Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes
<p>Abstract</p> <p>Background</p> <p>The 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, membe...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2013-01-01
|
| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | http://www.biomedcentral.com/1471-2148/13/12 |
| _version_ | 1818775677832265728 |
|---|---|
| author | Sultana Tahera Kim Jiyeon Lee Sang-Hwa Han Hyerim Kim Sanghee Min Gi-Sik Nadler Steven A Park Joogn-Ki |
| author_facet | Sultana Tahera Kim Jiyeon Lee Sang-Hwa Han Hyerim Kim Sanghee Min Gi-Sik Nadler Steven A Park Joogn-Ki |
| author_sort | Sultana Tahera |
| collection | DOAJ |
| description | <p>Abstract</p> <p>Background</p> <p>The 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 <it>Bursaphelenchus</it> 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 <it>Aphelenchus</it> spp. within Tylenchomorpha, but <it>Bursaphelenchus</it> and <it>Aphelenchoides</it> 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 <it>Bursaphelenchus xylophilus</it> (Aphelenchoidea) and <it>Pratylenchus vulnus</it> (Tylenchoidea).</p> <p>Results</p> <p>The complete mitochondrial genomes of <it>B. xylophilus</it> and <it>P. vulnus</it> are 14,778 bp and 21,656 bp, respectively, and identical to all other chromadorean nematode mtDNAs in that they contain 36 genes (lacking <it>atp8</it>) 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 <it>B. xylophilus</it> as most closely related to Tylenchomorpha (Tylenchoidea). Instead, <it>B. xylophilus,</it> was nested within a strongly supported clade consisting of species from infraorders Rhabditomorpha, Panagrolaimomorpha, Diplogasteromorpha, and Ascaridomorpha. The clade containing sampled Tylenchoidea (<it>P. vulnus, H. glycines</it>, and <it>R. similis</it>) 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 <it>B. xylophilus</it> (Aphelenchoidea) plus Tylenchoidea, Tylenchoidea plus Diplogasteromorpha (<it>Pristionchus pacificus</it>), or <it>B. xylophilus</it> plus Diplogasteromorpha were significantly worse interpretations of the mtDNA data.</p> <p>Conclusions</p> <p>Phylogenetic trees inferred from nucleotide and amino acid sequences of mtDNA coding genes are in agreement that <it>B. xylophilus</it> (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 certain morphological similarities between these stylet-bearing nematodes must result from convergent evolution. In addition, the exceptionally large mtDNA genome size of <it>P. vulnus</it>, which is the largest among chromadorean nematode mtDNAs sequenced to date, results from lengthy repeated segments in non-coding regions.</p> |
| first_indexed | 2024-12-18T11:00:51Z |
| format | Article |
| id | doaj.art-f4f78f0ab6744a1abc6771814eb05373 |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-18T11:00:51Z |
| publishDate | 2013-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-f4f78f0ab6744a1abc6771814eb053732022-12-21T21:10:13ZengBMCBMC Evolutionary Biology1471-21482013-01-011311210.1186/1471-2148-13-12Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodesSultana TaheraKim JiyeonLee Sang-HwaHan HyerimKim SangheeMin Gi-SikNadler Steven APark Joogn-Ki<p>Abstract</p> <p>Background</p> <p>The 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 <it>Bursaphelenchus</it> 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 <it>Aphelenchus</it> spp. within Tylenchomorpha, but <it>Bursaphelenchus</it> and <it>Aphelenchoides</it> 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 <it>Bursaphelenchus xylophilus</it> (Aphelenchoidea) and <it>Pratylenchus vulnus</it> (Tylenchoidea).</p> <p>Results</p> <p>The complete mitochondrial genomes of <it>B. xylophilus</it> and <it>P. vulnus</it> are 14,778 bp and 21,656 bp, respectively, and identical to all other chromadorean nematode mtDNAs in that they contain 36 genes (lacking <it>atp8</it>) 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 <it>B. xylophilus</it> as most closely related to Tylenchomorpha (Tylenchoidea). Instead, <it>B. xylophilus,</it> was nested within a strongly supported clade consisting of species from infraorders Rhabditomorpha, Panagrolaimomorpha, Diplogasteromorpha, and Ascaridomorpha. The clade containing sampled Tylenchoidea (<it>P. vulnus, H. glycines</it>, and <it>R. similis</it>) 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 <it>B. xylophilus</it> (Aphelenchoidea) plus Tylenchoidea, Tylenchoidea plus Diplogasteromorpha (<it>Pristionchus pacificus</it>), or <it>B. xylophilus</it> plus Diplogasteromorpha were significantly worse interpretations of the mtDNA data.</p> <p>Conclusions</p> <p>Phylogenetic trees inferred from nucleotide and amino acid sequences of mtDNA coding genes are in agreement that <it>B. xylophilus</it> (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 certain morphological similarities between these stylet-bearing nematodes must result from convergent evolution. In addition, the exceptionally large mtDNA genome size of <it>P. vulnus</it>, which is the largest among chromadorean nematode mtDNAs sequenced to date, results from lengthy repeated segments in non-coding regions.</p>http://www.biomedcentral.com/1471-2148/13/12Plant parasitismTylenchomorphaChromadoreaNematodaMitochondrial genomeMolecular phylogeny |
| spellingShingle | Sultana Tahera Kim Jiyeon Lee Sang-Hwa Han Hyerim Kim Sanghee Min Gi-Sik Nadler Steven A Park Joogn-Ki Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes BMC Evolutionary Biology Plant parasitism Tylenchomorpha Chromadorea Nematoda Mitochondrial genome Molecular phylogeny |
| title | Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes |
| title_full | Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes |
| title_fullStr | Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes |
| title_full_unstemmed | Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes |
| title_short | Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes |
| title_sort | comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant parasitic nematodes |
| topic | Plant parasitism Tylenchomorpha Chromadorea Nematoda Mitochondrial genome Molecular phylogeny |
| url | http://www.biomedcentral.com/1471-2148/13/12 |
| work_keys_str_mv | AT sultanatahera comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT kimjiyeon comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT leesanghwa comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT hanhyerim comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT kimsanghee comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT mingisik comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT nadlerstevena comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes AT parkjoognki comparativeanalysisofcompletemitochondrialgenomesequencesconfirmsindependentoriginsofplantparasiticnematodes |