Abstract
Among the digenetic trematodes, paramphistomes are known to be the causative agent of “amphistomiasis” or the stomach fluke disease of domestic and wild animals, mainly ruminants. The use of 28S (divergent domains) and 18S rRNA for phylogenetic inference is significantly warranted for these flukes since it is as yet limited to merely the exploration of the second internal transcribed spacer (ITS2) region. The present study intended to explore the divergent domains (D1–D3) of 28S rRNA and simultaneously equate the phylogenetic information with 18S rRNA in paramphistomes. Divergence of the 28S rRNA domains was evident amongst the divergent (D) domains, where D1 domain emerged as the most variable and D2, the most robust domain, since the latter could provide a higher resolution of the species. D2 was the only domain that comprised compensatory mutations in the helices of its structural constraints; this domain is thus well suited for species distinction and may be considered a potential DNA barcode complementary to mitochondrial DNA. 28S (D1 + D2 + D3) rRNA provided a significant resolution of the taxa corroborating with the taxonomy of these flukes and thus proved to be more robust as a phylogenetic marker for lower levels than 18S rRNA. Phylogenetic inferences of paramphitomes are still scarcely explored; additional data from other taxa belonging to this family may estimate better the biodiversity of these flukes.
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Abele LG, Kim W, Felegenhauer BE (1989) Molecular evidence for inclusion of the phylum Pentastomida in the Crustacea. Mol Biol Evol 6:685–691
Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud'homme B, de Rosa R (2000) The new animal phylogeny: reliability and implications. Proc Natl Acad Sci U S A 97:4453–4456
Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493
Al-Banna L, Willamson VM, Gardner SL (1997) Phylogenetic analysis of nematodes of the genus Pratylenchus using nuclear 26S rDNA. Mol Phylogenet Evol 7:94–102
Al-Banna L, Ploeg AT, Williamson VM, Kaloshian A (2004) Discrimination of six Pratylenchus species using PCR and species-specific primers. J Nematol 36:142–146
Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434
Anuracpreeda P, Wanichanon C, Sobhon P (2008) Paramphistomum cervi: antigenic profile of adults as recognized by infected cattle sera. Exp Parasitol 118:203–207
Bachellerie JP, Michot B (1989) Evolution of large subunit rRNA structure The 3' terminal domain contains elements of secondary structure specific to major phylogenetic groups. Biochimie 71:701–709
Bae CH, Robbins RT, Szalanski AL (2010) Secondary structure models of D2-D3 expansion segments of 28S rRNA for Hoplolaiminae species. J Nematol 42(3):218–229
Barker SC, Blair D, Garrett AR, Cribb TH (1993) Utility of the D1 domain of nuclear 28S rRNA for phylogenetic inference in the Digenea. Syst Parasitol 26:181–188
Blair D, Campos A, Cummings MP, Laclette JP (1996) Evolutionary biology of parasitic platyhelminths: the role of molecular phylogenetics. Parasitol Today 12:66–71
Campos A, Cummings MP, Reyes JL, Laclette JP (1998) Phylogenetic relationships of Platyhelminthes based on 18S ribosomal gene sequences. Mol Phylogenet Evol 10(1):1–10
Chethanon U, Ausavamatha P, Piriyayon S, (1985) Parasitological survey of cattle in the south of Thailand. Proceedings of the 4th Annual Livestock Conference, Department Livestock Development 281–290
Chilton NB, Hoste H, Newton LA, Beveridge I, Gasser RB (2001) Evolutionary relationships of trichostrongyloid nematodes (Strongylid) inferred from ribosomal DNA sequence data. Mol Phylogenet Evol 19:367–386
Chilton NB, Huby-Chilton F, Gasser RB (2003) First complete large subunit ribosomal RNA sequence and secondary structure for a parasitic nematode: phylogenetic and diagnostic implications. Mol Cell Probes 17:33–39
