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.

Biomedical Research Foundation Academy of Athens Athens Greece

Center for Tropical and Emerging Global Diseases and Department of Cellular Biology University of Georgia Athens Georgia United States of America

Centre de Résonance Magnétique des Systèmes Biologiques Université Bordeaux Segalen CNRS UMR 5536 Bordeaux France

Centre for Immunity Infection and Evolution Institute of Immunology and Infection Research School of Biological Sciences University of Edinburgh Edinburgh United Kingdom

CIRAD TA A 98 F Campus International de Baillarguet Montpellier France

Commissariat à l'Energie Atomique Genoscope Evry France

Commissariat à l'Energie Atomique UMR 8030 Evry France

Department of Microbiology Immunology and Molecular Genetics David Geffen School of Medicine University of California at Los Angeles Los Angeles California United States of America

Department of Pathology University of Cambridge Cambridge United Kingdom

e Duve Institute Université catholique de Louvain Brussels Belgium

Faculty of Biology Technion Israel Institute of Technology Haifa Israel

Institute of Infection Immunity and Inflammation College of Medical Veterinary and Life Sciences University of Glasgow Glasgow United Kingdom

Institute of Parasitology Biology Centre and Faculty of Sciences University of South Bohemia České Budějovice Czech Republic

The Mina and Everard Goodman Faculty of Life Sciences Bar Ilan University Ramat Gan Israel

Wellcome Trust Centre for Molecular Parasitology Institute of Infection Immunity and Inflammation College of Medical Veterinary and Life Sciences University of Glasgow Glasgow United Kingdom

Zobrazit více v PubMed

Daniels JP, Gull K, Wickstead B (2010) Cell biology of the trypanosome genome. Microbiol Mol Biol Rev 74: 552–569. PubMed PMC

Malvy D, Chappuis F (2011) Sleeping sickness. Clin Microbiol Infect 17: 986–995. PubMed

Coura JR, Borges-Pereira J (2010) Chagas disease: 100 years after its discovery. A systemic review. Acta Trop 115: 5–13. PubMed

den Boer M, Argaw D, Jannin J, Alvar J (2011) Leishmaniasis impact and treatment access. Clin Microbiol Infect 17: 1471–1477. PubMed

Pennisi E (2010) Armed and dangerous. Science 327: 804–805. PubMed

Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10: 417–430. PubMed

Kamper J, Kahmann R, Bolker M, Ma LJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101. PubMed

Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, et al. (2011) Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 9: e1001094. PubMed PMC

Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, et al. (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7: e1002230. PubMed PMC

Dollet M (1984) Plant diseases caused by flagellate protozoa (Phytomonas). Annual Review Phytopathology 22: 115–125.

Camargo EP (1999) Phytomonas and other trypanosomatid parasites of plants and fruit. Adv Parasitol 42: 29–112. PubMed

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.

Camargo EP, Wallace G (1994) Vectors of plant parasites of the genus Phytomonas (Protozoa, Zoomastigophorea, Kinetoplastida); Harris KF, editor. New York: Springer-Verlag.

Desmier De Chenon R (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.

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.

Louise C, Dollet M, Mariau D (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.

Donovan C (1909) Kala-Azar in Madras, especially with regard to its connexion with the dog and the bug (Conorrhinus). Lancet 177: 1495–1496.

Muller E, Gargani D, Banuls AL, Tibayrenc M, Dollet M (1997) Classification of plant trypanosomatids (Phytomonas spp.): parity between random-primer DNA typing and multilocus enzyme electrophoresis. Parasitology 115 (Pt 4) 403–409. PubMed

Dollet M (2001) Phloem-restricted trypanosomatids form a clearly characterised monophyletic group among trypanosomatids isolated from plants. Int J Parasitol 31: 459–467. PubMed

Dollet M, Sturm NR, Campbell DA (2001) The spliced leader RNA gene array in phloem-restricted plant trypanosomatids (Phytomonas) partitions into two major groupings: epidemiological implications. Parasitology 122: 289–297. PubMed

Sturm NR, Dollet M, Lukes J, Campbell DA (2007) Rational sub-division of plant trypanosomes (Phytomonas spp.) based on minicircle conserved region analysis. Infect Genet Evol 7: 570–576. PubMed

