A nucleotide metabolite controls stress-responsive gene expression and plant development

Handle URI:
http://hdl.handle.net/10754/325296
Title:
A nucleotide metabolite controls stress-responsive gene expression and plant development
Authors:
Chen, Hao; Zhang, Baichen; Hicks, Leslie M.; Xiong, Liming ( 0000-0001-8099-0806 )
Abstract:
Abiotic 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.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Chen 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.
Publisher:
Public Library of Science
Journal:
PLoS ONE
Issue Date:
19-Oct-2011
DOI:
10.1371/journal.pone.0026661
PubMed ID:
22028934
PubMed Central ID:
PMC3197580
Type:
Article
ISSN:
19326203
Appears in Collections:
Articles; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorChen, Haoen
dc.contributor.authorZhang, Baichenen
dc.contributor.authorHicks, Leslie M.en
dc.contributor.authorXiong, Limingen
dc.date.accessioned2014-08-27T09:45:35Z-
dc.date.available2014-08-27T09:45:35Z-
dc.date.issued2011-10-19en
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.en
dc.identifier.issn19326203en
dc.identifier.pmid22028934en
dc.identifier.doi10.1371/journal.pone.0026661en
dc.identifier.urihttp://hdl.handle.net/10754/325296en
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.en
dc.language.isoenen
dc.publisherPublic Library of Scienceen
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.en
dc.rightsArchived with thanks to PLoS ONEen
dc.subjectabscisic aciden
dc.subjectadenosine 3' phosphate 5' phosphosulfateen
dc.subjectadenosine 3',5' diphosphateen
dc.subjectadenosine derivativeen
dc.subjectadenylylsulfate kinaseen
dc.subjectadenylylsulfate kinase APK1en
dc.subjectadenylylsulfate kinase APK2en
dc.subjectArabidopsis proteinen
dc.subjectnucleotidaseen
dc.subjectprotein FRY1en
dc.subjectunclassified drugen
dc.subjectABH1 protein, Arabidopsisen
dc.subjectabscisic aciden
dc.subjectadenosine 3' phosphate 5' phosphateen
dc.subjectadenosine 3'-phosphate-5'-phosphateen
dc.subjectadenosine diphosphateen
dc.subjectadenylylsulfate kinaseen
dc.subjectArabidopsis proteinen
dc.subjectcap binding proteinen
dc.subjectlithium chlorideen
dc.subjectnucleotidaseen
dc.subjectphosphotransferaseen
dc.subjectRD29a protein, Arabidopsisen
dc.subjectSAL1 protein, Arabidopsisen
dc.subjectsodium chlorideen
dc.subjectArabidopsisen
dc.subjectarticleen
dc.subjectbioaccumulationen
dc.subjectcold stressen
dc.subjectcontrolled studyen
dc.subjectenzyme activityen
dc.subjectfry1 geneen
dc.subjectgene expression regulationen
dc.subjectgene functionen
dc.subjectgene inductionen
dc.subjectgene mutationen
dc.subjectgene overexpressionen
dc.subjecthydrolysisen
dc.subjectin vitro studyen
dc.subjectin vivo studyen
dc.subjectliquid chromatographyen
dc.subjectmutanten
dc.subjectnonhumanen
dc.subjectphysical toleranceen
dc.subjectplant developmenten
dc.subjectplant geneen
dc.subjectplant stressen
dc.subjectprotein localizationen
dc.subjectprotein structureen
dc.subjectregulator geneen
dc.subjectreporter geneen
dc.subjectsalt stressen
dc.subjectsequence homologyen
dc.subjectsignal transductionen
dc.subjecttandem mass spectrometryen
dc.subjectwild planten
dc.subjectArabidopsisen
dc.subjectdrug effecten
dc.subjectgeneticsen
dc.subjectgrowth, development and agingen
dc.subjectintracellular spaceen
dc.subjectmetabolismen
dc.subjectmutationen
dc.subjectphysiological stressen
dc.subjectphysiologyen
dc.subjectprotein transporten
dc.subjectsalt toleranceen
dc.subjectseedlingen
dc.subjecttemperatureen
dc.subjectArabidopsisen
dc.subjectAbscisic Aciden
dc.subjectAdenosine Diphosphateen
dc.subjectArabidopsisen
dc.subjectArabidopsis Proteinsen
dc.subjectGene Expression Regulation, Planten
dc.subjectGenes, Reporteren
dc.subjectIntracellular Spaceen
dc.subjectLithium Chlorideen
dc.subjectMutationen
dc.subjectNucleotidasesen
dc.subjectPhosphotransferases (Alcohol Group Acceptor)en
dc.subjectProtein Transporten
dc.subjectRNA Cap-Binding Proteinsen
dc.subjectSalt-Toleranceen
dc.subjectSeedlingen
dc.subjectSequence Homology, Nucleic Aciden
dc.subjectSodium Chlorideen
dc.subjectStress, Physiologicalen
dc.subjectTemperatureen
dc.titleA nucleotide metabolite controls stress-responsive gene expression and plant developmenten
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalPLoS ONEen
dc.identifier.pmcidPMC3197580en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionDonald Danforth Plant Science Center, St Louis, Missouri, United Statesen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorXiong, Limingen
kaust.authorChen, Haoen
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