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The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure

Identifieur interne : 000002 ( Pmc/Curation ); précédent : 000001; suivant : 000003

The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure

Auteurs : Sateesh Kagale [Canada] ; Chushin Koh [Canada] ; John Nixon [Canada] ; Venkatesh Bollina [Canada] ; Wayne E. Clarke [Canada] ; Reetu Tuteja [Irlande (pays)] ; Charles Spillane [Irlande (pays)] ; Stephen J. Robinson [Canada] ; Matthew G. Links [Canada] ; Carling Clarke [Canada] ; Erin E. Higgins [Canada] ; Terry Huebert [Canada] ; Andrew G. Sharpe [Canada] ; Isobel A. P. Parkin [Canada]

Source :

RBID : PMC:4015329

Abstract

Camelina sativa is an oilseed with desirable agronomic and oil-quality attributes for a viable industrial oil platform crop. Here we generate the first chromosome-scale high-quality reference genome sequence for C. sativa and annotated 89,418 protein-coding genes, representing a whole-genome triplication event relative to the crucifer model Arabidopsis thaliana. C. sativa represents the first crop species to be sequenced from lineage I of the Brassicaceae. The well-preserved hexaploid genome structure of C. sativa surprisingly mirrors those of economically important amphidiploid Brassica crop species from lineage II as well as wheat and cotton. The three genomes of C. sativa show no evidence of fractionation bias and limited expression-level bias, both characteristics commonly associated with polyploid evolution. The highly undifferentiated polyploid genome of C. sativa presents significant consequences for breeding and genetic manipulation of this industrial oil crop.


