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Evolution of Vertebrate Vision by Means of Whole Genome Duplications: Zebrafish as a Model for Gene Specialisation
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience. Uppsala University, Science for Life Laboratory, SciLifeLab.
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The signalling cascade of rods and cones use different but related protein components. Rods and cones, emerged in the common ancestor of vertebrates around 500 million years ago around when two whole genome duplications took place, named 1R and 2R. These generated a large number of additional genes that could evolve new or more specialised functions. A third event, 3R, occurred in the ancestor of teleost fish. 

This thesis describes extensive phylogenetic and comparative synteny analyses of the opsins, transducin and phosphodiesterase (PDE6) of this cascade by including data from a wide selection of vertebrates. The expression of the zebrafish genes was also investigated. The results show that genes for these proteins duplicated in 1R and 2R as well as some in 3R.

Expression analyses of the zebrafish genes revealed additional specialisations for the 3R gene duplicates. The transducin beta subunit genes, gnb1a and gnb1b, show co-localisation in rods but are expressed at different levels. Gnb3a and gnb3b show different expression in the adult retina with low expression of gnb3a and expression of gnb3b in cones of the dorso-medial retina. The transducin gamma subunit genes gngt2a and gngt2b are expressed in the ventral and dorso-medial retina respectively. The both of PDE6 gamma subunit genes, pde6ga and pde6gb are both expressed in rods but pde6ga shows rhythmic changes of expression with low daytime levels. Pde6ha and pde6hb are expressed in cones however pde6ha show high daytime expression. All investigated transducin and PDE6 subunit genes, but gnb1b, were also expressed in the adult pineal complex or at some point during development.

These results provide compelling evidence that the 1R and 2R genome duplications facilitated the evolution of rods and cones by generating gene duplicates that could evolve distinct expression and function. This supports existence of colour vision before the origin of vertebrates, elaboration of this in the early vertebrate ancestor, along with origin of the black-and-white dim-light vision of rods. Furthermore, the different expression patterns observed in the zebrafish retina for teleost 3R duplicates demonstrate multiple additional specialisations. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. , 57 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1070
Keyword [en]
phylogenetics, evolution, vision, visual opsin, transducin, PDE6, genome duplications, subfunctionalisation
National Category
Biological Sciences
Research subject
Medical Science
Identifiers
URN: urn:nbn:se:uu:diva-242781ISBN: 978-91-554-9155-0 (print)OAI: oai:DiVA.org:uu-242781DiVA: diva2:785090
Public defence
2015-03-20, B:41, Biomedicinskt centrum, Husargatan 3, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2015-02-26 Created: 2015-02-02 Last updated: 2015-03-11
List of papers
1. The vertebrate ancestral repertoire of visual opsins, transducin alpha subunits and oxytocin/vasopressin receptors was established by duplication of their shared genomic region in the two rounds of early vertebrate genome duplications
Open this publication in new window or tab >>The vertebrate ancestral repertoire of visual opsins, transducin alpha subunits and oxytocin/vasopressin receptors was established by duplication of their shared genomic region in the two rounds of early vertebrate genome duplications
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2013 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 13, 238- p.Article in journal (Refereed) Published
Abstract [en]

