Plant Molecular Biology

, Volume 62, Issue 4–5, pp 593–609 | Cite as

Response diversity of Arabidopsis thaliana ecotypes in elevated [CO2] in the field

  • Pinghua Li
  • Allan Sioson
  • Shrinivasrao P. Mane
  • Alexander Ulanov
  • Gregory Grothaus
  • Lenwood S. Heath
  • T. M. Murali
  • Hans J. Bohnert
  • Ruth Grene
Article

Abstract

Free Air [CO2] Enrichment (FACE) allows for plant growth under fully open-air conditions of elevated [CO2] at concentrations expected to be reached by mid-century. We used Arabidopsis thaliana ecotypes Col-0, Cvi-0, and WS to analyze changes in gene expression and metabolite profiles of plants grown in “SoyFACE” (http://www.soyface.uiuc.edu/), a system of open-air rings within which [CO2] is elevated to ~550 ppm. Data from multiple rings, comparing plants in ambient air and elevated [CO2], were analyzed by mixed model ANOVA, linear discriminant analysis (LDA) and data-mining tools. In elevated [CO2], decreases in the expression of genes related to chloroplast functions characterized all lines but individual members of distinct multi-gene families were regulated differently between lines. Also, different strategies distinguished the lines with respect to the␣regulation of genes related to carbohydrate biosynthesis and partitioning, N-allocation and amino acid metabolism, cell wall biosynthesis, and hormone responses, irrespective of the plants’ developmental status. Metabolite results paralleled reactions seen at the level of transcript expression. Evolutionary adaptation of species to their habitat and intrinsic genetic plasticity seem to determine the nature of responses to elevated [CO2]. Irrespective of their underlying genetic diversity, and evolutionary adaptation to different habitats, a small number of common, predominantly stress-responsive, signature transcripts appear to characterize responses of the Arabidopsis ecotypes in FACE.

Keywords

Arabidopsis thaliana ecotypes Elevated [CO2FACE Transcript profiling Metabolite profiling 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

