Members of the family Trypanosomatidae infect many organisms, including animals, plants and humans. Plant-infecting trypanosomes are grouped under the single genus Phytomonas, failing to reflect the wide biological and pathological diversity of these protists. While some Phytomonas spp. multiply in the latex of plants, or in fruit or seeds without apparent pathogenicity, others colonize the phloem sap and afflict plants of substantial economic value, including the coffee tree, coconut and oil palms. Plant trypanosomes have not been studied extensively at the genome level, a major gap in understanding and controlling pathogenesis. We describe the genome sequences of two plant trypanosomatids, one pathogenic isolate from a Guianan coconut and one non-symptomatic isolate from Euphorbia collected in France. Although these parasites have extremely distinct pathogenic impacts, very few genes are unique to either, with the vast majority of genes shared by both isolates. Significantly, both Phytomonas spp. genomes consist essentially of single copy genes for the bulk of their metabolic enzymes, whereas other trypanosomatids e.g. Leishmania and Trypanosoma possess multiple paralogous genes or families. Indeed, comparison with other trypanosomatid genomes revealed a highly streamlined genome, encoding for a minimized metabolic system while conserving the major pathways, and with retention of a full complement of endomembrane organelles, but with no evidence for functional complexity. Identification of the metabolic genes of Phytomonas provides opportunities for establishing in vitro culturing of these fastidious parasites and new tools for the control of agricultural plant disease.
Vyšlo v časopise: The Streamlined Genome of spp. Relative to Human Pathogenic Kinetoplastids Reveals a Parasite Tailored for Plants. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004007 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004007
1. DanielsJP, GullK, WicksteadB (2010) Cell biology of the trypanosome genome. Microbiol Mol Biol Rev 74 : 552–569.
2. MalvyD, ChappuisF (2011) Sleeping sickness. Clin Microbiol Infect 17 : 986–995.
3. CouraJR, Borges-PereiraJ (2010) Chagas disease: 100 years after its discovery. A systemic review. Acta Trop 115 : 5–13.
4. den BoerM, ArgawD, JanninJ, AlvarJ (2011) Leishmaniasis impact and treatment access. Clin Microbiol Infect 17 : 1471–1477.
5. PennisiE (2010) Armed and dangerous. Science 327 : 804–805.
6. RaffaeleS, KamounS (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10 : 417–430.
7. KamperJ, KahmannR, BolkerM, MaLJ, BrefortT, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444 : 97–101.
8. KemenE, GardinerA, Schultz-LarsenT, KemenAC, BalmuthAL, et al. (2011) Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 9: e1001094.
9. AmselemJ, CuomoCA, van KanJA, ViaudM, BenitoEP, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230.
10. DolletM (1984) Plant diseases caused by flagellate protozoa (Phytomonas). Annual Review Phytopathology 22 : 115–125.
11. CamargoEP (1999) Phytomonas and other trypanosomatid parasites of plants and fruit. Adv Parasitol 42 : 29–112.
12. Wallace FG, Roitman I, Camargo EP (1992) Trypanosomatids of plants. In: Kreir JP, Baker JR, editors. Parasitic protozoa. 2nd ed. New York: Academic Press. pp. 55–84.
13. Camargo EP, Wallace G (1994) Vectors of plant parasites of the genus Phytomonas (Protozoa, Zoomastigophorea, Kinetoplastida); Harris KF, editor. New York: Springer-Verlag.
14. Desmier De ChenonR (1984) Research on the genus Lincus Stal, Hemiptera Pentatomidae Discocephalinae, and its possible role in the transmission of Marchitez of oil palm and hartrot of coconut. Oléagineux 39 : 1–6.
15. Dollet M., Alvanil F., Diaz A., Louvet C., Gargani D., et al.. (1993) Les Pentatomides vecteurs des Trypanosomes associés au Hartrot du cocotier et Marchitez du palmier. In: Plantes ANdlPd, editor. 3ème Conférence Internationale sur les Ravageurs en Agriculture. Montpellier, France. pp. 1321–1328.
