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Consequences of lineage-specific gene loss on functional evolution of surviving paralogs: ALDH1A and retinoic acid signaling in vertebrate genomes.

Cañestro C, Catchen JM, Rodríguez-Marí A, Yokoi H, Postlethwait JH - PLoS Genet. (2009)

Bottom Line: Interestingly, results revealed asymmetric distribution of surviving ohnologs between co-orthologous teleost chromosome segments, suggesting that local genome architecture can influence ohnolog survival.We propose a model that reconstructs the chromosomal history of the Aldh1a family in the ancestral vertebrate genome, coupled with the evolution of gene functions in surviving Aldh1a ohnologs after R1, R2, and R3 genome duplications.Results provide evidence for early subfunctionalization and late subfunction-partitioning and suggest a mechanistic model based on altered regulation leading to heterochronic gene expression to explain the acquisition or modification of subfunctions by surviving ohnologs that preserve unaltered ancestral developmental programs in the face of gene loss.

View Article: PubMed Central - PubMed

Affiliation: Institute of Neuroscience, University of Oregon, Eugene, OR, USA.

ABSTRACT
Genome duplications increase genetic diversity and may facilitate the evolution of gene subfunctions. Little attention, however, has focused on the evolutionary impact of lineage-specific gene loss. Here, we show that identifying lineage-specific gene loss after genome duplication is important for understanding the evolution of gene subfunctions in surviving paralogs and for improving functional connectivity among human and model organism genomes. We examine the general principles of gene loss following duplication, coupled with expression analysis of the retinaldehyde dehydrogenase Aldh1a gene family during retinoic acid signaling in eye development as a case study. Humans have three ALDH1A genes, but teleosts have just one or two. We used comparative genomics and conserved syntenies to identify loss of ohnologs (paralogs derived from genome duplication) and to clarify uncertain phylogenies. Analysis showed that Aldh1a1 and Aldh1a2 form a clade that is sister to Aldh1a3-related genes. Genome comparisons showed secondarily loss of aldh1a1 in teleosts, revealing that Aldh1a1 is not a tetrapod innovation and that aldh1a3 was recently lost in medaka, making it the first known vertebrate with a single aldh1a gene. Interestingly, results revealed asymmetric distribution of surviving ohnologs between co-orthologous teleost chromosome segments, suggesting that local genome architecture can influence ohnolog survival. We propose a model that reconstructs the chromosomal history of the Aldh1a family in the ancestral vertebrate genome, coupled with the evolution of gene functions in surviving Aldh1a ohnologs after R1, R2, and R3 genome duplications. Results provide evidence for early subfunctionalization and late subfunction-partitioning and suggest a mechanistic model based on altered regulation leading to heterochronic gene expression to explain the acquisition or modification of subfunctions by surviving ohnologs that preserve unaltered ancestral developmental programs in the face of gene loss.

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Consequences of lineage-specific gene loss on functional evolution of surviving paralogs.(A) Evolutionary model reconstructing the evolution of Aldh1a gene subfunctions in the developing retina. Mechanisms of early subfunctionalization, late subfunction partitioning, and acquisition or modification of ancestral subfunctions associated to events of gene duplication or gene loss (dotted lines) are indicated in the horizontal plane of a three-dimensional tree, in which events of vertebrate diversification are indicated in the vertical plane. A schematic retina at the stage of complete cup invagination represents dorso ventral (DV) expression domains of Aldh1a genes in different colors is indicated for present species and inferred for ancestral conditions. Bars indicate co-expression in the same dorso-ventral domains (or expression of ancestral genes), and dots refer to weak or remaining expression from earlier developmental stages. Aldh1a1: red, Aldh1a2: blue and Aldh1a3: green. Aldh1a expression data have been obtained from [58], [65], [69], [77], [79], [80], [84]–[87], [111]–[120] and this work Figure 6B). (B) Evolutionary mechanistic model to explain how the ancestral developmental program can remain unaltered after gene loss. This general model, extrapolated from our findings on the evolution of the expression of Aldh1a paralogs during eye development, is based on how heterochronic expression could facilitate the loss of a paralog, while leading to an apparent shuffling of functions between a lost paralog and a surviving paralog without the gain of new regulatory elements, but the loss of negative regulators.
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pgen-1000496-g008: Consequences of lineage-specific gene loss on functional evolution of surviving paralogs.(A) Evolutionary model reconstructing the evolution of Aldh1a gene subfunctions in the developing retina. Mechanisms of early subfunctionalization, late subfunction partitioning, and acquisition or modification of ancestral subfunctions associated to events of gene duplication or gene loss (dotted lines) are indicated in the horizontal plane of a three-dimensional tree, in which events of vertebrate diversification are indicated in the vertical plane. A schematic retina at the stage of complete cup invagination represents dorso ventral (DV) expression domains of Aldh1a genes in different colors is indicated for present species and inferred for ancestral conditions. Bars indicate co-expression in the same dorso-ventral domains (or expression of ancestral genes), and dots refer to weak or remaining expression from earlier developmental stages. Aldh1a1: red, Aldh1a2: blue and Aldh1a3: green. Aldh1a expression data have been obtained from [58], [65], [69], [77], [79], [80], [84]–[87], [111]–[120] and this work Figure 6B). (B) Evolutionary mechanistic model to explain how the ancestral developmental program can remain unaltered after gene loss. This general model, extrapolated from our findings on the evolution of the expression of Aldh1a paralogs during eye development, is based on how heterochronic expression could facilitate the loss of a paralog, while leading to an apparent shuffling of functions between a lost paralog and a surviving paralog without the gain of new regulatory elements, but the loss of negative regulators.

