Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
Identifieur interne : 000207 ( Pmc/Checkpoint ); précédent : 000206; suivant : 000208Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut
Auteurs : Matan Shelomi [États-Unis, Allemagne] ; W Cameron Jasper [États-Unis] ; Joel Atallah [États-Unis] ; Lynn S. Kimsey [États-Unis] ; Brian R. Johnson [États-Unis]Source :
- BMC Genomics [ 1471-2164 ] ; 2014.
Abstract
Stick and leaf insects (Phasmatodea) are an exclusively leaf-feeding order of insects with no record of omnivory, unlike other “herbivorous” Polyneoptera. They represent an ideal system for investigating the adaptations necessary for obligate folivory, including plant cell wall degrading enzymes (PCWDEs). However, their physiology and internal anatomy is poorly understood, with limited genomic resources available.
We
We identified a large and diverse PCWDE repertoire endogenous to the phasmids. If these expressed genes are translated into active enzymes, then phasmids can theoretically break plant cell walls into their monomer components independently of microbial symbionts. The differential gene expression between the two midgut sections provides the first molecular hints as to their function in living phasmids. Our work expands the resources available for industrial applications of animal-derived PCWDEs, and facilitates evolutionary analysis of lower Polyneopteran digestive enzymes, including the pectinases whose origin in Phasmatodea may have been a horizontal transfer event from bacteria.
The online version of this article (doi:10.1186/1471-2164-15-917) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/1471-2164-15-917
PubMed: 25331961
PubMed Central: 4221708
Affiliations:
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>Stick and leaf insects (Phasmatodea) are an exclusively leaf-feeding order of insects with no record of omnivory, unlike other “herbivorous” Polyneoptera. They represent an ideal system for investigating the adaptations necessary for obligate folivory, including plant cell wall degrading enzymes (PCWDEs). However, their physiology and internal anatomy is poorly understood, with limited genomic resources available.</p>
</sec>
<sec><title>Results</title>
<p>We <italic>de novo</italic>
assembled transcriptomes for the anterior and posterior midguts of six diverse Phasmatodea species, with RNA-Seq on one exemplar species, <italic>Peruphasma schultei</italic>
. The latter’s assembly yielded >100,000 transcripts, with over 4000 transcripts uniquely or more highly expressed in specific midgut sections. Two to three dozen PCWDE encoding gene families, including cellulases and pectinases, were differentially expressed in the anterior midgut. These genes were also found in genomic DNA from phasmid brain tissue, suggesting endogenous production. Sequence alignments revealed catalytic sites on most PCWDE transcripts. While most phasmid PCWDE genes showed homology with those of other insects, the pectinases were homologous to bacterial genes.</p>
</sec>
<sec><title>Conclusions</title>
<p>We identified a large and diverse PCWDE repertoire endogenous to the phasmids. If these expressed genes are translated into active enzymes, then phasmids can theoretically break plant cell walls into their monomer components independently of microbial symbionts. The differential gene expression between the two midgut sections provides the first molecular hints as to their function in living phasmids. Our work expands the resources available for industrial applications of animal-derived PCWDEs, and facilitates evolutionary analysis of lower Polyneopteran digestive enzymes, including the pectinases whose origin in Phasmatodea may have been a horizontal transfer event from bacteria.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/1471-2164-15-917) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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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 Genomics</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Genomics</journal-id>
<journal-title-group><journal-title>BMC Genomics</journal-title>
</journal-title-group>
<issn pub-type="epub">1471-2164</issn>
<publisher><publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25331961</article-id>
<article-id pub-id-type="pmc">4221708</article-id>
<article-id pub-id-type="publisher-id">6620</article-id>
<article-id pub-id-type="doi">10.1186/1471-2164-15-917</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Shelomi</surname>
<given-names>Matan</given-names>
</name>
<address><email>mshelomi@ice.mpg.de</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jasper</surname>
<given-names>W Cameron</given-names>
</name>
<address><email>wcjasper@ucdavis.edu</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Atallah</surname>
