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Transducin duplicates in the zebrafish retina and pineal complex: differential specialisation after the teleost tetraploidisation.

Lagman D, Callado-Pérez A, Franzén IE, Larhammar D, Abalo XM - PLoS ONE (2015)

Bottom Line: We describe here the results of 350 million years of evolution of three functionally related gene families: the alpha, beta and gamma subunits of transducins, the G protein involved in vision.These retina-pineal distinctions presumably reflect their distinct functional roles in vision and circadian rhythmicity.In summary, this study describes several functional differences between transducin gene duplicates resulting from the teleost-specific tetraploidisation.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

ABSTRACT
Gene duplications provide raw materials that can be selected for functional adaptations by evolutionary mechanisms. We describe here the results of 350 million years of evolution of three functionally related gene families: the alpha, beta and gamma subunits of transducins, the G protein involved in vision. Early vertebrate tetraploidisations resulted in separate transducin heterotrimers: gnat1/gnb1/gngt1 for rods, and gnat2/gnb3/gngt2 for cones. The teleost-specific tetraploidisation generated additional duplicates for gnb1, gnb3 and gngt2. We report here that the duplicates have undergone several types of subfunctionalisation or neofunctionalisation in the zebrafish. We have found that gnb1a and gnb1b are co-expressed at different levels in rods; gnb3a and gnb3b have undergone compartmentalisation restricting gnb3b to the dorsal and medial retina, however, gnb3a expression was detected only at very low levels in both larvae and adult retina; gngt2b expression is restricted to the dorsal and medial retina, whereas gngt2a is expressed ventrally. This dorsoventral distinction could be an adaptation to protect the lower part of the retina from intense light damage. The ontogenetic analysis shows earlier onset of expression in the pineal complex than in the retina, in accordance with its earlier maturation. Additionally, gnb1a but not gnb1b is expressed in the pineal complex, and gnb3b and gngt2b are transiently expressed in the pineal during ontogeny, thus showing partial temporal subfunctionalisation. These retina-pineal distinctions presumably reflect their distinct functional roles in vision and circadian rhythmicity. In summary, this study describes several functional differences between transducin gene duplicates resulting from the teleost-specific tetraploidisation.

No MeSH data available.


Related in: MedlinePlus

Expression patterns of each transducin subunit gene in the adult zebrafish retina.Nomarski contrast photomicrographs from radial sections of adult zebrafish retina showing the expression of all the transducin mRNAs. Panels A, C, D and G show the rod-specific expression of gnat1, gnb1a, gnb1b and gngt1, respectively. Their expression is observed in the rod nuclei of the rONL, but the strongest staining is observed in their myoids, which are embedded in the cONL sublayer (thin arrows). Panels B, F, H and I show the expression of gnat2, gnb3b, gngt2a and gngt2b, respectively, in all cones: DC (arrowheads), LSC (asterisks) and SSC (stars). The brown retinal pigment epithelium is shown the uppermost part for each picture. The stratification of the outer retina is evident in all panels except H, due to the exclusive ventral expression of gngt2a, where the stratification becomes unclear. Panel E shows the lack of staining in the adult retina for the gnb3a gene. Note that the weaker stained band into the ONLc for the cone-specific transducin subunits (thick arrows) corresponds to the rods’ myoid position (thin arrows in rods photomicrographs). Scale bar in panel A: 50 μm. For abbreviations see Fig. 2 legend.
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pone.0121330.g003: Expression patterns of each transducin subunit gene in the adult zebrafish retina.Nomarski contrast photomicrographs from radial sections of adult zebrafish retina showing the expression of all the transducin mRNAs. Panels A, C, D and G show the rod-specific expression of gnat1, gnb1a, gnb1b and gngt1, respectively. Their expression is observed in the rod nuclei of the rONL, but the strongest staining is observed in their myoids, which are embedded in the cONL sublayer (thin arrows). Panels B, F, H and I show the expression of gnat2, gnb3b, gngt2a and gngt2b, respectively, in all cones: DC (arrowheads), LSC (asterisks) and SSC (stars). The brown retinal pigment epithelium is shown the uppermost part for each picture. The stratification of the outer retina is evident in all panels except H, due to the exclusive ventral expression of gngt2a, where the stratification becomes unclear. Panel E shows the lack of staining in the adult retina for the gnb3a gene. Note that the weaker stained band into the ONLc for the cone-specific transducin subunits (thick arrows) corresponds to the rods’ myoid position (thin arrows in rods photomicrographs). Scale bar in panel A: 50 μm. For abbreviations see Fig. 2 legend.

Mentions: The presence in the zebrafish genome of all the transducin genes: gnat1, gnat2, gnb1a, gnb1b, gnb3a, gnb3b, gngt1, gngt2a and gngt2b was verified by PCR using genomic DNA and the 3´UTR primers designed for each gene (see Table 1). The same primers were also used to investigate the transducin gene expression in the retina by RT-PCR using retina cDNA and confirmed that all transducin genes, except gnb3a, are transcribed in the retina. Subsequently, subtype-specific antisense DIG/FITC-labelled riboprobes were used in ISH. Positive staining was observed in the outer retina for all the genes, with the exception of gnb3a (Fig. 3). Some of the mRNAs were also detected in the pineal complex (see description below), but not in any other part of the head.