References

  1. Ainsworth EA, Long SP (2005) What have learned from fifteen years of Free Air Carbon Dioxide Enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165:351–372PubMedCrossRefGoogle Scholar
  2. Ainsworth EA, Rogers A, Blum H, Nosberger J, Long SP (2003) Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to Free-Air CO2 Enrichment (FACE). J Exp Bot 54:276–284CrossRefGoogle Scholar
  3. Allison DB, Cui X, Page GP, Sabripour M (2006) Microarray data analysis: from disarray to consolidation and consensus. Nat Rev Genet 7:55–65PubMedCrossRefGoogle Scholar
  4. Alonso-Blanco C, El-Assal SE, Coupland G, Koornneef M (1998) Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. Genetics 149:749–764PubMedGoogle Scholar
  5. Bohmert K, Balbo I, Kopka J, Mittendorf V, Nawrath C, Poirier Y, Tischendorf G, Trethewey RN, Willmitzer L (2000) Transgenic Arabidopsis plants can accumulate polyhydroxybutyrate to up to 4% of their fresh weight. Planta 211:841–845PubMedCrossRefGoogle Scholar
  6. Bowes G (1993) Facing the inevitable: Plants and increasing atmospheric CO2. Annu Rev Plant Physiol Plant Mol Biol 44:309–332CrossRefGoogle Scholar
  7. Brinker M, van Zyl L, Liu W, Craig D, Sederoff R, Clapham D, von Arnold S (2004) Microarray analyses of gene expression during adventitious root development in Pinus contorta. Plant Physiol 135:1526–1539PubMedCrossRefGoogle Scholar
  8. Byrne KA, Wang YH, Lehnert SA, Harper GS, McWilliam SM, Bruce HL, Reverter A (2005) Gene expression profiling of muscle tissue in Brahman steers during nutritional restriction. J Anim Sci 83:1–12PubMedGoogle Scholar
  9. Carnal NW, Agostino A, Hatch MD (1993) Photosynthesis in Phosphoenolpyruvate carboxykinase-type C4 plants: mechanism and regulation of C4 acid decarboxylation in bundle sheath cells. Arch Biochem Biophys 306:360–367PubMedCrossRefGoogle Scholar
  10. Catchpole GS, Beckmann M, Enot DP, Mondhe M, Zywicki B, Taylor J, Hardy N, Smith A, King RD, Kell DB, Fiehn O, Draper J (2005) Hierarchical metabolomics demonstrates substantial compositional similarity between genetically modified and conventional potato crops. Proc Natl Acad Sci USA 102:14458–14462PubMedCrossRefGoogle Scholar
  11. Cheng SH, Moore B, Seemann JR (1998) Effects of short- and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiol 116:715–723PubMedCrossRefGoogle Scholar
  12. Chu TM, Weir B, Wolfinger R (2002) A systematic statistical linear modeling approach to oligonucleotide array experiments. Math Biosci 176:35–51PubMedCrossRefGoogle Scholar
  13. Cui X, Churchill G (2003) Statistical tests for differential expression in cDNA microarray experiments. Genome Biol 4:201CrossRefGoogle Scholar
  14. Drake BJ, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2. Annu Rev Plant Physiol Plant Mol Biol 48:609–639PubMedCrossRefGoogle Scholar
  15. Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93– 102PubMedCrossRefGoogle Scholar
  16. Gupta P, Duplessis S, White H, Karnosky DF, Martin F, Podila GK (2005) Gene expression patterns of trembling aspen trees following long-term exposure to interacting elevated CO2 and tropospheric O3. New Phytologist 167:129–142PubMedCrossRefGoogle Scholar
  17. Heath LS, Ramakrishnan N, Sederoff RR, Whetten RW, Chevone BI, Struble CA, Jouenne VY, Chen DW, van Zyl L, Grene R (2002) Studying the functional genomics of stress responses in loblolly pine with the Expresso microarray experiment management system. Comp Functional Genomics 3:226–243CrossRefGoogle Scholar
  18. Hegde P, Qi R, Abernathy K, Gay C, Dharap S, Gaspard R, Hughes JE, Snesrud E, Lee N, Quackenbush J (2000) A concise guide to cDNA microarray analysis. Biotechniques 29:548–550PubMedGoogle Scholar
  19. Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, Awazuhara M, Arita M, Fujiwara T, Saito K (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:10205–10210PubMedCrossRefGoogle Scholar
  20. Jaakola L, Pirttila AM, Halonen M, Hohtola A (2001) Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Mol Biotechnol 19:210–203CrossRefGoogle Scholar
  21. Jifon J, Wolfe D (2002) Photosynthetic acclimation to elevated CO2 in Phaseolus vulgaris L. is altered by growth response to nitrogen supply. Global Change Biol 8:1018–1027CrossRefGoogle Scholar
  22. Jobson JD (1992) Applied multivariate data analysis. Volume II: Categorical and Multivariate Methods. Springer Verlag, New York, pp 483–568Google Scholar
