Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
Identifieur interne : 000211 ( Main/Exploration ); précédent : 000210; suivant : 000212Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
Auteurs : Pedro A. B. Reis ; Paola A. Carpinetti ; Paula P. J. Freitas ; Eulálio G. D. Santos ; Luiz F. Camargos ; Igor H. T. Oliveira ; José Cleydson F. Silva ; Humberto H. Carvalho ; Maximiller Dal-Bianco ; Juliana R. L. Soares-Ramos ; Elizabeth P. B. FontesSource :
- BMC Plant Biology [ 1471-2229 ] ; 2016.
Abstract
The developmental and cell death domain (DCD)-containing asparagine-rich proteins (NRPs) were first identified in soybean (
Here, we demonstrated that the DCD/NRP-mediated signaling also propagates a stress-induced cell death signal in other plant species with features of a programmed cell death (PCD) response.
Our results indicated that the NRP-mediated cell death signaling operates in the plant kingdom with conserved regulatory mechanisms and hence may be target for engineering stress tolerance and adaptation in crops.
The online version of this article (doi:10.1186/s12870-016-0843-z) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12870-016-0843-z
PubMed: 27405371
PubMed Central: 4943007
Affiliations:
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Camargos</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Oliveira, Igor H T" sort="Oliveira, Igor H T" uniqKey="Oliveira I" first="Igor H. T." last="Oliveira">Igor H. T. Oliveira</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Silva, Jose Cleydson F" sort="Silva, Jose Cleydson F" uniqKey="Silva J" first="José Cleydson F." last="Silva">José Cleydson F. Silva</name><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Carvalho, Humberto H" sort="Carvalho, Humberto H" uniqKey="Carvalho H" first="Humberto H." last="Carvalho">Humberto H. Carvalho</name><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Dal Bianco, Maximiller" sort="Dal Bianco, Maximiller" uniqKey="Dal Bianco M" first="Maximiller" last="Dal-Bianco">Maximiller Dal-Bianco</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Soares Ramos, Juliana R L" sort="Soares Ramos, Juliana R L" uniqKey="Soares Ramos J" first="Juliana R. L." last="Soares-Ramos">Juliana R. L. Soares-Ramos</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Fontes, Elizabeth P B" sort="Fontes, Elizabeth P B" uniqKey="Fontes E" first="Elizabeth P. B." last="Fontes">Elizabeth P. B. Fontes</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27405371</idno><idno type="pmc">4943007</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4943007</idno><idno type="RBID">PMC:4943007</idno><idno type="doi">10.1186/s12870-016-0843-z</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000645</idno><idno type="wicri:Area/Pmc/Curation">000644</idno><idno type="wicri:Area/Pmc/Checkpoint">000173</idno><idno type="wicri:Area/Ncbi/Merge">002109</idno><idno type="wicri:Area/Ncbi/Curation">002109</idno><idno type="wicri:Area/Ncbi/Checkpoint">002109</idno><idno type="wicri:Area/Main/Merge">000211</idno><idno type="wicri:Area/Main/Curation">000211</idno><idno type="wicri:Area/Main/Exploration">000211</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants</title><author><name sortKey="Reis, Pedro A B" sort="Reis, Pedro A B" uniqKey="Reis P" first="Pedro A. B." last="Reis">Pedro A. B. Reis</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Carpinetti, Paola A" sort="Carpinetti, Paola A" uniqKey="Carpinetti P" first="Paola A." last="Carpinetti">Paola A. Carpinetti</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Freitas, Paula P J" sort="Freitas, Paula P J" uniqKey="Freitas P" first="Paula P. J." last="Freitas">Paula P. J. Freitas</name><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Santos, Eulalio G D" sort="Santos, Eulalio G D" uniqKey="Santos E" first="Eulálio G. D." last="Santos">Eulálio G. D. Santos</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Camargos, Luiz F" sort="Camargos, Luiz F" uniqKey="Camargos L" first="Luiz F." last="Camargos">Luiz F. Camargos</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Oliveira, Igor H T" sort="Oliveira, Igor H T" uniqKey="Oliveira I" first="Igor H. T." last="Oliveira">Igor H. T. Oliveira</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Silva, Jose Cleydson F" sort="Silva, Jose Cleydson F" uniqKey="Silva J" first="José Cleydson F." last="Silva">José Cleydson F. Silva</name><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Carvalho, Humberto H" sort="Carvalho, Humberto H" uniqKey="Carvalho H" first="Humberto H." last="Carvalho">Humberto H. Carvalho</name><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Dal Bianco, Maximiller" sort="Dal Bianco, Maximiller" uniqKey="Dal Bianco M" first="Maximiller" last="Dal-Bianco">Maximiller Dal-Bianco</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Soares Ramos, Juliana R L" sort="Soares Ramos, Juliana R L" uniqKey="Soares Ramos J" first="Juliana R. L." last="Soares-Ramos">Juliana R. L. Soares-Ramos</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author><author><name sortKey="Fontes, Elizabeth P B" sort="Fontes, Elizabeth P B" uniqKey="Fontes E" first="Elizabeth P. B." last="Fontes">Elizabeth P. B. Fontes</name><affiliation><nlm:aff id="Aff1">Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</nlm:aff><wicri:noCountry