Abstract

Meloidogyne graminicola is a facultative meiotic parthenogenetic root-knot nematode (RKN) that seriously threatens agriculture worldwide. We have little understanding of its origin, genomic structure, and intraspecific diversity. Such information would offer better knowledge of how this nematode successfully damages rice in many different environments. Previous studies on nuclear ribosomal DNA (nrDNA) suggested a close phylogenetic relationship between M. graminicola and Meloidogyne oryzae, despite their different modes of reproduction and geographical distribution. In order to clarify the evolutionary history of these two species and explore their molecular intraspecific diversity, we sequenced the genome of 12 M. graminicola isolates, representing populations of worldwide origins, and two South American isolates of M. oryzae. k-mer analysis of their nuclear genome and the detection of divergent homologous genomic sequences indicate that both species show a high proportion of heterozygous sites (ca. 1–2%), which had never been previously reported in facultative meiotic parthenogenetic RKNs. These analyses also point to a distinct ploidy level in each species, compatible with a diploid M. graminicola and a triploid M. oryzae. Phylogenetic analyses of mitochondrial genomes and three nuclear genomic sequences confirm close relationships between these two species, with M. graminicola being a putative parent of M. oryzae. In addition, comparative mitogenomics of those 12 M. graminicola isolates with a Chinese published isolate reveal only 15 polymorphisms that are phylogenetically non-informative. Eight mitotypes are distinguished, the most common one being shared by distant populations from Asia and America. This low intraspecific diversity, coupled with a lack of phylogeographic signal, suggests a recent worldwide expansion of M. graminicola.

Highlights

  • Nematodes constitute an ancient and diverse animal phylum [1] representing 80% of multicellular animals on Earth [2]

  • Obligatory cross-fertilization was reported in M. kikuyensis, facultative meiosis in M. graminicola, obligatory mitotic parthenogenesis in M. oryzae, and automictic or apomictic parthenogenesis in different polyploid or aneuploid forms, such as M. arenaria, M. incognita and M. javanica [9]

  • These sequences are AT-rich (83.2%) as previously reported in other two mitogenomes of M. oryzae were assembled, the first produced for this species

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Summary

Introduction

Nematodes constitute an ancient and diverse animal phylum [1] representing 80% of multicellular animals on Earth [2]. Plant parasitic nematodes (PPNs) cause an annual economic loss of over $US80 billion in agriculture worldwide [3]. Obligatory cross-fertilization was reported in M. kikuyensis, facultative meiosis (automixis) in M. graminicola, obligatory mitotic parthenogenesis (apomixis) in M. oryzae, and automictic or apomictic parthenogenesis in different polyploid or aneuploid forms, such as M. arenaria, M. incognita and M. javanica [9]. These variations in reproductive modes within RKNs were related to specific ploidy levels and host range [7,9]. He concluded that those features were characteristic of the establishment of meiotic and mitotic parthenogenesis in association with various degrees of polyploidy and aneuploidy

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