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miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis

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Resumo:The SnRK1 protein kinase, the plant ortholog of mammalian AMPK and yeast Snf1, is activated by the energy depletion caused by adverse environmental conditions. Upon activation, SnRK1 triggers extensive transcriptional changes to restore homeostasis and promote stress tolerance and survival partly through the inhibition of anabolism and the activation of catabolism. Despite the identification of a few bZIP transcription factors as downstream effectors, the mechanisms underlying gene regulation, and in particular gene repression by SnRK1, remain mostly unknown. microRNAs (miRNAs) are 20-24 nt RNAs that regulate gene expression post-transcriptionally by driving the cleavage and/or translation attenuation of complementary mRNA targets. In addition to their role in plant development, mounting evidence implicates miRNAs in the response to environmental stress. Given the involvement of miRNAs in stress responses and the fact that some of the SnRK1-regulated genes are miRNA targets, we postulated that miRNAs drive part of the transcriptional reprogramming triggered by SnRK1. By comparing the transcriptional response to energy deprivation between WT and dcl1-9, a mutant deficient in miRNA biogenesis, we identified 831 starvation genes misregulated in the dcl1-9 mutant, out of which 155 are validated or predicted miRNA targets. Functional clustering analysis revealed that the main cellular processes potentially co-regulated by SnRK1 and miRNAs are translation and organelle function and uncover TCP transcription factors as one of the most highly enriched functional clusters. TCP repression during energy deprivation was impaired in miR319 knockdown (MIM319) plants, demonstrating the involvement of miR319 in the stress-dependent regulation of TCPs. Altogether, our data indicates that miRNAs are components of the SnRK1 signaling cascade contributing to the regulation of specific mRNA targets and possibly tuning down particular cellular processes during the stress response.
Autores principais:Confraria, Ana
Outros Autores:Martinho, Cláudia; Elias, Alexandre; Rubio-Somoza, Ignacio; Baena-González, Elena
Assunto:Arabidopsis SnRK1 stress miRNA energy signaling DCL1
Ano:2013
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso aberto
Instituição associada:Repositório do GIMM – Gulbenkian Institute for Molecular Medicine
Idioma:inglês
Origem:ARCA
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author Confraria, Ana
author2 Martinho, Cláudia
Elias, Alexandre
Rubio-Somoza, Ignacio
Baena-González, Elena
author2_role author
author
author
author
author_facet Confraria, Ana
Martinho, Cláudia
Elias, Alexandre
Rubio-Somoza, Ignacio
Baena-González, Elena
author_role author
contributor_name_str_mv ARCA
country_str PT
creators_json_txt [{\"Person.name\":\"Confraria, Ana\"},{\"Person.name\":\"Martinho, Cláudia\"},{\"Person.name\":\"Elias, Alexandre\"},{\"Person.name\":\"Rubio-Somoza, Ignacio\"},{\"Person.name\":\"Baena-González, Elena\"}]
datacite.contributors.contributor.contributorName.fl_str_mv ARCA
datacite.creators.creator.creatorName.fl_str_mv Confraria, Ana
Martinho, Cláudia
Elias, Alexandre
Rubio-Somoza, Ignacio
Baena-González, Elena
datacite.date.Accepted.fl_str_mv 2013-06-20T00:00:00Z
datacite.date.available.fl_str_mv 2015-10-26T13:02:06Z
datacite.date.embargoed.fl_str_mv 2015-10-26T13:02:06Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_abf2
datacite.subjects.subject.fl_str_mv Arabidopsis
SnRK1
stress
miRNA
energy signaling
DCL1
datacite.titles.title.fl_str_mv miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
dc.contributor.none.fl_str_mv ARCA
dc.creator.none.fl_str_mv Confraria, Ana
Martinho, Cláudia
Elias, Alexandre
Rubio-Somoza, Ignacio
Baena-González, Elena
dc.date.Accepted.fl_str_mv 2013-06-20T00:00:00Z
dc.date.available.fl_str_mv 2015-10-26T13:02:06Z
dc.date.embargoed.fl_str_mv 2015-10-26T13:02:06Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10400.7/442
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Frontiers Research Foundation
dc.rights.cclincense.fl_str_mv http://creativecommons.org/licenses/by/4.0/
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.subject.none.fl_str_mv Arabidopsis
SnRK1
stress
miRNA
energy signaling
DCL1
dc.title.fl_str_mv miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description The SnRK1 protein kinase, the plant ortholog of mammalian AMPK and yeast Snf1, is activated by the energy depletion caused by adverse environmental conditions. Upon activation, SnRK1 triggers extensive transcriptional changes to restore homeostasis and promote stress tolerance and survival partly through the inhibition of anabolism and the activation of catabolism. Despite the identification of a few bZIP transcription factors as downstream effectors, the mechanisms underlying gene regulation, and in particular gene repression by SnRK1, remain mostly unknown. microRNAs (miRNAs) are 20-24 nt RNAs that regulate gene expression post-transcriptionally by driving the cleavage and/or translation attenuation of complementary mRNA targets. In addition to their role in plant development, mounting evidence implicates miRNAs in the response to environmental stress. Given the involvement of miRNAs in stress responses and the fact that some of the SnRK1-regulated genes are miRNA targets, we postulated that miRNAs drive part of the transcriptional reprogramming triggered by SnRK1. By comparing the transcriptional response to energy deprivation between WT and dcl1-9, a mutant deficient in miRNA biogenesis, we identified 831 starvation genes misregulated in the dcl1-9 mutant, out of which 155 are validated or predicted miRNA targets. Functional clustering analysis revealed that the main cellular processes potentially co-regulated by SnRK1 and miRNAs are translation and organelle function and uncover TCP transcription factors as one of the most highly enriched functional clusters. TCP repression during energy deprivation was impaired in miR319 knockdown (MIM319) plants, demonstrating the involvement of miR319 in the stress-dependent regulation of TCPs. Altogether, our data indicates that miRNAs are components of the SnRK1 signaling cascade contributing to the regulation of specific mRNA targets and possibly tuning down particular cellular processes during the stress response.