16. LouiseC, DolletM, MariauD (1986) Research into Hartrot of the Coconut, a Disease Caused by Phytomonas (Trypanosomatidae), and into Its Vector Lincus Sp (Pentatomidae) in Guiana. Oléagineux 41 : 437–446.
17. DonovanC (1909) Kala-Azar in Madras, especially with regard to its connexion with the dog and the bug (Conorrhinus). Lancet 177 : 1495–1496.
18. MullerE, GarganiD, BanulsAL, TibayrencM, DolletM (1997) Classification of plant trypanosomatids (Phytomonas spp.): parity between random-primer DNA typing and multilocus enzyme electrophoresis. Parasitology 115 (Pt 4) 403–409.
19. DolletM (2001) Phloem-restricted trypanosomatids form a clearly characterised monophyletic group among trypanosomatids isolated from plants. Int J Parasitol 31 : 459–467.
20. DolletM, SturmNR, CampbellDA (2001) The spliced leader RNA gene array in phloem-restricted plant trypanosomatids (Phytomonas) partitions into two major groupings: epidemiological implications. Parasitology 122 : 289–297.
21. SturmNR, DolletM, LukesJ, CampbellDA (2007) Rational sub-division of plant trypanosomes (Phytomonas spp.) based on minicircle conserved region analysis. Infect Genet Evol 7 : 570–576.
22. DolletM, SturmNR, CampbellDA (2012) The internal transcribed spacer of ribosomal RNA genes in plant trypanosomes (Phytomonas spp.) resolves 10 groups. Infect Genet Evol 12 : 299–308.
23. CamargoEP, KasteleinP, RoitmanI (1990) Trypanosomatid parasites of plants (phytomonas). Parasitol Today 6 : 22–25.
24. StahelG (1931) Zur Kenntnis der Siebröhrenkrankheit (Phloëmnekrose) des Kaffeebaumes in Surinam. Mikroskopische Untersuchungen und Infektionsversuche 4 : 65–82.
25. VermeulenH (1968) Investigations into the cause of the phloem necrosis disease of Coffea liberica in Surinam, South America. Netherlands Journal of Plant Pathology 74 : 202–218.
26. LopezG, GentyP, OllagnierM (1975) Control preventivo de la “Marchitez sorpresiva” del Elaeis guineensis en America Latina. Oleagineux 30 : 243–250.
27. ParthasarathyMV, WGVANS, SoudantC (1976) Trypanosomatid flagellate in the Phloem of diseased coconut palms. Science 192 : 1346–1348.
28. BerrimanM, GhedinE, Hertz-FowlerC, BlandinG, RenauldH, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309 : 416–422.
29. IvensAC, PeacockCS, WortheyEA, MurphyL, AggarwalG, et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309 : 436–442.
30. El-SayedNM, MylerPJ, BartholomeuDC, NilssonD, AggarwalG, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309 : 409–415.
31. El-SayedNM, MylerPJ, BlandinG, BerrimanM, CrabtreeJ, et al. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309 : 404–409.
32. PeacockCS, SeegerK, HarrisD, MurphyL, RuizJC, et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39 : 839–847.
33. AslettM, AurrecoecheaC, BerrimanM, BrestelliJ, BrunkBP, et al. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38: D457–462.
34. RaymondF, BoisvertS, RoyG, RittJF, LegareD, et al. (2012) Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species. Nucleic Acids Res 40 : 1131–1147.
35. JacksonAP, BerryA, AslettM, AllisonHC, BurtonP, et al. (2012) Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species. Proc Natl Acad Sci U S A 109 : 3416–3421.
36. KorenyL, SobotkaR, KovarovaJ, GnipovaA, FlegontovP, et al. (2012) Aerobic kinetoplastid flagellate Phytomonas does not require heme for viability. Proc Natl Acad Sci U S A 109 : 3808–3813.
37. MarinC, AlbergeB, DolletM, PagesM, BastienP (2008) First complete chromosomal organization of a protozoan plant parasite (Phytomonas spp.). Genomics 91 : 88–93.
