Specificities of Metabolite Profiles in Alpine Plants



Given that plants cannot escape their environment, they have evolved many strategies to survive, grow, and reproduce, including the capability to synthesise over 200,000 specialized and highly variable metabolites (Yonekura-Sakakibara and Saito 2009). In the severe alpine environment plants experience particularly low and high temperature extremes, intense solar radiation under clear conditions, strong wind effects, and variable mean dates for snow melting depending on slope and exposure (Körner 2003). Demanding environmental conditions have long been shown to exert a profound influence on the soluble metabolite composition of plants, although plants from high elevation habitats have been poorly analysed (Harborne 1982; Alonso-Amelot 2008).


Metabolite Profile Alpine Plant Intense Solar Radiation Polygonum Viviparum Subterranean Organ 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



gluconate 6-phosphate


L-ascorbic acid

m asl

metres above sea level




perchloric acid


pentose phosphate pathway


reactive oxygen species


superoxide dismutase



We are grateful to Dr. Elisabeth Gout and to Dr. Peter Streb for critical reading of the manuscript, and to Anne-Marie Boisson for the preparation of cell extracts. We acknowledge Pr. Claude Roby and Jean-Luc Le Bail for NMR facilities.


  1. Alonso-Amelot ME (2008) High altitude plants, chemistry of acclimation and adaptation. In: Atta-ur-Rahman (ed) Studies in natural products chemistry, vol 34. Elsevier, Amsterdam, pp 883–981Google Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  3. Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. Bios Scientific Publishers, Oxford, pp 129–142Google Scholar
  4. Asada K (1996) Radical production and scavenging in the chloroplasts. In: Baker NR (ed) Advances in Photosynthesis: photosynthesis and the environment, vol 5. Kluwer Academic Publishers, Dordrecht, pp 123–150CrossRefGoogle Scholar
  5. Aubert S, Bligny R, Douce R (1996) NMR studies of metabolism in cell suspensions and tissue cultures. In: Shachar-Hill Y, Pfeffer P (eds) Nuclear magnetic resonance in plant biology. Am Soc Plant Physiol, Rockville, pp 109–144Google Scholar
  6. Aubert S, Hennion F, Bouchereau A, Gout E, Bligny R, Dorne AJ (1999) Subcellular compartmentation of proline in the leaves of the subantarctic Kerguelen cabbage Pringlea antiscorbutica R-Br. in vivo 13C-NMR study. Plant Cell Environ 22:255–259CrossRefGoogle Scholar
  7. Aubert S, Choler P, Pratt J, Douzet R, Gout E, Bligny R (2004) Methyl-β-D-glucopyranoside in higher plants: accumulation and intracellular localization in Geum montanum L. leaves and in model systems studied by 13C nuclear magnetic resonance. J Exp Bot 406:2179–2189CrossRefGoogle Scholar
  8. Aubert S, Juge C, Boisson A-M, Gout E, Bligny R (2007) Metabolic processes sustaining the reviviscence of lichen Xanthoria elegans (Link) in high mountain environments. Planta 226:1287–1297PubMedCrossRefGoogle Scholar
  9. Bacic A, Harris PJ, Stone BA (1988) Structure and function of plant cell walls. In: Preiss J (ed) Encyclopedia of plant physiology, vol 14. Springer, Berlin, pp 297–371Google Scholar
  10. Bewley JD (1979) Physiological aspects of desiccation tolerance. Ann Rev Plant Physiol 30:195–238CrossRefGoogle Scholar
  11. Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066PubMedCrossRefGoogle Scholar
  12. Bilger W, Rimke S, Schreiber U, Lange OL (1989) Inhibition of energy transfer to photosystem II in lichens by dehydration: different properties of reversibility with green and blue-green photobionts. J Plant Physiol 134:261–268Google Scholar
