Nuclear rDNA pseudogenes in Chagas disease vectors: Evolutionary implications of a new 5.8S+ITS-2 paralogous sequence marker in triatomines of North, Central and northern South America

Infection, Genetics and Evolution

Volumn 21, Issue , 2014, Pages 134-156

  Bargues, M Dolores ^a   Zuriaga, M Angeles ^a   Mas Coma, Santiago ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Chagas disease; Fundamental and applied characterization; New marker; Nuclear rDNA; Pseudogenic 5.8S and ITS 2 sequences; Triatomine vectors

Indexed keywords

INTERNAL TRANSCRIBED SPACER 2; RNA 5.8S; RIBOSOME DNA;

5.8S GENE; ANIMAL EXPERIMENT; ARTICLE; CENTRAL AMERICA; CHAGAS DISEASE; DNA SEQUENCE; EVOLUTIONARY RATE; GENE AMPLIFICATION; GENE IDENTIFICATION; GENETIC CONSERVATION; INDEL MUTATION; INHERITANCE; ITS 2 GENE; MOLECULAR CLOCK; MOLECULAR CLONING; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PSEUDOGENE; SOUTH AMERICA; TRIATOMA; TRIATOMINAE; ANIMAL; CELL NUCLEUS; CLASSIFICATION; DISEASE CARRIER; GENE; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY; PHYLOGEOGRAPHY; TRANSMISSION; WESTERN HEMISPHERE;

ANIMALIA; TRIATOMA MEXICANA; TRIATOMA NITIDA; TRIATOMA SANGUISUGA;

AMERICAS; ANIMALS; BASE SEQUENCE; CELL NUCLEUS; CHAGAS DISEASE; DNA, RIBOSOMAL; EVOLUTION, MOLECULAR; GENES, INSECT; INSECT VECTORS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; PSEUDOGENES; TRIATOMINAE;

EID: 84888784225     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.10.028     Document Type: Article

References (83)

