Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses.
The Chlamydomonas reinhardtii PSR1 gene is required for proper acclimation of the cells to phosphorus (P) deficiency. P-starved psr1 mutants show signs of secondary sulfur (S) starvation, exemplified by the synthesis of extracellular arylsulfatase and the accumulation of transcripts encoding proteins involved in S scavenging and assimilation. Epistasis analysis reveals that induction of the S-starvation responses in P-limited psr1 cells requires the regulatory protein kinase SNRK2.1, but bypasses the membrane-targeted activator, SAC1. The inhibitory kinase SNRK2.2 is necessary for repression of S-starvation responses during both nutrient-replete growth and P limitation; arylsulfatase activity and S deficiency-responsive genes are partially induced in the P-deficient snrk2.2 mutants and become fully activated in the P-deficient psr1snrk2.2 double mutant. During P starvation, the sac1snrk2.2 double mutants or the psr1sac1snrk2.2 triple mutants exhibit reduced arylsulfatase activity compared to snrk2.2 or psr1snrk2.2, respectively, but the sac1 mutation has little effect on the abundance of S deficiency-responsive transcripts in these strains, suggesting a post-transcriptional role for SAC1 in elicitation of S-starvation responses. Interestingly, P-starved psr1snrk2.2 cells bleach and die more rapidly than wild-type or psr1 strains, suggesting that activation of S-starvation responses during P deprivation is deleterious to the cell. From these results we infer that (i) P-deficient growth causes some internal S limitation, but the S-deficiency responses are normally inhibited during acclimation to P deprivation; (ii) the S-deficiency responses are not completely suppressed in P-deficient psr1 cells and consequently these cells synthesize some arylsulfatase and exhibit elevated levels of transcripts for S-deprivation genes; and (iii) this increased expression is controlled by regulators that modulate transcription of S-responsive genes during S-deprivation conditions. Overall, the work strongly suggests integration of the different circuits that control nutrient-deprivation responses in Chlamydomonas.
Moseley
Jeffrey L
JL
Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, USA. Jeffrey.Moseley@stanford.edu
Gonzalez-Ballester
David
D
Pootakham
Wirulda
W
Bailey
Shaun
S
Grossman
Arthur R
AR
D000818:Animals; D001192:Arylsulfatases / Q000378:metabolism; D002696:Chlamydomonas / Q000166:cytology / Q000235:genetics* / Q000378:metabolism / Q000502:physiology*; D004268:DNA-Binding Proteins / Q000378:metabolism; D004843:Epistasis, Genetic; D017125:Genes, Protozoan / Q000235:genetics*; D009154:Mutation; D009687:Nuclear Proteins / Q000378:metabolism; D010758:Phosphorus / Q000172:deficiency*; D010940:Plant Proteins / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction; D013431:Sulfates / Q000378:metabolism; D013455:Sulfur / Q000172:deficiency*
D004268:DNA-Binding Proteins; D009687:Nuclear Proteins; D010940:Plant Proteins; C403075:Psr1 protein, Chlamydomonas; D012333:RNA, Messenger; D013431:Sulfates; D010758:Phosphorus; D013455:Sulfur; D001192:Arylsulfatases