Coleman AW (2000) The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151:1–9
Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. TIG 19:370–375
Coleman AW (2007) Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Res 35(10):3322–3329
Coleman AW, Vacquier V (2002) Exploring the phylogenetic utility of ITS sequences for animals: a test case for Abalone (Haliotis). J Mol Evol 54:246–257
Cruickshank RH (2002) Molecular markers for the phylogenetics of mites and ticks. Syst Appl Acarol 7:3–14
De Ley P, De Ley IT, Morris K, Abebe E, Mundo-Ocampo M, Yoder M, Heras J, Waumann D, Rocha-Olivares A, Jay Burr AH, Baldwin JG, Thomas WK (2005) An integrated approach to fast and informative morphological vouchering of nematodes for applications in molecular barcoding. J Philos Trans R Soc Lond B; Biol Sci 360(1462):1945–1958
De Rijk P, Van de Peer Y, Van den Broeck I, DeWachter R (1995) Evolution according to large ribosomal subunit RNA. J Mol Evol 41:366–375
Díez B, Pedrós-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941
Dixon MT, Hillis DM (1993) Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis. Mol Biol Evol 10(1):256–267
Duncan LW, Inserra RN, Thomas WK, Dunn D, Mustika I, Frisse LM, Mendes ML, Morris K, Kaplan DT (1999) Molecular and morphological analysis of isolates of Pratylenchus coffeae and closely related species. Nematropica 29:61–80
Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753
Fontaneto D (2011) Biogeography of microscopic organisms is everything small everywhere? Cambridge University Press, Imperial College London
Friedrich M, Tautz D (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376:165–167
Ghatani S, Shylla JA, Tandon V, Chatterjee A, Roy B (2012) Molecular characterization of pouched amphistome parasites (Trematoda: Gastrothylacidae) using ribosomal ITS2 sequence and secondary structures. J Helminthologia 86:117–124
Gillespie JJ, Munro JB, Heraty JM, Yoder MJ, Owen AK, Carmichael AE (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Mol Biol Evol 22(7):1593–1608
Goswami LM, Prasad PK, Tandon V, Chatterjee A (2009) Molecular characterization of Gastrodiscoides hominis (Platyhelminthes: Trematoda: Digenea) inferred from ITS rDNA sequence analysis. Parasitol Res 104:1485–1490
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hancock JM, Tautz D, Dover GA (1988) Evolution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster. Mol Biol Evol 5:393–414
Hassouna N, Michot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene: implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583
Hershkovitz M, Lewis L (1996) Deep level diagnostic value of the rDNA-ITS region: the case of an algal interloper. Mol Biol Evol 13:167–177
Hofacker IL, Fontana W, Stadler PF, Bonhoeffer S, Tacker M, Schuster P (1994) Fast folding and comparison of RNA secondary structures. Monatsh Chem 125:167–188
Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755
Hwang UW, Kim W (1999) General properties and phylogenetic utilities of nuclear ribosomal DNA and mitochondrial DNA commonly used in molecular systematics. Korean J Parasitol 37:215–228
Hwang UW, Ree HI, Kim W (2000) Evolution of hypervariable regions, V4 and V7, of insect 18S rRNA and their phylogenetic implications. Zool Sci 17:111–121
Ilha MR, Loretti AP, Reis AC (2005) Wasting and mortality in beef cattle parasitized by Eurytrema coelamaticum in the state of Parana, southern Brazil. Vet Parasitol 133:49–60
Itagaki T, Tsumagari N, Tsutsumi K, Chinone S (2003) Discrimination of three amphistome species by PCR-RFLP based on rDNA ITS2 markers. J Vet Med Sci 65:931–933
Jarmen SN, Nicol S, Elliott NG, McMinn A (2000) 28S rDNA evolution in the eumalacostraca and the phylogenetic position of krill. Mol Phylogenet Evol 17:26–36
Jones A (1990) Techniques for sectioning thick-bodied platyhelminths. Syst Parasitol 15:211–218
