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Evolutionary origins of Brassicaceae specific genes in Arabidopsis thaliana.

Donoghue MT, Keshavaiah C, Swamidatta SH, Spillane C - BMC Evol. Biol. (2011)

Bottom Line: Over half of the subset of the 958 lineage-specific genes found only in Arabidopsis thaliana have alignments to intergenic regions in Arabidopsis lyrata, consistent with either de novo origination or differential gene loss and retention, with both evolutionary scenarios explaining the lineage-specific status of these genes.This study comprehensively identifies all of the Brassicaceae-specific genes in Arabidopsis thaliana and identifies how the majority of such lineage-specific genes have arisen.Insights regarding the functional roles of lineage-specific genes are further advanced through identification of enrichment for stress responsiveness in lineage-specific genes, highlighting their likely importance for environmental adaptation strategies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, University College Cork, Cork, Ireland.

ABSTRACT

Background: All sequenced genomes contain a proportion of lineage-specific genes, which exhibit no sequence similarity to any genes outside the lineage. Despite their prevalence, the origins and functions of most lineage-specific genes remain largely unknown. As more genomes are sequenced opportunities for understanding evolutionary origins and functions of lineage-specific genes are increasing.

Results: This study provides a comprehensive analysis of the origins of lineage-specific genes (LSGs) in Arabidopsis thaliana that are restricted to the Brassicaceae family. In this study, lineage-specific genes within the nuclear (1761 genes) and mitochondrial (28 genes) genomes are identified. The evolutionary origins of two thirds of the lineage-specific genes within the Arabidopsis thaliana genome are also identified. Almost a quarter of lineage-specific genes originate from non-lineage-specific paralogs, while the origins of ~10% of lineage-specific genes are partly derived from DNA exapted from transposable elements (twice the proportion observed for non-lineage-specific genes). Lineage-specific genes are also enriched in genes that have overlapping CDS, which is consistent with such novel genes arising from overprinting. Over half of the subset of the 958 lineage-specific genes found only in Arabidopsis thaliana have alignments to intergenic regions in Arabidopsis lyrata, consistent with either de novo origination or differential gene loss and retention, with both evolutionary scenarios explaining the lineage-specific status of these genes. A smaller number of lineage-specific genes with an incomplete open reading frame across different Arabidopsis thaliana accessions are further identified as accession-specific genes, most likely of recent origin in Arabidopsis thaliana. Putative de novo origination for two of the Arabidopsis thaliana-only genes is identified via additional sequencing across accessions of Arabidopsis thaliana and closely related sister species lineages. We demonstrate that lineage-specific genes have high tissue specificity and low expression levels across multiple tissues and developmental stages. Finally, stress responsiveness is identified as a distinct feature of Brassicaceae-specific genes; where these LSGs are enriched for genes responsive to a wide range of abiotic stresses.

Conclusion: Improving our understanding of the origins of lineage-specific genes is key to gaining insights regarding how novel genes can arise and acquire functionality in different lineages. This study comprehensively identifies all of the Brassicaceae-specific genes in Arabidopsis thaliana and identifies how the majority of such lineage-specific genes have arisen. The analysis allows the relative importance (and prevalence) of different evolutionary routes to the genesis of novel ORFs within lineages to be assessed. Insights regarding the functional roles of lineage-specific genes are further advanced through identification of enrichment for stress responsiveness in lineage-specific genes, highlighting their likely importance for environmental adaptation strategies.

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Tissue expression patterns in LSGs and non-LSGs. a) Distribution of the number of tissues/developmental-stage each gene called as present (expressed) in the AtGenExpress developmental series microarray experiment (see methods). White bars represent all representative gene models tested. Light gray bars represent non-LSGs. Dark gray bars represent LSGs. b) Distribution of log2 median expression of genes called as present for each tissue/developmental stage in the AtGenExpress developmental series microarray experiment.
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Figure 5: Tissue expression patterns in LSGs and non-LSGs. a) Distribution of the number of tissues/developmental-stage each gene called as present (expressed) in the AtGenExpress developmental series microarray experiment (see methods). White bars represent all representative gene models tested. Light gray bars represent non-LSGs. Dark gray bars represent LSGs. b) Distribution of log2 median expression of genes called as present for each tissue/developmental stage in the AtGenExpress developmental series microarray experiment.

Mentions: To test whether LSGs in Arabidopsis thaliana display any distinct signature expression patterns, the expression patterns of 497 LSGs (with unique probesets on the affymetrix Ath1 microarray) were identified using the AtGenExpress developmental and stress series array datasets [59]. The expression patterns investigated were; (a) tissue specificity, (b) overall expression level, and (c) stress response. Tissue and developmental specificity was defined as the number of tissues and/or developmental stages that a gene was expressed using a gene expression present or absent call (i.e. present = expressed, absent = not expressed). LSGs and non-LSGs were compared by the percentage of each group that was expressed in n number of tissues. LSGs display greater tissue/developmental stage specificity compared to non-LSGs. The median number of tissues/developmental stages non-LSGs are expressed is 51 ± 18.5 compared to 4 ± 11.0 for LSGs. 52.72% of LSGs are expressed in four or fewer tissues/developmental stages, in comparison only 1.27% of non-LSGs are expressed in four or less tissues/developmental stages (Figure 5.a).