Dollet M, Sturm NR, Campbell DA (2012) The internal transcribed spacer of ribosomal RNA genes in plant trypanosomes (Phytomonas spp.) resolves 10 groups. Infect Genet Evol 12: 299–308. PubMed

Camargo EP, Kastelein P, Roitman I (1990) Trypanosomatid parasites of plants (phytomonas). Parasitol Today 6: 22–25. PubMed

Stahel G (1931) Zur Kenntnis der Siebröhrenkrankheit (Phloëmnekrose) des Kaffeebaumes in Surinam. Mikroskopische Untersuchungen und Infektionsversuche 4: 65–82.

Vermeulen H (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.

Lopez G, Genty P, Ollagnier M (1975) Control preventivo de la “Marchitez sorpresiva” del Elaeis guineensis en America Latina. Oleagineux 30: 243–250.

Parthasarathy MV, WG VANS, Soudant C (1976) Trypanosomatid flagellate in the Phloem of diseased coconut palms. Science 192: 1346–1348. PubMed

Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416–422. PubMed

Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436–442. PubMed PMC

El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409–415. PubMed

El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, et al. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309: 404–409. PubMed

Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39: 839–847. PubMed PMC

Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, et al. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38: D457–462. PubMed PMC

Raymond F, Boisvert S, Roy G, Ritt JF, Legare D, 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. PubMed PMC

Jackson AP, Berry A, Aslett M, Allison HC, Burton P, 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. PubMed PMC

Koreny L, Sobotka R, Kovarova J, Gnipova A, Flegontov P, et al. (2012) Aerobic kinetoplastid flagellate Phytomonas does not require heme for viability. Proc Natl Acad Sci U S A 109: 3808–3813. PubMed PMC

Marin C, Alberge B, Dollet M, Pages M, Bastien P (2008) First complete chromosomal organization of a protozoan plant parasite (Phytomonas spp.). Genomics 91: 88–93. PubMed

Marin C, Dollet M, Pages M, Bastien P (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. PubMed

Aury JM, Cruaud C, Barbe V, Rogier O, Mangenot S, et al. (2008) High quality draft sequences for prokaryotic genomes using a mix of new sequencing technologies. BMC Genomics 9: 603. PubMed PMC

Rogers MB, Hilley JD, Dickens NJ, Wilkes J, Bates PA, et al. (2011) Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res 21: 2129–2142. PubMed PMC

Akopyants NS, Kimblin N, Secundino N, Patrick R, Peters N, et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324: 265–268. PubMed PMC

Marche S, Roth C, Philippe H, Dollet M, Baltz T (1995) Characterization and detection of plant trypanosomatids by sequence analysis of the small subunit ribosomal RNA gene. Mol Biochem Parasitol 71: 15–26. PubMed

Arner E, Kindlund E, Nilsson D, Farzana F, Ferella M, et al. (2007) Database of Trypanosoma cruzi repeated genes: 20,000 additional gene variants. BMC Genomics 8: 391. PubMed PMC

Andersson B (2011) The Trypanosoma cruzi genome; conserved core genes and extremely variable surface molecule families. Res Microbiol 162: 619–625. PubMed

Mauricio IL, Gaunt MW, Stothard JR, Miles MA (2007) Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. Int J Parasitol 37: 565–576. PubMed

d'Avila-Levy CM, Santos LO, Marinho FA, Dias FA, Lopes AH, et al. (2006) Gp63-like molecules in Phytomonas serpens: possible role in the insect interaction. Curr Microbiol 52: 439–444. PubMed

Santos AL, d'Avila-Levy CM, Dias FA, Ribeiro RO, Pereira FM, et al. (2006) Phytomonas serpens: cysteine peptidase inhibitors interfere with growth, ultrastructure and host adhesion. Int J Parasitol 36: 47–56. PubMed

Elias CG, Chagas MG, Souza-Goncalves AL, Pascarelli BM, d'Avila-Levy CM, 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. PubMed

Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, et al. (2009) Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 23: 1063–1076. PubMed PMC

Martinez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martinez LE, Manning-Cela RG, Figueroa-Angulo EE (2010) Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010: 525241. PubMed PMC