1. Abad-Franch F., Monteiro F.A. Molecular research and the control of Chagas disease vectors. An. Acad. Bras. Ciênc. 2005, 77:437-454.
2. Akaike H. A new look at the statistical model identification. IEEE Trans. Autom. Control 1974, 19:716-723.
3. Balakirev E.S., Ayala F.J. Pseudogenes: are they "junk" or functional DNA?. Annu. Rev. Genet. 2003, 237:123-151.
4. Bargues M.D., Klisiowicz D.R., Gonzalez-Candelas F., Ramsey J.M., Monroy C., Ponce C., Salazar-Schettino P.M., Panzera F., Abad-Franch F., Sousa O.E., Schofield C.J., Dujardin J.P., Guhl F., Mas-Coma S. Phylogeography and genetic variation of Triatoma dimidiata, the main Chagas disease vector in Central America, and its position within the genus Triatoma. PLoS Negl. Trop. Dis. 2008, 2:e233.
5. Bargues M.D., Klisiowicz D.R., Panzera F., Noireau F., Marcilla A., Perez R., Rojas M.G., O'Connor J.E., Gonzalez-Candelas F., Galvao C., Jurberg J., Carcavallo R.U., Dujardin J.P., Mas-Coma S. Origin and phylogeography of the Chagas disease main vector Triatoma infestans based on nuclear rDNA sequences and genome size. Infect. Genet. Evol. 2006, 6:46-62.
6. Bargues M.D., Marcilla A., Dujardin J.P., Mas-Coma S. Triatomine vectors of Trypanosoma cruzi: a molecular perspective based on nuclear ribosomal DNA markers. Trans. R. Soc. Trop. Med. Hyg. 2002, 96:159-164.
7. Bargues M.D., Marcilla A., Ramsey J.M., Dujardin J.P., Schofield C.J., Mas-Coma S. Nuclear rDNA-based molecular clock of the evolution of Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease. Mem. Inst. Oswaldo Cruz 2000, 95:567-573.
8. Bargues M.D., Schofield J.C., Dujardin J.P. Classification and phylogeny of Triatominae. American Trypanosomiasis: Chagas disease. One Hundred Years of Research 2010, 115-149. Elsevier Inc., MA. J. Telleria, M. Tibayrenc (Eds.).
9. Blandón-Naranjo M., Zuriaga M.A., Azofeifa G., Zeledón R., Bargues M.D. Molecular evidence of intraspecific variability in different habitat-related populations of Triatoma dimidiata (Hemiptera: Reduviidae) from Costa Rica. Parasitol. Res. 2010, 106:895-905.
10. Buckler E.S., Ippolito A., Holtsford T.P. The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 1997, 145:821-832.
11. Calleros L., Panzera F., Bargues M.D., Monteiro F.A., Klisiowicz D.R., Zuriaga M.A., Mas-Coma S., Perez R. Systematics of Mepraia (Hempitera - Reduviidae): cytogenetic and molecular variation. Infect. Genet. Evol. 2010, 10:221-228.
12. Carcavallo R.U., Curto de Casas S.I., Sherlock I.A., Giron I.G., Jurberg J., Galvao C., Mena Segura C.A., Noireau F. Geographical distribution and alti-latitudinal dispersion. Atlas of Chagas Disease Vectors in the Americas 1999, 747-792. Editora FIOCRUZ, Rio de Janeiro. R.U. Carcavallo, I.G. Girón, J. Jurberg, H. Lent (Eds.).
13. Cooper D.N. Pseudogenes and their formation. Human Gene Evolution 1999, 265-285. BIOS Scientific Publishers, Oxford. D.N. Cooper (Ed.).
14. CÔté C.A., Peculis B.A. Role of the ITS2-proximal stem and evidence for indirect recognition of processing sites in pre-rRNA processing in yeast. Nucleic Acids Res. 2001, 29:2106-2116.
15. Dorn P.L., Calderon C., Melgar S., Moguel B., Solorzano E., Dumonteil E., Rodas A., de la Rua N., Garnica R., Monroy C. Two distinct Triatoma dimidiata (Latreille, 1811) taxa are found in sympatry in Guatemala and Mexico. PLoS Negl. Trop. Dis. 2009, 3:e393.
16. Dotson E., Beard C.B. Sequence and organization of the mitochondrial genome of the Chagas disease vector Triatoma dimidiata. Insect Mol. Biol. 2001, 10:205-215.
17. Dujardin J.P. Population genetics and the natural history of domestication in Triatominae. Mem. Inst. Oswaldo Cruz. 1998, 93:34-36.
18. Dujardin J.P., Schofield C.J., Panzera F. Les Vecteurs de la Maladie de Chagas. Recherches taxonomiques, biologiques et génétiques, new series, book 24. Section of Natural and Medical Sciences 2000, Académie Royale des Sciences d'Outre Mer, Belgium.
