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The Complexity of Posttranscriptional Small RNA Regulatory Networks Revealed by In Silico Analysis of Gossypium arboreum L. Leaf, Flower and Boll Small Regulatory RNAs

Identifieur interne : 001B73 ( Ncbi/Merge ); précédent : 001B72; suivant : 001B74

The Complexity of Posttranscriptional Small RNA Regulatory Networks Revealed by In Silico Analysis of Gossypium arboreum L. Leaf, Flower and Boll Small Regulatory RNAs

Auteurs : Hongtao Hu [États-Unis] ; Aaron M. Rashotte [États-Unis] ; Narendra K. Singh [États-Unis] ; David B. Weaver [États-Unis] ; Leslie R. Goertzen [États-Unis] ; Shree R. Singh [États-Unis] ; Robert D. Locy [États-Unis]

Source :

RBID : PMC:4466472

Abstract

MicroRNAs (miRNAs) and secondary small interfering RNAs (principally phased siRNAs or trans-acting siRNAs) are two distinct subfamilies of small RNAs (sRNAs) that are emerging as key regulators of posttranscriptional gene expression in plants. Both miRNAs and secondary-siRNAs (sec-siRNAs) are processed from longer RNA precursors by DICER-LIKE proteins (DCLs). Gossypium arboreum L., also known as tree cotton or Asian cotton, is a diploid, possibly ancestral relative of tetraploid Gossypium hirsutum L., the predominant type of commercially grown cotton worldwide known as upland cotton. To understand the biological significance of these gene regulators in G. arboreum, a bioinformatics analysis was performed on G. arboreum small RNAs produced from G. arboreum leaf, flower, and boll tissues. Consequently, 263 miRNAs derived from 353 precursors, including 155 conserved miRNAs (cs-miRNAs) and 108 novel lineage-specific miRNAs (ls-miRNAs). Along with miRNAs, 2,033 miRNA variants (isomiRNAs) were identified as well. Those isomiRNAs with variation at the 3’-miRNA end were expressed at the highest levels, compared to other types of variants. In addition, 755 pha-siRNAs derived 319 pha-siRNA gene transcripts (PGTs) were identified, and the potential pha-siRNA initiators were predicted. Also, 2,251 non-phased siRNAs were found as well, of which 1,088 appeared to be produced by so-called cis- or trans-cleavage of the PGTs observed at positions differing from pha-siRNAs. Of those sRNAs, 148 miRNAs/isomiRNAs and 274 phased/non-phased siRNAs were differentially expressed in one or more pairs of tissues examined. Target analysis revealed that target genes for both miRNAs and pha-siRNAs are involved a broad range of metabolic and enzymatic activities. We demonstrate that secondary siRNA production could result from initial cleavage of precursors by both miRNAs or isomiRNAs, and that subsequently produced phased and unphased siRNAs could result that also serve as triggers of a second round of both cis- and trans-cleavage of additional siRNAs, leading to the formation of complex sRNA regulatory networks mediating posttranscriptional gene silencing. Results from this study extended our knowledge on G. arboreum sRNAs and their biological importance, which would facilitate future studies on regulatory mechanism of tissue development in cotton and other plant species.


