Species discrimination and phylogenetic inference of 17 Chinese Leishmania isolates based on internal transcribed spacer 1 (ITS1) sequences

Parasitology Research

Volumn 107, Issue 5, 2010, Pages 1049-1065

  Yang, Bin Bin ^a   Guo, Xian Guang ^b   Hu, Xiao Su ^a   Zhang, Jian Guo ^a   Liao, Lin ^a   Chen, Da Li ^a   Chen, Jian Ping ^a  

^a SICHUAN UNIVERSITY   (China)

^b CHENGDU INSTITUTE OF BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL DNA; PROTOZOAL RNA; RIBOSOMAL SPACER DNA; RNA 5.8S;

ANIMAL; ANIMAL DISEASE; ARTICLE; CHEMISTRY; CHINA; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LEISHMANIA; LEISHMANIASIS; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY; RNA GENE;

ANIMALS; CHINA; CLUSTER ANALYSIS; DNA, PROTOZOAN; DNA, RIBOSOMAL SPACER; GENES, RRNA; HUMANS; LEISHMANIA; LEISHMANIASIS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, PROTOZOAN; RNA, RIBOSOMAL, 5.8S; SEQUENCE ANALYSIS, DNA;

EID: 79952114197     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-010-1969-9     Document Type: Article

References (84)