Mentions: The finding of the loss of aldh1a3 in medaka makes this organism the first known vertebrate with a single surviving Aldh1a paralog (i.e. aldh1a2), and made us wonder about the functional implications of gene loss. As a measure of gene function, consider expression patterns of Aldh1a genes. In the developing retina of mouse, frog, zebrafish and medaka, Aldh1a genes are expressed in a dorsal sector and in a ventral sector at the completion of optic cup invagination (about E11.5 in mouse, stage 35 in frog, and 1.5 days post fertilization in zebrafish and medaka; Figure 8A). Different vertebrates express different Aldh1a genes in different dorso-ventral sectors of the eye. The right column of Figure 8 summarizes the main expression patterns of the Aldh1a family in the retina of different animals (Aldh1a1 in red, Aldh1a2 in blue, and Aldh1a3 in green). Aldh1a paralogs expressed in the dorsal sector of the retina include Aldh1a1 (but not Aldh1a2) in mouse; both Aldh1a1 and Aldh1a2 in frogs and birds (e.g. chicken and quail, not included in Figure 8A for simplicity); and Aldh1a2 (but not Aldh1a1) in teleosts (e.g. zebrafish and medaka). The main Aldh1a paralog expressed in the ventral sector of the retina is Aldh1a3 both in tetrapods (e.g. mouse, frog and birds) and in at least one teleost (e.g. zebrafish). In contrast, in medaka, which lacks an aldh1a3 paralog, we found strong expression of aldh1a2 ventrally (Figure 6). Dotted regions depict weak expression of Aldh1a genes in a small part of each dorso-ventral sector or from earlier developmental stages prior to the complete invagination of the optic cup in Figure 8A.


Consequences of lineage-specific gene loss on functional evolution of surviving paralogs: ALDH1A and retinoic acid signaling in vertebrate genomes.

Cañestro C, Catchen JM, Rodríguez-Marí A, Yokoi H, Postlethwait JH - PLoS Genet. (2009)

Consequences of lineage-specific gene loss on functional evolution of surviving paralogs.(A) Evolutionary model reconstructing the evolution of Aldh1a gene subfunctions in the developing retina. Mechanisms of early subfunctionalization, late subfunction partitioning, and acquisition or modification of ancestral subfunctions associated to events of gene duplication or gene loss (dotted lines) are indicated in the horizontal plane of a three-dimensional tree, in which events of vertebrate diversification are indicated in the vertical plane. A schematic retina at the stage of complete cup invagination represents dorso ventral (DV) expression domains of Aldh1a genes in different colors is indicated for present species and inferred for ancestral conditions. Bars indicate co-expression in the same dorso-ventral domains (or expression of ancestral genes), and dots refer to weak or remaining expression from earlier developmental stages. Aldh1a1: red, Aldh1a2: blue and Aldh1a3: green. Aldh1a expression data have been obtained from [58], [65], [69], [77], [79], [80], [84]–[87], [111]–[120] and this work Figure 6B). (B) Evolutionary mechanistic model to explain how the ancestral developmental program can remain unaltered after gene loss. This general model, extrapolated from our findings on the evolution of the expression of Aldh1a paralogs during eye development, is based on how heterochronic expression could facilitate the loss of a paralog, while leading to an apparent shuffling of functions between a lost paralog and a surviving paralog without the gain of new regulatory elements, but the loss of negative regulators.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2682703&req=5

