Integration of chloroplast nucleic acid metabolism into the phosphate deprivation response in Chlamydomonas reinhardtii.
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.
Yehudai-Resheff
Shlomit
S
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York 14853, USA.
Zimmer
Sara L
SL
Komine
Yutaka
Y
Stern
David B
DB
D000818:Animals; D002470:Cell Survival / Q000187:drug effects; D016825:Chlamydomonas reinhardtii / Q000187:drug effects / Q000201:enzymology / Q000378:metabolism*; D002736:Chloroplasts / Q000187:drug effects / Q000201:enzymology / Q000378:metabolism*; D018742:DNA, Chloroplast / Q000378:metabolism*; D004268:DNA-Binding Proteins / Q000096:biosynthesis; D004794:Enzyme Repression / Q000187:drug effects; D005095:Exoribonucleases / Q000378:metabolism; D018628:Gene Dosage; D018745:Genome, Plant / Q000235:genetics; D008954:Models, Biological; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D009687:Nuclear Proteins / Q000096:biosynthesis; D010710:Phosphates / Q000172:deficiency*; D017905:Phosphites / Q000378:metabolism; D010940:Plant Proteins / Q000096:biosynthesis; D011117:Polyribonucleotide Nucleotidyltransferase / Q000172:deficiency; D020871:RNA Stability / Q000187:drug effects; D018747:RNA, Chloroplast / Q000378:metabolism*; D012293:Rifampin / Q000494:pharmacology; D017386:Sequence Homology, Amino Acid
D018742:DNA, Chloroplast; D004268:DNA-Binding Proteins; D009687:Nuclear Proteins; D010710:Phosphates; D017905:Phosphites; D010940:Plant Proteins; C403075:Psr1 protein, Chlamydomonas; D018747:RNA, Chloroplast; D011117:Polyribonucleotide Nucleotidyltransferase; D005095:Exoribonucleases; C022535:exoribonuclease II; D012293:Rifampin