19. Dunham I., Shimizu N., Roe B.A., Chissoe S., Hunt A.R., Collins J.E., Bruskiewich R., Beare D.M., Clamp M., Smink L.J., Ainscough R., Almeida J.P., Babbage A., et al. The DNA sequence of human chromosome 22. Nature 1999, 402:489-495. + erratum in 404, 904.
20. Esnault C., Maestre J., Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 2000, 24:363-367.
21. Friedberg F., Rhoads A.R. Calculation and verification of the ages of retroprocessed pseudogenes. Mol. Phylogenet. Evol. 2000, 16:127-130.
22. Gibson L.J. Pseudogenes and origins. Origins 1994, 21:91-108.
23. Glass D.J., Takebayashi N., Olson L.E., Taylor D.L. Evaluation of the authenticity of a highly novel environmental sequence from boreal forest soil using ribosomal RNA secondary structure modeling. Mol. Phylogenet. Evol. 2013, 67:234-245.
24. Gray T.A., Wilson A., Fortin P.J., Nicholls R.D. The putatively functional Mkrn1-p1 pseudogene is neither expressed nor imprinted, nor does it regulate its source gene in trans. Proc. Natl. Acad. Sci. USA 2006, 103:12039-12044.
25. Hammock E.A.D., Young L.J. Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 2005, 308:1630-1634.
26. Harpke D., Peterson A. Non-concerted ITS evolution in Mammillaria (Cactaceae). Mol. Phylogenet. Evol. 2006, 41:579-593.
27. Harrison P.M., Zheng D., Zhang Z., Carriero N., Gerstein M. Transcribed processed pseudogenes in the human genome: an intermediate form of expressed retrosequence lacking protein-coding ability. Nucleic Acids Res. 2005, 33:2374-2383.
28. Hofacker I.L., Fontana W., Stadler P.F., Bonhoeffer S.L., Tacker M., Schuster P. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 1994, 125:167-188.
29. Hotez P.J., Molyneux D.H., Fenwick A., Kumaresan J., Sachs S.E., Sachs J.D., Savioli L. Control of neglected tropical diseases. New Engl. J. Med. 2007, 357:1018-1027.
30. Keller I., Chintauan-Marquier I.C., Veltsos P., Nichols R.A. Ribosomal DNA in the grasshopper Podisma pedestris: escape from concerted evolution. Genetics 2006, 174:863-874.
31. Leite L.A.R. Mitochondrial pseudogenes in insect DNA barcoding: differing points of view on the same issue. Biota Neotrop. 2012, 12:301-308.
32. Larkin M., Blackshields G., Brown N., Chenna R., McGettigan P., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. ClustalW and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
33. Leo N.P., Barker S.C. Intragenomic variation in ITS2 rDNA in the louse of humans, Pediculus humanus: ITS2 is not a suitable marker for population studies in this species. Insect Mol. Biol. 2002, 11:651-657.
34. Li C., Wilkerson R.C. Intragenomic rDNA ITS2 variation in the neotropical Anopheles (Nyssorhynchus) albitarsis complex (Diptera: Culicidae). J. Heredity 2007, 98:51-59.
35. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-δδC(T)) method. Methods 2001, 25:402-408.
36. Lorenz W.A., Clote P. Computing the partition function for kinetically trapped RNA secondary structures. PLoS One 2011, 6:e16178.
37. Manen J.F. Are both sympatric species Ilex perado and Ilex canariensis secretly hybridizing? Indication from nuclear markers collected in Tenerife. BMC Evol. Biol. 2004, 4:46.
38. Marcilla A., Bargues M.D., Abad-Franch F., Panzera F., Carcavallo R.U., Noireau F., Galvao C., Jurberg J., Miles M.A., Dujardin J.P., Mas-Coma S. Nuclear rDNA ITS-2 sequences reveal polyphyly of Panstrongylus species (Hemiptera: Reduviidae: Triatominae), vectors of Trypanosoma cruzi. Infect. Genet. Evol. 2002, 1:225-235.
39. Marcilla A., Bargues M.D., Ramsey J.M., Magallón-Gastélum E., Salazar-Schettino P.M., Abad-Franch F., Dujardin J.P., Schofield C.J., Mas-Coma S. The ITS-2 of the nuclear rDNA as a molecular marker for populations, species, and phylogenetic relationships in Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease. Mol. Phylogenet. Evol. 2001, 18:136-142.
