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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Abnormal Physiological and Molecular Mutant Phenotypes Link Chloroplast Polynucleotide Phosphorylase to the Phosphorus Deprivation Response in Arabidopsis^{1,[C],[W],[OA]}

Boyce Thompson Institute for Plant Research, Ithaca, New York 14853 (C.M., S.Y.-R., A.G., J.J., D.B.S.); United States Department of Agriculture Robert W. Holley Center for Agriculture and Health, Ithaca, New York 14853 (Z.F.); College of Life Sciences, South China Agricultural University, Guangzhou 510642, People's Republic of China (X.J., H.W.); and Max-Planck-Institut für Molekulare Pflanzenphysiologie, 14476 Potsdam-Golm, Germany (A.R.F., A.F.)

A prominent enzyme in organellar RNA metabolism is the exoribonuclease polynucleotide phosphorylase (PNPase), whose reversible activity is governed by the nucleotide diphosphate-inorganic phosphate ratio. In Chlamydomonas reinhardtii, PNPase regulates chloroplast transcript accumulation in response to phosphorus (P) starvation, and PNPase expression is repressed by the response regulator PSR1 (for PHOSPHORUS STARVATION RESPONSE1) under these conditions. Here, we investigated the role of PNPase in the Arabidopsis (Arabidopsis thaliana) P deprivation response by comparing wild-type and pnp mutant plants with respect to their morphology, metabolite profiles, and transcriptomes. We found that P-deprived pnp mutants develop aborted clusters of lateral roots, which are characterized by decreased auxin responsiveness and cell division, and exhibit cell death at the root tips. Electron microscopy revealed that the collapse of root organelles is enhanced in the pnp mutant under P deprivation and occurred with low frequency under P-replete conditions. Global analyses of metabolites and transcripts were carried out to understand the molecular bases of these altered P deprivation responses. We found that the pnp mutant expresses some elements of the deprivation response even when grown on a full nutrient medium, including altered transcript accumulation, although its total and inorganic P contents are not reduced. The pnp mutation also confers P status-independent responses, including but not limited to stress responses. Taken together, our data support the hypothesis that the activity of the chloroplast PNPase is involved in plant acclimation to P availability and that it may help maintain an appropriate balance of P metabolites even under normal growth conditions.

² Present address: Physics Department, Technion-Israel Institute of Technology, Haifa 32000, Israel.

³ Present address: Boyce Thompson Institute for Plant Research, Ithaca, NY 14853.

⁴ Present address: Department of Chemistry and Biochemistry, Ohio Northern University, Ada, OH 45810.

⁵ Present address: Ben-Gurion University of the Negev, Jacob Blaustein Institutes for Desert Research, French Associates Institute for Agriculture and Biotechnology of Drylands, Midreshet Ben-Gurion 84990, Israel.

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: David B. Stern (ds28{at}cornell.edu).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

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

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.145144

^* Corresponding author; e-mail ds28{at}cornell.edu.

Received July 21, 2009; accepted August 19, 2009; published August 26, 2009.