Abnormal physiological and molecular mutant phenotypes link chloroplast polynucleotide phosphorylase to the phosphorus deprivation response in Arabidopsis.
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.
Marchive
Chloe
C
Boyce Thompson Institute for Plant Research, Ithaca, New York 14853, USA.
Yehudai-Resheff
Shlomit
S
Germain
Arnaud
A
Fei
Zhangjun
Z
Jiang
Xingshan
X
Judkins
Joshua
J
Wu
Hong
H
Fernie
Alisdair R
AR
Fait
Aaron
A
Stern
David B
DB
D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics / Q000502:physiology*; D002455:Cell Division / Q000187:drug effects; D002736:Chloroplasts / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics; D004269:DNA, Bacterial / Q000235:genetics; D015536:Down-Regulation / Q000187:drug effects / Q000235:genetics; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D017343:Genes, Plant; D016254:Mutagenesis, Insertional / Q000187:drug effects; D009154:Mutation / Q000235:genetics*; D010641:Phenotype; D010758:Phosphorus / Q000172:deficiency* / Q000378:metabolism / Q000494:pharmacology; D018515:Plant Leaves / Q000187:drug effects / Q000378:metabolism; D018517:Plant Roots / Q000166:cytology / Q000254:growth & development / Q000378:metabolism / Q000648:ultrastructure; D011117:Polyribonucleotide Nucleotidyltransferase / Q000378:metabolism*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015203:Reproducibility of Results; D015854:Up-Regulation / Q000187:drug effects / Q000235:genetics
D004269:DNA, Bacterial; D012333:RNA, Messenger; C036483:T-DNA; D010758:Phosphorus; D011117:Polyribonucleotide Nucleotidyltransferase