38. MarinC, DolletM, PagesM, BastienP (2009) Large differences in the genome organization of different plant Trypanosomatid parasites (Phytomonas spp.) reveal wide evolutionary divergences between taxa. Infect Genet Evol 9 : 235–240.
39. AuryJM, CruaudC, BarbeV, RogierO, MangenotS, et al. (2008) High quality draft sequences for prokaryotic genomes using a mix of new sequencing technologies. BMC Genomics 9 : 603.
40. RogersMB, HilleyJD, DickensNJ, WilkesJ, BatesPA, et al. (2011) Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res 21 : 2129–2142.
41. AkopyantsNS, KimblinN, SecundinoN, PatrickR, PetersN, et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324 : 265–268.
42. MarcheS, RothC, PhilippeH, DolletM, BaltzT (1995) Characterization and detection of plant trypanosomatids by sequence analysis of the small subunit ribosomal RNA gene. Mol Biochem Parasitol 71 : 15–26.
43. ArnerE, KindlundE, NilssonD, FarzanaF, FerellaM, et al. (2007) Database of Trypanosoma cruzi repeated genes: 20,000 additional gene variants. BMC Genomics 8 : 391.
44. AnderssonB (2011) The Trypanosoma cruzi genome; conserved core genes and extremely variable surface molecule families. Res Microbiol 162 : 619–625.
45. MauricioIL, GauntMW, StothardJR, MilesMA (2007) Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. Int J Parasitol 37 : 565–576.
46. d'Avila-LevyCM, SantosLO, MarinhoFA, DiasFA, LopesAH, et al. (2006) Gp63-like molecules in Phytomonas serpens: possible role in the insect interaction. Curr Microbiol 52 : 439–444.
47. SantosAL, d'Avila-LevyCM, DiasFA, RibeiroRO, PereiraFM, et al. (2006) Phytomonas serpens: cysteine peptidase inhibitors interfere with growth, ultrastructure and host adhesion. Int J Parasitol 36 : 47–56.
48. EliasCG, ChagasMG, Souza-GoncalvesAL, PascarelliBM, d'Avila-LevyCM, et al. (2012) Differential expression of cruzipain - and gp63-like molecules in the phytoflagellate trypanosomatid Phytomonas serpens induced by exogenous proteins. Exp Parasitol 130 : 13–21.
49. SiegelTN, HekstraDR, KempLE, FigueiredoLM, LowellJE, et al. (2009) Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 23 : 1063–1076.
50. Martinez-CalvilloS, Vizuet-de-RuedaJC, Florencio-MartinezLE, Manning-CelaRG, Figueroa-AnguloEE (2010) Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010 : 525241.
51. MairG, ShiH, LiH, DjikengA, AvilesHO, et al. (2000) A new twist in trypanosome RNA metabolism: cis-splicing of pre-mRNA. RNA 6 : 163–169.
52. OpperdoesFR, MichelsPA (2007) Horizontal gene transfer in trypanosomatids. Trends Parasitol 23 : 470–476.
53. HannaertV, SaavedraE, DuffieuxF, SzikoraJP, RigdenDJ, et al. (2003) Plant-like traits associated with metabolism of Trypanosoma parasites. Proc Natl Acad Sci U S A 100 : 1067–1071.
54. NawatheanP, MaslovDA (2000) The absence of genes for cytochrome c oxidase and reductase subunits in maxicircle kinetoplast DNA of the respiration-deficient plant trypanosomatid Phytomonas serpens. Curr Genet 38 : 95–103.
55. LukesJ, HashimiH, ZikovaA (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48 : 277–299.
56. SimpsonL, MaslovDA (1999) Evolution of the U-insertion/deletion RNA editing in mitochondria of kinetoplastid protozoa. Ann N Y Acad Sci 870 : 190–205.
57. VotypkaJ, KlepetkovaH, JirkuM, KmentP, LukesJ (2012) Phylogenetic relationships of trypanosomatids parasitising true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol 42 : 489–500.