Transducin duplicates in the zebrafish retina and pineal complex: differential specialisation after the teleost tetraploidisation.

Lagman D, Callado-Pérez A, Franzén IE, Larhammar D, Abalo XM - PLoS ONE (2015)

Expression patterns of each transducin subunit gene in the adult zebrafish retina.Nomarski contrast photomicrographs from radial sections of adult zebrafish retina showing the expression of all the transducin mRNAs. Panels A, C, D and G show the rod-specific expression of gnat1, gnb1a, gnb1b and gngt1, respectively. Their expression is observed in the rod nuclei of the rONL, but the strongest staining is observed in their myoids, which are embedded in the cONL sublayer (thin arrows). Panels B, F, H and I show the expression of gnat2, gnb3b, gngt2a and gngt2b, respectively, in all cones: DC (arrowheads), LSC (asterisks) and SSC (stars). The brown retinal pigment epithelium is shown the uppermost part for each picture. The stratification of the outer retina is evident in all panels except H, due to the exclusive ventral expression of gngt2a, where the stratification becomes unclear. Panel E shows the lack of staining in the adult retina for the gnb3a gene. Note that the weaker stained band into the ONLc for the cone-specific transducin subunits (thick arrows) corresponds to the rods’ myoid position (thin arrows in rods photomicrographs). Scale bar in panel A: 50 μm. For abbreviations see Fig. 2 legend.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4373759&req=5

pone.0121330.g003: Expression patterns of each transducin subunit gene in the adult zebrafish retina.Nomarski contrast photomicrographs from radial sections of adult zebrafish retina showing the expression of all the transducin mRNAs. Panels A, C, D and G show the rod-specific expression of gnat1, gnb1a, gnb1b and gngt1, respectively. Their expression is observed in the rod nuclei of the rONL, but the strongest staining is observed in their myoids, which are embedded in the cONL sublayer (thin arrows). Panels B, F, H and I show the expression of gnat2, gnb3b, gngt2a and gngt2b, respectively, in all cones: DC (arrowheads), LSC (asterisks) and SSC (stars). The brown retinal pigment epithelium is shown the uppermost part for each picture. The stratification of the outer retina is evident in all panels except H, due to the exclusive ventral expression of gngt2a, where the stratification becomes unclear. Panel E shows the lack of staining in the adult retina for the gnb3a gene. Note that the weaker stained band into the ONLc for the cone-specific transducin subunits (thick arrows) corresponds to the rods’ myoid position (thin arrows in rods photomicrographs). Scale bar in panel A: 50 μm. For abbreviations see Fig. 2 legend.
Mentions: The presence in the zebrafish genome of all the transducin genes: gnat1, gnat2, gnb1a, gnb1b, gnb3a, gnb3b, gngt1, gngt2a and gngt2b was verified by PCR using genomic DNA and the 3´UTR primers designed for each gene (see Table 1). The same primers were also used to investigate the transducin gene expression in the retina by RT-PCR using retina cDNA and confirmed that all transducin genes, except gnb3a, are transcribed in the retina. Subsequently, subtype-specific antisense DIG/FITC-labelled riboprobes were used in ISH. Positive staining was observed in the outer retina for all the genes, with the exception of gnb3a (Fig. 3). Some of the mRNAs were also detected in the pineal complex (see description below), but not in any other part of the head.

Bottom Line: We describe here the results of 350 million years of evolution of three functionally related gene families: the alpha, beta and gamma subunits of transducins, the G protein involved in vision.These retina-pineal distinctions presumably reflect their distinct functional roles in vision and circadian rhythmicity.In summary, this study describes several functional differences between transducin gene duplicates resulting from the teleost-specific tetraploidisation.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

ABSTRACT
Gene duplications provide raw materials that can be selected for functional adaptations by evolutionary mechanisms. We describe here the results of 350 million years of evolution of three functionally related gene families: the alpha, beta and gamma subunits of transducins, the G protein involved in vision. Early vertebrate tetraploidisations resulted in separate transducin heterotrimers: gnat1/gnb1/gngt1 for rods, and gnat2/gnb3/gngt2 for cones. The teleost-specific tetraploidisation generated additional duplicates for gnb1, gnb3 and gngt2. We report here that the duplicates have undergone several types of subfunctionalisation or neofunctionalisation in the zebrafish. We have found that gnb1a and gnb1b are co-expressed at different levels in rods; gnb3a and gnb3b have undergone compartmentalisation restricting gnb3b to the dorsal and medial retina, however, gnb3a expression was detected only at very low levels in both larvae and adult retina; gngt2b expression is restricted to the dorsal and medial retina, whereas gngt2a is expressed ventrally. This dorsoventral distinction could be an adaptation to protect the lower part of the retina from intense light damage. The ontogenetic analysis shows earlier onset of expression in the pineal complex than in the retina, in accordance with its earlier maturation. Additionally, gnb1a but not gnb1b is expressed in the pineal complex, and gnb3b and gngt2b are transiently expressed in the pineal during ontogeny, thus showing partial temporal subfunctionalisation. These retina-pineal distinctions presumably reflect their distinct functional roles in vision and circadian rhythmicity. In summary, this study describes several functional differences between transducin gene duplicates resulting from the teleost-specific tetraploidisation.

No MeSH data available.


Related in: MedlinePlus