Functional Gene Polymorphism to Reveal Species History: The Case of the CRTISO Gene in Cultivated Carrots

Vanessa Soufflet-Freslon,Sébastien Huet,Emmanuel Geoffriau,Mathilde Briard,Jérémy Clotault,Matthieu Jourdan,Didier Peltier

doi:10.1371/journal.pone.0070801

Vanessa Soufflet-Freslon, Sébastien Huet + Show 5 more

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https://doi.org/10.1371/journal.pone.0070801

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Abstract

BackgroundCarrot is a vegetable cultivated worldwide for the consumption of its root. Historical data indicate that root colour has been differentially selected over time and according to geographical areas. Root pigmentation depends on the relative proportion of different carotenoids for the white, yellow, orange and red types but only internally for the purple one. The genetic control for root carotenoid content might be partially associated with carotenoid biosynthetic genes. Carotenoid isomerase (CRTISO) has emerged as a regulatory step in the carotenoid biosynthesis pathway and could be a good candidate to show how a metabolic pathway gene reflects a species genetic history.Methodology/Principal FindingsIn this study, the nucleotide polymorphism and the linkage disequilibrium among the complete CRTISO sequence, and the deviation from neutral expectation were analysed by considering population subdivision revealed with 17 microsatellite markers. A sample of 39 accessions, which represented different geographical origins and root colours, was used. Cultivated carrot was divided into two genetic groups: one from Middle East and Asia (Eastern group), and another one mainly from Europe (Western group). The Western and Eastern genetic groups were suggested to be differentially affected by selection: a signature of balancing selection was detected within the first group whereas the second one showed no selection. A focus on orange-rooted carrots revealed that cultivars cultivated in Asia were mainly assigned to the Western group but showed CRTISO haplotypes common to Eastern carrots.ConclusionThe carotenoid pathway CRTISO gene data proved to be complementary to neutral markers in order to bring critical insight in the cultivated carrot history. We confirmed the occurrence of two migration events since domestication. Our results showed a European background in material from Japan and Central Asia. While confirming the introduction of European carrots in Japanese resources, the history of Central Asia material remains unclear.

Highlights

Selection events along the species or breeding history generally lead to signatures of selection at the molecular level, i.e. local variations of diversity or allele frequencies at genes underlying phenotypic variations or in their surrounding region
The second cluster contained 20 individuals, only sampled in Middle East or Asia, except the Swiss cultivar ‘Kuttinger’. Most of these individuals showed red, purple or yellow roots. This second cluster was considered as the Eastern genetic group
This significant positive value was observed for the whole dataset and the Western genetic group, whereas the Eastern genetic group exhibited a neutral evolution pattern. It appears that Carotenoid isomerase (CRTISO) evolved differentially in the Western and Eastern genetic groups. These results suggest balancing selection as the force governing CRTISO evolution in the Western genetic group, and are congruent with the high linkage disequilibrium and the high silent-site nucleotide diversity detected in this genetic group

Summary

Introduction

Selection events along the species or breeding history generally lead to signatures of selection at the molecular level, i.e. local variations of diversity or allele frequencies at genes underlying phenotypic variations or in their surrounding region. Signatures of selection are detected or not, according to the targeted genomic region and the linkage disequilibrium (LD; i.e., the nonrandom association of alleles at different loci) throughout the gene. Sativus), cultivated worldwide, might have lead to such selection signatures The domestication of this species is thought to have occurred in the Afghanistan region before the 900 s [4]. The first cultivated carrots were purple or yellow rooted Their cultivation spread along trade routes, reaching Middle East and North Africa, and to Europe in the Middle Ages. They were gradually replaced by white- and orange-rooted forms, which appeared in the 1600 s [5]. Carotenoid isomerase (CRTISO) has emerged as a regulatory step in the carotenoid biosynthesis pathway and could be a good candidate to show how a metabolic pathway gene reflects a species genetic history

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