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Metabolic processes sustaining the reviviscence of lichen Xanthoria elegans (Link) in high mountain environments

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Abstract

To survive in high mountain environments lichens must adapt themselves to alternating periods of desiccation and hydration. Respiration and photosynthesis of the foliaceous lichen, Xanthoria elegans, in the dehydrated state were below the threshold of CO2-detection by infrared gas analysis. Following hydration, respiration totally recovered within seconds and photosynthesis within minutes. In order to identify metabolic processes that may contribute to the quick and efficient reactivation of lichen physiological processes, we analysed the metabolite profile of lichen thalli step by step during hydration/dehydration cycles, using 31P- and 13C-NMR. It appeared that the recovery of respiration was prepared during dehydration by the accumulation of a reserve of gluconate 6-P (glcn-6-P) and by the preservation of nucleotide pools, whereas glycolytic and photosynthetic intermediates like glucose 6-P and ribulose 1,5-diphosphate were absent. The large pools of polyols present in both X. elegans photo- and mycobiont are likely to contribute to the protection of cell constituents like nucleotides, proteins, and membrane lipids, and to preserve the integrity of intracellular structures during desiccation. Our data indicate that glcn-6-P accumulated due to activation of the oxidative pentose phosphate pathway, in response to a need for reducing power (NADPH) during the dehydration-triggered down-regulation of cell metabolism. On the contrary, glcn-6-P was metabolised immediately after hydration, supplying respiration with substrates during the replenishment of pools of glycolytic and photosynthetic intermediates. Finally, the high net photosynthetic activity of wet X. elegans thalli at low temperature may help this alpine lichen to take advantage of brief hydration opportunities such as ice melting, thus favouring its growth in harsh high mountain climates.

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Abbreviations

CDTA:

1,2-Cyclohexylenedinitrilotetraacetic acid

Glcn-6-P:

Gluconate 6-P

GPG:

Glycerophosphoglycerol

GPC:

Glycerophosphocholine

PCA:

Perchloric acid

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Acknowledgments

The authors are indebted to Pr Ulrich Heber (Univ. Wuerzburg, Germany) for his kind encouragements and for his participation in fluorescence assays. We thank Peter Streb (Univ. Orsay-Paris XI, France), Fabrice Rébeillé and Philippe Choler for their critical reading of the manuscript, Matt Robson for style revision, and Juliette Asta for having introduced us to the world of lichens. We also thank the reviewers for helpful comments and we are also grateful to Odile and Roland Donzel (Café de la Ferme, Col du Lautaret) for their friendly help and Jean-luc Lebail for his dedicated technical assistance with the NMR spectrometer and perfusion system.

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Aubert, S., Juge, C., Boisson, AM. et al. Metabolic processes sustaining the reviviscence of lichen Xanthoria elegans (Link) in high mountain environments. Planta 226, 1287–1297 (2007). https://doi.org/10.1007/s00425-007-0563-6

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  • DOI: https://doi.org/10.1007/s00425-007-0563-6

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