Jones A (2005a) Superfamily Paramphistomoidea Fischoeder, 1901. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI Publishing and The Natural History Museum, London, pp 221–227
Jones A (2005b) Family Gastrodiscidae Monticelli, 1892. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI Publishing and The Natural History Museum, London, pp 325–336
Juyal PD, Kasur K, Hassan SS, Kaur P (2003) Epidemiological status of paramphistomiasis in domestic ruminants in Punjab. J Parasit Dis 231–235
Kaukas A, Neto ED, Simpson AJG, Southgate VR, Rollinson D (1994) A phylogenetic analysis of Schistosoma haematobium group species based on randomly amplified polymorphic DNA. Int J Parasitol 24:285–290
Khan UJ, Tanveer A, Maqbool A, Masood S (2008) Epidemiological studies of paramphistomosis in cattle. Vet Arh 78:243–251
Kilani K, Guillot J, Chermett R (2003) Amphistomes digestive. In: Lefevre PC, Blanco J, Chermatt J (eds) Principales maladies infectieuses et parasitaires du betail, 1st edn. Tec & Doc, Paris, pp 1400–1410
Kjer KM (1995) Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. Mol Phylogenet Evol 4:314–330
Leon-Regagnon V, Paredes-Calderon EL (2002) Haematoloechus danbrooksi n. sp (Digenea: Plagiorchioidea) from Rana vaillanti from Los Tuxtlas, Veracruz, Mexico. J Parasitol 88:1215–1221
Littlewood DTJ (1994) Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Mol Phylogenet Evol 3:221–229
Litvaitis MK, Bates JW, Hope WD, Moens T (2000) Inferring a classification of the Adenophorea (Nematoda) from nucleotide sequences of the D3 expansion segment (26/28S rDNA). Can J Zool 78:911–922
Lotfy WM, Brant SV, Ashmawy KI, Devkota R, Mkojie GM, Loker ES (2010) A molecular approach for identification of paramphistomes from Africa and Asia. Vet Parasitol 174:234–240
Mage C, Bourgne H, Toullieu JM, Rondelaud D, Dreyfuss G (2002) Fasciola hepatica and Paramphistomum daubneyi: changes in the prevalence of natural infections in cattle and Lymnaea truncatula from Central France over the past 12 years. Vet Res 33:439–447
Mallatt J, Sullivan J (1998) 28S and 18S rDNA sequences support the monophyly of lampreys and hagfishes. Mol Biol Evol 15:1706–1718
Medina M, Collins AG, Silberman JD, Sogin ML (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci U S A 98:9707–9712
Müller T, Philippi N, Dandekar T, Schultz J, Wolf M (2007) Distinguishing species. RNA 1:1469–1472
Nolan MJ, Cribb TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol 60:101–163
Prasitirat T, Chompoochan S, Nithiuthai S, Wongkasemjit T, Punmamoamg P, Pongrut S, Chinone S, Itagaki H (1997) Prevalence of amphistomes of cattle in Thailand. Parasitol Hung 29–30:27–32
Ramirez J, Ramírez R (2010) Analysis of the secondary structure of mitochondrial LSU rRNA of Peruvian land snails (Orthalicidae: Gastropoda). Rev Peru Biol 17(1):053–057
Rinaldi L, Perugini AG, Capuano F, Fenizia D, Musella V, Veneziano V, Cringoli G (2005) Characterization of the second internal transcribed spacer of ribosomal DNA of Calicophoron daubneyi from various hosts and locations in southern Italy. Vet Parasitol 131:247–253
Ronquist F, Huelsenbeck JP (2003) MrBayes version 3.0: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Roy B, Tandon V (1992) Trematodiasis in North-East India: a study on the spectrum of Digenetic trematodes among pigs, buffaloes, cattle, goats and sheep. Indian J Anim Health 13:5–14
Ruhl MW, Wolf M, Jenkins TM (2009) Compensatory base changes illuminate taxonomically difficult taxonomy. Mol Phylogenet Evol 54:664–669
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Sanabria R, Romero J (2008) Review and update of paramphistomosis. Helminthologia 45:64–68
Seemann ES, Menzel KP, Backofen R, Gorodkin J (2011) The PETfold and PETcofold web servers for intra- and intermolecular structures of multiple RNA sequences. Nucleic Acids Res 39(2):107–111