  13. Bligny R, Douce R (1980) A precise localization of cardiolipin in plant cells. Biochim Biophys Acta 617:254–263PubMedGoogle Scholar
  14. Bligny R, Douce R (2001) NMR and plant metabolism. Curr Opin Plant Biol 4:191–196PubMedCrossRefGoogle Scholar
  15. Bonnier G, Douin R (1911–1935) Flore complète illustrée en couleurs de la France, Suisse et Belgique. Paris, Neuchâtel, BruxellesGoogle Scholar
  16. Colquhoun I (2007) Use of NMR for metabolic profiling in plant systems. J Pestic Sci 32:200–212CrossRefGoogle Scholar
  17. Conklin PL (2001) Recent advances in the role and biogenesis of ascorbic acid in plants. Plant Cell Environ 24:383–476CrossRefGoogle Scholar
  18. Connolly JD, Hill RA (1991) Cardenolides. In: Charlwood BV, Harborne DV (eds) Methods in plant biochemistry. Academic, New York, pp 361–368Google Scholar
  19. Cunningham AB, Garnett S, Gorman J, Courtenay K, Boehme D (2009) Eco-Enterprises and Terminalia ferdinandiana: “Best Laid Plans” and Australian policy lessons. Econ Bot 63:16–28CrossRefGoogle Scholar
  20. Davey MW, Van Montagu M, Inzé D, San Martin M, Kanellis A, Smirnoff N, Benzie IJJ, Strain JJ, Favell D, Fletcher J (2000) Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability, and effects of processing. J Sci Food Agric 80:825–860CrossRefGoogle Scholar
  21. Detrich HW, Parker SK, Williams RC, Nogales E, Downing KH (2000) Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes in the alpha- and beta-tubulin of Antarctic fishes. J Biol Chem 275:37038–37047PubMedCrossRefGoogle Scholar
  22. Dudley S, Lechowicz MJ (1987) Losses of polyol through leaching in subarctic lichens. Plant Physiol 83:813–815PubMedCrossRefGoogle Scholar
  23. Dulermo T, Rascle C, Billon-Grand G, Gout E, Bligny R, Cotton P (2010) Novel insights into mannitol metabolism in the fungal plant pathogen Botrytis cinerea. Biochem J 427:323–332PubMedCrossRefGoogle Scholar
  24. Fall R, Benson AA (1996) Leaf methanol – the simplest natural product from plants. Trends Plant Sci 1:296–301Google Scholar
  25. Fan TW-M (1996) Metabolic profiling by one- and two-dimentional NMR analysis of complex mixtures. Progr NMR Spectrosc 28:161–169Google Scholar
  26. Farrar JF (1988) Physiological buffering. In: Galun M (ed) Handbook of lichenology II. CRC Press, Boca Raton, pp 101–105Google Scholar
  27. Farrar JF, Smith DC (1976) Ecological physiology of the lichen Hypogymnia physodes. III. The importance of the rewetting phase. New Phytol 77:115–125CrossRefGoogle Scholar
  28. Foyer CH (1993) Ascorbic acid. In: Alscher RG, Hess JL (eds) Antioxidants in higher plants. CRC Press, Boca Raton, pp 32–57Google Scholar
  29. Foyer CH, Halliwell B (1976) Presence of glutathione and glutatione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefGoogle Scholar
  30. Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717CrossRefGoogle Scholar
  31. Fraser PD, Pinto ME, Holloway DE, Bramley PM (2000) Application of high-performance liqid chromatography with photoperiod array detection to the metabolic profiling of plant isoprenoids. Plant J 24:551–558PubMedCrossRefGoogle Scholar
  32. Gaff DF (1997) Mechanisms of desiccation-tolerance in resurrection vascular plants. In: Basra AS, Basra RK (eds) Mechanisms of environmental stress resistance in plants. Harwood Academic Publishers, The Netherlands, pp 43–58Google Scholar
  33. Glaser BL, Brown DH (1955) Purification and properties of D-glucose 6-phosphate dehydrogenase. J Biol Chem 216:67–79PubMedGoogle Scholar
