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The mitochondrial genome of Paragyrodactylus variegatus (Platyhelminthes: Monogenea): differences in major non-coding region and gene order compared to Gyrodactylus.

Ye F, King SD, Cone DK, You P - Parasit Vectors (2014)

Bottom Line: The gene order (tRNAGln, tRNAMet and NCR) differs in arrangement compared to the mitochondrial genomes reported from Gyrodactylus spp.Both morphological characters and characteristics of the mitochondrial genome support Paragyrodactylus as a distinct genus from Gyrodactylus.Considering their specific distribution and known hosts, we believe that Paragyrodactylus is a relict freshwater lineage of viviparous monogenean isolated in the high plateaus of central Asia on closely related river loaches.

View Article: PubMed Central - PubMed

Affiliation: Co-Innovation Center for Qinba regions' sustainable development, College of Life Science, Shaanxi Normal University, Xi'an 710062, China. youping@snnu.edu.cn.

ABSTRACT

Background: Paragyrodactylus Gvosdev and Martechov, 1953, a viviparous genus of ectoparasite within the Gyrodactylidae, contains three nominal species all of which infect Asian river loaches. The group is suspected to be a basal lineage within Gyrodactylus Nordmann, 1832 sensu lato although this remains unclear. Further molecular study, beyond characterization of the standard Internal Transcribed Spacer region, is needed to clarify the evolutionary relationships within the family and the placement of this genus.

Methods: The mitochondrial genome of Paragyrodactylus variegatus You, King, Ye and Cone, 2014 was amplified in six parts from a single worm, sequenced using primer walking, annotated and analyzed using bioinformatic tools.

Results: The mitochondrial genome of P. variegatus is 14,517 bp, containing 12 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, two ribosomal RNA (rRNA) genes and a major non-coding region (NCR). The overall A + T content of the mitochondrial genome is 76.3%, which is higher than all reported mitochondrial genomes of monogeneans. All of the 22 tRNAs have the typical cloverleaf secondary structure, except tRNACys, tRNASer1 and tRNASer2 that lack the dihydrouridine (DHU) arm. There are six domains (domain III is absent) and three domains in the inferred secondary structures of the large ribosomal subunit (rrnL) and small ribosomal subunit (rrnS), respectively. The NCR includes six 40 bp tandem repeat units and has the double identical poly-T stretches, stem-loop structure and some surrounding structure elements. The gene order (tRNAGln, tRNAMet and NCR) differs in arrangement compared to the mitochondrial genomes reported from Gyrodactylus spp.

Conclusion: The Duplication and Random Loss Model and Recombination Model together are the most plausible explanations for the variation in gene order. Both morphological characters and characteristics of the mitochondrial genome support Paragyrodactylus as a distinct genus from Gyrodactylus. Considering their specific distribution and known hosts, we believe that Paragyrodactylus is a relict freshwater lineage of viviparous monogenean isolated in the high plateaus of central Asia on closely related river loaches.

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Gene arrangements of ten monogenean species. Gene and genome size are not to scale. All genes are transcribed in the same direction (form left to right). Red and black box shows the conserved gene cluster and gene rearrangement hot spot, respectively. The non-coding region (>500 bp) is denoted by the NCR. The same gene arrangement of three Gyrodactylus species (G. salaris, G. derjavinoides and G. thymalli) is shown as Gyrodactylus spp.
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Fig7: Gene arrangements of ten monogenean species. Gene and genome size are not to scale. All genes are transcribed in the same direction (form left to right). Red and black box shows the conserved gene cluster and gene rearrangement hot spot, respectively. The non-coding region (>500 bp) is denoted by the NCR. The same gene arrangement of three Gyrodactylus species (G. salaris, G. derjavinoides and G. thymalli) is shown as Gyrodactylus spp.

Mentions: Five available mitochondrial gene arrangements of monopisthocotylids are shown in Figure 7. The arrangement of all rRNA and protein coding genes are identical throughout all samples, however, the tRNA genes differ in arrangement showing some translocation, particularly long-range translocation. No notable rearrangement hot spot could be found in gene arrangements of monopisthocotylids, however, the major change of gene arrangement among polyopisthocotylids is limited in the COIII-ND5 junction as a gene rearrangement hot spot [26]. Two gene clusters (tRNAAsn-tRNAPro-tRNAIle-tRNALys and rrnL-tRNACys-rrnS) were found to be conserved in all mitochondrial genomes of monopisthocotyleans. Nevertheless, the tRNALys and tRNACys were found in the gene rearrangement hot spot of polyopisthocotyleans. The conserved gene clusters could potentially be a marker used to help define the Polyopisthocotylea and Monopisthocotylea within the monogenea, as well as providing information for a deeper understanding of the evolution of monogenean mitochondrial genomes.Figure 7


The mitochondrial genome of Paragyrodactylus variegatus (Platyhelminthes: Monogenea): differences in major non-coding region and gene order compared to Gyrodactylus.

