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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Differential Response of Gray Poplar Leaves and Roots Underpins Stress Adaptation during Hypoxia^1,[W]

Albert-Ludwigs-Universität Freiburg, Institut für Forstbotanik und Baumphysiologie, D–79110 Freiburg, Germany (J.K., J.H., H.R.); Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, M316 Crawley, Western Australia 6009, Australia (J.K., K.A.H., A.C., A.H.M., J.W.); and Max-Planck-Institut für Molekulare Pflanzenphysiologie, 4476 Potsdam-Golm, Germany (K.A.H.)

The molecular and physiological responses of gray poplar (Populus x canescens) following root hypoxia were studied in roots and leaves using transcript and metabolite profiling. The results indicate that there were changes in metabolite levels in both organs, but changes in transcript abundance were restricted to the roots. In roots, starch and sucrose degradation were altered under hypoxia, and concurrently, the availability of carbohydrates was enhanced, concomitant with depletion of sucrose from leaves and elevation of sucrose in the phloem. Consistent with the above, glycolytic flux and ethanolic fermentation were stimulated in roots but not in leaves. Various messenger RNAs encoding components of biosynthetic pathways such as secondary cell wall formation (i.e. cellulose and lignin biosynthesis) and other energy-demanding processes such as transport of nutrients were significantly down-regulated in roots but not in leaves. The reduction of biosynthesis was unexpected, as shoot growth was not affected by root hypoxia, suggesting that the up-regulation of glycolysis yields sufficient energy to maintain growth. Besides carbon metabolism, nitrogen metabolism was severely affected in roots, as seen from numerous changes in the transcriptome and the metabolome related to nitrogen uptake, nitrogen assimilation, and amino acid metabolism. The coordinated physiological and molecular responses in leaves and roots, coupled with the transport of metabolites, reveal important stress adaptations to ensure survival during long periods of root hypoxia.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jürgen Kreuzwieser (juergen.kreuzwieser{at}ctp.uni-freiburg.de).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.125989

^* Corresponding author; e-mail juergen.kreuzwieser{at}ctp.uni-freiburg.de.

Received July 8, 2008; accepted November 5, 2008; published November 12, 2008.