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Comparative genomics and phylogenetic discordance of cultivated tomato and close wild relatives.

Strickler SR, Bombarely A, Munkvold JD, York T, Menda N, Martin GB, Mueller LA - PeerJ (2015)

Bottom Line: As a result, the phylogeny in relation to its closest relatives remains uncertain.Conclusions.The use of an heirloom line is helpful in deducing true phylogenetic information of S. lycopersicum and identifying regions of introgression from wild species.

View Article: PubMed Central - HTML - PubMed

Affiliation: Boyce Thompson Institute for Plant Research , Ithaca, NY , USA.

ABSTRACT
Background. Studies of ancestry are difficult in the tomato because it crosses with many wild relatives and species in the tomato clade that have diverged very recently. As a result, the phylogeny in relation to its closest relatives remains uncertain. By using the coding sequence from Solanum lycopersicum, S. galapagense, S. pimpinellifolium, S. corneliomuelleri, and S. tuberosum and the genomic sequence from S. lycopersicum 'Heinz', an heirloom line, S. lycopersicum 'Yellow Pear', and two of cultivated tomato's closest relatives, S. galapagense and S. pimpinellifolium, we have aimed to resolve the phylogenies of these closely related species as well as identify phylogenetic discordance in the reference cultivated tomato. Results. Divergence date estimates suggest that the divergence of S. lycopersicum, S. galapagense, and S. pimpinellifolium happened less than 0.5 MYA. Phylogenies based on 8,857 coding sequences support grouping of S. lycopersicum and S. galapagense, although two secondary trees are also highly represented. A total of 25 genes in our analysis had sites with evidence of positive selection along the S. lycopersicum lineage. Whole genome phylogenies showed that while incongruence is prevalent in genomic comparisons between these genotypes, likely as a result of introgression and incomplete lineage sorting, a primary phylogenetic history was strongly supported. Conclusions. Based on analysis of these genotypes, S. galapagense appears to be closely related to S. lycopersicum, suggesting they had a common ancestor prior to the arrival of an S. galapagense ancestor to the Galápagos Islands, but after divergence of the sequenced S. pimpinellifolium. Genes showing selection along the S. lycopersicum lineage may be important in domestication or selection occurring post-domestication. Further analysis of intraspecific data in these species will help to establish the evolutionary history of cultivated tomato. The use of an heirloom line is helpful in deducing true phylogenetic information of S. lycopersicum and identifying regions of introgression from wild species.

No MeSH data available.


Feature density of Yellow Pear, S. galapagense, and S.pimpinellifolium in comparison to H1706.Red arrow points to putative introgression. (A) SNP density on chromosome 4 of sequenced genotypes. (B) SNP density on chromosome 5 of sequenced genotypes. (C) Read depth on chromosome 4 of sequenced genotypes. (D) Read depth on chromosome 5 of sequenced genotypes (E) Gene density on chromosome 4 based on H1706 annotations (F) Gene density on chromosome 5 based on H1706 annotations.
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fig-1: Feature density of Yellow Pear, S. galapagense, and S.pimpinellifolium in comparison to H1706.Red arrow points to putative introgression. (A) SNP density on chromosome 4 of sequenced genotypes. (B) SNP density on chromosome 5 of sequenced genotypes. (C) Read depth on chromosome 4 of sequenced genotypes. (D) Read depth on chromosome 5 of sequenced genotypes (E) Gene density on chromosome 4 based on H1706 annotations (F) Gene density on chromosome 5 based on H1706 annotations.

Mentions: Over 500,000 single nucleotide polymorphisms (SNPs) were found between YP-1 and H1706 (Table S3). S. galapagense was found to have approximately 4.7 million SNPs, whereas S. pimpinellifolium had 6 million when compared to H1706 (Table S3). Variation in SNP density was found across the genome, and was found to differ between chromosomes and genotypes (Fig. 1 and Fig. S1). In particular, regions on chromosomes 4 (∼59 Mbp) and 11 (∼4 Mbp) show reduced SNP density in S. pimpinellifolium and elevated density in YP-1 (Fig. 1 and Fig. S1). A large assembly coverage gap in S. pimpinellifolium located at approximately 11 Mbp on chromosome 1 is found at the position of the tomato self-incompatibility locus (Tanksley & Loaiza-Figueroa, 1985) (Fig. S1). Large assembly coverage gaps were also detected in S. pimpinellifolium on chromosomes 3 (∼37 Mbp), 8 (∼40 Mbp), 10 (∼30 Mbp), and S. galapagense chromosomes 8 (∼16 Mbp), and 12 (∼60 Mbp) (Fig. S1). As expected, more SNPs were found in noncoding regions than coding regions (Table S3). SNPs were found in approximately 0.05%, 0.5%, and 0.8% of the YP-1, S. galapagense, and S. pimpinellifolium intergenic regions respectively, while affecting only 0.04%, 0.3%, and 0.4% of the coding regions of these genomes (Table S3). A total of 3,418 YP-1, 20,447 S. galapagense, and 12,143 S. pimpinellifolium genes were found to have nonsynonymous SNPs associated with them. Additionally, 242,165 SNPs were identified using the aligned Illumina data from H1706 to the reference H1706 v 2.40 assembly, of which 225,625 were predicted to be heterozygous with the reference genome (please see solgenomics.net for vcf file).