1. Ababneh F, Jermiin LS, Ma C, Robinson J (2006) Matched-pairs tests of homogeneity with applications to homologous nucleotide sequences. Bioinformatics 22:1225-1231 (Pubitemid 43779015)
2. Alam MZ, Kuhls K, Schweynoch C, Sundar S, Rijal S, Shamsuzzaman AK, Raju BV, Salotra P, Dujardin JC, Schönian G (2009a) Multilocus microsatellite typing (MLMT) reveals genetic homogeneity of Leishmania donovani strains in the Indian subcontinent. Infect Genet Evol 9:24-31
3. Alam MZ, Kovalenko DA, Kuhls K, Nasyrova RM, Ponomareva VI, Fatullaeva AA, Razakov SA, Schnur LF, Schönian G (2009b) Identification of the agent causing visceral leishmaniasis in Uzbeki and Tajiki foci by analysing parasite DNA extracted from patients' Giemsa-stained tissue preparations. Parasitology 136:981-986
4. Al-Kandari WY, Al-Bustan SA (2010) Molecular identification of Probolocoryphe uca (Sarkisian, 1957; Digenea: Microphallidae) from Kuwait Bay using ITS1 and ITS2 sequences. Parasitol Res 106:1189-1195
5. Asato Y, Oshiro M, Myint CK, Yamamoto Y, Kato H, Marco JD, Mimori T, Gomez EA, HashiguchiY UH (2009) Phylogenic analysis of the genus Leishmania by cytochrome b gene sequencing. Exp Parasitol 121:352-361
6. Bañuls A-L, Hide M, Tibayrenc M (2002) Evolutionary genetics and molecular diagnosis of Leishmania species. Trans R Soc Trop Med Hyg 96(Suppl 1):S9-S13
7. Bañuls A-L, Hide M, Prugnolle F (2007) Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans. Adv Parasitol 64:1-109
8. Berzunza-Cruz M, Cabrera N, Crippa-Rossi M, Cabrera TS, Pérez-Montfort R, Becker I (2002) Polymorphism analysis of the internal transcribed spacer and small subunit of ribosomal RNA genes of Leishmania mexicana. Parasitol Res 88:918-925 (Pubitemid 35025142)
9. Chen D-L, Wang G-T, Yao W-J, Nie P (2007) Utility of ITS1-5.8S-ITS2 sequences for species discrimination and phylogenetic inference of two closely related bucephalid digeneans (Digenea: Bucephalidae): Dollfustrema vaneyi and Dollfustrema hefeiensis. Parasitol Res 101:791-800
10. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657-1660
11. Dávila AMR, Memen H (2000) Internal-transcribed-spacer (ITS) sequences used to explore phylogenetic relationships within Leishmania. Ann Trop Med Parasitol 94:651-654
12. De Meeûs T, Durand P, Renaud F (2003) Species concepts: what for? Trend Parasitology 19:425-427
13. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879-886
14. Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27:305-318
15. Dessimoz C, Gil M (2010) Phylogenetic assessment of alignments reveals neglected tree signal in gaps. Genome Biol 11: R37
16. El Tai NO, Osman OF, El Fari M, Presber W, Schönian G (2000) Genetic heterogeneity of ribosomal internal transcribed spacer (ITS) in clinical samples of Leishmania donovani spotted on filter papers as revealed by single-strand conformation polymorphisms (SSCP) and sequencing. Trans R Soc Trop Med Hyg 94:575-579
17. El Tai NO, El Fari M, Mauricio I, Miles MA, Oskam L, El Safi SH, Presber WH, Schönian G (2001) Leishmania donovani: intraspecific polymorphisms of Sudanese isolates revealed by PCR-based analyses and DNA sequencing. Exp Parasitol 97:35-44 (Pubitemid 32989014)
18. Felsensten JP (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
19. Fraga J, Montalvo AM, de Doncker S, Dujardin J-C, der Auwera GV (2010) Phylogeny of Leishmania species based on the heat-shock protein 70 gene. Infect Genet Evol 10:238-245
20. Fryauff DJ, Hanafi HA, Klena JD, Hoel DF, Appawu M, Rogers W, Puplampu N, Odoom S, Kweku M, Koram K, Wilson MD, Raczniak G, Boakye D (2006) ITS-1 DNA sequence confirmation of Leishmania major as a cause of cutaneous leishmaniasis from an outbreak focus in the Ho district southeastern Ghana. Am J Trop Med Hyg 75:502-504 (Pubitemid 46941313)
21. Gadagkar SR, Kumar S (2005) Maximum likelihood outperforms maximum parsimony even when evolutionary rates are heterotachous. Mol Biol Evol 22:2139-2141 (Pubitemid 41437794)
22. Gaucher EA, Miyamoto MM (2005) A call for likelihood phylogenetics even when the process of sequence evolution is heterogeneous. Mol Phylogenet Evol 35:624-636
23. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221-224
24. Guan L-R, Yang Y-Q, Ren H-Y, Chai J-J (1992a) Eight cutaneous Leishmaniasis cases detected in Karamay, Xinjiang Uygur Autonomous Region, China. Southeast Asian J Trop Med Public Health 23:803-804
25. Guan L-R, Yang Y-Q, Xu Y-X, Wu J-T (1992b) Leishmaniasis in Karamay XI. The development of cutaneous leishmaniasis in monkey and man experimentally infected with Leishmania from Karamay big gerbil. Endemic Diseases Bulletin 10:263-266 (in Chinese with English abstract)
26. Guan L-R, Yang Y-Q, Ren H-Y, Shen W-X (1995) Discovery and study of Leishmania turanica for the first time in China. Bull World Health Organ 69:595-601
27. Hickson RE, Simon C, Perrey SW (2000) The performance of several multiple-sequence alignment programs in relation to secondarystructure features for an rRNA sequence. Mol Biol Evol 17:530-539 (Pubitemid 30210699)
