Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing

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Abstract

We explored genetic variation by sequencing a selection of 84 tomato accessions and related wild species representative for the Lycopersicon, Arcanum, Eriopersicon, and Neolycopersicon groups which has yielded a huge amount of precious data on sequence diversity in the tomato clade. Three new reference genomes were reconstructed to support our comparative genome analyses. Comparative sequence alignment reveals group-, species-, and accession-specific polymorphisms, which explains characteristic fruit traits and growth habits in the different cultivars. Using gene models from the annotated Heinz 1706 reference genome, we observed differences dN/dS ratio in fruit and growth diversification genes compared to a random set of genes, pointing to positive selection and to differences in selection pressure between crop accessions and wild species. In wild species SNPs are found in excess of 10 million, i.e. 20 fold higher than found in most of the crop accessions, indicating dramatic genetic erosion of crop and heirloom tomatoes. In addition, highest levels of heterozygosity were found for allogamous SI wild species, while facultative and autogamous SC species display a lower heterozygosity level. Using whole genome SNP information for Maximum Likelihood analysis we achieved complete tree resolution, whereas ML trees based on SNPs from 10 fruit and growth genes show incomplete resolution for the crop accessions, partly due to the effect of heterozygous SNPs. Finally, results suggest that phylogenetic relationships are correlated with habitat pointing at the occurrence of geographical races within these groups, which is of practical importance for Solanum genome evolution studies.
Original languageEnglish
Pages (from-to)136-148
JournalThe Plant Journal
Volume80
Issue number1
DOIs
Publication statusPublished - 2014

Fingerprint

Solanum
Lycopersicon esculentum
tomatoes
Single Nucleotide Polymorphism
Genome
genetic variation
genome
Fruit
crops
Genes
fruits
heterozygosity
genes
Growth
probability analysis
Sequence Alignment
growth habit
sequence alignment
Habits
Ecosystem

Keywords

  • single-nucleotide polymorphisms
  • burrows-wheeler transform
  • wild tomatoes
  • genus lycopersicon
  • read alignment
  • fruit size
  • evolution
  • domestication
  • solanaceae
  • plant

Cite this

@article{bbff1eab65e643fd83f484e7185c6c10,
title = "Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing",
abstract = "We explored genetic variation by sequencing a selection of 84 tomato accessions and related wild species representative for the Lycopersicon, Arcanum, Eriopersicon, and Neolycopersicon groups which has yielded a huge amount of precious data on sequence diversity in the tomato clade. Three new reference genomes were reconstructed to support our comparative genome analyses. Comparative sequence alignment reveals group-, species-, and accession-specific polymorphisms, which explains characteristic fruit traits and growth habits in the different cultivars. Using gene models from the annotated Heinz 1706 reference genome, we observed differences dN/dS ratio in fruit and growth diversification genes compared to a random set of genes, pointing to positive selection and to differences in selection pressure between crop accessions and wild species. In wild species SNPs are found in excess of 10 million, i.e. 20 fold higher than found in most of the crop accessions, indicating dramatic genetic erosion of crop and heirloom tomatoes. In addition, highest levels of heterozygosity were found for allogamous SI wild species, while facultative and autogamous SC species display a lower heterozygosity level. Using whole genome SNP information for Maximum Likelihood analysis we achieved complete tree resolution, whereas ML trees based on SNPs from 10 fruit and growth genes show incomplete resolution for the crop accessions, partly due to the effect of heterozygous SNPs. Finally, results suggest that phylogenetic relationships are correlated with habitat pointing at the occurrence of geographical races within these groups, which is of practical importance for Solanum genome evolution studies.",
keywords = "single-nucleotide polymorphisms, burrows-wheeler transform, wild tomatoes, genus lycopersicon, read alignment, fruit size, evolution, domestication, solanaceae, plant",
author = "S.A. Aflitos and E.G.W.M. Schijlen and {de Jong}, J.H.S.G.M. and {de Ridder}, D. and S. Smit and H.J. Finkers and F.T. Bakker and {van de Geest}, H.C. and {te Lintel Hekkert}, B. and {van Haarst}, J.C. and L.W.M. Smits and A.J. Koops and M.J. Sanchez-Perez and {van Heusden}, A.W. and R.G.F. Visser and M.E. Schranz and S.A. Peters",
year = "2014",
doi = "10.1111/tpj.12616",
language = "English",
volume = "80",
pages = "136--148",
journal = "The Plant Journal",
issn = "0960-7412",
publisher = "Wiley",
number = "1",

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TY - JOUR

T1 - Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing

AU - Aflitos, S.A.