Comparative genomics and phylogenetic discordance of cultivated tomato and close wild relatives.

Strickler SR, Bombarely A, Munkvold JD, York T, Menda N, Martin GB, Mueller LA - PeerJ (2015)

Feature density of Yellow Pear, S. galapagense, and S.pimpinellifolium in comparison to H1706.Red arrow points to putative introgression. (A) SNP density on chromosome 4 of sequenced genotypes. (B) SNP density on chromosome 5 of sequenced genotypes. (C) Read depth on chromosome 4 of sequenced genotypes. (D) Read depth on chromosome 5 of sequenced genotypes (E) Gene density on chromosome 4 based on H1706 annotations (F) Gene density on chromosome 5 based on H1706 annotations.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4358695&req=5

fig-1: Feature density of Yellow Pear, S. galapagense, and S.pimpinellifolium in comparison to H1706.Red arrow points to putative introgression. (A) SNP density on chromosome 4 of sequenced genotypes. (B) SNP density on chromosome 5 of sequenced genotypes. (C) Read depth on chromosome 4 of sequenced genotypes. (D) Read depth on chromosome 5 of sequenced genotypes (E) Gene density on chromosome 4 based on H1706 annotations (F) Gene density on chromosome 5 based on H1706 annotations.
Mentions: Over 500,000 single nucleotide polymorphisms (SNPs) were found between YP-1 and H1706 (Table S3). S. galapagense was found to have approximately 4.7 million SNPs, whereas S. pimpinellifolium had 6 million when compared to H1706 (Table S3). Variation in SNP density was found across the genome, and was found to differ between chromosomes and genotypes (Fig. 1 and Fig. S1). In particular, regions on chromosomes 4 (∼59 Mbp) and 11 (∼4 Mbp) show reduced SNP density in S. pimpinellifolium and elevated density in YP-1 (Fig. 1 and Fig. S1). A large assembly coverage gap in S. pimpinellifolium located at approximately 11 Mbp on chromosome 1 is found at the position of the tomato self-incompatibility locus (Tanksley & Loaiza-Figueroa, 1985) (Fig. S1). Large assembly coverage gaps were also detected in S. pimpinellifolium on chromosomes 3 (∼37 Mbp), 8 (∼40 Mbp), 10 (∼30 Mbp), and S. galapagense chromosomes 8 (∼16 Mbp), and 12 (∼60 Mbp) (Fig. S1). As expected, more SNPs were found in noncoding regions than coding regions (Table S3). SNPs were found in approximately 0.05%, 0.5%, and 0.8% of the YP-1, S. galapagense, and S. pimpinellifolium intergenic regions respectively, while affecting only 0.04%, 0.3%, and 0.4% of the coding regions of these genomes (Table S3). A total of 3,418 YP-1, 20,447 S. galapagense, and 12,143 S. pimpinellifolium genes were found to have nonsynonymous SNPs associated with them. Additionally, 242,165 SNPs were identified using the aligned Illumina data from H1706 to the reference H1706 v 2.40 assembly, of which 225,625 were predicted to be heterozygous with the reference genome (please see solgenomics.net for vcf file).

Bottom Line: As a result, the phylogeny in relation to its closest relatives remains uncertain.Conclusions.The use of an heirloom line is helpful in deducing true phylogenetic information of S. lycopersicum and identifying regions of introgression from wild species.

View Article: PubMed Central - HTML - PubMed

Affiliation: Boyce Thompson Institute for Plant Research , Ithaca, NY , USA.

ABSTRACT
Background. Studies of ancestry are difficult in the tomato because it crosses with many wild relatives and species in the tomato clade that have diverged very recently. As a result, the phylogeny in relation to its closest relatives remains uncertain. By using the coding sequence from Solanum lycopersicum, S. galapagense, S. pimpinellifolium, S. corneliomuelleri, and S. tuberosum and the genomic sequence from S. lycopersicum 'Heinz', an heirloom line, S. lycopersicum 'Yellow Pear', and two of cultivated tomato's closest relatives, S. galapagense and S. pimpinellifolium, we have aimed to resolve the phylogenies of these closely related species as well as identify phylogenetic discordance in the reference cultivated tomato. Results. Divergence date estimates suggest that the divergence of S. lycopersicum, S. galapagense, and S. pimpinellifolium happened less than 0.5 MYA. Phylogenies based on 8,857 coding sequences support grouping of S. lycopersicum and S. galapagense, although two secondary trees are also highly represented. A total of 25 genes in our analysis had sites with evidence of positive selection along the S. lycopersicum lineage. Whole genome phylogenies showed that while incongruence is prevalent in genomic comparisons between these genotypes, likely as a result of introgression and incomplete lineage sorting, a primary phylogenetic history was strongly supported. Conclusions. Based on analysis of these genotypes, S. galapagense appears to be closely related to S. lycopersicum, suggesting they had a common ancestor prior to the arrival of an S. galapagense ancestor to the Galápagos Islands, but after divergence of the sequenced S. pimpinellifolium. Genes showing selection along the S. lycopersicum lineage may be important in domestication or selection occurring post-domestication. Further analysis of intraspecific data in these species will help to establish the evolutionary history of cultivated tomato. The use of an heirloom line is helpful in deducing true phylogenetic information of S. lycopersicum and identifying regions of introgression from wild species.

No MeSH data available.