58. MaslovDA, VotypkaJ, YurchenkoV, LukesJ (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29 : 43–52.
59. MaslovDA, HollarL, HaghighatP, NawatheanP (1998) Demonstration of mRNA editing and localization of guide RNA genes in kinetoplast-mitochondria of the plant trypanosomatid Phytomonas serpens. Mol Biochem Parasitol 93 : 225–236.
60. SimpsonL (1997) The genomic organization of guide RNA genes in kinetoplastid protozoa: several conundrums and their solutions. Mol Biochem Parasitol 86 : 133–141.
61. DolletM, SturmNR, AhomadegbeJC, CampbellDA (2001) Kinetoplast DNA minicircles of phloem-restricted Phytomonas associated with wilt diseases of coconut and oil palms have a two-domain structure. FEMS Microbiol Lett 205 : 65–69.
62. BringaudF, BiteauN, ZuiderwijkE, BerrimanM, El-SayedNM, et al. (2004) The ingi and RIME non-LTR retrotransposons are not randomly distributed in the genome of Trypanosoma brucei. Mol Biol Evol 21 : 520–528.
63. BringaudF, BartholomeuDC, BlandinG, DelcherA, BaltzT, et al. (2006) The Trypanosoma cruzi L1Tc and NARTc non-LTR retrotransposons show relative site specificity for insertion. Mol Biol Evol 23 : 411–420.
64. BringaudF, GhedinE, BlandinG, BartholomeuDC, CalerE, et al. (2006) Evolution of non-LTR retrotransposons in the trypanosomatid genomes: Leishmania major has lost the active elements. Mol Biochem Parasitol 145 : 158–170.
65. BringaudF, MullerM, CerqueiraGC, SmithM, RochetteA, et al. (2007) Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog 3 : 1291–1307.
66. BringaudF, BerrimanM, Hertz-FowlerC (2009) Trypanosomatid genomes contain several subfamilies of ingi-related retroposons. Eukaryot Cell 8 : 1532–1542.
67. SmithM, BringaudF, PapadopoulouB (2009) Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics 10 : 240.
68. BringaudF, Garcia-PerezJL, HerasSR, GhedinE, El-SayedNM, et al. (2002) Identification of non-autonomous non-LTR retrotransposons in the genome of Trypanosoma cruzi. Mol Biochem Parasitol 124 : 73–78.
69. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13 : 2178–2189.
70. GuerreiroLT, SouzaSS, WagnerG, De SouzaEA, MendesPN, et al. (2005) Exploring the genome of Trypanosoma vivax through GSS and in silico comparative analysis. OMICS 9 : 116–128.
71. Ulrich P, Cintron R, Docampo R (2010) Calcium homeostasis and acidocalcisomes in Trypanosoma cruzi. In: de Souza W, editor. Structures and Organelles in Pathogenic Protists. Berlin: Springer-Verlag. pp. 299–318.
72. LiuB, LiuY, MotykaSA, AgboEE, EnglundPT (2005) Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol 21 : 363–369.
73. StuartKD, SchnauferA, ErnstNL, PanigrahiAK (2005) Complex management: RNA editing in trypanosomes. Trends Biochem Sci 30 : 97–105.
74. AmmermanML, DowneyKM, HashimiH, FiskJC, TomaselloDL, et al. (2012) Architecture of the trypanosome RNA editing accessory complex, MRB1. Nucleic Acids Res 40 : 5637–5650.
75. ParsonsM, WortheyEA, WardPN, MottramJC (2005) Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6 : 127.
76. AlonsoA, SasinJ, BottiniN, FriedbergI, FriedbergI, et al. (2004) Protein tyrosine phosphatases in the human genome. Cell 117 : 699–711.
77. SzoorB (2010) Trypanosomatid protein phosphatases. Mol Biochem Parasitol 173 : 53–63.
78. BrenchleyR, TariqH, McElhinneyH, SzoorB, Huxley-JonesJ, et al. (2007) The TriTryp phosphatome: analysis of the protein phosphatase catalytic domains. BMC Genomics 8 : 434.
79. StegmeierF, AmonA (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38 : 203–232.
80. AndreevaAV, KutuzovMA (2004) Widespread presence of “bacterial-like” PPP phosphatases in eukaryotes. BMC Evol Biol 4 : 47.