Url:
DOI: 10.1038/ncomms4706
PubMed: 24759634
PubMed Central: 4015329

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PMC:4015329

Le document en format XML

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<title xml:lang="en" level="a" type="main">The emerging biofuel crop
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retains a highly undifferentiated hexaploid genome structure</title>
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S7N 0X2</nlm:aff>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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S7N 0W9</nlm:aff>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<name sortKey="Bollina, Venkatesh" sort="Bollina, Venkatesh" uniqKey="Bollina V" first="Venkatesh" last="Bollina">Venkatesh Bollina</name>
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S7N 0X2</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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, Galway,
<country>Ireland</country>
</nlm:aff>
<country xml:lang="fr">Irlande (pays)</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<name sortKey="Robinson, Stephen J" sort="Robinson, Stephen J" uniqKey="Robinson S" first="Stephen J." last="Robinson">Stephen J. Robinson</name>
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<institution>Saskatoon Research Centre, Agriculture and Agri-Food Canada</institution>
, 107 Science Place, Saskatoon, Saskatchewan,
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S7N 0X2</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<name sortKey="Links, Matthew G" sort="Links, Matthew G" uniqKey="Links M" first="Matthew G." last="Links">Matthew G. Links</name>
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<institution>Saskatoon Research Centre, Agriculture and Agri-Food Canada</institution>
, 107 Science Place, Saskatoon, Saskatchewan,
<country>Canada</country>
S7N 0X2</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<name sortKey="Clarke, Carling" sort="Clarke, Carling" uniqKey="Clarke C" first="Carling" last="Clarke">Carling Clarke</name>
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<nlm:aff id="a2">
<institution>National Research Council Canada</institution>
, 110 Gymnasium Place, Saskatoon, Saskatchewan,
<country>Canada</country>
S7N 0W9</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<name sortKey="Higgins, Erin E" sort="Higgins, Erin E" uniqKey="Higgins E" first="Erin E." last="Higgins">Erin E. Higgins</name>
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<country>Canada</country>
S7N 0X2</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<nlm:aff id="a1">
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, 107 Science Place, Saskatoon, Saskatchewan,
<country>Canada</country>
S7N 0X2</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<country>Canada</country>
S7N 0W9</nlm:aff>
<country xml:lang="fr">Canada</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<p>
<italic>Camelina sativa</italic>
is an oilseed with desirable agronomic and oil-quality attributes for a viable industrial oil platform crop. Here we generate the first chromosome-scale high-quality reference genome sequence for
<italic>C. sativa</italic>
and annotated 89,418 protein-coding genes, representing a whole-genome triplication event relative to the crucifer model
<italic>Arabidopsis thaliana</italic>
.
<italic>C. sativa</italic>
represents the first crop species to be sequenced from lineage I of the Brassicaceae. The well-preserved hexaploid genome structure of
<italic>C. sativa</italic>
surprisingly mirrors those of economically important amphidiploid
<italic>Brassica</italic>
crop species from lineage II as well as wheat and cotton. The three genomes of
<italic>C. sativa</italic>
show no evidence of fractionation bias and limited expression-level bias, both characteristics commonly associated with polyploid evolution. The highly undifferentiated polyploid genome of
<italic>C. sativa</italic>
presents significant consequences for breeding and genetic manipulation of this industrial oil crop.</p>
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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">Nat Commun</journal-id>
<journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id>
<journal-title-group>
<journal-title>Nature Communications</journal-title>
</journal-title-group>
<issn pub-type="epub">2041-1723</issn>
<publisher>
<publisher-name>Nature Pub. Group</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24759634</article-id>
<article-id pub-id-type="pmc">4015329</article-id>
<article-id pub-id-type="pii">ncomms4706</article-id>