pgen-1000496-g008: Consequences of lineage-specific gene loss on functional evolution of surviving paralogs.(A) Evolutionary model reconstructing the evolution of Aldh1a gene subfunctions in the developing retina. Mechanisms of early subfunctionalization, late subfunction partitioning, and acquisition or modification of ancestral subfunctions associated to events of gene duplication or gene loss (dotted lines) are indicated in the horizontal plane of a three-dimensional tree, in which events of vertebrate diversification are indicated in the vertical plane. A schematic retina at the stage of complete cup invagination represents dorso ventral (DV) expression domains of Aldh1a genes in different colors is indicated for present species and inferred for ancestral conditions. Bars indicate co-expression in the same dorso-ventral domains (or expression of ancestral genes), and dots refer to weak or remaining expression from earlier developmental stages. Aldh1a1: red, Aldh1a2: blue and Aldh1a3: green. Aldh1a expression data have been obtained from [58], [65], [69], [77], [79], [80], [84]–[87], [111]–[120] and this work Figure 6B). (B) Evolutionary mechanistic model to explain how the ancestral developmental program can remain unaltered after gene loss. This general model, extrapolated from our findings on the evolution of the expression of Aldh1a paralogs during eye development, is based on how heterochronic expression could facilitate the loss of a paralog, while leading to an apparent shuffling of functions between a lost paralog and a surviving paralog without the gain of new regulatory elements, but the loss of negative regulators.
Mentions: The finding of the loss of aldh1a3 in medaka makes this organism the first known vertebrate with a single surviving Aldh1a paralog (i.e. aldh1a2), and made us wonder about the functional implications of gene loss. As a measure of gene function, consider expression patterns of Aldh1a genes. In the developing retina of mouse, frog, zebrafish and medaka, Aldh1a genes are expressed in a dorsal sector and in a ventral sector at the completion of optic cup invagination (about E11.5 in mouse, stage 35 in frog, and 1.5 days post fertilization in zebrafish and medaka; Figure 8A). Different vertebrates express different Aldh1a genes in different dorso-ventral sectors of the eye. The right column of Figure 8 summarizes the main expression patterns of the Aldh1a family in the retina of different animals (Aldh1a1 in red, Aldh1a2 in blue, and Aldh1a3 in green). Aldh1a paralogs expressed in the dorsal sector of the retina include Aldh1a1 (but not Aldh1a2) in mouse; both Aldh1a1 and Aldh1a2 in frogs and birds (e.g. chicken and quail, not included in Figure 8A for simplicity); and Aldh1a2 (but not Aldh1a1) in teleosts (e.g. zebrafish and medaka). The main Aldh1a paralog expressed in the ventral sector of the retina is Aldh1a3 both in tetrapods (e.g. mouse, frog and birds) and in at least one teleost (e.g. zebrafish). In contrast, in medaka, which lacks an aldh1a3 paralog, we found strong expression of aldh1a2 ventrally (Figure 6). Dotted regions depict weak expression of Aldh1a genes in a small part of each dorso-ventral sector or from earlier developmental stages prior to the complete invagination of the optic cup in Figure 8A.

Bottom Line: Interestingly, results revealed asymmetric distribution of surviving ohnologs between co-orthologous teleost chromosome segments, suggesting that local genome architecture can influence ohnolog survival.We propose a model that reconstructs the chromosomal history of the Aldh1a family in the ancestral vertebrate genome, coupled with the evolution of gene functions in surviving Aldh1a ohnologs after R1, R2, and R3 genome duplications.Results provide evidence for early subfunctionalization and late subfunction-partitioning and suggest a mechanistic model based on altered regulation leading to heterochronic gene expression to explain the acquisition or modification of subfunctions by surviving ohnologs that preserve unaltered ancestral developmental programs in the face of gene loss.

View Article: PubMed Central - PubMed

Affiliation: Institute of Neuroscience, University of Oregon, Eugene, OR, USA.

ABSTRACT
Genome duplications increase genetic diversity and may facilitate the evolution of gene subfunctions. Little attention, however, has focused on the evolutionary impact of lineage-specific gene loss. Here, we show that identifying lineage-specific gene loss after genome duplication is important for understanding the evolution of gene subfunctions in surviving paralogs and for improving functional connectivity among human and model organism genomes. We examine the general principles of gene loss following duplication, coupled with expression analysis of the retinaldehyde dehydrogenase Aldh1a gene family during retinoic acid signaling in eye development as a case study. Humans have three ALDH1A genes, but teleosts have just one or two. We used comparative genomics and conserved syntenies to identify loss of ohnologs (paralogs derived from genome duplication) and to clarify uncertain phylogenies. Analysis showed that Aldh1a1 and Aldh1a2 form a clade that is sister to Aldh1a3-related genes. Genome comparisons showed secondarily loss of aldh1a1 in teleosts, revealing that Aldh1a1 is not a tetrapod innovation and that aldh1a3 was recently lost in medaka, making it the first known vertebrate with a single aldh1a gene. Interestingly, results revealed asymmetric distribution of surviving ohnologs between co-orthologous teleost chromosome segments, suggesting that local genome architecture can influence ohnolog survival. We propose a model that reconstructs the chromosomal history of the Aldh1a family in the ancestral vertebrate genome, coupled with the evolution of gene functions in surviving Aldh1a ohnologs after R1, R2, and R3 genome duplications. Results provide evidence for early subfunctionalization and late subfunction-partitioning and suggest a mechanistic model based on altered regulation leading to heterochronic gene expression to explain the acquisition or modification of subfunctions by surviving ohnologs that preserve unaltered ancestral developmental programs in the face of gene loss.

Show MeSH
Related in: MedlinePlus