40. Márquez L.M., Miller D.J., Mackenzie J.B., van Oppen M.J.M. Pseudogenes contribute to extreme diversity of nuclear ribosomal DNA in the hard coral Acropora. Mol. Biol. Evol. 2003, 20:1077-1086.
41. Martínez F.H., Villalobos G.C., Cevallos A.M., Torre P.D., Laclette J.P., Alejandre-Aguilar R., Espinoza B. Taxonomic study of the Phyllosoma complex and other triatomine (Insecta: Hemiptera: Reduviidae) species of epidemiological importance in the transmission of Chagas disease: using ITS-2 and mtCytB sequences. Mol. Phylogenet. Evol. 2006, 41:279-287.
42. Martínez-Hernandez F., Martínez-Ibarra J.A., Catalá S., Villalobos G., de la Torre P., Laclette J.P., Alejandre-Aguilar R., Espinoza B. Natural crossbreeding between sympatric species of the phyllosoma complex (Insecta: Hemiptera: Reduviidae) indicate the existence of only one species with morphologic and genetic variations. Am. J. Trop. Med. Hyg. 2010, 82:74-82.
43. Mas-Coma S., Bargues M.D. Populations, hybrids and the systematic concepts of species and subspecies in Chagas disease triatomine vectors inferred from nuclear ribosomal and mitochondrial DNA. Acta Trop. 2009, 110:112-136.
44. Mathews D.H., Disney M.D., Childs J.L., Schroeder S., Zuker M., Turner D.H. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl. Acad. Sci. USA 2004, 101:7287-7292.
45. Panzera F., Dujardin J.P., Nicolini P., Coraccio M.N., Rose V., Tellez T., Bermudez H., Bargues M.D., Mas-Coma S., O'Connor J.E., Perez R. Genomic changes of Chagas disease vector, South America. Emerg. Infect. Dis. 2004, 10:438-446.
46. Pavlicek A., Gentles A.J., Paces J., Paces V., Jurka J. Retroposition of processed pseudogenes: the impact of RNA stability and translational control. Trends Genet. 2006, 22:69-73.
47. Pavlicek A., Paces J., Zika R., Hejnar J. Length distribution of long interspersed nucleotide elements (LINEs) and processed pseudogenes of human endogenous retroviruses: implications for retrotransposition and pseudogene detection. Gene 2002, 300:189-194.
48. Petrov D.A., Hartl D.L. Pseudogene evolution and natural selection for a compact genome. J. Hered. 2000, 91:221-227.
49. Piehler A.P., Hellum M., Wenzel J.J., Kaminsk E., Haug K.B.F., Kierulf P., Kaminski W.E. The human ABC transporter pseudogene family: evidence for transcription and genepseudogene interference. BMC Genomics 2008, 9:165.
50. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
51. Posada D., Buckley T.R. Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst. Biol. 2004, 53:793-808.
52. Ramsey J.M., Schofield C.J. Control of Chagas disease vectors. Salud Públ. Méx. 2003, 45:123-128.
53. Razafimandimbison S.G., Kellogg E., Bremer B. Recent origin and phylogenetic utility of divergent ITS putative pseudogenes: a case study from Naucleeae (Rubiaceae). Syst. Biol. 2004, 53:177-192.
54. Richard G.F., Kerrest A., Dujon B. Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol. Mol. Biol. Rev. 2008, 72:686-727.
55. Roselló J.A., Lázaro A., Cosín R., Molins A. Phylogeographic split in Buxus balearica (Buxaceae) as evidenced by nuclear ribosomal markers: when ITS paralogues are welcome. J. Mol. Evol. 2007, 64:143-157.
56. Rouchka E.C., Cha I.E. Current trends in pseudogene detection and characterization. Curr. Bioinform. 2009, 4:112-119.
57. Sasidharan R., Gerstein M. Genomics: protein fossils live on as RNA. Nature 2008, 453:729-731.
58. Schofield C.J. Triatominae. Biology and Control 1994, Eurocommunica Publications, West Sussex.
59. Schofield C.J., Diotaiuti L., Dujardin J.P. The process of domestication in Triatominae. Mem. Inst. Oswaldo Cruz 1999, 94:375-378.
60. Schofield C.J., Galvão C. Classification, evolution, and species groups within the Triatominae. Acta Trop. 2009, 110:88-100.