  34. Gout E, Bligny R, Pascal N, Douce R (1993) 13C nuclear magnetic resonance studies of malate and citrate synthesis and compartmentation in higher plant cells. J Biol Chem 268:3986–3992PubMedGoogle Scholar
  35. Gout E, Aubert S, Bligny R, Rébeillé F, Nonomura AR, Benson AA, Douce R (2000) Metabolism of methanol in plant cells. Carbon-13 nuclear magnetic resonance studies. Plant Physiol 123:287–296PubMedCrossRefGoogle Scholar
  36. Guenther A, Hewitt CN, Erickson D et al (1995) A global model of natural volatile organic compound emissions. J Geophys Res 100:8873–8892CrossRefGoogle Scholar
  37. Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Ann Rev Plant Physiol Plant Mol Biol 41:187–223CrossRefGoogle Scholar
  38. Harborne JB (1982) Introduction to ecological biochemistry, 2nd edn. Academic, London, 278 pGoogle Scholar
  39. Heber U, Bilger W, Bligny R, Lange OL (2000) Phototolerance of lichens, mosses and higher plants in an alpine environment: analysis of photoreactions. Planta 211:770–780PubMedCrossRefGoogle Scholar
  40. Heber U, Lange OL, Shuvalov VA (2005) Conservation and dissipation of light energy as complementary processes: homoiohydric and poikilohydric autotrophs. J Exp Bot 57:1211–1223CrossRefGoogle Scholar
  41. Helms GWF (2003) Taxonomy and symbiosis in associations of Physciaceae and Trebouxia. Dissertation zur Erlangung des Doktorgrades der Biologischen Fakultät der Georg-August Universität Göttingen 156 p 141 pGoogle Scholar
  42. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438PubMedCrossRefGoogle Scholar
  43. Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Physiol Plant Mol Biol 42:553–578CrossRefGoogle Scholar
  44. Ichimura K, Mukasa Y, Fujiwara T, Kohata K, Goto R, Suto K (1999) Possible roles of methyl glucoside and myo-inositol in the opening of cut rose flowers. Ann Bot 83:551–557CrossRefGoogle Scholar
  45. Jennings DB, Ehrenshaft M, Pharr DM, Williamson JD (1998) Roles of Mannitol and Mannitol dehydrogenase in active oxygen-mediated plant defense. Proc Natl Acad Sci USA 95:15129–15133PubMedCrossRefGoogle Scholar
  46. Joyard J, Block MA, Malherbe A, Maréchal E, Douce R (1993) Origin of the synthesis of galactolipids and sulfolipid head groups. In: Moore TS Jr (ed) Lipid metabolism in plants. CRC Press, Boca Raton, pp 231–258Google Scholar
  47. Kappen L (1988) Ecophysiological relationships in different climatic regions. In: Galun M (ed) Handbook of lichenology II. CRC Press, Boca Raton, pp 37–100Google Scholar
  48. Körner C (2003) Alpine plant life. Functional plant ecology of high mountain ecosystems. Springer, Berlin, HeidelbergGoogle Scholar
  49. Körner E, von Dahl CC, Bonaventure G, Baldwin IT (2009) Pectin methylesterase NaPME1 contributes to the emission of methanol during insect herbivory and to the helicitation of defence responses in Nicotiana attenuata. J Exp Bot 60:2631–2640PubMedCrossRefGoogle Scholar
  50. Kranner I, Grill D (1994) Rapid change of the glutathione status and the enzymes involved in the reduction of glutathione-disulfide during the initial stage of wetting of lichens. Crypt Bot 4:203–206Google Scholar
  51. Lange OL (1980) Moisture content and CO2 exchange of lichens. Oecologia 45:82–87CrossRefGoogle Scholar
  52. Lange OL, Bilger W, Rimke S, Schreiber U (1989) Chlorophyll fluorescence of lichens containing green and blue green algae during hydration by water vapour uptake and by addition of liquid water. Bot Acta 102:306–313Google Scholar
  53. Lange OL, Pfanz H, Kilian E, Meyer A (1990) Effect of low water potential on photosynthesis in intact lichens and there liberated algal components. Planta 182:467–472CrossRefGoogle Scholar