<given-names>Joel</given-names>
</name>
<address><email>joel.atallah@gmail.com</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kimsey</surname>
<given-names>Lynn S</given-names>
</name>
<address><email>lskimsey@ucdavis.edu</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Johnson</surname>
<given-names>Brian R</given-names>
</name>
<address><email>brnjohnson@ucdavis.edu</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<aff id="Aff1"><label></label>
Department of Entomology and Nematology, University of California-Davis, Davis, CA 95616 USA</aff>
<aff id="Aff2"><label></label>
Department of Entomology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany</aff>
</contrib-group>
<pub-date pub-type="epub"><day>21</day>
<month>10</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>21</day>
<month>10</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<volume>15</volume>
<issue>1</issue>
<elocation-id>917</elocation-id>
<history><date date-type="received"><day>8</day>
<month>8</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>1</day>
<month>10</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>© Shelomi et al.; licensee BioMed Central Ltd. 2014</copyright-statement>
<license license-type="open-access"><license-p>This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution 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 the original work is properly credited. 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>Stick and leaf insects (Phasmatodea) are an exclusively leaf-feeding order of insects with no record of omnivory, unlike other “herbivorous” Polyneoptera. They represent an ideal system for investigating the adaptations necessary for obligate folivory, including plant cell wall degrading enzymes (PCWDEs). However, their physiology and internal anatomy is poorly understood, with limited genomic resources available.</p>
</sec>
<sec><title>Results</title>
<p>We <italic>de novo</italic>
assembled transcriptomes for the anterior and posterior midguts of six diverse Phasmatodea species, with RNA-Seq on one exemplar species, <italic>Peruphasma schultei</italic>
. The latter’s assembly yielded >100,000 transcripts, with over 4000 transcripts uniquely or more highly expressed in specific midgut sections. Two to three dozen PCWDE encoding gene families, including cellulases and pectinases, were differentially expressed in the anterior midgut. These genes were also found in genomic DNA from phasmid brain tissue, suggesting endogenous production. Sequence alignments revealed catalytic sites on most PCWDE transcripts. While most phasmid PCWDE genes showed homology with those of other insects, the pectinases were homologous to bacterial genes.</p>
</sec>
<sec><title>Conclusions</title>
<p>We identified a large and diverse PCWDE repertoire endogenous to the phasmids. If these expressed genes are translated into active enzymes, then phasmids can theoretically break plant cell walls into their monomer components independently of microbial symbionts. The differential gene expression between the two midgut sections provides the first molecular hints as to their function in living phasmids. Our work expands the resources available for industrial applications of animal-derived PCWDEs, and facilitates evolutionary analysis of lower Polyneopteran digestive enzymes, including the pectinases whose origin in Phasmatodea may have been a horizontal transfer event from bacteria.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/1471-2164-15-917) contains supplementary material, which is available to authorized users.</p>
</sec>
</abstract>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2014</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>États-Unis</li>
</country>
<region><li>Californie</li>
</region>
</list>
<tree><country name="États-Unis"><region name="Californie"><name sortKey="Shelomi, Matan" sort="Shelomi, Matan" uniqKey="Shelomi M" first="Matan" last="Shelomi">Matan Shelomi</name>
</region>
<name sortKey="Atallah, Joel" sort="Atallah, Joel" uniqKey="Atallah J" first="Joel" last="Atallah">Joel Atallah</name>
<name sortKey="Jasper, W Cameron" sort="Jasper, W Cameron" uniqKey="Jasper W" first="W Cameron" last="Jasper">W Cameron Jasper</name>
<name sortKey="Johnson, Brian R" sort="Johnson, Brian R" uniqKey="Johnson B" first="Brian R" last="Johnson">Brian R. Johnson</name>
<name sortKey="Kimsey, Lynn S" sort="Kimsey, Lynn S" uniqKey="Kimsey L" first="Lynn S" last="Kimsey">Lynn S. Kimsey</name>
</country>
<country name="Allemagne"><noRegion><name sortKey="Shelomi, Matan" sort="Shelomi, Matan" uniqKey="Shelomi M" first="Matan" last="Shelomi">Matan Shelomi</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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