Background: Vertebrate color vision is dependent on four major color opsin subtypes: RH2 (green opsin), SWS1 (ultraviolet opsin), SWS2 (blue opsin), and LWS (red opsin). Together with the dim-light receptor rhodopsin (RH1), these form the family of vertebrate visual opsins. Vertebrate genomes contain many multi-membered gene families that can largely be explained by the two rounds of whole genome duplication (WGD) in the vertebrate ancestor (2R) followed by a third round in the teleost ancestor (3R). Related chromosome regions resulting from WGD or block duplications are said to form a paralogon. We describe here a paralogon containing the genes for visual opsins, the G-protein alpha subunit families for transducin (GNAT) and adenylyl cyclase inhibition (GNAI), the oxytocin and vasopressin receptors (OT/VP-R), and the L-type voltage-gated calcium channels (CACNA1-L). Results: Sequence-based phylogenies and analyses of conserved synteny show that the above-mentioned gene families, and many neighboring gene families, expanded in the early vertebrate WGDs. This allows us to deduce the following evolutionary scenario: The vertebrate ancestor had a chromosome containing the genes for two visual opsins, one GNAT, one GNAI, two OT/VP-Rs and one CACNA1-L gene. This chromosome was quadrupled in 2R. Subsequent gene losses resulted in a set of five visual opsin genes, three GNAT and GNAI genes, six OT/VP-R genes and four CACNA1-L genes. These regions were duplicated again in 3R resulting in additional teleost genes for some of the families. Major chromosomal rearrangements have taken place in the teleost genomes. By comparison with the corresponding chromosomal regions in the spotted gar, which diverged prior to 3R, we could time these rearrangements to post-3R. Conclusions: We present an extensive analysis of the paralogon housing the visual opsin, GNAT and GNAI, OT/VP-R, and CACNA1-L gene families. The combined data imply that the early vertebrate WGD events contributed to the evolution of vision and the other neuronal and neuroendocrine functions exerted by the proteins encoded by these gene families. In pouched lamprey all five visual opsin genes have previously been identified, suggesting that lampreys diverged from the jawed vertebrates after 2R.

Keyword
Visual opsins, Whole genome duplications, Chromosome rearrangements, Opsin evolution, Oxytocin receptors, Vasopressin receptors, G-protein alpha transducing subunits, Voltage-gated calcium channels
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:uu:diva-215296 (URN)10.1186/1471-2148-13-238 (DOI)000328459400001 ()
Note

De två (2) första författarna delar förstaförfattarskapet.

Available from: 2014-01-13 Created: 2014-01-13 Last updated: 2017-12-06Bibliographically approved
2. Expansion of transducin subunit gene families in early vertebrate tetraploidizations
Open this publication in new window or tab >>Expansion of transducin subunit gene families in early vertebrate tetraploidizations
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2012 (English)In: Genomics, ISSN 0888-7543, E-ISSN 1089-8646, Vol. 100, no 4, 203-211 p.Article in journal (Refereed) Published
Abstract [en]

Hundreds of gene families expanded in the early vertebrate tetraploidizations including many gene families in the phototransduction cascade. We have investigated the evolution of the heterotrimeric G-proteins of photoreceptors, the transducins, in relation to these events using both phylogenetic analyses and synteny comparisons. Three alpha subunit genes were identified in amniotes and the coelacanth, GNAT1-3; two of these were identified in amphibians and teleost fish, GNAT1 and GNAT2. Most tetrapods have four beta genes, GNB1-4, and teleosts have additional duplicates. Finally, three gamma genes were identified in mammals, GNGT1, GNG11 and GNGT2. Of these, GNGT1 and GNGT2 were found in the other vertebrates. In frog and zebrafish additional duplicates of GNGT2 were identified. Our analyses show all three transducin families expanded during the early vertebrate tetraploidizations and the beta and gamma families gained additional copies in the teleost-specific genome duplication. This suggests that the tetraploidizations contributed to visual specialisations.

Keyword
G-protein, Gene duplication, Phototransduction, Teleost fish, Tetraploidization, Transducin
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-181018 (URN)10.1016/j.ygeno.2012.07.005 (DOI)000308731600001 ()
Available from: 2012-09-14 Created: 2012-09-14 Last updated: 2017-12-07Bibliographically approved
3. Transducin duplicates in the zebrafish retina and pineal complex: differential specialisation after the teleost tetraploidisation
Open this publication in new window or tab >>Transducin duplicates in the zebrafish retina and pineal complex: differential specialisation after the teleost tetraploidisation
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(English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203Article in journal (Refereed) Accepted
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-242751 (URN)
Available from: 2015-02-02 Created: 2015-01-31 Last updated: 2017-12-05
4. Evolution and expression of phosphodiesterase 6 genes show vertebrate novelty in the control of photosensitivity
Open this publication in new window or tab >>Evolution and expression of phosphodiesterase 6 genes show vertebrate novelty in the control of photosensitivity
(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-242768 (URN)
Available from: 2015-02-02 Created: 2015-02-01 Last updated: 2015-03-11

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