  54. Larson DW (1981) Differential wetting in some lichens and mosses: the role of morphology. Bryologist 84:1–15CrossRefGoogle Scholar
  55. Last RL, Jones AD, Shachar-Hill Y (2007) Towards the plant metabolome and beyond. Mol Cell Biol 8:167–174Google Scholar
  56. Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–496PubMedCrossRefGoogle Scholar
  57. Longton RE (1988) The biology of polar bryophytes and lichens. Studies in polar research. Cambridge University Press, Cambridge, 391 pGoogle Scholar
  58. Lütz C (2010) Cell physiology of plants growing in cold environments. Protoplasma. doi: 10.1007/s00709-010-0161-5
  59. Manuel N, Cornic G, Aubert S, Choler P, Bligny R, Heber U (1999) Adaptation to high light and water stress in the alpine plant Geum montanum L. Oecologia 119:149–158CrossRefGoogle Scholar
  60. Mapson LW, Ischerwood FA, Chen YT (1954) Biological synthesis of L-ascorbic acid: the conversion of L-galactono-gamma-lactone into L-ascorbic acid by plant mitochondria. Biochem J 56:21–28PubMedGoogle Scholar
  61. Masakapalli SK, Le Lay P, Huddleston JE, Pollock NL, Kruger NJ, Ratcliffe RG (2010) Subcellular flux analysis of central metabolism in a heterotrophic Arabidopsis cell suspension using steady-state stable isotope labelling. Plant Physiol 152:602–619PubMedCrossRefGoogle Scholar
  62. McNeil PL, Steinhardt RA (1997) Loss, restoration, and maintenance of plasma membrane integrity. J Cell Biol 137:1–4PubMedCrossRefGoogle Scholar
  63. McNeil PL, Katsuya M, Vogel SS (2003) The endomembrane requirement for cell surface repair. Proc Natl Acad Sci USA 100:4592–4597PubMedCrossRefGoogle Scholar
  64. Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481PubMedCrossRefGoogle Scholar
  65. Nemecek-Marshall M, MacDonald RC, Franzen JJ, Wojciechowski CL, Fall R (1995) Methanol emission from leaves. Enzymatic detection of gas-phase methanol and relation of methanol fluxes to stomatal conductance and leaf development. Plant Physiol 108:1359–1368PubMedGoogle Scholar
  66. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  67. Oliver MJ, Dowd SE, Zaragoza J, Mauget SA, Payton PR (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: Transcript classification and analysis. BMC Genom 5(89):1–19Google Scholar
  68. Popp M, Smirnoff N (1995) Polyol accumulation and metabolism during water deficit. In: Smirnoff N (ed) Environment and plant metabolism: flexibility and acclimation. Bios Scientific Publishers, Oxford, pp 199–215Google Scholar
  69. Pugin A, Frachisse J-M, Tavernier E, Bligny R, Gout E, Douce R, Guern J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9:2077–2091PubMedCrossRefGoogle Scholar
  70. Rascio N, La Rocca N (2005) Resurrection plants: the puzzle of surviving extreme vegetative desiccation. Crit Rev Plant Sci 24:209–225CrossRefGoogle Scholar
  71. Ratcliffe RG (1994) In vivo nuclear magnetic resonance studies of higher plants and algae. Adv Bot Res 20:43–123CrossRefGoogle Scholar
  72. Ratcliffe RG, Shachar-Hill Y (2001) Probing plant metabolism with NMR. Annu Rev Plant Physiol Plant Mol Biol 52:499–526PubMedCrossRefGoogle Scholar
  73. Roberts JKM (2000) NMR adventures in the metabolic labyrinth within plants. Trends Plant Sci 5:30–34PubMedCrossRefGoogle Scholar
  74. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11–29PubMedCrossRefGoogle Scholar
  75. Rundel PW (1988) Water relations. In: Galun M (ed) Handbook of lichenology II. CRC Press, Boca Raton, pp 17–36Google Scholar
  76. Schroeter B, Jacobsen P, Kappen L (1991) Thallus moisture and microclimatic control of CO2 exchange of Peltigera aphthosa (L) Willd on Disco Island (West Greenland). Symbiosis 11:131–146Google Scholar