dirty 0
eu_rights_str_mv openAccess
format article
fulltext.url.fl_str_mv https://arca.gimm.pt/bitstreams/16f3bc86-835d-4cec-9cd2-1eddabc749a8/download
id arca_6cdc23db19fd2aa4d136dbaa41699bfc
identifier.url.fl_str_mv http://hdl.handle.net/10400.7/442
instacron_str arca
institution Repositório do GIMM – Gulbenkian Institute for Molecular Medicine
instname_str Repositório do GIMM – Gulbenkian Institute for Molecular Medicine
language eng
network_acronym_str arca
network_name_str ARCA
oai_identifier_str oai:arca.gimm.pt:10400.7/442
organization_str_mv urn:organizationAcronym:arca
person_str_mv Confraria, Ana
Martinho, Cláudia
Elias, Alexandre
Rubio-Somoza, Ignacio
Baena-González, Elena
publishDate 2013
publisher.none.fl_str_mv Frontiers Research Foundation
reponame_str ARCA
repository_id_str urn:repositoryAcronym:arca
service_str_mv urn:repositoryAcronym:arca
spelling engFrontiers Research Foundationpt_PTThe SnRK1 protein kinase, the plant ortholog of mammalian AMPK and yeast Snf1, is activated by the energy depletion caused by adverse environmental conditions. Upon activation, SnRK1 triggers extensive transcriptional changes to restore homeostasis and promote stress tolerance and survival partly through the inhibition of anabolism and the activation of catabolism. Despite the identification of a few bZIP transcription factors as downstream effectors, the mechanisms underlying gene regulation, and in particular gene repression by SnRK1, remain mostly unknown. microRNAs (miRNAs) are 20-24 nt RNAs that regulate gene expression post-transcriptionally by driving the cleavage and/or translation attenuation of complementary mRNA targets. In addition to their role in plant development, mounting evidence implicates miRNAs in the response to environmental stress. Given the involvement of miRNAs in stress responses and the fact that some of the SnRK1-regulated genes are miRNA targets, we postulated that miRNAs drive part of the transcriptional reprogramming triggered by SnRK1. By comparing the transcriptional response to energy deprivation between WT and dcl1-9, a mutant deficient in miRNA biogenesis, we identified 831 starvation genes misregulated in the dcl1-9 mutant, out of which 155 are validated or predicted miRNA targets. Functional clustering analysis revealed that the main cellular processes potentially co-regulated by SnRK1 and miRNAs are translation and organelle function and uncover TCP transcription factors as one of the most highly enriched functional clusters. TCP repression during energy deprivation was impaired in miR319 knockdown (MIM319) plants, demonstrating the involvement of miR319 in the stress-dependent regulation of TCPs. Altogether, our data indicates that miRNAs are components of the SnRK1 signaling cascade contributing to the regulation of specific mRNA targets and possibly tuning down particular cellular processes during the stress response.application/pdfpt_PTmiRNAs mediate SnRK1-dependent energy signaling in ArabidopsisConfraria, AnaMartinho, CláudiaElias, AlexandreRubio-Somoza, IgnacioBaena-González, ElenaHostingInstitutionOrganizationalARCAe-mailmailto:arca.repository@gimm.ptarca.repository@gimm.ptDOIIsPartOf10.3389/fpls.2013.001972015-10-26T13:02:06Z2013-06-202013-06-20T00:00:00ZHandlehttp://hdl.handle.net/10400.7/442http://purl.org/coar/access_right/c_abf2open accessArabidopsisSnRK1stressmiRNAenergy signalingDCL15464948 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal article2013-06-20http://creativecommons.org/licenses/by/4.0/http://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://arca.gimm.pt/bitstreams/16f3bc86-835d-4cec-9cd2-1eddabc749a8/downloadFrontiers in Plant Science4121
spellingShingle miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
Confraria, Ana
Arabidopsis
SnRK1
stress
miRNA
energy signaling
DCL1
status SINGLETON
subject.fl_str_mv Arabidopsis
SnRK1
stress
miRNA
energy signaling
DCL1
title miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
title_full miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
title_fullStr miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
title_full_unstemmed miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
title_short miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
title_sort miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis
topic Arabidopsis
SnRK1
stress
miRNA
energy signaling
DCL1
topic_facet Arabidopsis
SnRK1
stress
miRNA
energy signaling
DCL1
url http://hdl.handle.net/10400.7/442
visible 1