  23. Kauder F, Ludewig F, Heineke D (2000) Ontogenetic changes of potato plants during acclimation to elevated carbon dioxide. J Exp Bot 51:429–437PubMedCrossRefGoogle Scholar
  24. Kirst M, Basten CJ, Myburg AA, Zeng Z-B, Sederoff RR (2005) Genetic architecture of transcript level variation in Eucalyptus differentiating xylem. Genetics 169:2295–2303PubMedCrossRefGoogle Scholar
  25. Kliebenstein DJ, Kroymann J, Brown P, Figuth A, Pedersen D, Gershenzon J, Mitchell-Olds T (2001) Genetic Control of Natural Variation in Arabidopsis Glucosinolate Accumulation. Plant Physiol 126:811–825PubMedCrossRefGoogle Scholar
  26. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246PubMedCrossRefGoogle Scholar
  27. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102:11118–11123PubMedCrossRefGoogle Scholar
  28. Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172PubMedCrossRefGoogle Scholar
  29. Kruckeberg AL, Neuhaus HE, Feil R, Gottlieb LD, Stitt M (1989) Decreased-activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. Impact on mass-action ratios and fluxes to sucrose and starch, and estimation of Flux Control Coefficients and Elasticity Coefficients. Biochem J 261:457–467PubMedGoogle Scholar
  30. Levey S, Wingler A (2005) Natural variation in the regulation of leaf senescence and relation to other traits in Arabidopsis. Plant Cell Environ 28:223–231CrossRefGoogle Scholar
  31. Li P, Mane SP, Sioson A, Robinet C, Heath L, Bohnert HJ, Grene R (2006) Effects of chronic ozone exposure on gene expression in Arabidopsis thaliana ecotypes and in Thellungiella halophila. Plant, Cell Environ 29:854–868CrossRefGoogle Scholar
  32. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annu Rev Plant Biol 55:591–628PubMedCrossRefGoogle Scholar
  33. Ludewig F, Sonnewald U, Kauder F, Heineke D, Geiger M, Stitt M, Müller-Röber BT, Gillissen B, Kühn C, Frommer WB (1998) The role of transient starch in acclimation to elevated atmospheric CO2. FEBS Lett 429:147–151PubMedCrossRefGoogle Scholar
  34. Majeau N, Coleman JR (1996) Effect of CO2, concentration on carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase/oxygenase in pea. Plant Physiol 112:569–574PubMedGoogle Scholar
  35. Miglietta F, Hoosbeek MR, Foot J, Gigon F, Hassinen A, Heijmans M, Peressotti A, Saarinen T, van Breemen N, Wallen B (2001) Spatial and temporal performance of the MiniFACE (Free Air CO2 Enrichment) system on bog ecosystems in northern and central Europe. Environ Monitoring Assessment 66:107–127CrossRefGoogle Scholar
  36. Mitchell-Olds T (1995) The molecular basis of quantitative genetic variations in natural populations. Trends Ecol Evol 10:324–328CrossRefGoogle Scholar
  37. Mitchell-Olds T (2001) Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol Evol 16:693–700CrossRefGoogle Scholar
  38. Miyazaki S, Fredricksen M, Hollis KC, Poroyko V, Shepley D, Galbraith DW, Long S, Bohnert HJ (2004) Transcript expression profiles of Arabidopsis thaliana grown under controlled conditions and open-air elevated concentrations of CO2 and of O3. Field Crops Res 90:47–59CrossRefGoogle Scholar
  39. Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H, Liu Y-X, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336PubMedCrossRefGoogle Scholar
  40. Moore BD, Cheng S-H, Sims D, Seemann JR (1999) The biochemical and molecular mechanisms for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582CrossRefGoogle Scholar
  41. Nelson DE, Rammesmayer G, Bohnert HJ (1998) The regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. Plant Cell 10:753–764PubMedCrossRefGoogle Scholar
  42. Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87– 89PubMedCrossRefGoogle Scholar
  43. Pattanagul W, Madore MA (1999) Water Deficit Effects on Raffinose Family Oligosaccharide Metabolism in Coleus. Plant Physiol 121:987–993PubMedCrossRefGoogle Scholar
  44. Pego JV, Kortstee AJ, Huijser C, Smeekens CM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51:407–416PubMedCrossRefGoogle Scholar
  45. Porra RJ, Grimme LH (1974) A new procedure for the determination of chlorophylls a and b and its application to normal and regreening Chlorella. Anal Biochem 57:255– 267PubMedCrossRefGoogle Scholar
