Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape
Identifieur interne : 000409 ( Pmc/Corpus ); précédent : 000408; suivant : 000410Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape
Auteurs : Yasunori Ichihashi ; José Antonio Aguilar-Martínez ; Moran Farhi ; Daniel H. Chitwood ; Ravi Kumar ; Lee V. Millon ; Jie Peng ; Julin N. Maloof ; Neelima R. SinhaSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2014.
Abstract
Ever since Darwin’s pioneering research, a major challenge in biology has been to understand the genetic basis of morphological evolution. Utilizing the natural variation in leaf morphology between tomato and two related wild species, we identified a gene network module that leads to a dynamic rewiring of interactions in the whole leaf developmental gene regulatory network. Our work experimentally validates the hypothesis that peripheral regions of network, rather than network hubs, are more likely to contribute to evolutionary innovations. Our data also suggest that, likely due to their bottleneck location in the network, the regulation in KNOX homeobox genes was repeatedly manipulated to generate natural variation in leaf shape.
Url:
DOI: 10.1073/pnas.1402835111
PubMed: 24927584
PubMed Central: 4078850
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Chitwood</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Kumar, Ravi" sort="Kumar, Ravi" uniqKey="Kumar R" first="Ravi" last="Kumar">Ravi Kumar</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Millon, Lee V" sort="Millon, Lee V" uniqKey="Millon L" first="Lee V." last="Millon">Lee V. Millon</name><affiliation><nlm:aff wicri:cut=", and" id="aff2">School of Veterinary Medicine</nlm:aff></affiliation></author><author><name sortKey="Peng, Jie" sort="Peng, Jie" uniqKey="Peng J" first="Jie" last="Peng">Jie Peng</name><affiliation><nlm:aff wicri:cut="; and" id="aff3">Department of Statistics,<institution>University of California, Davis</institution>,<addr-line>CA</addr-line> 95616</nlm:aff></affiliation></author><author><name sortKey="Maloof, Julin N" sort="Maloof, Julin N" uniqKey="Maloof J" first="Julin N." last="Maloof">Julin N. Maloof</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Sinha, Neelima R" sort="Sinha, Neelima R" uniqKey="Sinha N" first="Neelima R." last="Sinha">Neelima R. Sinha</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24927584</idno><idno type="pmc">4078850</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4078850</idno><idno type="RBID">PMC:4078850</idno><idno type="doi">10.1073/pnas.1402835111</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000409</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape</title><author><name sortKey="Ichihashi, Yasunori" sort="Ichihashi, Yasunori" uniqKey="Ichihashi Y" first="Yasunori" last="Ichihashi">Yasunori Ichihashi</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation><affiliation><nlm:aff id="aff4">Center for Sustainable Resource Science,<institution>RIKEN</institution>, Yokohama, Kanagawa 230-0045,<country>Japan</country></nlm:aff></affiliation></author><author><name sortKey="Aguilar Martinez, Jose Antonio" sort="Aguilar Martinez, Jose Antonio" uniqKey="Aguilar Martinez J" first="José Antonio" last="Aguilar-Martínez">José Antonio Aguilar-Martínez</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Farhi, Moran" sort="Farhi, Moran" uniqKey="Farhi M" first="Moran" last="Farhi">Moran Farhi</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Chitwood, Daniel H" sort="Chitwood, Daniel H" uniqKey="Chitwood D" first="Daniel H." last="Chitwood">Daniel H. Chitwood</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Kumar, Ravi" sort="Kumar, Ravi" uniqKey="Kumar R" first="Ravi" last="Kumar">Ravi Kumar</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Millon, Lee V" sort="Millon, Lee V" uniqKey="Millon L" first="Lee V." last="Millon">Lee V. Millon</name><affiliation><nlm:aff wicri:cut=", and" id="aff2">School of Veterinary Medicine</nlm:aff></affiliation></author><author><name sortKey="Peng, Jie" sort="Peng, Jie" uniqKey="Peng J" first="Jie" last="Peng">Jie Peng</name><affiliation><nlm:aff wicri:cut="; and" id="aff3">Department of Statistics,<institution>University of California, Davis</institution>,<addr-line>CA</addr-line> 95616</nlm:aff></affiliation></author><author><name sortKey="Maloof, Julin N" sort="Maloof, Julin N" uniqKey="Maloof J" first="Julin N." last="Maloof">Julin N. Maloof</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author><author><name sortKey="Sinha, Neelima R" sort="Sinha, Neelima R" uniqKey="Sinha N" first="Neelima R." last="Sinha">Neelima R. Sinha</name><affiliation><nlm:aff id="aff1">Department of Plant Biology,</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Ever since Darwin’s pioneering research, a major challenge in biology has been to understand the genetic basis of morphological evolution. Utilizing the natural variation in leaf morphology between tomato and two related wild species, we identified a gene network module that leads to a dynamic rewiring of interactions in the whole leaf developmental gene regulatory network. Our work experimentally validates the hypothesis that peripheral regions of network, rather than network hubs, are more likely to contribute to evolutionary innovations. Our data also suggest that, likely due to their bottleneck location in the network, the regulation in KNOX homeobox genes was repeatedly manipulated to generate natural variation in leaf shape.