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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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Oxford grid showing the homeologous relationships which have been conserved between rainbow trout chromosome arms after the 4th Whole Genome Duplication specific to salmonids. Linkage group and chromosome arm numbers are indicated on first and second lines and rows respectively. Numbers of markers shared between duplicated regions are given. When two numbers per cell are given (i.e. 1 + 1), the second one corresponds to additional homeologies found by comparing the rainbow trout and model species linkage groups. Blue cells: previously well-characterised homeologies. Green and orange cells: homologies respectively based on a single marker or suggested in Danzmann et al. [22] and confirmed with additional duplicated markers in the current study. Red cells: newly identified homeologies supported by two or more markers. Grey cells: homeologies based on a single marker and not considered in this study.
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Figure 1: Oxford grid showing the homeologous relationships which have been conserved between rainbow trout chromosome arms after the 4th Whole Genome Duplication specific to salmonids. Linkage group and chromosome arm numbers are indicated on first and second lines and rows respectively. Numbers of markers shared between duplicated regions are given. When two numbers per cell are given (i.e. 1 + 1), the second one corresponds to additional homeologies found by comparing the rainbow trout and model species linkage groups. Blue cells: previously well-characterised homeologies. Green and orange cells: homologies respectively based on a single marker or suggested in Danzmann et al. [22] and confirmed with additional duplicated markers in the current study. Red cells: newly identified homeologies supported by two or more markers. Grey cells: homeologies based on a single marker and not considered in this study.

Mentions: The final synthetic map consisted of 2226 loci assigned to 29 linkage groups and spanned a total length of approximately 3600 cM (Additional file 2, sheet 4 and Additional file 4). Marker orders were identical to those of the INRA map in 20 linkage groups (RT03 to RT06, RT08 to RT12, RT14, RT15, RT17 to RT19, RT22, RT24 to RT30) (Additional file 2, sheets 6 to 34). The remaining nine linkage groups showed very minor inversions between some consecutive loci (Additional file 2, sheets 6 to 34). Approximate borders of centromeric regions were defined as described in [21] and included all the markers mapped within these borders. Two hundred and eighty-two pairs of duplicated loci (576 loci, i.e. 26% of the total number of loci) were found on all chromosomal arms, with the exception of Omy22p, Omy7q, Omy21p and Omy20q (Additional file 2, sheet 35). Numbers of shared duplicated loci between homeologous arms ranged from one to 35 between Omy12q and Omy13q and 21 pairs of arms had two or more duplicated loci in common (Figure 1 and Additional file 2, sheet 35).


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)

Oxford grid showing the homeologous relationships which have been conserved between rainbow trout chromosome arms after the 4th Whole Genome Duplication specific to salmonids. Linkage group and chromosome arm numbers are indicated on first and second lines and rows respectively. Numbers of markers shared between duplicated regions are given. When two numbers per cell are given (i.e. 1 + 1), the second one corresponds to additional homeologies found by comparing the rainbow trout and model species linkage groups. Blue cells: previously well-characterised homeologies. Green and orange cells: homologies respectively based on a single marker or suggested in Danzmann et al. [22] and confirmed with additional duplicated markers in the current study. Red cells: newly identified homeologies supported by two or more markers. Grey cells: homeologies based on a single marker and not considered in this study.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Oxford grid showing the homeologous relationships which have been conserved between rainbow trout chromosome arms after the 4th Whole Genome Duplication specific to salmonids. Linkage group and chromosome arm numbers are indicated on first and second lines and rows respectively. Numbers of markers shared between duplicated regions are given. When two numbers per cell are given (i.e. 1 + 1), the second one corresponds to additional homeologies found by comparing the rainbow trout and model species linkage groups. Blue cells: previously well-characterised homeologies. Green and orange cells: homologies respectively based on a single marker or suggested in Danzmann et al. [22] and confirmed with additional duplicated markers in the current study. Red cells: newly identified homeologies supported by two or more markers. Grey cells: homeologies based on a single marker and not considered in this study.
Mentions: The final synthetic map consisted of 2226 loci assigned to 29 linkage groups and spanned a total length of approximately 3600 cM (Additional file 2, sheet 4 and Additional file 4). Marker orders were identical to those of the INRA map in 20 linkage groups (RT03 to RT06, RT08 to RT12, RT14, RT15, RT17 to RT19, RT22, RT24 to RT30) (Additional file 2, sheets 6 to 34). The remaining nine linkage groups showed very minor inversions between some consecutive loci (Additional file 2, sheets 6 to 34). Approximate borders of centromeric regions were defined as described in [21] and included all the markers mapped within these borders. Two hundred and eighty-two pairs of duplicated loci (576 loci, i.e. 26% of the total number of loci) were found on all chromosomal arms, with the exception of Omy22p, Omy7q, Omy21p and Omy20q (Additional file 2, sheet 35). Numbers of shared duplicated loci between homeologous arms ranged from one to 35 between Omy12q and Omy13q and 21 pairs of arms had two or more duplicated loci in common (Figure 1 and Additional file 2, sheet 35).

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