A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana

Handle URI:
http://hdl.handle.net/10754/325268
Title:
A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana
Authors:
Meier, Stuart; Tzfadia, Oren; Vallabhaneni, Ratnakar; Gehring, Christoph A. ( 0000-0003-4355-4591 ) ; Wurtzel, Eleanore T
Abstract:
Background: The carotenoids are pure isoprenoids that are essential components of the photosynthetic apparatus and are coordinately synthesized with chlorophylls in chloroplasts. However, little is known about the mechanisms that regulate carotenoid biosynthesis or the mechanisms that coordinate this synthesis with that of chlorophylls and other plastidial synthesized isoprenoid-derived compounds, including quinones, gibberellic acid and abscisic acid. Here, a comprehensive transcriptional analysis of individual carotenoid and isoprenoid-related biosynthesis pathway genes was performed in order to elucidate the role of transcriptional regulation in the coordinated synthesis of these compounds and to identify regulatory components that may mediate this process in Arabidopsis thaliana.Results: A global microarray expression correlation analysis revealed that the phytoene synthase gene, which encodes the first dedicated and rate-limiting enzyme of carotenogenesis, is highly co-expressed with many photosynthesis-related genes including many isoprenoid-related biosynthesis pathway genes. Chemical and mutant analysis revealed that induction of the co-expressed genes following germination was dependent on gibberellic acid and brassinosteroids (BR) but was inhibited by abscisic acid (ABA). Mutant analyses further revealed that expression of many of the genes is suppressed in dark grown plants by Phytochrome Interacting transcription Factors (PIFs) and activated by photoactivated phytochromes, which in turn degrade PIFs and mediate a coordinated induction of the genes. The promoters of PSY and the co-expressed genes were found to contain an enrichment in putative BR-auxin response elements and G-boxes, which bind PIFs, further supporting a role for BRs and PIFs in regulating expression of the genes. In osmotically stressed root tissue, transcription of Calvin cycle, methylerythritol 4-phosphate pathway and carotenoid biosynthesis genes is induced and uncoupled from that of chlorophyll biosynthesis genes in a manner that is consistent with the increased synthesis of carotenoid precursors for ABA biosynthesis. In all tissues examined, induction of ?-carotene hydroxylase transcript levels are linked to an increased demand for ABA.Conclusions: This analysis provides compelling evidence to suggest that coordinated transcriptional regulation of isoprenoid-related biosynthesis pathway genes plays a major role in coordinating the synthesis of functionally related chloroplast localized isoprenoid-derived compounds. 2011 Meier et al; licensee BioMed Central Ltd.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Meier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Systems Biology 5: 77. doi:10.1186/1752-0509-5-77.
Publisher:
Springer Nature
Journal:
BMC Systems Biology
Issue Date:
19-May-2011
DOI:
10.1186/1752-0509-5-77
PubMed ID:
21595952
PubMed Central ID:
PMC3123201
Type:
Article
ISSN:
17520509
Appears in Collections:
Articles; Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorMeier, Stuarten
dc.contributor.authorTzfadia, Orenen
dc.contributor.authorVallabhaneni, Ratnakaren
dc.contributor.authorGehring, Christoph A.en
dc.contributor.authorWurtzel, Eleanore Ten
dc.date.accessioned2014-08-27T09:43:46Z-
dc.date.available2014-08-27T09:43:46Z-
dc.date.issued2011-05-19en
dc.identifier.citationMeier S, Tzfadia O, Vallabhaneni R, Gehring C, Wurtzel ET (2011) A transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thaliana. BMC Systems Biology 5: 77. doi:10.1186/1752-0509-5-77.en
dc.identifier.issn17520509en
dc.identifier.pmid21595952en
dc.identifier.doi10.1186/1752-0509-5-77en
dc.identifier.urihttp://hdl.handle.net/10754/325268en