  46. Pritchard S, Amthor J (2005) Crops and environmental change: an introduction to effects of global warming, rising Co2 and O3 concentrations, and soil salinization on crop physiology and yield. Haworth Press, Binghamton, NYGoogle Scholar
  47. Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L (2000) Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J 23:131–142PubMedCrossRefGoogle Scholar
  48. Roessner U, Willmitzer L, Fernie AR (2001) High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiol 127:749–764Google Scholar
  49. Rolland F, Sheen J (2005) Sugar sensing and signaling networks in plants. Biochem Soc Trans 33:269–271PubMedCrossRefGoogle Scholar
  50. Root TL, Price JT, K Hall R, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60PubMedCrossRefGoogle Scholar
  51. Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161:341–370CrossRefGoogle Scholar
  52. Sanda S, John M, Amasino R (1997) Analysis of flowering time in ecotypes of Arabidopsis thaliana. J Hered 88:69–72PubMedGoogle Scholar
  53. Sharkey TD, Laporte M, Lu Y, Weise S, Weber APM (2004) Engineering plants for elevated CO2: A relationship between starch degradation and sugar sensing. Plant Biol 6:280–289PubMedCrossRefGoogle Scholar
  54. Sharma S (1996) Applied multivariate techniques. John Wiley & Sons, New York, pp 90–143Google Scholar
  55. Sioson A, Watkinson JI, Vasquez-Robinet C, Ellis M, Shukla M, Kumar D, Ramakrishnan N, Heath LS, Grene R, Chevone BI, Kadafar K, Watson LT (2003) Expresso and Chips: Creating a Next Generation Microarray Experiment Management System, In 17th International Parallel and Distributed Processing Symposium (IPDPS’03), Nice, France, p 209Google Scholar
  56. Smith AM, Zeeman SC, Smith SM (2005) Starch Degradation. Annu Rev Plant Biol 56:73–98PubMedCrossRefGoogle Scholar
  57. Solberg HE (1978) Discriminant Analysis. CRC Crit Rev Clin Lab Sci 9:209–242PubMedCrossRefGoogle Scholar
  58. Taji T, Ohsumi C, Luchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426PubMedCrossRefGoogle Scholar
  59. Tan PK, Downey TJ, Spitznagel EL, Xu P, Fu D, Dimitrov DS, Lempicki RA, Raaka BM, Cam MC (2003) Evaluation of gene expression measurements from commercial microarray platforms. Nucleic Acids Res 31:5676–5684PubMedCrossRefGoogle Scholar
  60. Taylor G, Street NR, Tricker PJ, Sjodin A, Graham L, Skogstrom O, Calfapietra C, Scaracia-Mugnozza G, Janssen S (2005) The transcriptome of Populus in elevated CO2. New Phytologist 167:143–154PubMedCrossRefGoogle Scholar
  61. Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible WR, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 138:1195–1204PubMedCrossRefGoogle Scholar
  62. Wagner C, Sefkow M, Kopka J (2003) Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochem 62:887–900CrossRefGoogle Scholar
  63. Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kumar D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson LT, van Zyl L, Egertsdotter U, Sederoff RR, Grene R (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 133:1702–1716PubMedCrossRefGoogle Scholar
  64. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules RS (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8:625–637PubMedCrossRefGoogle Scholar
  65. Xiong L, Lee BH, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15:1971–1984PubMedCrossRefGoogle Scholar
  66. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox. Plant Physiol 136:2621–2632PubMedCrossRefGoogle Scholar
  67. Ziska LH (2003) Evaluation of the growth response of six invasive species to past, present and future atmospheric carbon dioxide. J Exp Bot 54:395–404PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Pinghua Li
    • 1
    • 5
  • Allan Sioson
    • 2
    • 6
  • Shrinivasrao P. Mane
    • 3
  • Alexander Ulanov
    • 4
  • Gregory Grothaus
    • 2
  • Lenwood S. Heath
    • 2
  • T. M. Murali
    • 2
  • Hans J. Bohnert
    • 1
    • 4
  • Ruth Grene
    • 3
  1. 1.Department of Plant BiologyUniversity of IllinoisUrbanaUSA
  2. 2.Department of Computer ScienceVirginia TechBlacksburgUSA
  3. 3.Department of Plant Pathology, Physiology, and Weed ScienceVirginia TechBlacksburgUSA
  4. 4.Department of Crop SciencesUniversity of IllinoisUrbanaUSA
  5. 5.Department of Biological SciencesState University of New York at AlbanyAlbanyUSA
  6. 6.Ateneo de Naga UniversityNaga CityPhilippines

Personalised recommendations