New insights into domestication of carrot from root transcriptome analyses

Jun Rong, Youri Lammers, Jared L. Strasburg, Natasha S. Schidlo, Yavuz Ariyurek, Tom J. De Jong, Peter G.L. Klinkhamer, Marinus J.M. Smulders, Klaas Vrieling

Research output: Contribution to journalArticlepeer-review

33 Scopus citations

Abstract

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.

Original languageEnglish (US)
Article number895
JournalBMC Genomics
Volume15
Issue number1
DOIs
StatePublished - 2014

Bibliographical note

Funding Information:
We thank Sophie Greve and colleagues of Leiden Genome Technology Center for their support of our study and Yu Sun and Songting Shi of Leiden University Medical Center for their help and comments. We thank Cilia Grebenstein for providing carrot seeds and Prof. Martien Groenen, Dr. Hendrik-Jan Megens, Laura Bertola and Dick Groenenberg for helping with phylogenetic analysis. We are grateful to Dandan Cheng, Karin A. M. van der Veen, Cilke M. Hermans and Henk W. Nell for helping grow the carrots. Peter J. Steenbergen is thanked for genotyping 21 cultivated and wild accessions at 89 SNP positions. Prof. Allison A. Snow of The Ohio State University is thanked for comments on the manuscript. We thank Warwick Genetic Resources Unit in the United Kingdom and The Genebank of the Leibniz Institute of Plant Genetics and Crop Plant Research (IPK Gatersleben) in Germany for providing carrot materials. We are grateful to Dorien Postma-Haarsma, Henk Huits and colleagues of Bejo Zaden B.V. for their supports in SNP validation. Finally, we thank Nigel Harle for his revision of our English. This work was supported by the research program “Ecology Regarding Genetically Modified Organisms” (ERGO) No. 838.06.031 of the Dutch Ministries for the Environment, Economic Affairs, Agriculture and Science and Education, implemented by the Earth and Life Sciences Council (ALW) of The Netherlands Organisation for Scientific Research (NWO).

Publisher Copyright:
© 2014 Rong et al.

Keywords

  • Crop and wild relative
  • Daucus carota
  • Domestication gene
  • Gene expression difference
  • High-throughput sequencing
  • Root transcriptome
  • Single nucleotide polymorphism

Fingerprint

Dive into the research topics of 'New insights into domestication of carrot from root transcriptome analyses'. Together they form a unique fingerprint.

Cite this