AU - Schijlen, E.G.W.M.

AU - de Jong, J.H.S.G.M.

AU - de Ridder, D.

AU - Smit, S.

AU - Finkers, H.J.

AU - Bakker, F.T.

AU - van de Geest, H.C.

AU - te Lintel Hekkert, B.

AU - van Haarst, J.C.

AU - Smits, L.W.M.

AU - Koops, A.J.

AU - Sanchez-Perez, M.J.

AU - van Heusden, A.W.

AU - Visser, R.G.F.

AU - Schranz, M.E.

AU - Peters, S.A.

PY - 2014

Y1 - 2014

N2 - We explored genetic variation by sequencing a selection of 84 tomato accessions and related wild species representative for the Lycopersicon, Arcanum, Eriopersicon, and Neolycopersicon groups which has yielded a huge amount of precious data on sequence diversity in the tomato clade. Three new reference genomes were reconstructed to support our comparative genome analyses. Comparative sequence alignment reveals group-, species-, and accession-specific polymorphisms, which explains characteristic fruit traits and growth habits in the different cultivars. Using gene models from the annotated Heinz 1706 reference genome, we observed differences dN/dS ratio in fruit and growth diversification genes compared to a random set of genes, pointing to positive selection and to differences in selection pressure between crop accessions and wild species. In wild species SNPs are found in excess of 10 million, i.e. 20 fold higher than found in most of the crop accessions, indicating dramatic genetic erosion of crop and heirloom tomatoes. In addition, highest levels of heterozygosity were found for allogamous SI wild species, while facultative and autogamous SC species display a lower heterozygosity level. Using whole genome SNP information for Maximum Likelihood analysis we achieved complete tree resolution, whereas ML trees based on SNPs from 10 fruit and growth genes show incomplete resolution for the crop accessions, partly due to the effect of heterozygous SNPs. Finally, results suggest that phylogenetic relationships are correlated with habitat pointing at the occurrence of geographical races within these groups, which is of practical importance for Solanum genome evolution studies.

AB - We explored genetic variation by sequencing a selection of 84 tomato accessions and related wild species representative for the Lycopersicon, Arcanum, Eriopersicon, and Neolycopersicon groups which has yielded a huge amount of precious data on sequence diversity in the tomato clade. Three new reference genomes were reconstructed to support our comparative genome analyses. Comparative sequence alignment reveals group-, species-, and accession-specific polymorphisms, which explains characteristic fruit traits and growth habits in the different cultivars. Using gene models from the annotated Heinz 1706 reference genome, we observed differences dN/dS ratio in fruit and growth diversification genes compared to a random set of genes, pointing to positive selection and to differences in selection pressure between crop accessions and wild species. In wild species SNPs are found in excess of 10 million, i.e. 20 fold higher than found in most of the crop accessions, indicating dramatic genetic erosion of crop and heirloom tomatoes. In addition, highest levels of heterozygosity were found for allogamous SI wild species, while facultative and autogamous SC species display a lower heterozygosity level. Using whole genome SNP information for Maximum Likelihood analysis we achieved complete tree resolution, whereas ML trees based on SNPs from 10 fruit and growth genes show incomplete resolution for the crop accessions, partly due to the effect of heterozygous SNPs. Finally, results suggest that phylogenetic relationships are correlated with habitat pointing at the occurrence of geographical races within these groups, which is of practical importance for Solanum genome evolution studies.

KW - single-nucleotide polymorphisms

KW - burrows-wheeler transform

KW - wild tomatoes

KW - genus lycopersicon

KW - read alignment

KW - fruit size

KW - evolution

KW - domestication

KW - solanaceae

KW - plant

U2 - 10.1111/tpj.12616

DO - 10.1111/tpj.12616

M3 - Article

VL - 80

SP - 136

EP - 148

JO - The Plant Journal

JF - The Plant Journal

SN - 0960-7412

IS - 1

ER -