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A synthetic rainbow trout linkage map provides new insights into the salmonid whole genome duplication and the conservation of synteny among teleosts.

Guyomard R, Boussaha M, Krieg F, Hervet C, Quillet E - BMC Genet. (2012)

Bottom Line: This resulted in a synthetic map consisting of 2226 markers and 29 linkage groups spanning over 3600 cM.Large conserved syntenies were also found between the genomes of rainbow trout and the reconstructed teleost ancestor.Finally, the persistence of large conserved syntenies across teleosts should facilitate the identification of candidate genes through comparative mapping, even if the occurrence of intra-chromosomal micro-rearrangement may hinder the accurate prediction their genomic location.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA, UMR1313, Animal Genetics and Integrative Biology, Domaine de Vilvert, 78350 Jouy-en-Josas, France. rene.guyomard@jouy.inra.fr

ABSTRACT

Background: Rainbow trout is an economically important fish and a suitable experimental organism in many fields of biology including genome evolution, owing to the occurrence of a salmonid specific whole-genome duplication (4th WGD). Rainbow trout is among some of the most studied teleosts and has benefited from substantial efforts to develop genomic resources (e.g., linkage maps. Here, we first generated a synthetic map by merging segregation data files derived from three independent linkage maps. Then, we used it to evaluate genome conservation between rainbow trout and three teleost models, medaka, stickleback and zebrafish and to further investigate the extent of the 4th WGD in trout genome.

Results: The INRA linkage map was updated by adding 211 new markers. After standardization of marker names, consistency of marker assignment to linkage groups and marker orders was checked across the three different data sets and only loci showing consistent location over all or almost all of the data sets were kept. This resulted in a synthetic map consisting of 2226 markers and 29 linkage groups spanning over 3600 cM. Blastn searches against medaka, stickleback, and zebrafish genomic databases resulted in 778, 824 and 730 significant hits respectively while blastx searches yielded 505, 513 and 510 significant hits. Homology search results revealed that, for most rainbow trout chromosomes, large syntenic regions encompassing nearly whole chromosome arms have been conserved between rainbow trout and its closest models, medaka and stickleback. Large conserved syntenies were also found between the genomes of rainbow trout and the reconstructed teleost ancestor. These syntenies consolidated the known homeologous affinities between rainbow trout chromosomes due to the 4th WGD and suggested new ones.

Conclusions: The synthetic map constructed herein further highlights the stability of the teleost genome over long evolutionary time scales. This map can be easily extended by incorporating new data sets and should help future rainbow trout whole genome sequence assembly. Finally, the persistence of large conserved syntenies across teleosts should facilitate the identification of candidate genes through comparative mapping, even if the occurrence of intra-chromosomal micro-rearrangement may hinder the accurate prediction their genomic location.

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Conserved syntenies between the rainbow trout RT02 linkage group and two homeologous chromosomes of the medaka (Figure 1a) and stickleback (1b). Ola01 and Ola08 in medaka, group IX and group XI in stickleback, result from the duplication of the same ancestral chromosome at the time of the 3rd Whole Genome Duplication in fish. Centromeric regions are approximately delineated by underlined, blue bold type, marker names following [21]. Red and green lines identify the two chromosome arms of RT02. See Additional file 7, Additional file 8 and Additional file 9 for complete graphic representation of the conserved syntenies between rainbow trout and the three model species.
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Figure 2: Conserved syntenies between the rainbow trout RT02 linkage group and two homeologous chromosomes of the medaka (Figure 1a) and stickleback (1b). Ola01 and Ola08 in medaka, group IX and group XI in stickleback, result from the duplication of the same ancestral chromosome at the time of the 3rd Whole Genome Duplication in fish. Centromeric regions are approximately delineated by underlined, blue bold type, marker names following [21]. Red and green lines identify the two chromosome arms of RT02. See Additional file 7, Additional file 8 and Additional file 9 for complete graphic representation of the conserved syntenies between rainbow trout and the three model species.

Mentions: Shared homologies involving a rainbow trout arm and two medaka (or stikleback) homeologous chromosomes arisen from the 3rd WGD could not be clearly interpreted (see above and discussion) and could reflect homology with only one of the two homeologs. Therefore, when such a situation occurred, only the medaka (or stickleback) homeolog (thereafter named "expected homologous chromosome") which had the highest number of sequence homologies with the rainbow trout arm was conserved in graphic representations of the alignments of the medaka or stickleback chromosomes to rainbow trout ones. For example, only groupVIII and groupVI were kept for RT06 in the comparison between rainbow trout and stickleback; homology of RT06 with groupV, which is homeologous to groupVI, was ignored. This led to parsimonious graphic representations of the genome evolution between rainbow trout and these two model species (Additional file 7 and Additional file 8). Alignment of the stickleback linkage groups on the rainbow trout map is partly represented in Figure 2. Under these conditions, despite the high number of chromosome arms in rainbow trout (n = 52), a rather limited number of syntenic fragments were found between this species and each of the two model species, medaka (68) and stickleback (63). In the case of zebrafish, which showed the highest number of synteny disruptions with rainbow trout, all the homologies based on more than one marker, i.e. 123, were conserved (Additional file 9). Localisation of centromeres on the rainbow trout map showed that, in many cases, a trout chromosome arm was syntenic to a single large chromosome fragment in medaka or stickleback. However, gene orders were poorly conserved between species in both the synthetic (Figure 2 and Additional file 7, Additional file 8 and Additional file 9) and the second generation INRA maps (data not shown).