  77. Sharkey TD (1996) Emission of low molecular mass hydrocarbons from plants. Trends Plant Sci 1:78–82CrossRefGoogle Scholar
  78. Smith DC, Molesworth S (1973) Lichen Physiology. XIII. Effects of rewetting dry lichens. New Phytol 72:525–533CrossRefGoogle Scholar
  79. Smith AE, Phillips DV (1981) Identification of methyl β-D-glucopyranoside in white clover foliage. J Agric Food Chem 29:850–852CrossRefGoogle Scholar
  80. Spitaler R, Schlorhaufer PD, Ellmerer EP, Merfort I, Bortenschlager S, Stuppner H, Zidorn C (2006) Altitudinal variation of secondary metabolite profiles in flowering heads of Arnica Montana cv. ARBO. Phytochemistry 67:409–417PubMedCrossRefGoogle Scholar
  81. Streb P, Feierabend J (1999) Significance of antioxidants and electron sinks for the cold-hardening-induced resistance of winter rye leaves to photo-oxidative stress. Plant Cell Environ 22:1225–1237CrossRefGoogle Scholar
  82. Streb P, Feierabend J, Bligny R (1997) Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants. Plant Cell Environ 20:1030–1040CrossRefGoogle Scholar
  83. Streb P, Shang W, Feierabend J, Bligny R (1998) Divergent strategies of photoprotection in high-mountain plants. Planta 207:313–324CrossRefGoogle Scholar
  84. Streb P, Aubert S, Gout E, Bligny R (2003) Reversibility of cold- and light-stress tolerance and accompanying changes of metabolite and antioxidant levels in the two high mountain plant species Soldanella alpina and Ranunculus glacialis. J Exp Bot 54:405–418PubMedCrossRefGoogle Scholar
  85. Sumner LW, Mendes P, Dixon R (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62:817–836PubMedCrossRefGoogle Scholar
  86. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182PubMedCrossRefGoogle Scholar
  87. van der Rest B, Boisson A-M, Gout E, Bligny R, Douce R (2002) Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiol 130:244–255PubMedCrossRefGoogle Scholar
  88. Vicente C, Legaz ME (1988) Lichen enzymology. In: Galun M (ed) Handbook of lichenology I. CRC Press, Boca Raton, pp 239–284Google Scholar
  89. von Dahl CC, Hävecker M, Schlögl R, Baldwin IT (2006) Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? Plant J 46:948–960CrossRefGoogle Scholar
  90. Wang Y, He W, Huang H, An L, Wang D, Zhang F (2009) Antioxidative responses to different altitudes in leaves of alpine plant Polygonum viviparum in summer. Acta Physiol Plant 31:839–848CrossRefGoogle Scholar
  91. Weissman L, Garty J, Hochman A (2005) Characterization of enzymatic antioxidant in the lichen Ramalina lacera and their response to rehydration. Appl Environ Microbiol 71:6508–6514PubMedCrossRefGoogle Scholar
  92. Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369PubMedCrossRefGoogle Scholar
  93. Wildi B, Lütz C (1996) Antioxidant composition of selected high alpine plant species from different altitudes. Plant Cell Environ 19:138–146CrossRefGoogle Scholar
  94. Yonekura-Sakakibara K, Saito K (2009) Functional genomics for plant natural product biosynthesis. Nat Prod Rep 26:1466–1487PubMedCrossRefGoogle Scholar
  95. Zidorn C (2009) Altitudinal variation of secondary metabolites in flowering heads of Asteraceae: trends and causes. Phytochem Rev 9:197–203, 7 pCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratoire de Physiologie Cellulaire & Végétale, Unité Mixte de RechercheInstitut de Recherche en Technologies et Sciences pour le VivantGrenoble cedex 9France
  2. 2.Station Alpine Joseph Fourier, Unité Mixte de ServiceUniversité Joseph FourierGrenoble cedex 9France

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