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<title xml:lang="en">Evidence for a SAL1-PAP Chloroplast Retrograde Pathway That Functions in Drought and High Light Signaling in
<italic>Arabidopsis</italic>
<xref ref-type="author-notes" rid="fn1">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[W]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[OA]</sup>
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<name sortKey="Estavillo, Gonzalo M" sort="Estavillo, Gonzalo M" uniqKey="Estavillo G" first="Gonzalo M." last="Estavillo">Gonzalo M. Estavillo</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Crisp, Peter A" sort="Crisp, Peter A" uniqKey="Crisp P" first="Peter A." last="Crisp">Peter A. Crisp</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pornsiriwong, Wannarat" sort="Pornsiriwong, Wannarat" uniqKey="Pornsiriwong W" first="Wannarat" last="Pornsiriwong">Wannarat Pornsiriwong</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wirtz, Markus" sort="Wirtz, Markus" uniqKey="Wirtz M" first="Markus" last="Wirtz">Markus Wirtz</name>
<affiliation>
<nlm:aff id="aff2">University of Heidelberg, Heidelberg Institute for Plant Sciences, 69120 Heidelberg, Germany</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Collinge, Derek" sort="Collinge, Derek" uniqKey="Collinge D" first="Derek" last="Collinge">Derek Collinge</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Carrie, Chris" sort="Carrie, Chris" uniqKey="Carrie C" first="Chris" last="Carrie">Chris Carrie</name>
<affiliation>
<nlm:aff id="aff3">ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Giraud, Estelle" sort="Giraud, Estelle" uniqKey="Giraud E" first="Estelle" last="Giraud">Estelle Giraud</name>
<affiliation>
<nlm:aff id="aff3">ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Whelan, James" sort="Whelan, James" uniqKey="Whelan J" first="James" last="Whelan">James Whelan</name>
<affiliation>
<nlm:aff id="aff3">ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="David, Pascale" sort="David, Pascale" uniqKey="David P" first="Pascale" last="David">Pascale David</name>
<affiliation>
<nlm:aff id="aff4">Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Javot, Helene" sort="Javot, Helene" uniqKey="Javot H" first="Hélène" last="Javot">Hélène Javot</name>
<affiliation>
<nlm:aff id="aff4">Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brearley, Charles" sort="Brearley, Charles" uniqKey="Brearley C" first="Charles" last="Brearley">Charles Brearley</name>
<affiliation>
<nlm:aff id="aff5">School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Hell, Rudiger" sort="Hell, Rudiger" uniqKey="Hell R" first="Rüdiger" last="Hell">Rüdiger Hell</name>
<affiliation>
<nlm:aff id="aff2">University of Heidelberg, Heidelberg Institute for Plant Sciences, 69120 Heidelberg, Germany</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Marin, Elena" sort="Marin, Elena" uniqKey="Marin E" first="Elena" last="Marin">Elena Marin</name>
<affiliation>
<nlm:aff id="aff4">Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pogson, Barry J" sort="Pogson, Barry J" uniqKey="Pogson B" first="Barry J." last="Pogson">Barry J. Pogson</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
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<title xml:lang="en" level="a" type="main">Evidence for a SAL1-PAP Chloroplast Retrograde Pathway That Functions in Drought and High Light Signaling in
<italic>Arabidopsis</italic>
<xref ref-type="author-notes" rid="fn1">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[W]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[OA]</sup>
</xref>
</title>
<author>
<name sortKey="Estavillo, Gonzalo M" sort="Estavillo, Gonzalo M" uniqKey="Estavillo G" first="Gonzalo M." last="Estavillo">Gonzalo M. Estavillo</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Crisp, Peter A" sort="Crisp, Peter A" uniqKey="Crisp P" first="Peter A." last="Crisp">Peter A. Crisp</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pornsiriwong, Wannarat" sort="Pornsiriwong, Wannarat" uniqKey="Pornsiriwong W" first="Wannarat" last="Pornsiriwong">Wannarat Pornsiriwong</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wirtz, Markus" sort="Wirtz, Markus" uniqKey="Wirtz M" first="Markus" last="Wirtz">Markus Wirtz</name>
<affiliation>
<nlm:aff id="aff2">University of Heidelberg, Heidelberg Institute for Plant Sciences, 69120 Heidelberg, Germany</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Collinge, Derek" sort="Collinge, Derek" uniqKey="Collinge D" first="Derek" last="Collinge">Derek Collinge</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Carrie, Chris" sort="Carrie, Chris" uniqKey="Carrie C" first="Chris" last="Carrie">Chris Carrie</name>
<affiliation>
