMID: 16791187
  35. Naturally occurring genetic variation in Arabidopsis thaliana.
    Annu Rev Plant Biol. 2004;55:141-72 PMID: 15377217
  36. Potential of metabolomics as a functional genomics tool.
    Trends Plant Sci. 2004 Sep;9(9):418-25 PMID: 15337491
  37. Current challenges and developments in GC-MS based metabolite profiling technology.
    J Biotechnol. 2006 Jun 25;124(1):312-22 PMID: 16434119
  38. Significance analysis of microarrays applied to the ionizing radiation response.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21 PMID: 11309499
  39. Metabolomics of temperature stress.
    Physiol Plant. 2008 Feb;132(2):220-35 PMID: 18251863
  40. Unused natural variation can lift yield barriers in plant breeding.
    PLoS Biol. 2004 Oct;2(10):e245 PMID: 15328532
  41. Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis.
    Plant Physiol. 2005 Nov;139(3):1304-12 PMID: 16244146
  42. pcaMethods--a bioconductor package providing PCA methods for incomplete data.
    Bioinformatics. 2007 May 1;23(9):1164-7 PMID: 17344241
  43. Living with water stress: evolution of osmolyte systems.
    Science. 1982 Sep 24;217(4566):1214-22 PMID: 7112124
  44. Heterosis: revisiting the magic.
    Trends Genet. 2007 Feb;23(2):60-6 PMID: 17188398
  45. The genetics of plant metabolism.
    Nat Genet. 2006 Jul;38(7):842-9 PMID: 16751770
  46. Improved heterosis prediction by combining information on DNA- and metabolic markers.
    PLoS One. 2009;4(4):e5220 PMID: 19370148
  47. Heterosis of biomass production in Arabidopsis. Establishment during early development.
    Plant Physiol. 2004 Apr;134(4):1813-23 PMID: 15064384
Article Info
Journal
Molecular plant
Abbr.
Mol Plant
ISSN
1674-2052
DOI
10.1093/mp/ssp105
Published
2010-01-00
Epub
2009-00-21
Pages
224-35
Language
English
Region
England
NLM ID
101465514
PMCID
PMC2807929
Subset
IM
External Links
PubMed source DOI: 10.1093/mp/ssp105 PMC Full Text View journal details
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