28. Ho JWK, Adams CE, Lew JB, Maatthews TJ, Ng CC, Shahabi-Sirjan A, Tan LH, Zhao Y, Easteal S, Wilson SR, Jermin LS (2006) SeqVis: visualization of compositional heterogeneity in large alignments of nucleotides. Bioinformatics 22:2162-2163 (Pubitemid 44390910)
29. Hu X-S, Bu L, Ma Y, Wang Y, Jing B, Yi T (2002) Difference in DNA sequences in SSU rDNA variable regions among pathogens isolated from different epidemic foci of visceral leishmaniasis in China. Chin Med J (Engl) 115:1457-1459 (Pubitemid 35282900)
30. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673-688 (Pubitemid 35294801)
31. Ibrahim ME, Barker DC (2001) The origin and evolution of the Leishmania donovani complex as inferred from a mitochondrial cytochrome oxidase II gene sequence. Infect Genet Evol 1:61-68 (Pubitemid 33586016)
32. Jamjoom MB, Ashford RW, Bates PA, Chance ML, Kemp SJ, Watts PC, Noyes HA (2004) Leishmania donovani is the only cause of visceral leishmaniasis in East Africa; previous descriptions of L. infantum and "L. archibaldi" from this region are a consequence of convergent evolution in the isoenzyme data. Parasitology 129:399-409 (Pubitemid 39371869)
33. Jeffreys H (1935) Some tests of significance, treated by the theory of probability. Proc Cambridge Philos Soc 31:201-222
34. Jeffreys H (1961) Theory of probability. Oxford University Press, London
35. Jermiin LS, Jayaswal V, Ababneh F, Robinson J (2008) Phylogenetic model evaluation. In: Keith J (ed) Methods in molecular biology: bioinformatics. Humana Press, Totowa
36. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773-795
37. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120
38. Kuhls K, Mauricio IL, Pratlong F, Presber W, Schönian G (2005) Analysis of ribosomal DNA internal transcribed spacer sequences of the Leishmania donovani complex. Microbes Infect 7:1224-1234 (Pubitemid 41476436)
39. Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50:913-925
40. Lin R-Q, Dong S-J, Nie K, Wang C-R, Song H-Q, Li A-X, Huang W-Y, Zhu X-Q (2007) Sequence analysis of the first internal transcribed spacer of rDNA supports the existence of the intermediate Fasciola between F. hepatica and F. gigantica in mainland China. Parasitol Res 101:813-817 (Pubitemid 47101413)
41. Lu H-G, Zhong L, Guan L-R, Qu J-Q, Hu X-S, Chai J-C, Xu Z-B, Wang C-T, Chang K-P (1994) Separation of Chinese Leishmania isolates into five genotypes by kinetoplast and chromosomal DNA heterogeneity. Am J Trop Med Hyg 50:763-770 (Pubitemid 24228085)
42. Lu F-L, Hu X-S, Jing B-Q, Luo P, Lin F-Q (1997) Analysis of kDNA of Leishmania isolates from hill and plain foci of China. Chin J Parasitol Parasit Dis 5:101-103 (in Chinese with English abstract)
43. Lu F-L, Hu X-S, Jing B-Q, Ma Y (1998) Analysis of nuclear DNA gene types of Leishmania isolates from hilly and plain foci of China. Chin J Parasitol Parasit Dis 16:432-435 (in Chinese with English abstract)
44. Lu D-M, Hu X-S, Qiao Z-D (2001) Analysis of Leishmania species and strains from China by RAPD technique. Chin J Parasitol Parasit Dis 19:290-293 (in Chinese with English abstract)
45. Lukeš J,Mauricio IL, Schönian G, Dujardin J-C, Soteriadou K, Dedet J-P, Kuhls K, Tintaya KWQ, Jirků M, Chocholová E, Haralambous C, Pratlong F, Oborník M, Horák A, Ayala FJ, Miles MA (2007) Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc Natl Acad Sci USA 104:9375-9380 (Pubitemid 47185787)
46. Montalvo AM, Fraga J, Monzote L, Montano I, de Doncker S, Dujardin JC, der Auwera GV (2010) Heat-shock protein 70 PCRRFLP: a universal simple tool for Leishmania species discrimination in the New and Old World. Parasitology. doi:10.1017/S0031182010000089
47. Müller K (2005) SeqState: primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinform 4:65-69
48. Noyes HA, Arana BA, Chance ML, Maingon R (1997) The Leishmania hertigi (Kinetoplastida; Trypanosomatidae) complex and the lizard Leishmania: their classification and evidence for a neotropical origin of the Leishmania- Endotrypanum clade. J Eukaryot Microbiol 44:511-517 (Pubitemid 27401027)
49. Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581-583 (Pubitemid 351256305)
50. Parvizi P, Ready PD (2008) Nested PCRs and sequencing of nuclear ITS-rDNA fragments detect three Leishmania species of gerbils in sandflies from Iranian foci of zoonotic cutaneous leishmaniasis. Trop Med Int Health 13:1159-1171
51. Parvizi P, Moradi G, Akbari G, Farahmand M, Ready PD, Piazak N, Assmar M, Amirkhani A (2008) PCR detection and sequencing of parasite ITS-rDNA gene from reservoirs host of zoonotic cutaneous leishmaniasis in central Iran. Parasitol Res 103:1273-1278
52. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, Peters N, Adlem E, Tivey A, Aslett M, Kerhornou A, Ivens A, Fraser A, Rajandream MA, Carver T, Norbertczak H, Chillingworth T, Hance Z, Jagels K, Moule S, Ormond D, Rutter S, Squares R, Whitehead S, Rabbinowitsch E, Arrowsmith C, White B, Thurston S, Bringaud F, Baldauf SL, Faulconbridge A, Jeffares D, Depledge DP, Oyola SO, Hilley JD, Brito LO, Tosi LR, Barrell B, Cruz AK, Mottram JC, Smith DF, Berriman M (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39:839-847 (Pubitemid 47014491)