81. AkermanM, Shaked-MishanP, MazarebS, VolpinH, ZilbersteinD (2004) Novel motifs in amino acid permease genes from Leishmania. Biochem Biophys Res Commun 325 : 353–366.
82. JacksonAP (2007) Origins of amino acid transporter loci in trypanosomatid parasites. BMC Evol Biol 7 : 26.
83. SaierMHJr (1999) A functional-phylogenetic system for the classification of transport proteins. J Cell Biochem Suppl 32–33 : 84–94.
84. BuschW, SaierMHJr (2003) The IUBMB-endorsed transporter classification system. Methods Mol Biol 227 : 21–36.
85. MirandaK, RodriguesCO, HentchelJ, VercesiA, PlattnerH, et al. (2004) Acidocalcisomes of Phytomonas francai possess distinct morphological characteristics and contain iron. Microsc Microanal 10 : 647–655.
86. FuruyaT, OkuraM, RuizFA, ScottDA, DocampoR (2001) TcSCA complements yeast mutants defective in Ca2+ pumps and encodes a Ca2+-ATPase that localizes to the endoplasmic reticulum of Trypanosoma cruzi. J Biol Chem 276 : 32437–32445.
87. BrighouseA, DacksJB, FieldMC (2010) Rab protein evolution and the history of the eukaryotic endomembrane system. Cell Mol Life Sci 67 : 3449–3465.
88. NatesanSK, PeacockL, LeungKF, MatthewsKR, GibsonW, et al. (2009) The trypanosome Rab-related proteins RabX1 and RabX2 play no role in intracellular trafficking but may be involved in fly infectivity. PLoS One 4: e7217.
89. AckersJP, DhirV, FieldMC (2005) A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol Biochem Parasitol 141 : 89–97.
90. EliasM, BrighouseA, Gabernet-CastelloC, FieldMC, DacksJB (2012) Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci 125 : 2500–2508.
91. Sanchez-MorenoM, LasztityD, CoppensI, OpperdoesFR (1992) Characterization of carbohydrate metabolism and demonstration of glycosomes in a Phytomonas sp. isolated from Euphorbia characias. Mol Biochem Parasitol 54 : 185–199.
92. ChaumontF, SchanckAN, BlumJJ, OpperdoesFR (1994) Aerobic and anaerobic glucose metabolism of Phytomonas sp. isolated from Euphorbia characias. Mol Biochem Parasitol 67 : 321–331.
93. MolinasSM, AltabeSG, OpperdoesFR, RiderMH, MichelsPA, et al. (2003) The multifunctional isopropyl alcohol dehydrogenase of Phytomonas sp. could be the result of a horizontal gene transfer from a bacterium to the trypanosomatid lineage. J Biol Chem 278 : 36169–36175.
94. UttaroAD, OpperdoesFR (1997) Characterisation of the two malate dehydrogenases from Phytomonas sp. Purification of the glycosomal isoenzyme. Mol Biochem Parasitol 89 : 51–59.
95. CanepaGE, CarrilloC, MirandaMR, SayeM, PereiraCA (2011) Arginine kinase in Phytomonas, a trypanosomatid parasite of plants. Comp Biochem Physiol B Biochem Mol Biol 160 : 40–43.
96. FairlambAH, CeramiA (1992) Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 46 : 695–729.
97. MarcheS, RothC, ManoharSK, DolletM, BaltzT (1993) RNA virus-like particles in pathogenic plant trypanosomatids. Mol Biochem Parasitol 57 : 261–267.
98. WidmerG, ComeauAM, FurlongDB, WirthDF, PattersonJL (1989) Characterization of a RNA virus from the parasite Leishmania. Proc Natl Acad Sci U S A 86 : 5979–5982.
99. WeeksR, AlineRFJr, MylerPJ, StuartK (1992) LRV1 viral particles in Leishmania guyanensis contain double-stranded or single-stranded RNA. J Virol 66 : 1389–1393.
100. NaglikJR, ChallacombeSJ, HubeB (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67 : 400–428 table of contents.
