Abstract

The soil-borne nematode Xiphinema index is closely linked to its main host, the grapevine, and presents a major threat to vineyards worldwide due to its ability to transmit Grapevine fanleaf virus (GFLV). The phylogeography of X. index has been studied using mitochondrial and microsatellite markers in samples from most regions of its worldwide distribution to reveal its genetic diversity. We first used the mitochondrial marker CytB and illustrated the low intraspecific divergence of this mainly meiotic parthenogenetic species. To generate a higher polymorphism level, we then concatenated the sequences of CytB and three mitochondrial markers, ATP6, CO1 and ND4, to obtain a 3044-bp fragment. We differentiated two clades, which each contained two well-supported subclades. Samples from the eastern Mediterranean and the Near and Middle East were grouped into three of these subclades, whereas the samples from the western Mediterranean, Europe and the Americas all belonged to the fourth subclade. The highest polymorphism level was found in the samples of one of the Middle and Near East subclades, strongly suggesting that this region contained the native area of the nematode. An east-to-west nematode dissemination hypothesis appeared to match the routes of the domesticated grapevine during Antiquity, presumably mainly dispersed by the Greeks and the Romans. Surprisingly, the samples of the western subclade comprised only two highly similar mitochondrial haplotypes. The first haplotype, from southern Iberian Peninsula, Bordeaux and Provence vineyards, exhibited a high microsatellite polymorphism level that suggests introductions dating from Antiquity. The second haplotype contained a highly predominant microsatellite genotype widespread in distant western countries that may be a consequence of the massive grapevine replanting following the 19th-century phylloxera crisis. Finally, our study enabled us to draw a first scaffold of X. index diversity at the global scale.

Highlights

  • To date, more than 4,100 species of plant-parasitic nematodes have been described[1] worldwide

  • Because of the low resolution of this single marker, we described the nematode phylogeographical patterns using Cytochrome B (CytB) concatenated with three other mitochondrial genes, ATP synthase subunit 6 (ATP6), Cytochrome c oxidase subunit 1 (CO1) and NADH dehydrogenase subunit 4 (ND4)

  • Our study first allowed us to evaluate the overall diversity of X. index, a species reproducing mainly by meiotic parthenogenesis

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Summary

Introduction

More than 4,100 species of plant-parasitic nematodes have been described[1] worldwide. GFLV is known as the most severe viral disease of grapevines It is responsible for fanleaf degeneration[6], which occurs in temperate regions of vine cultivation[7,8]. The vector X. index is an ectoparasitic nematode present in Mediterranean environments and temperate climates where grapevine grows. It has a limited host range, and domesticated grapevine We report hereafter a diversity study using mitochondrial (maternal coding DNA) and microsatellite (nuclear noncoding DNA) markers. These markers are complementary and characterize different evolutionary time scales. In the model nematode Pristionchus pacificus, microsatellite markers have shown much higher mutation rates[31] (approx. 104-fold) than mitochondrial markers[32]

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