</p></div></front></TEI><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">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24927584</article-id><article-id pub-id-type="pmc">4078850</article-id><article-id pub-id-type="publisher-id">201402835</article-id><article-id pub-id-type="doi">10.1073/pnas.1402835111</article-id><article-categories><subj-group subj-group-type="heading"><subject>PNAS Plus</subject></subj-group><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Plant Biology</subject></subj-group></subj-group><series-title>PNAS Plus</series-title></article-categories><title-group><article-title>Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape</article-title><alt-title alt-title-type="short">Gene network module regulating leaf shape</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Ichihashi</surname><given-names>Yasunori</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff4"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Aguilar-Martínez</surname><given-names>José Antonio</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Farhi</surname><given-names>Moran</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chitwood</surname><given-names>Daniel H.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kumar</surname><given-names>Ravi</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Millon</surname><given-names>Lee V.</given-names></name><xref ref-type="aff" rid="aff2"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Peng</surname><given-names>Jie</given-names></name><xref ref-type="aff" rid="aff3"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Maloof</surname><given-names>Julin N.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sinha</surname><given-names>Neelima R.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>3</sup></xref></contrib><aff id="aff1"><sup>a</sup>Department of Plant Biology,</aff><aff id="aff2"><sup>c</sup>School of Veterinary Medicine, and</aff><aff id="aff3"><sup>d</sup>Department of Statistics,<institution>University of California, Davis</institution>,<addr-line>CA</addr-line> 95616; and</aff><aff id="aff4"><sup>b</sup>Center for Sustainable Resource Science,<institution>RIKEN</institution>, Yokohama, Kanagawa 230-0045,<country>Japan</country></aff></contrib-group><author-notes><corresp id="cor1"><sup>3</sup>To whom correspondence should be addressed. E-mail: <email>nrsinha@ucdavis.edu</email>.</corresp><fn fn-type="edited-by"><p>Edited by Philip N. Benfey, Duke University, Durham, NC, and approved May 14, 2014 (received for review February 14, 2014)</p></fn><fn fn-type="con"><p>Author contributions: Y.I. and N.R.S. designed research; Y.I., J.A.A.-M., M.F., D.H.C., R.K., and L.V.M. performed research; J.P. and J.N.M. contributed new reagents/analytic tools; Y.I. analyzed data; and Y.I. and N.R.S. wrote the paper.</p></fn><fn fn-type="present-address" id="fn1"><p><sup>1</sup>Present address: Donald Danforth Plant Science Center, St. Louis, MO 63132.</p></fn><fn fn-type="present-address" id="fn2"><p><sup>2</sup>Present address: Novozymes, Inc., Davis, CA 95618.</p></fn></author-notes><pub-date pub-type="ppub"><day>24</day><month>6</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>9</day><month>6</month><year>2014</year></pub-date><pub-date pub-type="pmc-release"><day>9</day><month>6</month><year>2014</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>111</volume><issue>25</issue><fpage>E2616</fpage><lpage>E2621</lpage><permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p></license></permissions><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201402835.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Ever since Darwin’s pioneering research, a major challenge in biology has been to understand the genetic basis of morphological evolution. Utilizing the natural variation in leaf morphology between tomato and two related wild species, we identified a gene network module that leads to a dynamic rewiring of interactions in the whole leaf developmental gene regulatory network. Our work experimentally validates the hypothesis that peripheral regions of network, rather than network hubs, are more likely to contribute to evolutionary innovations. Our data also suggest that, likely due to their bottleneck location in the network, the regulation in KNOX homeobox genes was repeatedly manipulated to generate natural variation in leaf shape.</p></abstract><abstract><p>Despite a long-standing interest in the genetic basis of morphological diversity, the molecular mechanisms that give rise to developmental variation are incompletely understood. Here, we use comparative transcriptomics coupled with the construction of gene coexpression networks to predict a gene regulatory network (GRN) for leaf development in tomato and two related wild species with strikingly different leaf morphologies. The core network in the leaf developmental GRN contains regulators of leaf morphology that function in global cell proliferation with peripheral gene network modules (GNMs). The <italic>BLADE-ON-PETIOLE</italic> (<italic>BOP</italic>) transcription factor in one GNM controls the core network by altering effective concentration of the KNOTTED-like HOMEOBOX gene product. Comparative network analysis and experimental perturbations of <italic>BOP</italic> levels suggest that variation in <italic>BOP</italic> expression could explain the diversity in leaf complexity among these species through dynamic rewiring of interactions in the GRN. The peripheral location of the <italic>BOP</italic>-containing GNM in the leaf developmental GRN and the phenotypic mimics of evolutionary diversity caused by alteration in <italic>BOP</italic> levels identify a key role for this GNM in canalizing the leaf morphospace by modifying the maturation schedule of leaves to create morphological diversity.</p></abstract><kwd-group><kwd><italic>Solanum</italic> species</kwd><kwd>RNA-seq</kwd><kwd>bioinformatics</kwd></kwd-group><counts><page-count count="6"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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