61. Song H.X., Gao S.P., Jiang M.Y., Liu G.L., Yu X.F., Chen Q.B. The evolution and utility of ribosomal ITS sequences in Bambusinae and related species: divergence, pseudogenes, and implications for phylogeny. J. Genet. 2012, 91:129-139.
62. Swoffod D.L. PAUP/: phylogenetic analysis using parsimony (/and other methods). Version 4. Computer program distributed by the Smithsonian Institution 2002, Sinauer Associates Inc., Sunderland, MA.
63. Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol. Biol. Evol. 1984, 1:269-285.
64. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., Hodges E., Anger M., Sachidanandam R., Schultz R.M., Hannon G.J. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538.
65. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
66. Thornill D.J., Lajeunesse T., Santos S.R. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol. Ecol. 2007, 16:5326-5340.
67. Van Nues R.W., Rientjes J.M.J., Morre S.A., Mollee E., Planta R.J., Venema J., Raue H.A. Evolutionarily conserved structural elements are critical for processing of internal transcribed spacer 2 from Saccharomyces cerevisiae precursor ribosomal RNA. J. Mol. Biol. 1995, 250:24-36.
68. Van Nues R.W., Rientjes J.M., van der Sande C.A.F.M., Zerp S.F., Sluiter C., Venema J., Planta R.J., Raue H.A. Separate structural elements within internal transcribed spacer 1 of Saccharomyces cerevisiae precursor ribosomal RNA direct the formation of 17S and 26S rRNA. Nucleic Acids Res. 1995, 22:912-919.
69. Venema J., Tollervey D. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 1999, 33:261-311.
70. WHO, 1991. Control of Chagas disease. Report of a WHO expert committee. World Health Organization, Geneva, WHO Technical Report Series 811, 1-95.
71. WHO Working to Overcome the Global Impact of Neglected Tropical Diseases: First WHO Report on Neglected Tropical Diseases 2010, World Health Organization, Geneva.
72. Wolf J.N., Shearman D.C.A., Brooks R.C., Ballard J.W. Selective enrichment and sequencing of whole mitochondrial genomes in the presence of nuclear encoded mitochondrial pseudogenes (Numts). PLoS One 2012, 7:e37142.
73. Xiao L.Q., Möller M., Zhu H. High nrDNA ITS polymorphism in the ancient extant seed plant Cycas: incomplete concerted evolution and the origin of pseudogenes. Mol. Phylogenet. Evol. 2010, 55:168-177.
74. Xu J., Zhang Q., Xu X., Wanga Z., Qi J. Intragenomic variability and pseudogenes of ribosomal DNA in Stone flounder Kareius bicoloratus. Mol. Phylogenet. Evol. 2009, 52:157-166.
75. Zhang Z., Carriero N., Gerstein M. Comparative analysis of processed pseudogenes in the mouse and human genomes. TrendsGenet. 2004, 20:62-67.
76. Zhang Z.D., Cayting P., Weinstock G., Gerstein M. Analysis of nuclear receptor pseudogenes in vertebrates: how the silent tell their stories. Mol. Biol. Evol. 2008, 25:131-143.
77. Zhang Z., Gerstein M. The human genome has 49 cytochrome c pseudogenes, including a relic of a primordial gene that still functions in mouse. Gene 2003, 312:61-72.
78. Zheng D., Gerstein M.B. The ambiguous boundary between genes and pseudogenes: the dead rise up, or do they?. Trends Genet. 2007, 23:219-224.
79. Zheng X., Cai D., Yao L., Teng Y. Non-concerted ITS evolution, early origin and phylogenetic utility of ITS pseudogenes in Pyrus. Mol. Phylogenet. Evol. 2008, 48:892-903.
80. Zheng D., Zhang Z., Harrison P.M., Karro J., Carriero N., Gerstein M. Integrated pseudogene annotation for human chromosome 22: evidence for transcription. J. Mol. Biol. 2005, 349:27-45.
81. Zuker M. On finding all suboptimal foldings of an RNA molecule. Science 1989, 244:48-52.
82. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981, 9:133-148.
83. Zuriaga M.A., Blandón-Naranjo M., Valerio-Campos I., Salas R., Zeledón R., Bargues M.D. Molecular characterization of Trypanosoma cruzi and infection rate of the vector Triatoma dimidiata in Costa Rica. Parasitol. Res. 2012, 111:1615-1620.