53. Philippe H, Zhou Y, Brinkmann H, Rodrigue N, Delsuc F (2005) Heterotachy and long-branch attraction in phylogenetics. BMC Evol Biol 5:50
54. Piarroux R, Fontes M, Perasso R, Gambarelli F, Joblet C, Dumon H, Auilici M (1995) Phylogenetic relationships between Old World Leishmania strains revealed by analysis of a repetitive DNA sequence. Mol Biochem Parasitol 73:249-252
55. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approach. Syst Biol 53:793-808 (Pubitemid 39568279)
56. Posada D, Crandal KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37-45 (Pubitemid 32102347)
57. Posda D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253-1256
58. Raftery AE (1996) Hypothesis testing and model selection. In: Gilks WR, Spiegelhalter DJ, Richardson S (eds) Markov chain Monte Carlo in practice. Chapman and Hall, London, pp 163-188
59. Rambaut A, Drummond AJ (2009) Tracer v1.5, available from http://beast.bio.ed.ac.uk/Tracer
60. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574 (Pubitemid 37038874)
61. Rotureau B, Ravel C, Couppie P, Pratlong F, Nacher M, Dedet JP, Carme B (2006) Use of PCR-restriction fragment length polymorphism analysis to identify the main New World Leishmania species and analyze their taxonomic properties and polymorphism by application of the assay to clinical samples. J Clin Microbiol 44:459-467 (Pubitemid 43222238)
62. Sambrook J, Russell DW(2001)Molecular cloning: a laboratory-manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
63. Schönian G, Akuffo H, Lewin S, Maasho K, Nylén S, Pratlong F, Eisenberger CL, Schnur LF, Presber W (2000) Genetic variability within the species Leishmania aethiopica does not correlate with clinical variations of cutaneous Leishmaniasis. Mol Biochem Parasitol 106:239-248 (Pubitemid 30123070)
64. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461-464
65. Shehata MG, Samy AM, Doha S, Fahmy AR, Kaldas RM, Furman BD, Villinski JT (2009) First report of Leishmania tropica from a classical focus of L. major in North-Sinai Egypt. Am J Trop Med Hyg 81:213-218
66. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analysis. Syst Biol 49:369-381
67. Spencer M, Susko E, Roger AJ (2005) Likelihood, parsimony, and heterogeneous evolution. Mol Biol Evol 22:1161-1164 (Pubitemid 40577753)
68. Strelkova MV, Shurkhal AV, Kellina OI, Eliseev LN, Evans DA, Peters W, Chapman CJ, Le Blancq SM, van Eys GJ (1990) A new species of Leishmania isolated from the great gerbil Rhombomys opimus. Parasitology 101:327-335
69. Suchard MA, Weiss RE, Sinsheimer JS (2001) Bayesian selection of continuous time Markov chain evolutionary models. Mol Biol Evol 18:1001-1013 (Pubitemid 32520473)
70. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland, MA
71. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599
72. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882 (Pubitemid 28022245)
73. Tibayrenc M (1998) Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol 28:85-104
74. Wang J, Qu J-Q, Guan L-R (1964a) A study on the Leishmania parasites of the great gerbil in northwest China. Acta Parasitologica Sinica 1:105-117 (in Chinese with English abstract)
75. Wang J, Xiong G-H, Hu Y-D, Lui P-Z, Niu H-F, Sai S-Y (1964b) The Leishmania infection found in Rhombomys opimus its transmission and relation to man. Acta Parasitologica Sinica 1:17-23 (in Chinese with English abstract)
76. Wang J-Y, Gao C-H, Yang Y-T, Chen H-T, Zhu X-H, Lv S, Chen S-B, Tong S-X, Steinmann P, Ziegelbauer K, Zhou X-N (2010) An outbreak of the desert sub-type of zoonotic visceral leishmaniasis in Jiashi, Xinjiang Uygur Autonomous Region, People's Republic of China. Parasitol Int. doi:10.1016/j.parint.2010.04.002
77. WHO (1990) Control of leishmaniases. World Health Organization, Geneva
78. Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Lemey P (ed) The phylogenetic handbook. Cambridge University Press, Cambridge, pp 611-626
79. Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371-373 (Pubitemid 32848767)
80. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1-7 (Pubitemid 36029247)
81. Xu Z-B, Le Blancq S, Evans DA, Peters W (1984) The characterization by isoenzyme electrophoresis of Leishmania isolated in the People's Republic of China. Trans R Soc Trop Med Hyg 78:689-693 (Pubitemid 15062066)
82. Xu Z-B, Liu Z-T, Long J-Y, Chai J-J, Chen W-K (1989) Further characterization of Chinese Leishmania isolates by isoenzyme electrophoresis. Chin Med J (Engl) 102:679-685
83. Zemanova E, Jirku M, Mauricio IL, Miles MA, Lukeš J (2004) Genetic polymorphism within the Leishmania donovani complex: correlation with geographic origin. Am J Trop Med Hyg 70:613-617 (Pubitemid 38802389)
84. Zheng C-J, Wang L-Y, Xu X, Zhu X-H, Wu W-P (2009) Visceral Leishmaniasis in China during 2004-2007. Chin J Parasitol Parasit Dis 27:344-346 (in Chinese with English abstract)