<article-id pub-id-type="doi">10.1038/ncomms4706</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>The emerging biofuel crop
<italic>Camelina sativa</italic>
retains a highly undifferentiated hexaploid genome structure</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Kagale</surname>
<given-names>Sateesh</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Koh</surname>
<given-names>Chushin</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nixon</surname>
<given-names>John</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bollina</surname>
<given-names>Venkatesh</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Clarke</surname>
<given-names>Wayne E.</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tuteja</surname>
<given-names>Reetu</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Spillane</surname>
<given-names>Charles</given-names>
</name>
<xref ref-type="aff" rid="a3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Robinson</surname>
<given-names>Stephen J.</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Links</surname>
<given-names>Matthew G.</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Clarke</surname>
<given-names>Carling</given-names>
</name>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Higgins</surname>
<given-names>Erin E.</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Huebert</surname>
<given-names>Terry</given-names>
</name>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sharpe</surname>
<given-names>Andrew G.</given-names>
</name>
<xref ref-type="corresp" rid="c1">a</xref>
<xref ref-type="aff" rid="a2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Parkin</surname>
<given-names>Isobel A. P.</given-names>
</name>
<xref ref-type="corresp" rid="c2">b</xref>
<xref ref-type="aff" rid="a1">1</xref>
</contrib>
<aff id="a1">
<label>1</label>
<institution>Saskatoon Research Centre, Agriculture and Agri-Food Canada</institution>
, 107 Science Place, Saskatoon, Saskatchewan,
<country>Canada</country>
S7N 0X2</aff>
<aff id="a2">
<label>2</label>
<institution>National Research Council Canada</institution>
, 110 Gymnasium Place, Saskatoon, Saskatchewan,
<country>Canada</country>
S7N 0W9</aff>
<aff id="a3">
<label>3</label>
<institution>Plant and AgriBiosciences Centre (PABC), School of Natural Sciences, National University of Ireland Galway</institution>
, Galway,
<country>Ireland</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="c1">
<label>a</label>
<email>andrew.sharpe@nrc-cnrc.gc.ca</email>
</corresp>
<corresp id="c2">
<label>b</label>
<email>isobel.parkin@agr.gc.ca</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>23</day>
<month>04</month>
<year>2014</year>
</pub-date>
<volume>5</volume>
<elocation-id>3706</elocation-id>
<history>
<date date-type="received">
<day>06</day>
<month>01</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>21</day>
<month>03</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2014, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0/">
<pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/</license-p>
</license>
</permissions>
<abstract>
<p>
<italic>Camelina sativa</italic>
is an oilseed with desirable agronomic and oil-quality attributes for a viable industrial oil platform crop. Here we generate the first chromosome-scale high-quality reference genome sequence for
<italic>C. sativa</italic>
and annotated 89,418 protein-coding genes, representing a whole-genome triplication event relative to the crucifer model
<italic>Arabidopsis thaliana</italic>
.
<italic>C. sativa</italic>
represents the first crop species to be sequenced from lineage I of the Brassicaceae. The well-preserved hexaploid genome structure of
<italic>C. sativa</italic>
surprisingly mirrors those of economically important amphidiploid
<italic>Brassica</italic>
crop species from lineage II as well as wheat and cotton. The three genomes of
<italic>C. sativa</italic>
show no evidence of fractionation bias and limited expression-level bias, both characteristics commonly associated with polyploid evolution. The highly undifferentiated polyploid genome of
<italic>C. sativa</italic>
presents significant consequences for breeding and genetic manipulation of this industrial oil crop.</p>
</abstract>
<abstract abstract-type="web-summary">
<p>
<inline-graphic id="i1" xlink:href="ncomms4706-i1.jpg"></inline-graphic>
<italic>Camelina sativa</italic>
is an oilseed crop with important industrial applications. Here, the authors sequence the
<italic>C. sativa</italic>
genome to investigate the genome organization and evolution of this species, and to provide a valuable tool for genetic engineering and potential crop improvement.</p>
</abstract>
</article-meta>