Mair G, Shi H, Li H, Djikeng A, Aviles HO, et al. (2000) A new twist in trypanosome RNA metabolism: cis-splicing of pre-mRNA. RNA 6: 163–169. PubMed PMC

Opperdoes FR, Michels PA (2007) Horizontal gene transfer in trypanosomatids. Trends Parasitol 23: 470–476. PubMed

Hannaert V, Saavedra E, Duffieux F, Szikora JP, Rigden DJ, et al. (2003) Plant-like traits associated with metabolism of Trypanosoma parasites. Proc Natl Acad Sci U S A 100: 1067–1071. PubMed PMC

Nawathean P, Maslov DA (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. PubMed

Lukes J, Hashimi H, Zikova A (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48: 277–299. PubMed

Simpson L, Maslov DA (1999) Evolution of the U-insertion/deletion RNA editing in mitochondria of kinetoplastid protozoa. Ann N Y Acad Sci 870: 190–205. PubMed

Votypka J, Klepetkova H, Jirku M, Kment P, Lukes J (2012) Phylogenetic relationships of trypanosomatids parasitising true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol 42: 489–500. PubMed

Maslov DA, Votypka J, Yurchenko V, Lukes J (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29: 43–52. PubMed

Maslov DA, Hollar L, Haghighat P, Nawathean P (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. PubMed

Simpson L (1997) The genomic organization of guide RNA genes in kinetoplastid protozoa: several conundrums and their solutions. Mol Biochem Parasitol 86: 133–141. PubMed

Dollet M, Sturm NR, Ahomadegbe JC, Campbell DA (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. PubMed

Bringaud F, Biteau N, Zuiderwijk E, Berriman M, El-Sayed NM, 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. PubMed

Bringaud F, Bartholomeu DC, Blandin G, Delcher A, Baltz T, et al. (2006) The Trypanosoma cruzi L1Tc and NARTc non-LTR retrotransposons show relative site specificity for insertion. Mol Biol Evol 23: 411–420. PubMed

Bringaud F, Ghedin E, Blandin G, Bartholomeu DC, Caler E, 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. PubMed

Bringaud F, Muller M, Cerqueira GC, Smith M, Rochette A, et al. (2007) Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog 3: 1291–1307. PubMed PMC

Bringaud F, Berriman M, Hertz-Fowler C (2009) Trypanosomatid genomes contain several subfamilies of ingi-related retroposons. Eukaryot Cell 8: 1532–1542. PubMed PMC

Smith M, Bringaud F, Papadopoulou B (2009) Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics 10: 240. PubMed PMC

Bringaud F, Garcia-Perez JL, Heras SR, Ghedin E, El-Sayed NM, et al. (2002) Identification of non-autonomous non-LTR retrotransposons in the genome of Trypanosoma cruzi. Mol Biochem Parasitol 124: 73–78. PubMed

Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189. PubMed PMC

Guerreiro LT, Souza SS, Wagner G, De Souza EA, Mendes PN, et al. (2005) Exploring the genome of Trypanosoma vivax through GSS and in silico comparative analysis. OMICS 9: 116–128. PubMed

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.

Liu B, Liu Y, Motyka SA, Agbo EE, Englund PT (2005) Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol 21: 363–369. PubMed

Stuart KD, Schnaufer A, Ernst NL, Panigrahi AK (2005) Complex management: RNA editing in trypanosomes. Trends Biochem Sci 30: 97–105. PubMed

Ammerman ML, Downey KM, Hashimi H, Fisk JC, Tomasello DL, et al. (2012) Architecture of the trypanosome RNA editing accessory complex, MRB1. Nucleic Acids Res 40: 5637–5650. PubMed PMC

Parsons M, Worthey EA, Ward PN, Mottram JC (2005) Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6: 127. PubMed PMC

Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, et al. (2004) Protein tyrosine phosphatases in the human genome. Cell 117: 699–711. PubMed

Szoor B (2010) Trypanosomatid protein phosphatases. Mol Biochem Parasitol 173: 53–63. PubMed PMC

Brenchley R, Tariq H, McElhinney H, Szoor B, Huxley-Jones J, et al. (2007) The TriTryp phosphatome: analysis of the protein phosphatase catalytic domains. BMC Genomics 8: 434. PubMed PMC