Url:
DOI: 10.1371/journal.pone.0127468
PubMed: 26070200
PubMed Central: 4466472

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<p>MicroRNAs (miRNAs) and secondary small interfering RNAs (principally phased siRNAs or trans-acting siRNAs) are two distinct subfamilies of small RNAs (sRNAs) that are emerging as key regulators of posttranscriptional gene expression in plants. Both miRNAs and secondary-siRNAs (sec-siRNAs) are processed from longer RNA precursors by DICER-LIKE proteins (DCLs).
<italic>Gossypium arboreum</italic>
L., also known as tree cotton or Asian cotton, is a diploid, possibly ancestral relative of tetraploid
<italic>Gossypium hirsutum</italic>
L., the predominant type of commercially grown cotton worldwide known as upland cotton. To understand the biological significance of these gene regulators in
<italic>G</italic>
.
<italic>arboreum</italic>
, a bioinformatics analysis was performed on
<italic>G</italic>
.
<italic>arboreum</italic>
small RNAs produced from
<italic>G</italic>
.
<italic>arboreum</italic>
leaf, flower, and boll tissues. Consequently, 263 miRNAs derived from 353 precursors, including 155 conserved miRNAs (cs-miRNAs) and 108 novel lineage-specific miRNAs (ls-miRNAs). Along with miRNAs, 2,033 miRNA variants (isomiRNAs) were identified as well. Those isomiRNAs with variation at the 3’-miRNA end were expressed at the highest levels, compared to other types of variants. In addition, 755 pha-siRNAs derived 319 pha-siRNA gene transcripts (PGTs) were identified, and the potential pha-siRNA initiators were predicted. Also, 2,251 non-phased siRNAs were found as well, of which 1,088 appeared to be produced by so-called
<italic>cis</italic>
- or
<italic>trans</italic>
-cleavage of the PGTs observed at positions differing from pha-siRNAs. Of those sRNAs, 148 miRNAs/isomiRNAs and 274 phased/non-phased siRNAs were differentially expressed in one or more pairs of tissues examined. Target analysis revealed that target genes for both miRNAs and pha-siRNAs are involved a broad range of metabolic and enzymatic activities. We demonstrate that secondary siRNA production could result from initial cleavage of precursors by both miRNAs or isomiRNAs, and that subsequently produced phased and unphased siRNAs could result that also serve as triggers of a second round of both
<italic>cis</italic>
- and
<italic>trans</italic>
-cleavage of additional siRNAs, leading to the formation of complex sRNA regulatory networks mediating posttranscriptional gene silencing. Results from this study extended our knowledge on
<italic>G</italic>
.
<italic>arboreum</italic>
sRNAs and their biological importance, which would facilitate future studies on regulatory mechanism of tissue development in cotton and other plant species.</p>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group>
<journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">26070200</article-id>
<article-id pub-id-type="pmc">4466472</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0127468</article-id>
<article-id pub-id-type="publisher-id">PONE-D-14-22019</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>The Complexity of Posttranscriptional Small RNA Regulatory Networks Revealed by
<italic>In Silico</italic>
Analysis of
<italic>Gossypium arboreum</italic>
L. Leaf, Flower and Boll Small Regulatory RNAs</article-title>
<alt-title alt-title-type="running-head">
<italic>G. arboreum</italic>
MiRNA and Phased-siRNA Identification and Expression</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Hu</surname>
<given-names>Hongtao</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rashotte</surname>
<given-names>Aaron M.</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Singh</surname>
<given-names>Narendra K.</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Weaver</surname>
<given-names>David B.</given-names>
</name>
<xref ref-type="aff" rid="aff002">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Goertzen</surname>
<given-names>Leslie R.</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Singh</surname>
<given-names>Shree R.</given-names>
</name>
<xref ref-type="aff" rid="aff003">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Locy</surname>
<given-names>Robert D.</given-names>
</name>
<xref ref-type="aff" rid="aff001">
<sup>1</sup>
</xref>
<xref rid="cor001" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="aff001">
<label>1</label>
<addr-line>Department of Biological Sciences, Auburn University, Auburn, AL 36849, United States of America</addr-line>
</aff>
<aff id="aff002">
<label>2</label>