code="subfield">MG Brazil</wicri:noCountry></affiliation></author></analytic><series><title level="j">BMC Plant Biology</title><idno type="eISSN">1471-2229</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>The developmental and cell death domain (DCD)-containing asparagine-rich proteins (NRPs) were first identified in soybean (<italic>Glycine max</italic>) as transducers of a cell death signal derived from prolonged endoplasmic reticulum (ER) stress, osmotic stress, drought or developmentally-programmed leaf senescence via the GmNAC81/GmNAC30/GmVPE signaling module. In spite of the relevance of the DCD/NRP-mediated signaling as a versatile adaptive response to multiple stresses, mechanistic knowledge of the pathway is lacking and the extent to which this pathway may operate in the plant kingdom has not been investigated.</p></sec><sec><title>Results</title><p>Here, we demonstrated that the DCD/NRP-mediated signaling also propagates a stress-induced cell death signal in other plant species with features of a programmed cell death (PCD) response. <italic>In silico</italic> analysis revealed that several plant genomes harbor conserved sequences of the pathway components, which share functional analogy with their soybean counterparts. We showed that GmNRPs, <italic>GmNAC81</italic>and <italic>VPE</italic> orthologs from Arabidopsis, designated as <italic>AtNRP</italic>-<italic>1</italic>, <italic>AtNRP</italic>-<italic>2</italic>, <italic>ANAC036</italic> and <italic>gVPE</italic>, respectively, induced cell death when transiently expressed <italic>in N. benthamiana</italic> leaves. In addition, loss of <italic>AtNRP1</italic> and <italic>AtNRP2</italic> function attenuated ER stress-induced cell death in Arabidopsis, which was in marked contrast with the enhanced cell death phenotype displayed by overexpressing lines as compared to Col-0. Furthermore, atnrp-1 knockout mutants displayed enhanced sensitivity to PEG-induced osmotic stress, a phenotype that could be complemented with ectopic expression of either <italic>GmNRP</italic>-<italic>A</italic> or <italic>GmNRP</italic>-<italic>B</italic>. In addition, AtNRPs, <italic>ANAC036</italic> and <italic>gVPE</italic> were induced by osmotic and ER stress to an extent that was modulated by the ER-resident molecular chaperone binding protein (BiP) similarly as in soybean. Finally, as putative downstream components of the NRP-mediated cell death signaling, the stress induction of <italic>AtNRP2</italic>, <italic>ANAC036</italic> and <italic>gVPE</italic> was dependent on the <italic>AtNRP1</italic> function. BiP overexpression also conferred tolerance to water stress in Arabidopsis, most likely due to modulation of the drought-induced NRP-mediated cell death response.</p></sec><sec><title>Conclusion</title><p>Our results indicated that the NRP-mediated cell death signaling operates in the plant kingdom with conserved regulatory mechanisms and hence may be target for engineering stress tolerance and adaptation in crops.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/s12870-016-0843-z) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Golldack, D" uniqKey="Golldack D">D Golldack</name></author><author><name sortKey="Li, C" uniqKey="Li C">C Li</name></author><author><name sortKey="Mohan, H" uniqKey="Mohan H">H Mohan</name></author><author><name sortKey="Probst, N" uniqKey="Probst N">N 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Prange</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list></list><tree><noCountry><name sortKey="Camargos, Luiz F" sort="Camargos, Luiz F" uniqKey="Camargos L" first="Luiz F." last="Camargos">Luiz F. Camargos</name><name sortKey="Carpinetti, Paola A" sort="Carpinetti, Paola A" uniqKey="Carpinetti P" first="Paola A." last="Carpinetti">Paola A. Carpinetti</name><name sortKey="Carvalho, Humberto H" sort="Carvalho, Humberto H" uniqKey="Carvalho H" first="Humberto H." last="Carvalho">Humberto H. Carvalho</name><name sortKey="Dal Bianco, Maximiller" sort="Dal Bianco, Maximiller" uniqKey="Dal Bianco M" first="Maximiller" last="Dal-Bianco">Maximiller Dal-Bianco</name><name sortKey="Fontes, Elizabeth P B" sort="Fontes, Elizabeth P B" uniqKey="Fontes E" first="Elizabeth P. B." last="Fontes">Elizabeth P. B. Fontes</name><name sortKey="Freitas, Paula P J" sort="Freitas, Paula P J" uniqKey="Freitas P" first="Paula P. J." last="Freitas">Paula P. J. Freitas</name><name sortKey="Oliveira, Igor H T" sort="Oliveira, Igor H T" uniqKey="Oliveira I" first="Igor H. T." last="Oliveira">Igor H. T. Oliveira</name><name sortKey="Reis, Pedro A B" sort="Reis, Pedro A B" uniqKey="Reis P" first="Pedro A. B." last="Reis">Pedro A. B. Reis</name><name sortKey="Santos, Eulalio G D" sort="Santos, Eulalio G D" uniqKey="Santos E" first="Eulálio G. D." last="Santos">Eulálio G. D. Santos</name><name sortKey="Silva, Jose Cleydson F" sort="Silva, Jose Cleydson F" uniqKey="Silva J" first="José Cleydson F." last="Silva">José Cleydson F. Silva</name><name sortKey="Soares Ramos, Juliana R L" sort="Soares Ramos, Juliana R L" uniqKey="Soares Ramos J" first="Juliana R. L." last="Soares-Ramos">Juliana R. L. Soares-Ramos</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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