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Research ArticleResearch Article
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Different Gene Families in Arabidopsis thaliana Transposed in Different Epochs and at Different Frequencies throughout the Rosids

Margaret R. Woodhouse, Haibao Tang, Michael Freeling
Margaret R. Woodhouse
aDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720
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  • For correspondence: branwen@berkeley.edu
Haibao Tang
bJ. Craig Venter Institute, Rockville, Maryland 20850
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Michael Freeling
aDepartment of Plant and Microbial Biology, University of California, Berkeley, California 94720
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Published December 2011. DOI: https://doi.org/10.1105/tpc.111.093567

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  • Figure 1.
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    Figure 1.

    Using Comparative Genomics to Define Synteny and Collinearity.

    Some genes shared between related species are syntenic or colocalized on corresponding chromosomes. They can also be collinear, meaning they remain in similar chromosomal orders over time. In comparison to the ancestral genome, genomes A and B share some genes that are syntenic and collinear, though not always the same ones. Rectangular genes represent nonsyntenic genes. Notice that a gene can be syntenic without necessarily being collinear.

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    Figure 2.

    Cladogram of the Key Species Used in This Study: A. thaliana and A. lyrata, Papaya, Poplar, and Grape.

    (A) The genus Arabidopsis belongs in the order Brassicales, as does papaya. A. thaliana and A. lyrata diverged from each other ~10 MYA. Papaya and A. thaliana diverged from each other ~72 MYA. A. thaliana and poplar diverged ~100 MYA. Grape is the most distantly related outgroup from A. thaliana and diverged from A. thaliana ~111 MYA. The red star represents the α-duplication event that occurred 20 to 60 MYA (Paterson et al., 2010); the gray star represents an earlier genome duplication event from the α; the larger star is a paleohexaploidy. Citations are provided by Jiao et al. (2011).

    (B) The positional history timeline and the epochs in which each existing A. thaliana gene had transposed throughout the A. thaliana lineage. Three time points are represented: the A. thaliana ancestral genes that transposed after poplar split from the A. thaliana lineage 100 MYA (72 to 100 MYA epoch), genes that had transposed after papaya split from the A. thaliana lineage 72 MYA (10 to 72 MYA), and genes that had transposed after A. lyrata had split from A. thaliana (10 MYA).

    (C) Genes that had transposed prior to the α-duplication event in the A. thaliana lineage. The insertion event is represented by the yellow arrow; the inserted gene is represented by the yellow rectangle. After the α-duplication event (red star), the inserted gene is now duplicated in the A. thaliana lineage. Both copies of the transposed gene are unlikely to be retained.

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    Figure 3.

    Illustration of Different Scenarios When Classifying the Positional History for a Gene in Question (Colored in Green).

    A 40-gene window was centered on every query A. thaliana (TAIR9) gene to check for a syntenic region in each target genome. LASTZ (default parameters) were used to define anchors and required that the syntenic region to have at least four collinear anchors (out of 40 possible anchors) in the interval. Each query gene is categorized based on the flank anchors and more sensitive search on the tight interval as follows: gene match in the interval, syntenic (S) or not syntenic but have both flankers (F) or one flanker (G). Genes labeled as F are further validated as follows: BLAST matches (e.g., to noncoding sequences) in the interval (FB) and contains assembly gaps (Ns) in the interval (FN). Because the region between flankers is unsequenced (FN), we cannot determine whether or not there is a gene in that space that could be syntenic with the query gene.

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    Figure 4.

    The Epoch Specificities of the Major Gene Families That Tend to Transpose in the Rosids.

    This chart describes the percentage over or under (y axis) expected incidence of transposition for each gene family based on the data from Supplemental Table 2. Expect values are based on frequency of transposition for each epoch per genome. Genes encoding ECA1s, thionins, and defensins transpose within the <10 MYA epoch, though their relative undetectability in poplar does not preclude their having transposed in earlier epochs. Genes encoding AGL and terpene synthases transposed primarily in the <10 MYA epoch, but some transposition occurred in the 10 to 72 MYA epoch. DC1 genes transposed almost equally within the <10 and 10 to 72 MYA epochs. NBS-LRRs and F-box genes mostly transposed in the 10 to 72 MYA epoch but also transposed more recently. Genes encoding B3, self-incompatibility, CLE, meprin, TRAF, and LCR proteins transposed exclusively within the 10 to 72 MYA epoch. PPR genes transposed in both the 10 to 72 and 72 to 100 MYA epoch. ATCHX genes transposed almost exclusively in the 72 to 100 MYA epoch.

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    Figure 5.

    Gene Expansion in the 10 to 72 MYA Epoch Occurred during or after the WGD Events in A. thaliana.

    The increase in genes for most of these gene families occurred after the papaya ancestor diverged from the A. thaliana lineage but before A. lyrata diverged from A. thaliana, sometime during one or both of the WGDs (represented by the shaded area and the two stars). The exception is the CHX family of genes, which shows an increase in numbers of genes in poplar but not after. Most of these new genes in the A. thaliana lineage were not syntenic with papaya (see Supplemental Table 4 online).

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    Figure 6.

    The Major Transposition Events Studied.

    This figure places the transposition events per epoch at their appropriate points over evolutionary time. Most of the transposition events occurred after papaya diverged from the A. thaliana ancestor. This may be due to the genome duplication events giving rise to an increase in gene transposition generally.

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    Table 1.