</front>
<floats-group>
<fig id="f1">
<label>Figure 1</label>
<caption>
<title>The
<italic>Camelina sativa</italic>
genome.</title>
<p>From the outside ring to the centre: (1) the twenty
<italic>C. sativa</italic>
pseudochromosomes (Chr1–20 represented on Mb scale) are shown in different colours with putative centromeric regions indicated by black bands; (2) gene expression levels (log10(average FPKM), bin=250 Kb)), values range from 0 (yellow) to 3.92 (red); (3) the distribution of protein-coding regions (nucleotides per 500 Kb; orange) compared with repetitive sequences (nucleotides per 500 Kb; yellow); and (4)
<italic>Ka</italic>
/
<italic>Ks</italic>
ratios (median, bin=500 kb) of syntenic (blue) and non-syntenic (green) genes. The centre shows a graphical view of the triplicated segments of annotated genes connected with lines of colours matching those for the pseudochromosomes.</p>
</caption>
<graphic xlink:href="ncomms4706-f1"></graphic>
</fig>
<fig id="f2">
<label>Figure 2</label>
<caption>
<title>Comparison of gene number in
<italic>C. sativa</italic>
plotted against genome size with a subset of completely sequenced plant genomes (
<italic>N</italic>
=35).</title>
<p>The significance test for a single outlier in regression data was performed as described in detail in
<xref ref-type="supplementary-material" rid="S1">Supplementary Note 8</xref>
and the confidence intervals for the regression line are shown as dotted lines. Mes,
<italic>Manihot esculenta</italic>
; Rco,
<italic>Ricinus communis</italic>
; Lus,
<italic>Linum usitatissimum</italic>
; Ptr,
<italic>Populus trichocarpa</italic>
; Mtr,
<italic>Medicago truncatula</italic>
; Pvu,
<italic>Phaseolus vulgaris</italic>
; Gma,
<italic>Glycine max</italic>
; Csa,
<italic>Cucumis sativis</italic>
; Ppe,
<italic>Prunus persica</italic>
; Mdo,
<italic>Malus domestica</italic>
; Fve,
<italic>Fragaria vesca</italic>
; Ath,
<italic>Arabidopsis thaliana</italic>
; Aly,
<italic>Arabidopsis lyrata</italic>
; Csa,
<italic>Camelina sativa</italic>
; Cru,
<italic>Capsella rubella</italic>
; Bra,
<italic>Brassica rapa</italic>
; Tha,
<italic>Thellungiella halophila</italic>
; Cpa,
<italic>Carica papaya</italic>
; Gra,
<italic>Gossypium raimondii</italic>
; Tca,
<italic>Theobroma cacao</italic>
; Csi,
<italic>Citrus sinensis</italic>
; Egr,
<italic>Eucalyptus grandis</italic>
; Vvi,
<italic>Vitis vinifera</italic>
; Stu,
<italic>Solanum tuberosum</italic>
; Sly,
<italic>Solanum lycopersicum</italic>
; Mgu,
<italic>Mimulus guttatus</italic>
; Aco,
<italic>Aquilegia coerulea</italic>
; Sbi,
<italic>Sorghum bicolour</italic>
; Zma,
<italic>Zea mays</italic>
; Sit,
<italic>Setaria italica</italic>
; Pvi,
<italic>Panicum virgatum</italic>
; Osa,
<italic>Oryza sativa</italic>
; Bdi,
<italic>Brachypodium distachyon</italic>
; Smo,
<italic>Selaginella moellendorfii</italic>
; Ppa,
<italic>Physcomitrella patens</italic>
.</p>
</caption>
<graphic xlink:href="ncomms4706-f2"></graphic>
</fig>
<fig id="f3">
<label>Figure 3</label>
<caption>
<title>Comparative analysis and evolution of the
<italic>C. sativa</italic>
genome.</title>
<p>(
<bold>a</bold>
) MUMer plot comparing the
<italic>C. sativa</italic>
and
<italic>A. lyrata</italic>
genomes. Syntenic and collinear regions making the three complete sub-genomes in
<italic>C. sativa</italic>
are circled in red, blue and green. (
<bold>b</bold>
) Reconstruction of the three sub-genomes of
<italic>C. sativa.</italic>
Chromosome and ancestral genomic-block-level organization of the sub-genomes in
<italic>C. sativa</italic>
is shown. Based on synteny and collinearity between
<italic>C. sativa</italic>
and
<italic>Arabidopsis</italic>
species, and GB contiguity in the ancestral karyotype, pseudochromosomes were assigned to three sub-genomes in
<italic>C. sativa</italic>
. Each pseudochromosome was subdivided among ancestral genomic blocks (A–X), which are coloured based on their occurrence in the ACK. (
<bold>c</bold>
) ACK consisting of the 24 conserved genomic blocks (A–X). (
<bold>d</bold>
) The ancestral diploid karyotype (derivative of ACK) of
<italic>C. sativa</italic>
. (
<bold>e</bold>
) The presumed origin and reconstruction of the fusion chromosome (AK2/4) of the dACK.</p>
</caption>
<graphic xlink:href="ncomms4706-f3"></graphic>
</fig>
<fig id="f4">
<label>Figure 4</label>
<caption>
<title>Phylogenetic relationship between the three sub-genomes of
<italic>C. sativa</italic>
and lower-chromosome
<italic>Camelina</italic>
species.</title>
<p>A maximum-likelihood tree produced from a supermatrix constructed using 4,867 orthologous sequences. Clade support values near nodes represent bootstrap proportions in percentages. Branch lengths represent estimated nucleotide substitutions per site.</p>