101. ten HaveA, EspinoJJ, DekkersE, Van SluyterSC, BritoN, et al. (2010) The Botrytis cinerea aspartic proteinase family. Fungal Genet Biol 47 : 53–65.
102. SilvermanJM, ChanSK, RobinsonDP, DwyerDM, NandanD, et al. (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9: R35.
103. CorralesRM, SerenoD, Mathieu-DaudeF (2010) Deciphering the Leishmania exoproteome: what we know and what we can learn. FEMS Immunol Med Microbiol 58 : 27–38.
104. HorvathP, NosanchukJD, HamariZ, VagvolgyiC, GacserA (2012) The identification of gene duplication and the role of secreted aspartyl proteinase 1 in Candida parapsilosis virulence. J Infect Dis 205 : 923–933.
105. WyattGR, KaleGF (1957) The chemistry of insect hemolymph. II. Trehalose and other carbohydrates. J Gen Physiol 40 : 833–847.
106. DocampoR, LukesJ (2012) Trypanosomes and the solution to a 50-year mitochondrial calcium mystery. Trends Parasitol 28 : 31–37.
107. LeeMC, MarxCJ (2012) Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genet 8: e1002651.
108. PeyretailladeE, El AlaouiH, DiogonM, PolonaisV, ParisotN, et al. (2011) Extreme reduction and compaction of microsporidian genomes. Res Microbiol 162 : 598–606.
109. KubeM, MitrovicJ, DudukB, RabusR, SeemullerE (2012) Current view on phytoplasma genomes and encoded metabolism. ScientificWorldJournal 2012 : 185942.
110. BaiX, ZhangJ, EwingA, MillerSA, Jancso RadekA, et al. (2006) Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J Bacteriol 188 : 3682–3696.
111. Tyler BM, Rouxel T (2013) Effectors of fungi and oomycetes: their virulence and avirulence functions and translocation from pathogen to host cells. In: Sessa G, editor. Molecular Plant Immunity: Wiley-Blackwell. pp. 123–154.
112. UttaroAD, MirkinN, RiderMH, MichelsM, OpperdoesFR (1999) Phytomonas sp. A model of trypanosomatid metabolism and drug. Mem Inst Oswaldo Cruz 94.
113. MaganR, MarinC, SalasJM, Barrera-PerezM, RosalesMJ, et al. (2004) Cytotoxicity of three new triazolo-pyrimidine derivatives against the plant trypanosomatid: Phytomonas sp. isolated from Euphorbia characias. Mem Inst Oswaldo Cruz 99 : 651–656.
114. LiR, LiY, KristiansenK, WangJ (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24 : 713–714.
115. LoweTM, EddySR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25 : 955–964.
116. HoweKL, ChothiaT, DurbinR (2002) GAZE: a generic framework for the integration of gene-prediction data by dynamic programming. Genome Res 12 : 1418–1427.
117. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 : 3389–3402.
118. KentWJ (2002) BLAT–the BLAST-like alignment tool. Genome Res 12 : 656–664.
119. BirneyE, DurbinR (2000) Using GeneWise in the Drosophila annotation experiment. Genome Res 10 : 547–548.
120. GertzEM, YuYK, AgarwalaR, SchafferAA, AltschulSF (2006) Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 4 : 41.
121. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215 : 403–410.
122. BendtsenJD, NielsenH, von HeijneG, BrunakS (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 : 783–795.
123. KroghA, LarssonB, von HeijneG, SonnhammerEL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305 : 567–580.
124. DereeperA, GuignonV, BlancG, AudicS, BuffetS, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465–469.
125. BinetR, MaurelliAT (2009) The chlamydial functional homolog of KsgA confers kasugamycin sensitivity to Chlamydia trachomatis and impacts bacterial fitness. BMC Microbiol 9 : 279.
126. CastresanaJ (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17 : 540–552.
127. MannaPT, KellyS, FieldMC (2013) Adaptin evolution in kinetoplastids and emergence of the variant surface glycoprotein coat in African trypanosomatids. Mol Phylogenet Evol 67 : 123–128.
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