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Plant Cell Advance Online Publication
Published on March 9, 2007; 10.1105/tpc.106.045427

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Received June 28, 2006
Returned for revision December 20, 2006
Accepted February 14, 2007

Integration of Chloroplast Nucleic Acid Metabolism into the Phosphate Deprivation Response in Chlamydomonas reinhardtii

Shlomit Yehudai-Resheff 1, Sara L. Zimmer 2, Yutaka Komine 1, and David B. Stern 1*

1 Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853
2 Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853; Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853

* To whom correspondence should be addressed. E-mail: ds28{at}cornell.edu.

Cell survival depends on the cell's ability to acclimate to phosphorus (P) limitation. We studied the chloroplast ribonuclease polynucleotide phosphorylase (PNPase), which consumes and generates phosphate, by comparing wild-type Chlamydomonas reinhardtii cells with strains with reduced PNPase expression. In the wild type, chloroplast RNA (cpRNA) accumulates under P limitation, correlating with reduced PNPase expression. PNPase-deficient strains do not exhibit cpRNA variation under these conditions, suggesting that in the wild type PNPase limits cpRNA accumulation under P stress. PNPase levels appear to be mediated by the P response regulator PHOSPHORUS STARVATION RESPONSE1 (PSR1), because in psr1 mutant cells, cpRNA declines under P limitation and PNPase expression is not reduced. PNPase-deficient cells begin to lose viability after 24 h of P depletion, suggesting that PNPase is important for cellular acclimation. PNPase-deficient strains do not have enhanced sensitivity to other physiological or nutrient stresses, and their RNA and cell growth phenotypes are not observed under P stress with phosphite, a phosphate analog that blocks the stress signal. In contrast with RNA metabolism, chloroplast DNA (cpDNA) levels declined under P deprivation, suggesting that P mobilization occurs from DNA rather than RNA. This unusual phenomenon, which is phosphite- and PSR1-insensitive, may have evolved as a result of the polyploid nature of cpDNA and the requirement of P for cpRNA degradation by PNPase.




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