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Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants

BACKGROUND: The developmental and cell death domain (DCD)-containing asparagine-rich proteins (NRPs) were first identified in soybean (Glycine max) as transducers of a cell death signal derived from prolonged endoplasmic reticulum (ER) stress, osmotic stress, drought or developmentally-programmed le...

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Autores principales: Reis, Pedro A. B., Carpinetti, Paola A., Freitas, Paula P.J., Santos, Eulálio G.D., Camargos, Luiz F., Oliveira, Igor H.T., Silva, José Cleydson F., Carvalho, Humberto H., Dal-Bianco, Maximiller, Soares-Ramos, Juliana R.L., Fontes, Elizabeth P. B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4943007/
https://www.ncbi.nlm.nih.gov/pubmed/27405371
http://dx.doi.org/10.1186/s12870-016-0843-z
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author Reis, Pedro A. B.
Carpinetti, Paola A.
Freitas, Paula P.J.
Santos, Eulálio G.D.
Camargos, Luiz F.
Oliveira, Igor H.T.
Silva, José Cleydson F.
Carvalho, Humberto H.
Dal-Bianco, Maximiller
Soares-Ramos, Juliana R.L.
Fontes, Elizabeth P. B.
author_facet Reis, Pedro A. B.
Carpinetti, Paola A.
Freitas, Paula P.J.
Santos, Eulálio G.D.
Camargos, Luiz F.
Oliveira, Igor H.T.
Silva, José Cleydson F.
Carvalho, Humberto H.
Dal-Bianco, Maximiller
Soares-Ramos, Juliana R.L.
Fontes, Elizabeth P. B.
author_sort Reis, Pedro A. B.
collection PubMed
description BACKGROUND: The developmental and cell death domain (DCD)-containing asparagine-rich proteins (NRPs) were first identified in soybean (Glycine max) 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. RESULTS: 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. In silico 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, GmNAC81and VPE orthologs from Arabidopsis, designated as AtNRP-1, AtNRP-2, ANAC036 and gVPE, respectively, induced cell death when transiently expressed in N. benthamiana leaves. In addition, loss of AtNRP1 and AtNRP2 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 GmNRP-A or GmNRP-B. In addition, AtNRPs, ANAC036 and gVPE 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 AtNRP2, ANAC036 and gVPE was dependent on the AtNRP1 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. CONCLUSION: 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0843-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-49430072016-07-14 Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants Reis, Pedro A. B. Carpinetti, Paola A. Freitas, Paula P.J. Santos, Eulálio G.D. Camargos, Luiz F. Oliveira, Igor H.T. Silva, José Cleydson F. Carvalho, Humberto H. Dal-Bianco, Maximiller Soares-Ramos, Juliana R.L. Fontes, Elizabeth P. B. BMC Plant Biol Research Article BACKGROUND: The developmental and cell death domain (DCD)-containing asparagine-rich proteins (NRPs) were first identified in soybean (Glycine max) 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. RESULTS: 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. In silico 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, GmNAC81and VPE orthologs from Arabidopsis, designated as AtNRP-1, AtNRP-2, ANAC036 and gVPE, respectively, induced cell death when transiently expressed in N. benthamiana leaves. In addition, loss of AtNRP1 and AtNRP2 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 GmNRP-A or GmNRP-B. In addition, AtNRPs, ANAC036 and gVPE 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 AtNRP2, ANAC036 and gVPE was dependent on the AtNRP1 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. CONCLUSION: 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0843-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-07-12 /pmc/articles/PMC4943007/ /pubmed/27405371 http://dx.doi.org/10.1186/s12870-016-0843-z Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Reis, Pedro A. B.
Carpinetti, Paola A.
Freitas, Paula P.J.
Santos, Eulálio G.D.
Camargos, Luiz F.
Oliveira, Igor H.T.
Silva, José Cleydson F.
Carvalho, Humberto H.
Dal-Bianco, Maximiller
Soares-Ramos, Juliana R.L.
Fontes, Elizabeth P. B.
Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
title Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
title_full Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
title_fullStr Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
title_full_unstemmed Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
title_short Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
title_sort functional and regulatory conservation of the soybean er stress-induced dcd/nrp-mediated cell death signaling in plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4943007/
https://www.ncbi.nlm.nih.gov/pubmed/27405371
http://dx.doi.org/10.1186/s12870-016-0843-z
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