dc.description.abstractBackground: The carotenoids are pure isoprenoids that are essential components of the photosynthetic apparatus and are coordinately synthesized with chlorophylls in chloroplasts. However, little is known about the mechanisms that regulate carotenoid biosynthesis or the mechanisms that coordinate this synthesis with that of chlorophylls and other plastidial synthesized isoprenoid-derived compounds, including quinones, gibberellic acid and abscisic acid. Here, a comprehensive transcriptional analysis of individual carotenoid and isoprenoid-related biosynthesis pathway genes was performed in order to elucidate the role of transcriptional regulation in the coordinated synthesis of these compounds and to identify regulatory components that may mediate this process in Arabidopsis thaliana.Results: A global microarray expression correlation analysis revealed that the phytoene synthase gene, which encodes the first dedicated and rate-limiting enzyme of carotenogenesis, is highly co-expressed with many photosynthesis-related genes including many isoprenoid-related biosynthesis pathway genes. Chemical and mutant analysis revealed that induction of the co-expressed genes following germination was dependent on gibberellic acid and brassinosteroids (BR) but was inhibited by abscisic acid (ABA). Mutant analyses further revealed that expression of many of the genes is suppressed in dark grown plants by Phytochrome Interacting transcription Factors (PIFs) and activated by photoactivated phytochromes, which in turn degrade PIFs and mediate a coordinated induction of the genes. The promoters of PSY and the co-expressed genes were found to contain an enrichment in putative BR-auxin response elements and G-boxes, which bind PIFs, further supporting a role for BRs and PIFs in regulating expression of the genes. In osmotically stressed root tissue, transcription of Calvin cycle, methylerythritol 4-phosphate pathway and carotenoid biosynthesis genes is induced and uncoupled from that of chlorophyll biosynthesis genes in a manner that is consistent with the increased synthesis of carotenoid precursors for ABA biosynthesis. In all tissues examined, induction of ?-carotene hydroxylase transcript levels are linked to an increased demand for ABA.Conclusions: This analysis provides compelling evidence to suggest that coordinated transcriptional regulation of isoprenoid-related biosynthesis pathway genes plays a major role in coordinating the synthesis of functionally related chloroplast localized isoprenoid-derived compounds. 2011 Meier et al; licensee BioMed Central Ltd.en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.rightsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.en
dc.rights.urihttp://creativecommons.org/licenses/by/2.0en
dc.subjectArabidopsisen
dc.subjectArabidopsis thalianaen
dc.subjectabscisic aciden
dc.subjectbeta caroteneen
dc.subjectcarotenoiden
dc.subjectchlorophyllen
dc.subjectterpeneen
dc.subjectArabidopsisen
dc.subjectbiological modelen
dc.subjectbiologyen
dc.subjectchemistryen
dc.subjectchloroplasten
dc.subjectDNA microarrayen
dc.subjectgene expression regulationen
dc.subjectgenetic transcriptionen
dc.subjectgeneticsen
dc.subjectmetabolismen
dc.subjectmethodologyen
dc.subjectmutationen
dc.subjectosmosisen
dc.subjectplastiden
dc.subjectpromoter regionen
dc.subjectsystems biologyen
dc.subjectAbscisic Aciden
dc.subjectArabidopsisen
dc.subjectbeta Caroteneen
dc.subjectCarotenoidsen
dc.subjectChlorophyllen
dc.subjectChloroplastsen
dc.subjectComputational Biologyen
dc.subjectGene Expression Regulation, Planten
dc.subjectModels, Biologicalen
dc.subjectMutationen
dc.subjectOligonucleotide Array Sequence Analysisen
dc.subjectOsmosisen
dc.subjectPlastidsen
dc.subjectPromoter Regions, Geneticen
dc.subjectSystems Biologyen
dc.subjectTerpenesen
dc.subjectTranscription, Geneticen
dc.titleA transcriptional analysis of carotenoid, chlorophyll and plastidial isoprenoid biosynthesis genes during development and osmotic stress responses in Arabidopsis thalianaen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalBMC Systems Biologyen
dc.identifier.pmcidPMC3123201en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionDepartment of Biological Sciences, Lehman College, The City University of New York, 250 Bedford Park Blvd. West, Bronx, NY 10468, United Statesen
dc.contributor.institutionThe Graduate School and University Center-CUNY, 365 Fifth Ave., New York, NY 10016-4309, United Statesen
dc.contributor.institutionDepartment of Biotechnology, University of the Western Cape, Private Bag X17, Cape Town - Bellville 7535, South Africaen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorMeier, Stuart Kurten
kaust.authorGehring, Christoph A.en
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