</caption>
<graphic xlink:href="ncomms4706-f4"></graphic>
</fig>
<fig id="f5">
<label>Figure 5</label>
<caption>
<title>Age distribution of duplicated genes in
<italic>C. sativa</italic>
.</title>
<p>Gaussian mixture models fitted to frequency distributions of
<italic>K</italic>
s (synonymous substitution) values obtained by comparing pairs of paralogous (
<italic>C. sativa</italic>
—neopolyploidy) and orthologous (Sub-genomes 1/2/3
<italic>versus A. thaliana</italic>
) genes are shown. The mixture model analysis is described in
<xref ref-type="supplementary-material" rid="S1">Supplementary Note 9</xref>
and the complete list of Gaussian components is provided in
<xref ref-type="supplementary-material" rid="S1">Supplementary Table 23</xref>
.</p>
</caption>
<graphic xlink:href="ncomms4706-f5"></graphic>
</fig>
<fig id="f6">
<label>Figure 6</label>
<caption>
<title>Gene expression dynamics reveal genome dominance and functional diversification of
<italic>C. sativa</italic>
homeologous genes.</title>
<p>(
<bold>a</bold>
) Relationship between gene retention rate following whole-genome triplication and the gene expression levels. (
<bold>b</bold>
) Cumulative frequency of homeologous genes belonging to the three sub-genomes within
<italic>C. sativa</italic>
with highest expression across all tissue types.
<italic>P</italic>
values (ANOVA test for interaction,
<italic>N</italic>
=108 per gene triplet) were calculated for interaction between sub-genomes (G) and tissue-type (T) effects on expression. To highlight differences between sub-genomes only the subset of the data with
<italic>P</italic>
>10
<sup>−10</sup>
is shown. (
<bold>c</bold>
) Scatterplot showing the magnitude of interaction effect calculated as the s.d. from a random effects model estimate for G × T interaction variance. Homeologous triplets were classified into groups, no interaction (
<italic>P</italic>
>0.05; ANOVA test for interaction,
<italic>N</italic>
=108), negligible interaction (
<italic>P</italic>
<0.05 and STDEV(G × T)<0.25) and interaction (
<italic>P</italic>
<0.05 and STDEV(G × T)>0.25).</p>
</caption>
<graphic xlink:href="ncomms4706-f6"></graphic>
</fig>
<table-wrap position="float" id="t1">
<label>Table 1</label>
<caption>
<title>Incidence of expression and functional diversification of fully retained acyl-lipid metabolism related genes in
<italic>C. sativa</italic>
.</title>
</caption>
<table frame="hsides" rules="groups" border="1">
<colgroup>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom">
<tr>
<th align="left" valign="top" charoff="50"> </th>
<th align="center" valign="top" charoff="50">
<bold>All</bold>
</th>
<th align="center" valign="top" charoff="50">
<bold>Acyl-lipid metabolism</bold>
</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left" valign="top" charoff="50">Fully retained triplets</td>
<td align="center" valign="top" charoff="50">18,565</td>
<td align="center" valign="top" charoff="50">586</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">Significant expression divergence
<xref ref-type="fn" rid="t1-fn1">*</xref>
</td>
<td align="char" valign="top" char="(" charoff="50">14,391 (77.5%)</td>
<td align="char" valign="top" char="(" charoff="50">497 (84.8%)</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">Significant interaction effect
<xref ref-type="fn" rid="t1-fn2"></xref>
</td>
<td align="char" valign="top" char="(" charoff="50">4,106 (22.1%)</td>
<td align="char" valign="top" char="(" charoff="50">181 (30.9%)</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">Gene silencing</td>
<td align="char" valign="top" char="(" charoff="50">900 (4.8%)</td>
<td align="char" valign="top" char="(" charoff="50">23 (3.9%)</td>
</tr>
<tr>
<td align="left" valign="top" charoff="50">Functional divergence</td>
<td align="char" valign="top" char="(" charoff="50">2,603 (14.0%)</td>
<td align="char" valign="top" char="(" charoff="50">90 (15.4%)</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<fn id="t1-fn1">
<p>
<sup>*</sup>
G × T interaction;
<italic>P</italic>
<0.05 (ANOVA test for interaction); sample size
<italic>N</italic>
=108 per gene triplet (number of genes × number of tissue types (12) × number of replications (3)).</p>
</fn>
<fn id="t1-fn2">
<p>
<sup></sup>
<italic>P</italic>
<0.05 (ANOVA test for interaction); STDEV (G × T random effects)>0.25); sample size
<italic>N</italic>
=108 per gene triplet (number of genes × number of tissue types (12) × number of replications (3)).</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>

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