<addr-line>Department of Crop, Soil & Environmental Sciences, Auburn University, Auburn, AL 36849, United States of America</addr-line>
</aff>
<aff id="aff003">
<label>3</label>
<addr-line>Center for Nano Biotechnology Research, Alabama State University, Montgomery, AL 33104, United States of America</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Zhang</surname>
<given-names>Xianlong</given-names>
</name>
<role>Academic Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>National Key Laboratory of Crop Genetic Improvement, CHINA</addr-line>
</aff>
<author-notes>
<fn fn-type="conflict" id="coi001">
<p>
<bold>Competing Interests: </bold>
The authors have the following interests. This work was funded in part with funding from Cotton, Inc.; Cary, NC. This funding was obtained in conjunction with the Alabama Cotton Commission - the grant numbers that funded these efforts were: 07-936AL; 10-675AL. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.</p>
</fn>
<fn fn-type="con" id="contrib001">
<p>Conceived and designed the experiments: HH RDL NKS DBW. Performed the experiments: HH. Analyzed the data: HH RDL NKS AMR LRG DBW. Contributed reagents/materials/analysis tools: HH RDL LRG. Wrote the paper: HH RDL NKS AMR DBW LRG SRS.</p>
</fn>
<corresp id="cor001">* E-mail:
<email>hzh0005@tigermail.auburn.edu</email>
(HH);
<email>locyrob@auburn.edu</email>
(RDL)</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>12</day>
<month>6</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2015</year>
</pub-date>
<volume>10</volume>
<issue>6</issue>
<elocation-id>e0127468</elocation-id>
<history>
<date date-type="received">
<day>16</day>
<month>5</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>15</day>
<month>4</month>
<year>2015</year>
</date>
</history>
<permissions>
<copyright-year>2015</copyright-year>
<copyright-holder>Hu et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p>This is an open access article distributed under the terms of the
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0127468.pdf"></self-uri>
<abstract>
<p>MicroRNAs (miRNAs) and secondary small interfering RNAs (principally phased siRNAs or trans-acting siRNAs) are two distinct subfamilies of small RNAs (sRNAs) that are emerging as key regulators of posttranscriptional gene expression in plants. Both miRNAs and secondary-siRNAs (sec-siRNAs) are processed from longer RNA precursors by DICER-LIKE proteins (DCLs).
<italic>Gossypium arboreum</italic>
L., also known as tree cotton or Asian cotton, is a diploid, possibly ancestral relative of tetraploid
<italic>Gossypium hirsutum</italic>
L., the predominant type of commercially grown cotton worldwide known as upland cotton. To understand the biological significance of these gene regulators in
<italic>G</italic>
.
<italic>arboreum</italic>
, a bioinformatics analysis was performed on
<italic>G</italic>
.
<italic>arboreum</italic>
small RNAs produced from
<italic>G</italic>
.
<italic>arboreum</italic>
leaf, flower, and boll tissues. Consequently, 263 miRNAs derived from 353 precursors, including 155 conserved miRNAs (cs-miRNAs) and 108 novel lineage-specific miRNAs (ls-miRNAs). Along with miRNAs, 2,033 miRNA variants (isomiRNAs) were identified as well. Those isomiRNAs with variation at the 3’-miRNA end were expressed at the highest levels, compared to other types of variants. In addition, 755 pha-siRNAs derived 319 pha-siRNA gene transcripts (PGTs) were identified, and the potential pha-siRNA initiators were predicted. Also, 2,251 non-phased siRNAs were found as well, of which 1,088 appeared to be produced by so-called
<italic>cis</italic>
- or
<italic>trans</italic>
-cleavage of the PGTs observed at positions differing from pha-siRNAs. Of those sRNAs, 148 miRNAs/isomiRNAs and 274 phased/non-phased siRNAs were differentially expressed in one or more pairs of tissues examined. Target analysis revealed that target genes for both miRNAs and pha-siRNAs are involved a broad range of metabolic and enzymatic activities. We demonstrate that secondary siRNA production could result from initial cleavage of precursors by both miRNAs or isomiRNAs, and that subsequently produced phased and unphased siRNAs could result that also serve as triggers of a second round of both
<italic>cis</italic>
- and
<italic>trans</italic>
-cleavage of additional siRNAs, leading to the formation of complex sRNA regulatory networks mediating posttranscriptional gene silencing. Results from this study extended our knowledge on
<italic>G</italic>
.
<italic>arboreum</italic>
sRNAs and their biological importance, which would facilitate future studies on regulatory mechanism of tissue development in cotton and other plant species.</p>