A synthetic rainbow trout linkage map provides new insights into the salmonid whole genome duplication and the conservation of synteny among teleosts.

Guyomard R, Boussaha M, Krieg F, Hervet C, Quillet E - BMC Genet. (2012)

Conserved syntenies between the rainbow trout RT02 linkage group and two homeologous chromosomes of the medaka (Figure 1a) and stickleback (1b). Ola01 and Ola08 in medaka, group IX and group XI in stickleback, result from the duplication of the same ancestral chromosome at the time of the 3rd Whole Genome Duplication in fish. Centromeric regions are approximately delineated by underlined, blue bold type, marker names following [21]. Red and green lines identify the two chromosome arms of RT02. See Additional file 7, Additional file 8 and Additional file 9 for complete graphic representation of the conserved syntenies between rainbow trout and the three model species.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3368724&req=5

Figure 2: Conserved syntenies between the rainbow trout RT02 linkage group and two homeologous chromosomes of the medaka (Figure 1a) and stickleback (1b). Ola01 and Ola08 in medaka, group IX and group XI in stickleback, result from the duplication of the same ancestral chromosome at the time of the 3rd Whole Genome Duplication in fish. Centromeric regions are approximately delineated by underlined, blue bold type, marker names following [21]. Red and green lines identify the two chromosome arms of RT02. See Additional file 7, Additional file 8 and Additional file 9 for complete graphic representation of the conserved syntenies between rainbow trout and the three model species.
Mentions: Shared homologies involving a rainbow trout arm and two medaka (or stikleback) homeologous chromosomes arisen from the 3rd WGD could not be clearly interpreted (see above and discussion) and could reflect homology with only one of the two homeologs. Therefore, when such a situation occurred, only the medaka (or stickleback) homeolog (thereafter named "expected homologous chromosome") which had the highest number of sequence homologies with the rainbow trout arm was conserved in graphic representations of the alignments of the medaka or stickleback chromosomes to rainbow trout ones. For example, only groupVIII and groupVI were kept for RT06 in the comparison between rainbow trout and stickleback; homology of RT06 with groupV, which is homeologous to groupVI, was ignored. This led to parsimonious graphic representations of the genome evolution between rainbow trout and these two model species (Additional file 7 and Additional file 8). Alignment of the stickleback linkage groups on the rainbow trout map is partly represented in Figure 2. Under these conditions, despite the high number of chromosome arms in rainbow trout (n = 52), a rather limited number of syntenic fragments were found between this species and each of the two model species, medaka (68) and stickleback (63). In the case of zebrafish, which showed the highest number of synteny disruptions with rainbow trout, all the homologies based on more than one marker, i.e. 123, were conserved (Additional file 9). Localisation of centromeres on the rainbow trout map showed that, in many cases, a trout chromosome arm was syntenic to a single large chromosome fragment in medaka or stickleback. However, gene orders were poorly conserved between species in both the synthetic (Figure 2 and Additional file 7, Additional file 8 and Additional file 9) and the second generation INRA maps (data not shown).

Bottom Line: This resulted in a synthetic map consisting of 2226 markers and 29 linkage groups spanning over 3600 cM.Large conserved syntenies were also found between the genomes of rainbow trout and the reconstructed teleost ancestor.Finally, the persistence of large conserved syntenies across teleosts should facilitate the identification of candidate genes through comparative mapping, even if the occurrence of intra-chromosomal micro-rearrangement may hinder the accurate prediction their genomic location.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA, UMR1313, Animal Genetics and Integrative Biology, Domaine de Vilvert, 78350 Jouy-en-Josas, France. rene.guyomard@jouy.inra.fr

ABSTRACT

Background: Rainbow trout is an economically important fish and a suitable experimental organism in many fields of biology including genome evolution, owing to the occurrence of a salmonid specific whole-genome duplication (4th WGD). Rainbow trout is among some of the most studied teleosts and has benefited from substantial efforts to develop genomic resources (e.g., linkage maps. Here, we first generated a synthetic map by merging segregation data files derived from three independent linkage maps. Then, we used it to evaluate genome conservation between rainbow trout and three teleost models, medaka, stickleback and zebrafish and to further investigate the extent of the 4th WGD in trout genome.

Results: The INRA linkage map was updated by adding 211 new markers. After standardization of marker names, consistency of marker assignment to linkage groups and marker orders was checked across the three different data sets and only loci showing consistent location over all or almost all of the data sets were kept. This resulted in a synthetic map consisting of 2226 markers and 29 linkage groups spanning over 3600 cM. Blastn searches against medaka, stickleback, and zebrafish genomic databases resulted in 778, 824 and 730 significant hits respectively while blastx searches yielded 505, 513 and 510 significant hits. Homology search results revealed that, for most rainbow trout chromosomes, large syntenic regions encompassing nearly whole chromosome arms have been conserved between rainbow trout and its closest models, medaka and stickleback. Large conserved syntenies were also found between the genomes of rainbow trout and the reconstructed teleost ancestor. These syntenies consolidated the known homeologous affinities between rainbow trout chromosomes due to the 4th WGD and suggested new ones.

Conclusions: The synthetic map constructed herein further highlights the stability of the teleost genome over long evolutionary time scales. This map can be easily extended by incorporating new data sets and should help future rainbow trout whole genome sequence assembly. Finally, the persistence of large conserved syntenies across teleosts should facilitate the identification of candidate genes through comparative mapping, even if the occurrence of intra-chromosomal micro-rearrangement may hinder the accurate prediction their genomic location.

Show MeSH
Related in: MedlinePlus