Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon)

Abstract

Background: Comparative genomic studies suggest that the modern day assemblage of ray-finned fishes have descended from an ancestral grouping of fishes that possessed 12-13 linkage groups. All jawed vertebrates are postulated to have experienced two whole genome duplications (WGD) in their ancestry (2R duplication). Salmonids have experienced one additional WGD (4R duplication event) compared to most extant teleosts which underwent a further 3R WGD compared to other vertebrates. We describe the organization of the 4R chromosomal segments of the proto-ray-finned fish karyotype in Atlantic salmon and rainbow trout based upon their comparative syntenies with two model species of 3R ray-finned fishes.

Results: Evidence is presented for the retention of large whole-arm affinities between the ancestral linkage groups of the ray-finned fishes, and the 50 homeologous chromosomal segments in Atlantic salmon and rainbow trout. In the comparisons between the two salmonid species, there is also evidence for the retention of large whole-arm homeologous affinities that are associated with the retention of duplicated markers. Five of the 7 pairs of chromosomal arm regions expressing the highest level of duplicate gene expression in rainbow trout share homologous synteny to the 5 pairs of homeologs with the greatest duplicate gene expression in Atlantic salmon. These regions are derived from proto-Actinopterygian linkage groups B, C, E, J and K.

Conclusion: Two chromosome arms in Danio rerio and Oryzias latipes (descendants of the 3R duplication) can, in most instances be related to at least 4 whole or partial chromosomal arms in the salmonid species. Multiple arm assignments in the two salmonid species do not clearly support a 13 proto-linkage group model, and suggest that a 12 proto-linkage group arrangement (i.e., a separate single chromosome duplication and ancestral fusion/fissions/recombination within the putative G/H/I groupings) may have occurred in the more basal soft-rayed fishes. We also found evidence supporting the model that ancestral linkage group M underwent a single chromosome duplication following the 3R duplication. In the salmonids, the M ancestral linkage groups are localized to 5 whole arm, and 3 partial arm regions (i.e., 6 whole arm regions expected). Thus, 3 distinct ancestral linkage groups are postulated to have existed in the G/H and M lineage chromosomes in the ancestor of the salmonids.

Figure 1

Distribution of 3R teleost (Danio rerio and Oryzias latipes) homologies within rainbow trout and Atlantic salmon linkage groups. The 13 ancestral linkage groups are designated according to Nakatani et al. 2007 [10], with two linkage groups (GH) examined as a single contributing region, assuming a 12 linkage group ancestral model [9]. Homologies detected solely in rainbow trout are depicted in black font. Homologies solely detected in Atlantic salmon are shown in blue font, while, shared homologies within both salmonid species are indicated in red font. Synteny blocks detected within salmonid linkage groups are shown in bold font, according to the color designations indicated.

Figure 2

Affinities of the 12/13 ancestral proto-Actinopterygian linkage groups [A – M] based upon the Kasahara et al. model [20] within the rainbow trout genome. Composite female map lengths are given in centiMorgans (cM) according to the scale shown in the bottom left-hand corner of the figure. In some instances female linkage groups are depicted as multiple separate LOD = 4.0 clusters. Centromeric locations within each linkage group [38] are shown as horizontal line segments and are indicated with a 'c' to the right of the linkage group. For certain linkage group arms, it is currently not possible to distinguish D and/or E ancestral affinities, or J and/or K ancestral affinities. These arm segments are indicated as D/E, and J/K regions on the figure and are indicated via diagonal cross-hatching. Short p arms are oriented towards the top of the figure according to [22].

Figure 3

Affinities of the 12/13 ancestral proto-Actinopterygian linkage groups [A – M] based upon the Kasahara et al. model [20] within the Atlantic salmon genome. Composite female map lengths are given in centiMorgans (cM) according to the scale shown in the bottom left-hand corner of the figure. In some instances female linkage groups are depicted as multiple separate LOD = 4.0 clusters. For certain linkage group arms, it is currently not possible to distinguish D and/or E ancestral affinities, or J and/or K ancestral affinities. These arm segments are indicated as D/E, and J/K regions on the figure and are indicated via diagonal cross-hatching. Short p arms are oriented towards the top of the figure according to [21].

Figure 4

Putative 4R homeologous linkage group affinities within the rainbow trout (Figure 4) and Atlantic salmon (Figure 5) genome based upon duplicated marker distributions. Acrocentric linkage groups composed of only a single ancestral arm are depicted in yellow background on the Oxford grid axes. Acrocentric linkage groups are expected to only possess a single 4R homeologous affinity while metacentric linkage groups should possess at least two 4R affinities. Several arm fusions have occurred in Atlantic salmon resulting in the expectation that metacentric chromosomes such as AS-17 possess 3 whole-arm affinities, while acrocentric chromosomes AS-2, -3, -5, -6, -8, -9, -13, -16, -22, -23, and -25 will have two whole-arm affinities. For AS-10, three whole-arm affinities are expected within this large acrocentric chromosome [21]. Homeologies based upon only a single duplicated marker are in some instances supported by the mapping of single non-duplicated markers in alternate mapping parents to either of the putative duplicated homeologous linkage groups. Inferred homeologies based upon the comparative synteny mapping with zebrafish and medaka (Figures 1 – 3) are indicated as orange blocks in the Oxford grids.

Figure 5

Putative 4R homeologous linkage group affinities within the rainbow trout (Figure 4) and Atlantic salmon (Figure 5) genome based upon duplicated marker distributions. Acrocentric linkage groups composed of only a single ancestral arm are depicted in yellow background on the Oxford grid axes. Acrocentric linkage groups are expected to only possess a single 4R homeologous affinity while metacentric linkage groups should possess at least two 4R affinities. Several arm fusions have occurred in Atlantic salmon resulting in the expectation that metacentric chromosomes such as AS-17 possess 3 whole-arm affinities, while acrocentric chromosomes AS-2, -3, -5, -6, -8, -9, -13, -16, -22, -23, and -25 will have two whole-arm affinities. For AS-10, three whole-arm affinities are expected within this large acrocentric chromosome [21]. Homeologies based upon only a single duplicated marker are in some instances supported by the mapping of single non-duplicated markers in alternate mapping parents to either of the putative duplicated homeologous linkage groups. Inferred homeologies based upon the comparative synteny mapping with zebrafish and medaka (Figures 1 – 3) are indicated as orange blocks in the Oxford grids.

Figure 6

Model of ancestral linkage group re-arrangements among G/H/I lineage chromosomes. Extensive cross syntenies among zebrafish chromosomes 5, 10, 15, and 21 suggest that a duplication and subsequent fission of one of the two 3R chromosomes in either the I, or presumptive G/H lineage may have occurred. This fission would give the appearance of extra ancestral groupings (i.e., greater than 4 linkage group arm homologies to either the G/H or the I lineage chromosomes). Reticulate exchange among segments from both ancestral groupings may also have occurred as evidenced by the retention of G/H/I synteny blocks within rainbow trout arms 1 and 9p. Rainbow trout chromosome arms possessing multiple affinities to zebrafish linkage groups 5/10/15/21 (i.e, suggestive of greater re-arrangements), are indicated in red font in the centre of the table.