</abstract>
<funding-group>
<funding-statement>This work was funded in part with funding from Cotton, Inc.; Cary, NC. This funding was obtained in conjunction with the Alabama Cotton Commission - the grant numbers that funded these efforts were: 07-936AL; 10-675AL. This funding was awarded to RDL, NKS, & DBW. Further, the authors declare that the funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The primary research funding for this work was derived from a Hatch Multistate Grant No. ALA021-1-10008 Awarded by the National Institute of Food and Agriculture, USDA. The award was made through the Alabama Agricultural Experiment Station to RDL, DBW, & NKS. Funding during the course of his PhD program to HH was obtained as a Teaching Assistantship from the Department of Biological Sciences, Auburn University, and Research Assistantship funding was obtained from the above mentioned NIFA-USDA Grant.</funding-statement>
</funding-group>
<counts>
<fig-count count="11"></fig-count>
<table-count count="8"></table-count>
<page-count count="31"></page-count>
</counts>
<custom-meta-group>
<custom-meta id="data-availability">
<meta-name>Data Availability</meta-name>
<meta-value>Small RNA data for
<italic>G. arboreum</italic>
leaf, flower and boll is available from Comparative Sequencing of Plant Small RNAs website (
<ext-link ext-link-type="uri" xlink:href="http://smallrna.udel.edu">http://smallrna.udel.edu</ext-link>
).
<italic>G. arboreum</italic>
Raw sequence data can be downloaded from Comparative Evolutionary Genomics of Cotton website (
<ext-link ext-link-type="uri" xlink:href="http://128.192.141.98/CottonFiber/pages/genome/sequence.aspx">http://128.192.141.98/CottonFiber/pages/genome/sequence.aspx</ext-link>
).
<italic>G. arboreum</italic>
Expressed Sequence Tags used in this study were collected from both NCBI (
<ext-link ext-link-type="uri" xlink:href="http://www.ncbi.nlm.nih.gov/nucest/?term=Gossypium+arboreum">http://www.ncbi.nlm.nih.gov/nucest/?term=Gossypium+arboreum</ext-link>
) and the Comparative Evolutionary Genomics of Cotton website (
<ext-link ext-link-type="uri" xlink:href="http://128.192.141.98/CottonFiber/">http://128.192.141.98/CottonFiber/</ext-link>
).</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes>
<title>Data Availability</title>
<p>Small RNA data for
<italic>G. arboreum</italic>
leaf, flower and boll is available from Comparative Sequencing of Plant Small RNAs website (
<ext-link ext-link-type="uri" xlink:href="http://smallrna.udel.edu">http://smallrna.udel.edu</ext-link>
).
<italic>G. arboreum</italic>
Raw sequence data can be downloaded from Comparative Evolutionary Genomics of Cotton website (
<ext-link ext-link-type="uri" xlink:href="http://128.192.141.98/CottonFiber/pages/genome/sequence.aspx">http://128.192.141.98/CottonFiber/pages/genome/sequence.aspx</ext-link>
).
<italic>G. arboreum</italic>
Expressed Sequence Tags used in this study were collected from both NCBI (
<ext-link ext-link-type="uri" xlink:href="http://www.ncbi.nlm.nih.gov/nucest/?term=Gossypium+arboreum">http://www.ncbi.nlm.nih.gov/nucest/?term=Gossypium+arboreum</ext-link>
) and the Comparative Evolutionary Genomics of Cotton website (
<ext-link ext-link-type="uri" xlink:href="http://128.192.141.98/CottonFiber/">http://128.192.141.98/CottonFiber/</ext-link>
).</p>
</notes>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
</list>
<tree>
<country name="États-Unis">
<noRegion>
<name sortKey="Hu, Hongtao" sort="Hu, Hongtao" uniqKey="Hu H" first="Hongtao" last="Hu">Hongtao Hu</name>
</noRegion>
<name sortKey="Goertzen, Leslie R" sort="Goertzen, Leslie R" uniqKey="Goertzen L" first="Leslie R." last="Goertzen">Leslie R. Goertzen</name>
<name sortKey="Hu, Hongtao" sort="Hu, Hongtao" uniqKey="Hu H" first="Hongtao" last="Hu">Hongtao Hu</name>
<name sortKey="Locy, Robert D" sort="Locy, Robert D" uniqKey="Locy R" first="Robert D." last="Locy">Robert D. Locy</name>
<name sortKey="Rashotte, Aaron M" sort="Rashotte, Aaron M" uniqKey="Rashotte A" first="Aaron M." last="Rashotte">Aaron M. Rashotte</name>
<name sortKey="Singh, Narendra K" sort="Singh, Narendra K" uniqKey="Singh N" first="Narendra K." last="Singh">Narendra K. Singh</name>
<name sortKey="Singh, Shree R" sort="Singh, Shree R" uniqKey="Singh S" first="Shree R." last="Singh">Shree R. Singh</name>
<name sortKey="Weaver, David B" sort="Weaver, David B" uniqKey="Weaver D" first="David B." last="Weaver">David B. Weaver</name>
</country>
</tree>
</affiliations>
</record>

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