<nlm:aff id="aff3">ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Giraud, Estelle" sort="Giraud, Estelle" uniqKey="Giraud E" first="Estelle" last="Giraud">Estelle Giraud</name>
<affiliation>
<nlm:aff id="aff3">ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Whelan, James" sort="Whelan, James" uniqKey="Whelan J" first="James" last="Whelan">James Whelan</name>
<affiliation>
<nlm:aff id="aff3">ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="David, Pascale" sort="David, Pascale" uniqKey="David P" first="Pascale" last="David">Pascale David</name>
<affiliation>
<nlm:aff id="aff4">Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Javot, Helene" sort="Javot, Helene" uniqKey="Javot H" first="Hélène" last="Javot">Hélène Javot</name>
<affiliation>
<nlm:aff id="aff4">Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brearley, Charles" sort="Brearley, Charles" uniqKey="Brearley C" first="Charles" last="Brearley">Charles Brearley</name>
<affiliation>
<nlm:aff id="aff5">School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Hell, Rudiger" sort="Hell, Rudiger" uniqKey="Hell R" first="Rüdiger" last="Hell">Rüdiger Hell</name>
<affiliation>
<nlm:aff id="aff2">University of Heidelberg, Heidelberg Institute for Plant Sciences, 69120 Heidelberg, Germany</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Marin, Elena" sort="Marin, Elena" uniqKey="Marin E" first="Elena" last="Marin">Elena Marin</name>
<affiliation>
<nlm:aff id="aff4">Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pogson, Barry J" sort="Pogson, Barry J" uniqKey="Pogson B" first="Barry J." last="Pogson">Barry J. Pogson</name>
<affiliation>
<nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">The Plant Cell</title>
<idno type="ISSN">1040-4651</idno>
<idno type="eISSN">1532-298X</idno>
<imprint>
<date when="2011">2011</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">
<p>This work describes a chloroplast-to-nucleus retrograde signaling pathway involving SAL1, a chloroplast and mitochondrial enzyme that degrades the phosphonucleotide 3′-phosphoadenosine 5′-phosphate (PAP). In the absence of SAL1 or in response to drought and high light, PAP accumulates and can move between the chloroplast and the nucleus, where it inhibits exoribonucleases, thereby inducing stress-responsive genes.</p>
</div>
</front>
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<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Plant Cell</journal-id>
<journal-id journal-id-type="hwp">plantcell</journal-id>
<journal-id journal-id-type="publisher-id">aspb</journal-id>
<journal-title-group>
<journal-title>The Plant Cell</journal-title>
</journal-title-group>
<issn pub-type="ppub">1040-4651</issn>
<issn pub-type="epub">1532-298X</issn>
<publisher>
<publisher-name>American Society of Plant Biologists</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">22128124</article-id>
<article-id pub-id-type="pmc">3246320</article-id>
<article-id pub-id-type="publisher-id">091033</article-id>
<article-id pub-id-type="doi">10.1105/tpc.111.091033</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Articles</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Evidence for a SAL1-PAP Chloroplast Retrograde Pathway That Functions in Drought and High Light Signaling in
<italic>Arabidopsis</italic>
<xref ref-type="author-notes" rid="fn1">
<sup>[C]</sup>
</xref>
<xref ref-type="author-notes" rid="fn2">
<sup>[W]</sup>
</xref>
<xref ref-type="author-notes" rid="fn3">
<sup>[OA]</sup>
</xref>
</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Estavillo</surname>
<given-names>Gonzalo M.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Crisp</surname>
<given-names>Peter A.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pornsiriwong</surname>
<given-names>Wannarat</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wirtz</surname>
<given-names>Markus</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Collinge</surname>
<given-names>Derek</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Carrie</surname>
<given-names>Chris</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Giraud</surname>
<given-names>Estelle</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Whelan</surname>
<given-names>James</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>David</surname>
<given-names>Pascale</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Javot</surname>
<given-names>Hélène</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brearley</surname>
<given-names>Charles</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hell</surname>
<given-names>Rüdiger</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Marin</surname>
<given-names>Elena</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pogson</surname>
<given-names>Barry J.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>1</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>a</label>
