Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants
Identifieur interne : 000644 ( Pmc/Curation ); précédent : 000643; suivant : 000645Functional 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
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Pedro A. B. Reis<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>
<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>
<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>
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<wicri:noCountry code="subfield">MG Brazil</wicri:noCountry>
</affiliation>
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<wicri:noCountry code="subfield">MG Brazil</wicri:noCountry>
</affiliation>
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<wicri:noCountry code="subfield">MG Brazil</wicri:noCountry>
</affiliation>
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<wicri:noCountry code="subfield">MG Brazil</wicri:noCountry>
</affiliation>
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<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>
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<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>
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<wicri:noCountry code="subfield">MG Brazil</wicri:noCountry>
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<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>
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<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>
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<wicri:noCountry code="subfield">MG Brazil</wicri:noCountry>
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<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>
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<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>
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<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>
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<biblStruct><analytic><author><name sortKey="Moreno, Aa" uniqKey="Moreno A">AA Moreno</name>
</author>
<author><name sortKey="Mukhtar, Ms" uniqKey="Mukhtar M">MS Mukhtar</name>
</author>
<author><name sortKey="Blanco, F" uniqKey="Blanco F">F Blanco</name>
</author>
<author><name sortKey="Boatwright, Jl" uniqKey="Boatwright J">JL Boatwright</name>
</author>
<author><name sortKey="Moreno, I" uniqKey="Moreno I">I Moreno</name>
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</biblStruct>
<biblStruct><analytic><author><name sortKey="Lichtenthaler, Hk" uniqKey="Lichtenthaler H">HK Lichtenthaler</name>
</author>
</analytic>
</biblStruct>
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</author>
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</author>
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<author><name sortKey="Prange, Rk" uniqKey="Prange R">RK Prange</name>
</author>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Plant Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Plant Biol</journal-id>
<journal-title-group><journal-title>BMC Plant Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">1471-2229</issn>
<publisher><publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27405371</article-id>
<article-id pub-id-type="pmc">4943007</article-id>
<article-id pub-id-type="publisher-id">843</article-id>
<article-id pub-id-type="doi">10.1186/s12870-016-0843-z</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Reis</surname>
<given-names>Pedro A. B.</given-names>
</name>
<address><email>pedrobqi@yahoo.com.br</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Carpinetti</surname>
<given-names>Paola A.</given-names>
</name>
<address><email>paolacarpinetti@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Freitas</surname>
<given-names>Paula P.J.</given-names>
</name>
<address><email>ppjfreitas@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Santos</surname>
<given-names>Eulálio G.D.</given-names>
</name>
<address><email>eulaliobqi@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Camargos</surname>
<given-names>Luiz F.</given-names>
</name>
<address><email>luizfcamargos@yahoo.com.br</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Oliveira</surname>
<given-names>Igor H.T.</given-names>
</name>
<address><email>igorhiroshi@hotmail.com</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Silva</surname>
<given-names>José Cleydson F.</given-names>
</name>
<address><email>cleysinhonv@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Carvalho</surname>
<given-names>Humberto H.</given-names>
</name>
<address><email>humberto_henriquec@hotmail.com</email>
</address>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dal-Bianco</surname>
<given-names>Maximiller</given-names>
</name>
<address><email>maximiller@ufv.br</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Soares-Ramos</surname>
<given-names>Juliana R.L.</given-names>
</name>
<address><email>juliramos@ufv.br</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Fontes</surname>
<given-names>Elizabeth P. B.</given-names>
</name>
<address><email>bbfontes@ufv.br</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<aff id="Aff1"><label></label>
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG Brazil</aff>
<aff id="Aff2"><label></label>
National Institute of Science and Technology in Plant-Pest Interactions, Bioagro, Universidade Federal de Viçosa, Viçosa, MG Brazil</aff>
</contrib-group>
<pub-date pub-type="epub"><day>12</day>
<month>7</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>12</day>
<month>7</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>16</volume>
<elocation-id>156</elocation-id>
<history><date date-type="received"><day>19</day>
<month>1</month>
<year>2016</year>
</date>
<date date-type="accepted"><day>1</day>
<month>7</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s). 2016</copyright-statement>
<license license-type="OpenAccess"><license-p><bold>Open Access</bold>
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), 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 (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1"><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>
</abstract>
<kwd-group xml:lang="en"><title>Keywords</title>
<kwd>Programmed cell death</kwd>
<kwd>Abiotic stresses</kwd>
<kwd>ER stress</kwd>
<kwd>N-rich proteins</kwd>
<kwd>NAC transcription factors</kwd>
<kwd>Vacuolar processing enzyme</kwd>
<kwd>VPE</kwd>
<kwd>NRPs</kwd>
<kwd>BiP</kwd>
<kwd>Binding protein</kwd>
</kwd-group>
<funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100003593</institution-id>
<institution>Conselho Nacional de Desenvolvimento Científico e Tecnológico</institution>
</institution-wrap>
</funding-source>
<award-id>573600/2008-2 and 447578/2014-6</award-id>
<principal-award-recipient><name><surname>Fontes</surname>
<given-names>Elizabeth P. B.</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100004901</institution-id>
<institution>Fundação de Amparo à Pesquisa do Estado de Minas Gerais</institution>
</institution-wrap>
</funding-source>
<award-id>CBB-APQ-03175-13 and CBB-APQ-01491-14</award-id>
<principal-award-recipient><name><surname>Fontes</surname>
<given-names>Elizabeth P. B.</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2016</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>
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