Stegmeier F, Amon A (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38: 203–232. PubMed

Andreeva AV, Kutuzov MA (2004) Widespread presence of “bacterial-like” PPP phosphatases in eukaryotes. BMC Evol Biol 4: 47. PubMed PMC

Akerman M, Shaked-Mishan P, Mazareb S, Volpin H, Zilberstein D (2004) Novel motifs in amino acid permease genes from Leishmania. Biochem Biophys Res Commun 325: 353–366. PubMed

Jackson AP (2007) Origins of amino acid transporter loci in trypanosomatid parasites. BMC Evol Biol 7: 26. PubMed PMC

Saier MH Jr (1999) A functional-phylogenetic system for the classification of transport proteins. J Cell Biochem Suppl 32–33: 84–94. PubMed

Busch W, Saier MH Jr (2003) The IUBMB-endorsed transporter classification system. Methods Mol Biol 227: 21–36. PubMed

Miranda K, Rodrigues CO, Hentchel J, Vercesi A, Plattner H, et al. (2004) Acidocalcisomes of Phytomonas francai possess distinct morphological characteristics and contain iron. Microsc Microanal 10: 647–655. PubMed

Furuya T, Okura M, Ruiz FA, Scott DA, Docampo R (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. PubMed

Brighouse A, Dacks JB, Field MC (2010) Rab protein evolution and the history of the eukaryotic endomembrane system. Cell Mol Life Sci 67: 3449–3465. PubMed PMC

Natesan SK, Peacock L, Leung KF, Matthews KR, Gibson W, 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. PubMed PMC

Ackers JP, Dhir V, Field MC (2005) A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol Biochem Parasitol 141: 89–97. PubMed

Elias M, Brighouse A, Gabernet-Castello C, Field MC, Dacks JB (2012) Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci 125: 2500–2508. PubMed PMC

Sanchez-Moreno M, Lasztity D, Coppens I, Opperdoes FR (1992) Characterization of carbohydrate metabolism and demonstration of glycosomes in a Phytomonas sp. isolated from Euphorbia characias. Mol Biochem Parasitol 54: 185–199. PubMed

Chaumont F, Schanck AN, Blum JJ, Opperdoes FR (1994) Aerobic and anaerobic glucose metabolism of Phytomonas sp. isolated from Euphorbia characias. Mol Biochem Parasitol 67: 321–331. PubMed

Molinas SM, Altabe SG, Opperdoes FR, Rider MH, Michels PA, 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. PubMed

Uttaro AD, Opperdoes FR (1997) Characterisation of the two malate dehydrogenases from Phytomonas sp. Purification of the glycosomal isoenzyme. Mol Biochem Parasitol 89: 51–59. PubMed

Canepa GE, Carrillo C, Miranda MR, Saye M, Pereira CA (2011) Arginine kinase in Phytomonas, a trypanosomatid parasite of plants. Comp Biochem Physiol B Biochem Mol Biol 160: 40–43. PubMed

Fairlamb AH, Cerami A (1992) Metabolism and functions of trypanothione in the Kinetoplastida. Annu Rev Microbiol 46: 695–729. PubMed

Marche S, Roth C, Manohar SK, Dollet M, Baltz T (1993) RNA virus-like particles in pathogenic plant trypanosomatids. Mol Biochem Parasitol 57: 261–267. PubMed

Widmer G, Comeau AM, Furlong DB, Wirth DF, Patterson JL (1989) Characterization of a RNA virus from the parasite Leishmania. Proc Natl Acad Sci U S A 86: 5979–5982. PubMed PMC

Weeks R, Aline RF Jr, Myler PJ, Stuart K (1992) LRV1 viral particles in Leishmania guyanensis contain double-stranded or single-stranded RNA. J Virol 66: 1389–1393. PubMed PMC

Naglik JR, Challacombe SJ, Hube B (2003) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67: 400–428 table of contents. PubMed PMC

ten Have A, Espino JJ, Dekkers E, Van Sluyter SC, Brito N, et al. (2010) The Botrytis cinerea aspartic proteinase family. Fungal Genet Biol 47: 53–65. PubMed

Silverman JM, Chan SK, Robinson DP, Dwyer DM, Nandan D, et al. (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9: R35. PubMed PMC