    Gene Stability versus Homoeolog Retention and CNSs

    CategoryGenomeSyntenicNonsyntenicTransposedSyntenic (%)Nonsyntenic (%)Transposed (%)χ2 Syntenic/Nonsyntenicχ2 Transposed
    All21,66510,77010,8954,57549.70%50.30%21.00%n/an/a
    Homoeolog5,1933,5021,68938367.50%32.50%7.00%<0.0001<0.0001
    Single-copy6,0763,1772,89997052.30%47.70%16.00%0.0046<0.0001
    Total CNS4,5023,2391,26119071.90%28.00%4.20%<0.0001<0.0001
    Total 5′ CNS2,0321,4505828871.40%28.60%4.30%<0.00010.0003
    Total 3′ CNS7995622354270.30%29.40%5.30%<0.00010.175
    Total intronic CNS1,6711,2274445673.40%26.60%3.40%<0.0001<0.0001
    >5 CNSs8256052181573.30%26.40%1.80%<0.0001<0.0001
    <5 CNSs2,7351,89384812569.20%31.00%4.60%<0.00010.0002
    • The number of genes that are syntenic, nonsyntenic, and transposed in the genome, among genes with a homoeolog, among single-copy genes, and among genes with CNSs. χ2 for transposed homoeologs is based on the number of genes that have transposed in the genome. χ2 for total CNSs is based on the number of transposed genes that had a homoeolog. n/a, not applicable.

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    Table 2.

    Genes That Have Transposed with Their CNSs

    Query TAIRNo. of CNSs5′ CNSs3′ CNSsIntronic CNSsHomoeolog of Query TAIRTransposed Best Hit TAIRNo. of CNSs Retained by TransposedTransposed CNS PositionTransposed CNS Distance
    AT3G0566011AT5G27060AT2G1508015′<50 bp
    AT3G2889015′<50 bp
    AT3G1101015′<50 bp
    AT4G1382015′6 kb (separated by two genes)
    AT4G1388015′<50 bp
    AT5G0721011AT5G62110AT2G2707015′<50 bp
    AT1G6400022AT5G41570AT2G4613015′<50 bp
    AT1G0557011110AT2G31960AT5G368707IntronicIntronic
    AT1G21140321AT1G76800AT3G4366015′<50 bp
    AT3G2519015′<50 bp
    AT1G2116033AT1G76825AT2G277001IntronicIntronic
    AT1G767202IntronicIntronic
    AT1G2947011AT2G34300AT5G278001IntronicIntronic
    AT1G6340011AT5G41170AT1G1262015′5 kb (separated by a gene)
    AT4G31650523AT2G24650AT2G1399015′<50 bp
    AT4G0026015′1 kb
    AT2G2474815′800 bp
    AT1G2668015′1 kb
    AT4G3726012102AT2G23290AT3G5006025′300 bp, 100 bp
    AT3G5573015′600 bp
    AT5G1808011101AT3G03820near AT3G1382015′500 bp
    AT1G1180315′500 bp
    AT4G3885015′500 bp
    AT2G2120013′100 bp
    AT5G6694044AT3G50410AT4G3800015′<50 bp
    • The TAIR9 ID of the CNS-containing gene’s query sequence, its description, the numbers and types of CNSs it has, the TAIR ID of its homoeolog, the TAIR ID of its best hit, and the number, position, and distance of the best hit’s sequences corresponding to the query sequence’s CNSs. Most transposition events where a gene took with it a CNS from the donor site have taken or retained only one CNS. Most CNSs transposed are proximal to the 5′ start site. There are cases where one query gene has many possible best hits; the empty cells are placeholders.

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    Table 3.

    Transposed Genes Have a Smaller Functional Gene Space Than Stable Genes and Fewer Introns

    Functional Gene Space (bp)No. of Introns
    Position>3,0003,0002,0001,000<1,000>500<500Total≥1 Intron0 IntronsTotal
    Syntenous1,9681,8053,3133,0526245477710,7649,3961,22810,624
    % Syntenous18%17%31%28%6%5%1%–88.40%11.60%–
    Transposed3223218301,4571,6337688654,5632,4701,0683,538
    % Transposed7%7%18%32%36%17%19%–69.80%30.20%–
    • Functional gene space is defined as the gene itself as well as all regulatory regions as inferred from CNS positions upstream and downstream of the gene. Units are in base pairs. Based on TAIR9 exon annotation data, we found that 30% of transposed genes lack introns, in comparison to only 11.6% of stable genes that lack introns.

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    Table 4.

    The Subclass Specificity of Gene Transposition within Three Representative Gene Families

    Gene FamilyTotalSyntenicNonsyntenicTransposed
    B391341443
    ARF211119
    REM5171232
    Other191612
    ATCHX2871110
    Pollen213910
    Roots8512
    Leaves11533
    • Shown are the different classes within each gene family and the number of genes total, the number of syntenic genes, the number of nonsyntenic genes, and the number of transposed genes for each class for which there was available data. In B3 genes, REM-type genes disproportionately transpose (Swaminathan et al., 2008); for ATCHX genes, all transposed genes are associated with strong pollen expression. Most syntenic genes are associated with leaf and root expression (Sze et al., 2004).

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    • Supplemental Dataset 2
    • Supplemental Dataset 3

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Different Gene Families in Arabidopsis thaliana Transposed in Different Epochs and at Different Frequencies throughout the Rosids
Margaret R. Woodhouse, Haibao Tang, Michael Freeling
The Plant Cell Dec 2011, 23 (12) 4241-4253; DOI: 10.1105/tpc.111.093567

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Different Gene Families in Arabidopsis thaliana Transposed in Different Epochs and at Different Frequencies throughout the Rosids
Margaret R. Woodhouse, Haibao Tang, Michael Freeling
The Plant Cell Dec 2011, 23 (12) 4241-4253; DOI: 10.1105/tpc.111.093567
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