: Trypanosomatids Adapted to Plant Environments
Over 100 years after trypanosomatids were first discovered in plant tissues, Phytomonas parasites have now been isolated across the globe from members of 24 different plant families. Most identified species have not been associated with any plant pathology and to date only two species are definitively known to cause plant disease. These diseases (wilt of palm and coffee phloem necrosis) are problematic in areas of South America where they threaten the economies of developing countries. In contrast to their mammalian infective relatives, our knowledge of the biology of Phytomonas parasites and how they interact with their plant hosts is limited. This review draws together a century of research into plant trypanosomatids, from the first isolations and experimental infections to the recent publication of the first Phytomonas genomes. The availability of genomic data for these plant parasites opens a new avenue for comparative investigations into trypanosomatid biology and provides fresh insight into how this important group of parasites have adapted to survive in a spectrum of hosts from crocodiles to coconuts.
Vyšlo v časopise:
: Trypanosomatids Adapted to Plant Environments. PLoS Pathog 11(1): e32767. doi:10.1371/journal.ppat.1004484
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004484
Souhrn
Over 100 years after trypanosomatids were first discovered in plant tissues, Phytomonas parasites have now been isolated across the globe from members of 24 different plant families. Most identified species have not been associated with any plant pathology and to date only two species are definitively known to cause plant disease. These diseases (wilt of palm and coffee phloem necrosis) are problematic in areas of South America where they threaten the economies of developing countries. In contrast to their mammalian infective relatives, our knowledge of the biology of Phytomonas parasites and how they interact with their plant hosts is limited. This review draws together a century of research into plant trypanosomatids, from the first isolations and experimental infections to the recent publication of the first Phytomonas genomes. The availability of genomic data for these plant parasites opens a new avenue for comparative investigations into trypanosomatid biology and provides fresh insight into how this important group of parasites have adapted to survive in a spectrum of hosts from crocodiles to coconuts.
Zdroje
1. Stuart K, Brun R, Croft S, Fairlamb A, Gürtler RE, et al. (2008) Kinetoplastids: related protozoan pathogens, different diseases. J Clin Invest 118: 1301–1310. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2276762&tool=pmcentrez&rendertype=abstract. Accessed 4 April 2014. doi: 10.1172/JCI33945 18382742
2. MacGregor P, Szöőr B, Savill NJ, Matthews KR (2012) Trypanosomal immune evasion, chronicity and transmission: an elegant balancing act. Nat Rev Microbiol 10: 431–438. http://www.ncbi.nlm.nih.gov/pubmed/22543519. Accessed 5 March 2013. doi: 10.1038/nrmicro2779 22543519
3. Ferguson MA (1999) The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J Cell Sci 112: 2799–2809. http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=GeneralSearch&qid=11&SID=R16dDneN8f2mlAjL72b&page=1&doc=1. Accessed 18 June 2013. 10444375
4. Benne R, Van den Burg J, Brakenhoff JP, Sloof P, Van Boom JH, et al. (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46: 819–826. http://www.ncbi.nlm.nih.gov/pubmed/3019552. Accessed 4 April 2014. 3019552
5. Siegel T, Gunasekera K (2011) Gene expression in Trypanosoma brucei: lessons from high-throughput RNA sequencing. Trends Parasitol 27: 434–441. http://www.sciencedirect.com/science/article/pii/S1471492211000997. Accessed 1 August 2014. doi: 10.1016/j.pt.2011.05.006 21737348
6. Sutton RE, Boothroyd JC (1986) Evidence for trans splicing in trypanosomes. Cell 47: 527–535. http://www.ncbi.nlm.nih.gov/pubmed/3022935. Accessed 31 July 2014. 3022935
7. Akiyoshi B, Gull K (2014) Discovery of unconventional kinetochores in kinetoplastids. Cell 156: 1247–1258. http://www.ncbi.nlm.nih.gov/pubmed/24582333. Accessed 20 March 2014. doi: 10.1016/j.cell.2014.01.049 24582333
8. Broadhead R, Dawe HR, Farr H, Griffiths S, Hart SR, et al. (2006) Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440: 224–227. http://www.ncbi.nlm.nih.gov/pubmed/16525475. Accessed 10 March 2013.
9. Lafont A (1909) Sur la présence d’un Leptomonas, parasite de la classe des Flagelles dans le lates de l’Euphorbia pilulifera. Comptes Rendus des Seances la Soc Biol 66: 1011–1013.
10. Donovan C (1909) Kala-azar in Madras, especially with regard to its connecxion with the dog and the bug (Chonnorrhinus). The Lanclet 177: 1195–1196.
11. Franca C (1920) La flagellose des Euphorbes II. Ann l’instutut Pasteur 34: 432–465. doi: 10.1167/iovs.14-15247 25190660
12. Bensaude M (1925) Flagellates in plants: a review of foreign literature. Phytopathology 15: 273–281.
13. Aragão H de B (1931) Untersuchungen über Phytomonas françai. Mem Inst Oswaldo Cruz 25: 299–306. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0074-02761931000400001&lng=en&nrm=iso&tlng=pt. Accessed 23 April 2014.