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia</aff>
<aff id="aff2">
<label>b</label>
University of Heidelberg, Heidelberg Institute for Plant Sciences, 69120 Heidelberg, Germany</aff>
<aff id="aff3">
<label>c</label>
ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia</aff>
<aff id="aff4">
<label>d</label>
Commissariat à l’Energie Atomique, Direction des Sciences du Vivant Institut de Biologie Environnementale et de Biotechnologie, Laboratoire de Biologie du Développement des Plantes, Unité Mixte de Recherche 6191 Centre National de la Recherche Scientifique, Commissariat à l’Energie Atomique, Aix-Marseille II, F-13108 Saint-Paul-lez-Durance, France</aff>
<aff id="aff5">
<label>e</label>
School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom</aff>
<author-notes>
<corresp id="cor1">
<label>1</label>
Address correspondence to
<email>barry.pogson@anu.edu.au</email>
.</corresp>
<fn>
<p>The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (
<ext-link ext-link-type="uri" xlink:href="www.plantcell.org">www.plantcell.org</ext-link>
) is: Barry J. Pogson (
<email>barry.pogson@anu.edu.au</email>
).</p>
</fn>
<fn id="fn1">
<label>[C]</label>
<p>Some figures in this article are displayed in color online but in black and white in the print edition.</p>
</fn>
<fn id="fn2">
<label>[W]</label>
<p>Online version contains Web-only data.</p>
</fn>
<fn id="fn3">
<label>[OA]</label>
<p>Open Access articles can be viewed online without a subscription.</p>
</fn>
<fn>
<p>
<ext-link ext-link-type="uri" xlink:href="www.plantcell.org/cgi/doi/10.1105/tpc.111.091033">www.plantcell.org/cgi/doi/10.1105/tpc.111.091033</ext-link>
</p>
</fn>
</author-notes>
<pmc-comment>Fake ppub date generated by PMC from publisher pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub">
<month>11</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="epub">
<day>29</day>
<month>11</month>
<year>2011</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>29</day>
<month>11</month>
<year>2011</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>23</volume>
<issue>11</issue>
<fpage>3992</fpage>
<lpage>4012</lpage>
<history>
<date date-type="received">
<day>2</day>
<month>9</month>
<year>2011</year>
</date>
<date date-type="rev-recd">
<day>18</day>
<month>10</month>
<year>2011</year>
</date>
<date date-type="accepted">
<day>10</day>
<month>11</month>
<year>2011</year>
</date>
</history>
<permissions>
<copyright-statement>© 2011 American Society of Plant Biologists. All rights reserved.</copyright-statement>
<copyright-year>2011</copyright-year>
<license license-type="open-access">
<license-p>Open Access articles can be viewed online without a subscription.</license-p>
</license>
</permissions>
<abstract abstract-type="precis">
<p>This work describes a chloroplast-to-nucleus retrograde signaling pathway involving SAL1, a chloroplast and mitochondrial enzyme that degrades the phosphonucleotide 3′-phosphoadenosine 5′-phosphate (PAP). In the absence of SAL1 or in response to drought and high light, PAP accumulates and can move between the chloroplast and the nucleus, where it inhibits exoribonucleases, thereby inducing stress-responsive genes.</p>
</abstract>
<abstract>
<p>Compartmentation of the eukaryotic cell requires a complex set of subcellular messages, including multiple retrograde signals from the chloroplast and mitochondria to the nucleus, to regulate gene expression. Here, we propose that one such signal is a phosphonucleotide (3′-phosphoadenosine 5′-phosphate [PAP]), which accumulates in
<italic>Arabidopsis thaliana</italic>
in response to drought and high light (HL) stress and that the enzyme SAL1 regulates its levels by dephosphorylating PAP to AMP. SAL1 accumulates in chloroplasts and mitochondria but not in the cytosol.
<italic>sal1</italic>
mutants accumulate 20-fold more PAP without a marked change in inositol phosphate levels, demonstrating that PAP is a primary in vivo substrate. Significantly, transgenic targeting of SAL1 to either the nucleus or chloroplast of
<italic>sal1</italic>
mutants lowers the total PAP levels and expression of the HL-inducible
<italic>ASCORBATE PEROXIDASE2</italic>
gene. This indicates that PAP must be able to move between cellular compartments. The mode of action for PAP could be inhibition of 5′ to 3′ exoribonucleases (XRNs), as SAL1 and the nuclear XRNs modulate the expression of a similar subset of HL and drought-inducible genes,
<italic>sal1</italic>
mutants accumulate XRN substrates, and PAP can inhibit yeast (
<italic>Saccharomyces cerevisiae</italic>
) XRNs. We propose a SAL1-PAP retrograde pathway that can alter nuclear gene expression during HL and drought stress.</p>
</abstract>
</article-meta>
</front>
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