Corrales RM, Sereno D, Mathieu-Daude F (2010) Deciphering the Leishmania exoproteome: what we know and what we can learn. FEMS Immunol Med Microbiol 58: 27–38. PubMed

Horvath P, Nosanchuk JD, Hamari Z, Vagvolgyi C, Gacser A (2012) The identification of gene duplication and the role of secreted aspartyl proteinase 1 in Candida parapsilosis virulence. J Infect Dis 205: 923–933. PubMed

Wyatt GR, Kale GF (1957) The chemistry of insect hemolymph. II. Trehalose and other carbohydrates. J Gen Physiol 40: 833–847. PubMed PMC

Docampo R, Lukes J (2012) Trypanosomes and the solution to a 50-year mitochondrial calcium mystery. Trends Parasitol 28: 31–37. PubMed PMC

Lee MC, Marx CJ (2012) Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genet 8: e1002651. PubMed PMC

Peyretaillade E, El Alaoui H, Diogon M, Polonais V, Parisot N, et al. (2011) Extreme reduction and compaction of microsporidian genomes. Res Microbiol 162: 598–606. PubMed

Kube M, Mitrovic J, Duduk B, Rabus R, Seemuller E (2012) Current view on phytoplasma genomes and encoded metabolism. ScientificWorldJournal 2012: 185942. PubMed PMC

Bai X, Zhang J, Ewing A, Miller SA, Jancso Radek A, 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. PubMed PMC

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.

Uttaro AD, Mirkin N, Rider MH, Michels M, Opperdoes FR (1999) Phytomonas sp. A model of trypanosomatid metabolism and drug. Mem Inst Oswaldo Cruz 94.

Magan R, Marin C, Salas JM, Barrera-Perez M, Rosales MJ, 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. PubMed

Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713–714. PubMed

Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955–964. PubMed PMC

Howe KL, Chothia T, Durbin R (2002) GAZE: a generic framework for the integration of gene-prediction data by dynamic programming. Genome Res 12: 1418–1427. PubMed PMC

Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402. PubMed PMC

Kent WJ (2002) BLAT–the BLAST-like alignment tool. Genome Res 12: 656–664. PubMed PMC

Birney E, Durbin R (2000) Using GeneWise in the Drosophila annotation experiment. Genome Res 10: 547–548. PubMed PMC

Gertz EM, Yu YK, Agarwala R, Schaffer AA, Altschul SF (2006) Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 4: 41. PubMed PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. PubMed

Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783–795. PubMed

Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567–580. PubMed

Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465–469. PubMed PMC

Binet R, Maurelli AT (2009) The chlamydial functional homolog of KsgA confers kasugamycin sensitivity to Chlamydia trachomatis and impacts bacterial fitness. BMC Microbiol 9: 279. PubMed PMC

Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552. PubMed

Manna PT, Kelly S, Field MC (2013) Adaptin evolution in kinetoplastids and emergence of the variant surface glycoprotein coat in African trypanosomatids. Mol Phylogenet Evol 67: 123–128. PubMed PMC

Distribution and Functional Analysis of Isocitrate Dehydrogenases across Kinetoplastids

Kinetoplast Genome of Leishmania spp. Is under Strong Purifying Selection

Genomics of Trypanosomatidae: Where We Stand and What Needs to Be Done?

Diverse telomeres in trypanosomatids

The Remarkable Metabolism of Vickermania ingenoplastis: Genomic Predictions

Large-Scale Phylogenetic Analysis of Trypanosomatid Adenylate Cyclases Reveals Associations with Extracellular Lifestyle and Host-Pathogen Interplay

Development of Phytomonas lipae sp. n. (Kinetoplastea: Trypanosomatidae) in the true bug Coreus marginatus (Heteroptera: Coreidae) and insights into the evolution of life cycles in the genus Phytomonas

Not in your usual Top 10: protists that infect plants and algae

Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis

Heme pathway evolution in kinetoplastid protists

Genome of Leptomonas pyrrhocoris: a high-quality reference for monoxenous trypanosomatids and new insights into evolution of Leishmania

Leptomonas seymouri: Adaptations to the Dixenous Life Cycle Analyzed by Genome Sequencing, Transcriptome Profiling and Co-infection with Leishmania donovani