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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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Possible mechanism of mitochondrial gene rearrangements occurring inParagyrodactylus variegatusandGyrodactylusspp.
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Fig8: Possible mechanism of mitochondrial gene rearrangements occurring inParagyrodactylus variegatusandGyrodactylusspp.

Mentions: Gene rearrangement can be mainly explained by three mechanisms: Duplication and Random Loss Model [31, 32], Duplication and Nonrandom Loss Model [33] and Recombination Model [34]. The variation (tRNAGln, tRNAMet and NCR) of mitochondrial gene order occurring between P. variegatus and Gyrodactylus spp. could be explained by the duplication and random loss model and recombination model together with the parsimonious scenario. We assume that the process contains three steps: one tandem duplication, random loss, followed by intramitochondrial recombination (Figure 8). We prefer this mechanism for the following reasons: the duplicate NCRs in the mitochondrial genomes of most metazoans can be explained by the duplication and random loss model, but the stepwise mechanism described above is more appropriate to interpret the duplicated NCRs and long-range translocation, meanwhile the rest of the genes remain in their original state. Furthermore, there are several examples of mitochondrial recombination in animals [35–38], and a similar mechanism accounts for the gene rearrangement of other metazoans [39, 40]. In addition, the tRNAMet genes of Gyrodactylus spp. are clearly homologous to the tRNAMet gene of P. variegatus with 80.6% sequence similarity. However, the tRNAGln region does have low sequence similarity (66.2%) between the mitochondrial genomes of Gyrodactylus spp. and P. variegatus, so we cannot be certain that the translocation event happened. As more mitochondrial genomes of gyrodactylids become available, all of the above hypotheses should be tested with respect to gene orders.Figure 8


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)

Possible mechanism of mitochondrial gene rearrangements occurring inParagyrodactylus variegatusandGyrodactylusspp.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig8: Possible mechanism of mitochondrial gene rearrangements occurring inParagyrodactylus variegatusandGyrodactylusspp.
Mentions: Gene rearrangement can be mainly explained by three mechanisms: Duplication and Random Loss Model [31, 32], Duplication and Nonrandom Loss Model [33] and Recombination Model [34]. The variation (tRNAGln, tRNAMet and NCR) of mitochondrial gene order occurring between P. variegatus and Gyrodactylus spp. could be explained by the duplication and random loss model and recombination model together with the parsimonious scenario. We assume that the process contains three steps: one tandem duplication, random loss, followed by intramitochondrial recombination (Figure 8). We prefer this mechanism for the following reasons: the duplicate NCRs in the mitochondrial genomes of most metazoans can be explained by the duplication and random loss model, but the stepwise mechanism described above is more appropriate to interpret the duplicated NCRs and long-range translocation, meanwhile the rest of the genes remain in their original state. Furthermore, there are several examples of mitochondrial recombination in animals [35–38], and a similar mechanism accounts for the gene rearrangement of other metazoans [39, 40]. In addition, the tRNAMet genes of Gyrodactylus spp. are clearly homologous to the tRNAMet gene of P. variegatus with 80.6% sequence similarity. However, the tRNAGln region does have low sequence similarity (66.2%) between the mitochondrial genomes of Gyrodactylus spp. and P. variegatus, so we cannot be certain that the translocation event happened. As more mitochondrial genomes of gyrodactylids become available, all of the above hypotheses should be tested with respect to gene orders.Figure 8

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