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New insights into domestication of carrot from root transcriptome analyses

BACKGROUND: Understanding the molecular basis of domestication can provide insights into the processes of rapid evolution and crop improvement. Here we demonstrated the processes of carrot domestication and identified genes under selection based on transcriptome analyses. RESULTS: The root transcrip...

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Autores principales: Rong, Jun, Lammers, Youri, Strasburg, Jared L, Schidlo, Natasha S, Ariyurek, Yavuz, de Jong, Tom J, Klinkhamer, Peter GL, Smulders, Marinus JM, Vrieling, Klaas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4213543/
https://www.ncbi.nlm.nih.gov/pubmed/25311557
http://dx.doi.org/10.1186/1471-2164-15-895
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author Rong, Jun
Lammers, Youri
Strasburg, Jared L
Schidlo, Natasha S
Ariyurek, Yavuz
de Jong, Tom J
Klinkhamer, Peter GL
Smulders, Marinus JM
Vrieling, Klaas
author_facet Rong, Jun
Lammers, Youri
Strasburg, Jared L
Schidlo, Natasha S
Ariyurek, Yavuz
de Jong, Tom J
Klinkhamer, Peter GL
Smulders, Marinus JM
Vrieling, Klaas
author_sort Rong, Jun
collection PubMed
description BACKGROUND: Understanding the molecular basis of domestication can provide insights into the processes of rapid evolution and crop improvement. Here we demonstrated the processes of carrot domestication and identified genes under selection based on transcriptome analyses. RESULTS: The root transcriptomes of widely differing cultivated and wild carrots were sequenced. A method accounting for sequencing errors was introduced to optimize SNP (single nucleotide polymorphism) discovery. 11,369 SNPs were identified. Of these, 622 (out of 1000 tested SNPs) were validated and used to genotype a large set of cultivated carrot, wild carrot and other wild Daucus carota subspecies, primarily of European origin. Phylogenetic analysis indicated that eastern carrot may originate from Western Asia and western carrot may be selected from eastern carrot. Different wild D. carota subspecies may have contributed to the domestication of cultivated carrot. Genetic diversity was significantly reduced in western cultivars, probably through bottlenecks and selection. However, a high proportion of genetic diversity (more than 85% of the genetic diversity in wild populations) is currently retained in western cultivars. Model simulation indicated high and asymmetric gene flow from wild to cultivated carrots, spontaneously and/or by introgression breeding. Nevertheless, high genetic differentiation exists between cultivated and wild carrots (Fst = 0.295) showing the strong effects of selection. Expression patterns differed radically for some genes between cultivated and wild carrot roots which may be related to changes in root traits. The up-regulation of water-channel-protein gene expression in cultivars might be involved in changing water content and transport in roots. The activated expression of carotenoid-binding-protein genes in cultivars could be related to the high carotenoid accumulation in roots. The silencing of allergen-protein-like genes in cultivated carrot roots suggested strong human selection to reduce allergy. These results suggest that regulatory changes of gene expressions may have played a predominant role in domestication. CONCLUSIONS: Western carrots may originate from eastern carrots. The reduction in genetic diversity in western cultivars due to domestication bottleneck/selection may have been offset by introgression from wild carrot. Differential gene expression patterns between cultivated and wild carrot roots may be a signature of strong selection for favorable cultivation traits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-895) contains supplementary material, which is available to authorized users.
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spelling pubmed-42135432014-10-31 New insights into domestication of carrot from root transcriptome analyses Rong, Jun Lammers, Youri Strasburg, Jared L Schidlo, Natasha S Ariyurek, Yavuz de Jong, Tom J Klinkhamer, Peter GL Smulders, Marinus JM Vrieling, Klaas BMC Genomics Research Article BACKGROUND: Understanding the molecular basis of domestication can provide insights into the processes of rapid evolution and crop improvement. Here we demonstrated the processes of carrot domestication and identified genes under selection based on transcriptome analyses. RESULTS: The root transcriptomes of widely differing cultivated and wild carrots were sequenced. A method accounting for sequencing errors was introduced to optimize SNP (single nucleotide polymorphism) discovery. 11,369 SNPs were identified. Of these, 622 (out of 1000 tested SNPs) were validated and used to genotype a large set of cultivated carrot, wild carrot and other wild Daucus carota subspecies, primarily of European origin. Phylogenetic analysis indicated that eastern carrot may originate from Western Asia and western carrot may be selected from eastern carrot. Different wild D. carota subspecies may have contributed to the domestication of cultivated carrot. Genetic diversity was significantly reduced in western cultivars, probably through bottlenecks and selection. However, a high proportion of genetic diversity (more than 85% of the genetic diversity in wild populations) is currently retained in western cultivars. Model simulation indicated high and asymmetric gene flow from wild to cultivated carrots, spontaneously and/or by introgression breeding. Nevertheless, high genetic differentiation exists between cultivated and wild carrots (Fst = 0.295) showing the strong effects of selection. Expression patterns differed radically for some genes between cultivated and wild carrot roots which may be related to changes in root traits. The up-regulation of water-channel-protein gene expression in cultivars might be involved in changing water content and transport in roots. The activated expression of carotenoid-binding-protein genes in cultivars could be related to the high carotenoid accumulation in roots. The silencing of allergen-protein-like genes in cultivated carrot roots suggested strong human selection to reduce allergy. These results suggest that regulatory changes of gene expressions may have played a predominant role in domestication. CONCLUSIONS: Western carrots may originate from eastern carrots. The reduction in genetic diversity in western cultivars due to domestication bottleneck/selection may have been offset by introgression from wild carrot. Differential gene expression patterns between cultivated and wild carrot roots may be a signature of strong selection for favorable cultivation traits. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-895) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-14 /pmc/articles/PMC4213543/ /pubmed/25311557 http://dx.doi.org/10.1186/1471-2164-15-895 Text en © Rong et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Rong, Jun
Lammers, Youri
Strasburg, Jared L
Schidlo, Natasha S
Ariyurek, Yavuz
de Jong, Tom J
Klinkhamer, Peter GL
Smulders, Marinus JM
Vrieling, Klaas
New insights into domestication of carrot from root transcriptome analyses
title New insights into domestication of carrot from root transcriptome analyses
title_full New insights into domestication of carrot from root transcriptome analyses
title_fullStr New insights into domestication of carrot from root transcriptome analyses
title_full_unstemmed New insights into domestication of carrot from root transcriptome analyses
title_short New insights into domestication of carrot from root transcriptome analyses
title_sort new insights into domestication of carrot from root transcriptome analyses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4213543/
https://www.ncbi.nlm.nih.gov/pubmed/25311557
http://dx.doi.org/10.1186/1471-2164-15-895
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