14. Parthasarathy M V, VAN Slobbe WG, Soudant C (1976) Trypanosomatid flagellate in the Phloem of diseased coconut palms. Science 192: 1346–1348. http://www.ncbi.nlm.nih.gov/pubmed/17739841. Accessed 14 July 2014. 17739841
15. Di Lucca AGT, Trinidad Chipana EF, Talledo Albújar MJ, Dávila Peralta W, Montoya Piedra YC, et al. (2013) Slow wilt: another form of Marchitez in oil palm associated with trypanosomatids in Peru. Trop Plant Pathol 38: 522–533. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1982-56762013000600008&lng=en&nrm=iso&tlng=en. Accessed 22 April 2014.
16. Camargo EP (1999) Phytomonas and other trypanosomatid parasites of plants and fruit. Adv Parasitol 42: 29–112. http://www.ncbi.nlm.nih.gov/pubmed/10050272. 10050272
17. Stahel G (1931) Zur Kenntis der Siebrohrenkrankheit (Phloemnekrose) des Kaffeebaumes in Surinam. I. Mikroskopische Untersuchungen und Infektionsversuche. Phytopathol Zeitschrift 4: 65–82.
18. Vainstein MH, Roitman I (1986) Cultivation of Phytomonas francai Associated with Poor Development of Root System of Cassava. J Protozool: 511–513.
19. Kitajima EW (1986) Flagellate Protozoon Associated with Poor Development of the Root System of Cassava in the Espirito Santo State, Brazil. Phytopathology 76: 638. http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=Refine&qid=10&SID=S1UzkZyWX6xs8ccJMLV&page=1&doc=3. Accessed 10 April 2014.
20. Aragão HDB (1927) Sur un flagellé du latex de Manihot palmata, Phytomonas francai nsp. CR Soc Biol 97: 1077–1080.
21. Teixeira MM, Campaner M, Camargo EP (1994) Detection of trypanosomatid Phytomonas parasitic in plants by polymerase chain reaction amplification of small subunit ribosomal DNA. Parasitol Res 80: 512–516. http://www.ncbi.nlm.nih.gov/pubmed/7809002. 7809002
22. Serrano MG, Nunes LR, Campaner M, Buck GA, Camargo EP, et al. (1999) Trypanosomatidae: Phytomonas detection in plants and phytophagous insects by PCR amplification of a genus-specific sequence of the spliced leader gene. Exp Parasitol 91: 268–279. http://www.sciencedirect.com/science/article/pii/S001448949894379X. Accessed 29 April 2014. 10072329
23. Bebber DP, Ramotowski MAT, Gurr SJ (2013) Crop pests and pathogens move polewards in a warming world. Nat Clim Chang 3: 985–988. http://dx.doi.org/10.1038/nclimate1990. Accessed 23 May 2014.
24. Berrio C, Ocho A (1991) La Marchitez Sorpresiva de la Palma Aceitera en la Zona Sur del Lago de Maracaibo. Rev difusión Tecnol agrícola y Pesq del FONAIAP 38.
25. Magán R, Marín C, Salas JM, Barrera-Pérez 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. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0074-02762004000600021&lng=en&nrm=iso&tlng=en. Accessed 26 January 2014. 15558180
26. Vainstein MH, Da Silva JBT, De Lima VMQG, Roitman I, De Souza W, et al. (1987) Electrophoretic Analysis of Isoenzymes in the Identification of Trypanosomatids of the Genus Phytomonas 1. J Protozool 34: 442–444. http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=GeneralSearch&qid=1&SID=V2fImhT6osjM9vFHpym&page=1&doc=1. Accessed 14 April 2014.
27. Teixeira MMG, Takata CSA, Conchon I, Campaner M, Camargo EP (1997) Ribosomal and kDNA Markers Distinguish Two Subgroups of Herpetomonas among Old Species and New Trypanosomatids Isolated from Flies. J Parasitol 83: 58. http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=GeneralSearch&qid=2&SID=X1jJ6r6FAiuwRfh4phT&page=1&doc=1. Accessed 5 May 2014. 9057697
28. 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. http://www.ncbi.nlm.nih.gov/pubmed/11289065. 11289065
29. 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. http://www.ncbi.nlm.nih.gov/pubmed/17499027. Accessed 29 April 2013. 17499027
30. 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. http://www.ncbi.nlm.nih.gov/pubmed/22155359. Accessed 29 April 2013. doi: 10.1016/j.meegid.2011.11.010 22155359
31. Koreny L, Lukes J, Al. E (2012) Aerobic kinetoplastid flagellate Phytomonas does not require heme for viability. PNAS 109: 3808–3813. doi: 10.1073/pnas.1201089109/-/DCSupplemental.www.pnas.org/cgi/doi/10.1073/pnas.1201089109 22355128
32. Porcel BM, Denoeud F, Opperdoes F, Noel B, Madoui M-A, et al. (2014) The streamlined genome of Phytomonas spp. relative to human pathogenic kinetoplastids reveals a parasite tailored for plants. PLoS Genet 10: e1004007. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3916237&tool=pmcentrez&rendertype=abstract. Accessed 26 March 2014. doi: 10.1371/journal.pgen.1004007 24516393
33. Santos ALS, d’Avila-Levy CM, Dias F a, 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. http://www.ncbi.nlm.nih.gov/pubmed/16310789. Accessed 21 March 2013. 16310789
34. Kelly S, Ivens A, Manna PT, Gibson W, Field MC (2014) A draft genome for the African crocodilian trypanosome Trypanosoma grayi. Sci Data 1. http://www.nature.com/articles/sdata201424. Accessed 8 August 2014.
