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dc.contributor.authorChen, Hao
dc.contributor.authorZhang, Baichen
dc.contributor.authorHicks, Leslie M.
dc.contributor.authorXiong, Liming
dc.date.accessioned2014-08-27T09:45:35Z
dc.date.available2014-08-27T09:45:35Z
dc.date.issued2011-10-19
dc.identifier.citationChen H, Zhang B, Hicks LM, Xiong L (2011) A Nucleotide Metabolite Controls Stress-Responsive Gene Expression and Plant Development. PLoS ONE 6: e26661. doi:10.1371/journal.pone.0026661.
dc.identifier.issn19326203
dc.identifier.pmid22028934
dc.identifier.doi10.1371/journal.pone.0026661
dc.identifier.urihttp://hdl.handle.net/10754/325296
dc.description.abstractAbiotic stress, such as drought and high salinity, activates a network of signaling cascades that lead to the expression of many stress-responsive genes in plants. The Arabidopsis FIERY1 (FRY1) protein is a negative regulator of stress and abscisic acid (ABA) signaling and exhibits both an inositol polyphosphatase and a 3?,5?-bisphosphate nucleotidase activity in vitro. The FRY1 nucleotidase degrades the sulfation byproduct 3?-phosphoadenosine-5?-phosphate (PAP), yet its in vivo functions and particularly its roles in stress gene regulation remain unclear. Here we developed a LC-MS/MS method to quantitatively measure PAP levels in plants and investigated the roles of this nucleotidase activity in stress response and plant development. It was found that PAP level was tightly controlled in plants and did not accumulate to any significant level either under normal conditions or under NaCl, LiCl, cold, or ABA treatments. In contrast, high levels of PAP were detected in multiple mutant alleles of FRY1 but not in mutants of other FRY1 family members, indicating that FRY1 is the major enzyme that hydrolyzes PAP in vivo. By genetically reducing PAP levels in fry1 mutants either through overexpression of a yeast PAP nucleotidase or by generating a triple mutant of fry1 apk1 apk2 that is defective in the biosynthesis of the PAP precursor 3?-phosphoadenosine-5?-phosphosulfate (PAPS), we demonstrated that the developmental defects and superinduction of stress-responsive genes in fry1 mutants correlate with PAP accumulation in planta. We also found that the hypersensitive stress gene regulation in fry1 requires ABH1 but not ABI1, two other negative regulators in ABA signaling pathways. Unlike in yeast, however, FRY1 overexpression in Arabidopsis could not enhance salt tolerance. Taken together, our results demonstrate that PAP is critical for stress gene regulation and plant development, yet the FRY1 nucleotidase that catabolizes PAP may not be an in vivo salt toxicity target in Arabidopsis. © 2011 Chen et al.
dc.language.isoen
dc.publisherPublic Library of Science (PLoS)
dc.rightsChen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
dc.rightsArchived with thanks to PLoS ONE
dc.subjectabscisic acid
dc.subjectadenosine 3' phosphate 5' phosphosulfate
dc.subjectadenosine 3',5' diphosphate
dc.subjectadenosine derivative
dc.subjectadenylylsulfate kinase
dc.subjectadenylylsulfate kinase APK1
dc.subjectadenylylsulfate kinase APK2
dc.subjectArabidopsis protein
dc.subjectnucleotidase
dc.subjectprotein FRY1
dc.subjectunclassified drug
dc.subjectABH1 protein, Arabidopsis
dc.subjectabscisic acid
dc.subjectadenosine 3' phosphate 5' phosphate
dc.subjectadenosine 3'-phosphate-5'-phosphate
dc.subjectadenosine diphosphate
dc.subjectadenylylsulfate kinase
dc.subjectArabidopsis protein
dc.subjectcap binding protein
dc.subjectlithium chloride
dc.subjectnucleotidase
dc.subjectphosphotransferase
dc.subjectRD29a protein, Arabidopsis
dc.subjectSAL1 protein, Arabidopsis
dc.subjectsodium chloride
dc.subjectArabidopsis
dc.subjectarticle
dc.subjectbioaccumulation
dc.subjectcold stress
dc.subjectcontrolled study
dc.subjectenzyme activity
dc.subjectfry1 gene
dc.subjectgene expression regulation
dc.subjectgene function
dc.subjectgene induction
dc.subjectgene mutation
dc.subjectgene overexpression
dc.subjecthydrolysis
dc.subjectin vitro study
dc.subjectin vivo study
dc.subjectliquid chromatography
dc.subjectmutant
dc.subjectnonhuman
dc.subjectphysical tolerance
dc.subjectplant development
dc.subjectplant gene
dc.subjectplant stress
dc.subjectprotein localization
dc.subjectprotein structure
dc.subjectregulator gene
dc.subjectreporter gene
dc.subjectsalt stress
dc.subjectsequence homology
dc.subjectsignal transduction
dc.subjecttandem mass spectrometry
dc.subjectwild plant
dc.subjectArabidopsis
dc.subjectdrug effect
dc.subjectgenetics
dc.subjectgrowth, development and aging
dc.subjectintracellular space
dc.subjectmetabolism
dc.subjectmutation
dc.subjectphysiological stress
dc.subjectphysiology
dc.subjectprotein transport
dc.subjectsalt tolerance
dc.subjectseedling
dc.subjecttemperature
dc.subjectArabidopsis
dc.subjectAbscisic Acid
dc.subjectAdenosine Diphosphate
dc.subjectArabidopsis
dc.subjectArabidopsis Proteins
dc.subjectGene Expression Regulation, Plant
dc.subjectGenes, Reporter
dc.subjectIntracellular Space
dc.subjectLithium Chloride
dc.subjectMutation
dc.subjectNucleotidases
dc.subjectPhosphotransferases (Alcohol Group Acceptor)
dc.subjectProtein Transport
dc.subjectRNA Cap-Binding Proteins
dc.subjectSalt-Tolerance
dc.subjectSeedling
dc.subjectSequence Homology, Nucleic Acid
dc.subjectSodium Chloride
dc.subjectStress, Physiological
dc.subjectTemperature
dc.titleA nucleotide metabolite controls stress-responsive gene expression and plant development
dc.typeArticle
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Division
dc.contributor.departmentPlant Science
dc.contributor.departmentPlant Stress Genomics Research Lab
dc.identifier.journalPLoS ONE
dc.identifier.pmcidPMC3197580
dc.eprint.versionPublisher's Version/PDF
dc.contributor.institutionDonald Danforth Plant Science Center, St Louis, Missouri, United States
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)
kaust.personXiong, Liming
kaust.personChen, Hao
refterms.dateFOA2018-06-13T14:50:34Z


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