Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes

Abstract

BackgroundThe nematode infraorder Tylenchomorpha (Class Chromadorea) includes plant parasites that are of agricultural and economic importance, as well as insect-associates and fungal feeding species. Among tylenchomorph plant parasites, members of the superfamily Tylenchoidea, such as root-knot nematodes, have great impact on agriculture. Of the five superfamilies within Tylenchomorpha, one (Aphelenchoidea) includes mainly fungal-feeding species, but also some damaging plant pathogens, including certain Bursaphelenchus spp. The evolutionary relationships of tylenchoid and aphelenchoid nematodes have been disputed based on classical morphological features and molecular data. For example, similarities in the structure of the stomatostylet suggested a common evolutionary origin. In contrast, phylogenetic hypotheses based on nuclear SSU ribosomal DNA sequences have revealed paraphyly of Aphelenchoidea, with, for example, fungal-feeding Aphelenchus spp. within Tylenchomorpha, but Bursaphelenchus and Aphelenchoides spp. more closely related to infraorder Panagrolaimomorpha. We investigated phylogenetic relationships of plant-parasitic tylenchoid and aphelenchoid species in the context of other chromadorean nematodes based on comparative analysis of complete mitochondrial genome data, including two newly sequenced genomes from Bursaphelenchus xylophilus (Aphelenchoidea) and Pratylenchus vulnus (Tylenchoidea).ResultsThe complete mitochondrial genomes of B. xylophilus and P. vulnus are 14,778 bp and 21,656 bp, respectively, and identical to all other chromadorean nematode mtDNAs in that they contain 36 genes (lacking atp8) encoded in the same direction. Their mitochondrial protein-coding genes are biased toward use of amino acids encoded by T-rich codons, resulting in high A+T richness. Phylogenetic analyses of both nucleotide and amino acid sequence datasets using maximum likelihood and Bayesian methods did not support B. xylophilus as most closely related to Tylenchomorpha (Tylenchoidea). Instead, B. xylophilus, was nested within a strongly supported clade consisting of species from infraorders Rhabditomorpha, Panagrolaimomorpha, Diplogasteromorpha, and Ascaridomorpha. The clade containing sampled Tylenchoidea (P. vulnus, H. glycines, and R. similis) was sister to all analyzed chromadoreans. Comparison of gene arrangement data was also consistent with the phylogenetic relationships as inferred from sequence data. Alternative tree topologies depicting a monophyletic grouping of B. xylophilus (Aphelenchoidea) plus Tylenchoidea, Tylenchoidea plus Diplogasteromorpha (Pristionchus pacificus), or B. xylophilus plus Diplogasteromorpha were significantly worse interpretations of the mtDNA data.ConclusionsPhylogenetic trees inferred from nucleotide and amino acid sequences of mtDNA coding genes are in agreement that B. xylophilus (the single representative of Aphelenchoidea) is not closely related to Tylenchoidea, indicating that these two groups of plant parasites do not share an exclusive most recent common ancestor, and that...

The complete mitochondrial genome of Toxascaris leonina: Comparison with other closely related species and phylogenetic implications

“…Some studies indicated that Ascarididae was more closely related to the Toxocaridae than to Anisakidae by molecular criteria (Nadler and Hudspeth, 1998;Nadler et al, 2007;Li et al, 2008b;Xie et al, 2011a), but were rejected by analyses using small subunit (SSU) and mt genome sequences (Blaxter et al, 1998;Meldal et al, 2007;Park et al, 2011;Sultana et al, 2013). The results of the present study supports that the Ascarididae was more closely related to the family Toxocaridae than to other families within the Ascaridomorpha, consistent with findings of a recent study (Liu et al, 2013b).…”

Mitochondrial genome plasticity among species of the nematode genus Meloidogyne (Nematoda: Tylenchina)

“…Using mt genes, Park et al (2011) found that Ascaridida, Oxyurida and Spirurida did not share a most recent common ancestor, which does not support the monophyly of Clade III. Furthermore, Sultana et al (2013b) demonstrated that B. xylophilus was not closely related to members of Tylenchoidea (Heterodera, Pratylenchus and Radopholus), confirming the independent origins of PPNs. In a recent study, Humphreys-Pereira and Elling (2014) used 12 mt PCGs to confirm the convergent evolution of sedentary endoparasitism in Meloidogyne and Heterodera.…”

“…At the time of this study (October 2014), there are 11 mt genomes of PPNs published, i.e., M. chitwoodi, M. incognita, Meloidogyne graminicola, Heterodera glycines, Globodera pallida, Globodera rostochiensis, Pratylenchus vulnus, R. similis, B. xylophilus, Bursaphelenchus mucronatus and Xiphinema americanum (Armstrong et al, 2000;He et al, 2005;Gibson et al, 2007Gibson et al, , 2011Jacob et al, 2009;Sultana et al, 2013aSultana et al, , 2013bSun et al, 2014;Besnard et al, 2014). It is likely that the development of new sequencing technologies will accelerate and improve the sequencing of more nematode mt genomes, e.g., Zasada et al (2014) describe the use of Illumina HTS for sequencing the mt genome of single individuals of X. americanum from 12 populations.…”

The mitochondrial genome of the pinewood nematode (Bursaphelenchus xylophilus) lineage introduced in Europe

“…We found that the COX3 termination codon (TAA) present in the recently reported mtDNA from a South Korean isolate [GQ332424 (Sultana et al, 2013)] is absent from the Portuguese isolates because of the deletion of a single base ( Figure 1A). The same deletion was observed in the partial mtDNA of a Japanese isolate identified in a BLAST search against B. xylophilus contigs available at http://www.genedb.org/ Homepage/Bxylophilus (Kikuchi et al, 2011).…”