Ye F, King SD, Cone DK, You P - Parasit Vectors (2014)

Gene arrangements of ten monogenean species. Gene and genome size are not to scale. All genes are transcribed in the same direction (form left to right). Red and black box shows the conserved gene cluster and gene rearrangement hot spot, respectively. The non-coding region (>500 bp) is denoted by the NCR. The same gene arrangement of three Gyrodactylus species (G. salaris, G. derjavinoides and G. thymalli) is shown as Gyrodactylus spp.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4150975&req=5

Fig7: Gene arrangements of ten monogenean species. Gene and genome size are not to scale. All genes are transcribed in the same direction (form left to right). Red and black box shows the conserved gene cluster and gene rearrangement hot spot, respectively. The non-coding region (>500 bp) is denoted by the NCR. The same gene arrangement of three Gyrodactylus species (G. salaris, G. derjavinoides and G. thymalli) is shown as Gyrodactylus spp.
Mentions: Five available mitochondrial gene arrangements of monopisthocotylids are shown in Figure 7. The arrangement of all rRNA and protein coding genes are identical throughout all samples, however, the tRNA genes differ in arrangement showing some translocation, particularly long-range translocation. No notable rearrangement hot spot could be found in gene arrangements of monopisthocotylids, however, the major change of gene arrangement among polyopisthocotylids is limited in the COIII-ND5 junction as a gene rearrangement hot spot [26]. Two gene clusters (tRNAAsn-tRNAPro-tRNAIle-tRNALys and rrnL-tRNACys-rrnS) were found to be conserved in all mitochondrial genomes of monopisthocotyleans. Nevertheless, the tRNALys and tRNACys were found in the gene rearrangement hot spot of polyopisthocotyleans. The conserved gene clusters could potentially be a marker used to help define the Polyopisthocotylea and Monopisthocotylea within the monogenea, as well as providing information for a deeper understanding of the evolution of monogenean mitochondrial genomes.Figure 7

Bottom Line: The gene order (tRNAGln, tRNAMet and NCR) differs in arrangement compared to the mitochondrial genomes reported from Gyrodactylus spp.Both morphological characters and characteristics of the mitochondrial genome support Paragyrodactylus as a distinct genus from Gyrodactylus.Considering their specific distribution and known hosts, we believe that Paragyrodactylus is a relict freshwater lineage of viviparous monogenean isolated in the high plateaus of central Asia on closely related river loaches.

View Article: PubMed Central - PubMed

Affiliation: Co-Innovation Center for Qinba regions' sustainable development, College of Life Science, Shaanxi Normal University, Xi'an 710062, China. youping@snnu.edu.cn.

ABSTRACT

Background: Paragyrodactylus Gvosdev and Martechov, 1953, a viviparous genus of ectoparasite within the Gyrodactylidae, contains three nominal species all of which infect Asian river loaches. The group is suspected to be a basal lineage within Gyrodactylus Nordmann, 1832 sensu lato although this remains unclear. Further molecular study, beyond characterization of the standard Internal Transcribed Spacer region, is needed to clarify the evolutionary relationships within the family and the placement of this genus.

Methods: The mitochondrial genome of Paragyrodactylus variegatus You, King, Ye and Cone, 2014 was amplified in six parts from a single worm, sequenced using primer walking, annotated and analyzed using bioinformatic tools.

Results: The mitochondrial genome of P. variegatus is 14,517 bp, containing 12 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, two ribosomal RNA (rRNA) genes and a major non-coding region (NCR). The overall A + T content of the mitochondrial genome is 76.3%, which is higher than all reported mitochondrial genomes of monogeneans. All of the 22 tRNAs have the typical cloverleaf secondary structure, except tRNACys, tRNASer1 and tRNASer2 that lack the dihydrouridine (DHU) arm. There are six domains (domain III is absent) and three domains in the inferred secondary structures of the large ribosomal subunit (rrnL) and small ribosomal subunit (rrnS), respectively. The NCR includes six 40 bp tandem repeat units and has the double identical poly-T stretches, stem-loop structure and some surrounding structure elements. The gene order (tRNAGln, tRNAMet and NCR) differs in arrangement compared to the mitochondrial genomes reported from Gyrodactylus spp.

Conclusion: The Duplication and Random Loss Model and Recombination Model together are the most plausible explanations for the variation in gene order. Both morphological characters and characteristics of the mitochondrial genome support Paragyrodactylus as a distinct genus from Gyrodactylus. Considering their specific distribution and known hosts, we believe that Paragyrodactylus is a relict freshwater lineage of viviparous monogenean isolated in the high plateaus of central Asia on closely related river loaches.

Show MeSH
Related in: MedlinePlus