Evolutionary origins of Brassicaceae specific genes in Arabidopsis thaliana.

Donoghue MT, Keshavaiah C, Swamidatta SH, Spillane C - BMC Evol. Biol. (2011)

Tissue expression patterns in LSGs and non-LSGs. a) Distribution of the number of tissues/developmental-stage each gene called as present (expressed) in the AtGenExpress developmental series microarray experiment (see methods). White bars represent all representative gene models tested. Light gray bars represent non-LSGs. Dark gray bars represent LSGs. b) Distribution of log2 median expression of genes called as present for each tissue/developmental stage in the AtGenExpress developmental series microarray experiment.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3049755&req=5

Figure 5: Tissue expression patterns in LSGs and non-LSGs. a) Distribution of the number of tissues/developmental-stage each gene called as present (expressed) in the AtGenExpress developmental series microarray experiment (see methods). White bars represent all representative gene models tested. Light gray bars represent non-LSGs. Dark gray bars represent LSGs. b) Distribution of log2 median expression of genes called as present for each tissue/developmental stage in the AtGenExpress developmental series microarray experiment.
Mentions: To test whether LSGs in Arabidopsis thaliana display any distinct signature expression patterns, the expression patterns of 497 LSGs (with unique probesets on the affymetrix Ath1 microarray) were identified using the AtGenExpress developmental and stress series array datasets [59]. The expression patterns investigated were; (a) tissue specificity, (b) overall expression level, and (c) stress response. Tissue and developmental specificity was defined as the number of tissues and/or developmental stages that a gene was expressed using a gene expression present or absent call (i.e. present = expressed, absent = not expressed). LSGs and non-LSGs were compared by the percentage of each group that was expressed in n number of tissues. LSGs display greater tissue/developmental stage specificity compared to non-LSGs. The median number of tissues/developmental stages non-LSGs are expressed is 51 ± 18.5 compared to 4 ± 11.0 for LSGs. 52.72% of LSGs are expressed in four or fewer tissues/developmental stages, in comparison only 1.27% of non-LSGs are expressed in four or less tissues/developmental stages (Figure 5.a).

Bottom Line: Over half of the subset of the 958 lineage-specific genes found only in Arabidopsis thaliana have alignments to intergenic regions in Arabidopsis lyrata, consistent with either de novo origination or differential gene loss and retention, with both evolutionary scenarios explaining the lineage-specific status of these genes.This study comprehensively identifies all of the Brassicaceae-specific genes in Arabidopsis thaliana and identifies how the majority of such lineage-specific genes have arisen.Insights regarding the functional roles of lineage-specific genes are further advanced through identification of enrichment for stress responsiveness in lineage-specific genes, highlighting their likely importance for environmental adaptation strategies.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, University College Cork, Cork, Ireland.

ABSTRACT

Background: All sequenced genomes contain a proportion of lineage-specific genes, which exhibit no sequence similarity to any genes outside the lineage. Despite their prevalence, the origins and functions of most lineage-specific genes remain largely unknown. As more genomes are sequenced opportunities for understanding evolutionary origins and functions of lineage-specific genes are increasing.

Results: This study provides a comprehensive analysis of the origins of lineage-specific genes (LSGs) in Arabidopsis thaliana that are restricted to the Brassicaceae family. In this study, lineage-specific genes within the nuclear (1761 genes) and mitochondrial (28 genes) genomes are identified. The evolutionary origins of two thirds of the lineage-specific genes within the Arabidopsis thaliana genome are also identified. Almost a quarter of lineage-specific genes originate from non-lineage-specific paralogs, while the origins of ~10% of lineage-specific genes are partly derived from DNA exapted from transposable elements (twice the proportion observed for non-lineage-specific genes). Lineage-specific genes are also enriched in genes that have overlapping CDS, which is consistent with such novel genes arising from overprinting. Over half of the subset of the 958 lineage-specific genes found only in Arabidopsis thaliana have alignments to intergenic regions in Arabidopsis lyrata, consistent with either de novo origination or differential gene loss and retention, with both evolutionary scenarios explaining the lineage-specific status of these genes. A smaller number of lineage-specific genes with an incomplete open reading frame across different Arabidopsis thaliana accessions are further identified as accession-specific genes, most likely of recent origin in Arabidopsis thaliana. Putative de novo origination for two of the Arabidopsis thaliana-only genes is identified via additional sequencing across accessions of Arabidopsis thaliana and closely related sister species lineages. We demonstrate that lineage-specific genes have high tissue specificity and low expression levels across multiple tissues and developmental stages. Finally, stress responsiveness is identified as a distinct feature of Brassicaceae-specific genes; where these LSGs are enriched for genes responsive to a wide range of abiotic stresses.

Conclusion: Improving our understanding of the origins of lineage-specific genes is key to gaining insights regarding how novel genes can arise and acquire functionality in different lineages. This study comprehensively identifies all of the Brassicaceae-specific genes in Arabidopsis thaliana and identifies how the majority of such lineage-specific genes have arisen. The analysis allows the relative importance (and prevalence) of different evolutionary routes to the genesis of novel ORFs within lineages to be assessed. Insights regarding the functional roles of lineage-specific genes are further advanced through identification of enrichment for stress responsiveness in lineage-specific genes, highlighting their likely importance for environmental adaptation strategies.

Show MeSH
Related in: MedlinePlus