Seibel PN, Muller T, Dandekar T, Schultz J, Wolf M (2006) 4SALE–a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinforma 7:498
Sey O (1991) CRC handbook of the zoology of Amphistomes. CRC Press, Florida, Boca Raton
Shylla JA, Ghatani S, Chatterjee A, Tandon V (2011) Secondary structure analysis of ITS2 in the rDNA of three Indian paramphistomid species found in local livestock. Parasitol Res 108:1027–1032
Snyder SD, Tkach VV (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). J Parasitol 87:1433–1440
Subbotin SA, Sturhan D, Vovlas N, Castillo P, Tanyi Tambe J, Moens M, Baldwin JG (2007) Application of secondary structure model of rRNA for phylogeny: D2-D3 expansion segments of the LSU gene of plant-parasitic nematodes from the family Hoplolaimidae Filipjev, 1934. Mol Phylogenet Evol 43:881–890
Subbotin SA, Vovlas N, Crozzoli R, Sturhan D, Lamberti F, Moens M, Baldwin JG (2005) Phylogeny of Criconematina Siddiqi, 1980 (Nematode: Tylenchida) based on morphology and D2-D3 expansion segments of the 28S-rRNA gene sequences with application of a secondary structure model. Nematology 7:927–944
Subbotin SA, Ragsdale EJ, Mullens T, Roberts PA, Mundo-Ocampo M, Baldwin JG (2008) A phylogenetic framework for root lesion nematodes of the genus Pratylenchus (Nematoda): evidence from 18S and D2-D3 expansion segments of 28S ribosomal RNA genes and morphological characters. Mol Phylogenet Evol 48:491–505
Thornhill DJ, LaJeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artefacts confound biodiversity estimates. Mol Ecol 16:5326–5340
Tkach VV, Pawlowski J, Mariaux J (2000) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 3:89–93
Tkach V, Pawlowski J, Mariaux J, Swiderski Z (2001) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 186–193
Van de Peer Y, Baldouf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565–576
Vovlas N, Subbotin SA, Troccoli A, Liebanas G, Castillo P (2008) Molecular phylogeny of the genus Rotylenchus (Nematoda, Tylenchida) and description of a new species. Zool Scr 37:521–537
Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolution and phylogenetic implications. Mol Biol Evol 5:90–96
Whiting MF (1998) Phylogenetic position of the Strepsiptera: review of molecular and morphological evidence. Int J Morphol Embryol 27:53–60
Wickramasinghe S, Yatawara L, Rajapakse RPVJ, Agatsuma T (2009) Toxocara canis and Toxocara vitulorum : molecular characterization, discrimination, and phylogenetic analysis based on mitochondrial (ATP synthase subunit 6 and 12S) and nuclear ribosomal (ITS-2 and 28S) genes. Parasitol Res 104:1425–1430
Winchell CJ, Sullivan J, Cameron CB, Swalla BJ, Mallatt J (2002) Evaluating hypotheses of deuterostome evolution with new LSU and SSU ribosomal DNA phylogenies. Mol Biol Evol 19:762–776
Yan H, Lou Z, Li L, Ni X, Guo A, Li H, Zheng Y, Dyachenko V, Jia W (2013) The nuclear 18S ribosomal RNA gene as a source of phylogenetic information in the genus Taenia. Parasitol Res 112:1343–1347
Zhao Ya-E W, Li-Ping H, Li X, Yang WZ-H, Wen-Yan L (2012) Sequencing for complete rDNA sequences (18S, ITS1, 5.8S, ITS2, and 28S rDNA) of Demodex and phylogenetic analysis of Acari based on 18S and 28S rDNA. Parasitol Res 111:2109–2114
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JAS is thankful to Council of Scientific and Industrial Research (CSIR), Delhi, for awarding her junior and senior research fellowships.
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Shylla, J.A., Ghatani, S. & Tandon, V. Utility of divergent domains of 28S ribosomal RNA in species discrimination of paramphistomes (Trematoda: Digenea: Paramphistomoidea). Parasitol Res 112, 4239–4253 (2013). https://doi.org/10.1007/s00436-013-3616-8
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DOI: https://doi.org/10.1007/s00436-013-3616-8