35. Ivens AC, Peacock CS, Worthey E a, Murphy L, Aggarwal G, et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436–442. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1470643&tool=pmcentrez&rendertype=abstract. Accessed 3 June 2013. 16020728
36. 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. http://www.ncbi.nlm.nih.gov/pubmed/16020726. Accessed 6 March 2013. 16020726
37. 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. http://www.sciencemag.org/content/309/5733/409.short. Accessed 15 July 2014. 16020725
38. Votýpka J, Klepetková H, Jirků M, Kment P, Lukeš J (2012) Phylogenetic relationships of trypanosomatids parasitising true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol 42: 489–500. http://www.ncbi.nlm.nih.gov/pubmed/22537738. Accessed 6 March 2013. doi: 10.1016/j.ijpara.2012.03.007 22537738
39. Maslov D a, Votýpka J, Yurchenko V, Lukeš J (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29: 43–52. http://www.ncbi.nlm.nih.gov/pubmed/23246083. Accessed 23 March 2013. doi: 10.1016/j.pt.2012.11.001 23246083
40. Breitenbach HH, Wenig M, Wittek F, Jordá L, Maldonado-Alconada AM, et al. (2014) Contrasting Roles of the Apoplastic Aspartyl Protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis Systemic Acquired Resistance. Plant Physiol 165: 791–809. http://www.plantphysiol.org/content/early/2014/04/22/pp.114.239665.short. Accessed 6 June 2014. 24755512
41. 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. http://www.sciencedirect.com/science/article/pii/S1087184509001765. Accessed 5 May 2014. doi: 10.1016/j.fgb.2009.10.008 19853057
42. Kehr J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J Exp Bot 57: 767–774. http://jxb.oxfordjournals.org/content/57/4/767.full. Accessed 28 May 2014. 16495410
43. Hoare CA, Wallace FG (1966) Developmental Stages of Trypanosomatid Flagellates: a New Terminology. Nature 212: 1385–1386. http://dx.doi.org/10.1038/2121385a0. Accessed 14 April 2014.
44. Wheeler RJ, Gluenz E, Gull K (2013) The limits on trypanosomatid morphological diversity. PLoS One 8: e79581. http://www.plosone.org/article/info:doi/10.1371/journal.pone.0079581#s3. Accessed 3 April 2014. doi: 10.1371/journal.pone.0079581 24260255
45. Gibbs AJ (1957) Leptomonas-serpens nsp. parasitic in the digestive tract and salivary glands of Nezara-viridula (Pentatomidae) and in the sap of Solanum-lycopersicum (tomato) and other plants. Parasitology 47: 297–303. http://apps.webofknowledge.com/full_record.do?product=UA&search_mode=GeneralSearch&qid=5&SID=W2qYUfkCAoQXYhjPlT4&page=1&doc=1. Accessed 9 January 2014. 13504849
46. Wheeler RJ, Gluenz E, Gull K (2011) The cell cycle of Leishmania: morphogenetic events and their implications for parasite biology. Mol Microbiol 79: 647–662. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3166656&tool=pmcentrez&rendertype=abstract. Accessed 21 March 2014. doi: 10.1111/j.1365-2958.2010.07479.x 21255109
47. Lafont A (1910) Sur la présence d’un Leptomonas, parasite de la classe des Flagelles, dans le latex de trois Euphorbiacees. Ann l’instutut Pasteur, Paris 24: 205–219. doi: 10.1167/iovs.14-15247 25190660
48. Franchini G (1922) Sur un flagelle nouveau du latex de deux Apocynees. Bull la Soc Pathol Exot 15: 109–113.
49. Franchini G (1922) Sur un trypanosome du latex de deux especes d’Euphorbes. Bull la Soc Pathol Exot 15: 18–23.
50. Lafont A (1911) Sur la transmission du Leptomonas Davidi des euphorbes par un hemiptere, Nysius euphorbiae. Comptes Rendus des Seances la Soc Biol 70: 58–59.
51. Gluenz E, Höög JL, Smith AE, Dawe HR, Shaw MK, et al. (2010) Beyond 9+0: noncanonical axoneme structures characterize sensory cilia from protists to humans. FASEB J 24: 3117–3121. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2923350&tool=pmcentrez&rendertype=abstract. Accessed 20 May 2014. doi: 10.1096/fj.09-151381 20371625
52. Overath P, Haag J, Mameza MG, Lischke A (1999) Freshwater fish trypanosomes: definition of two types, host control by antibodies and lack of antigenic variation. Parasitology 119: 591–601. http://journals.cambridge.org/abstract_S0031182099005089. Accessed 11 April 2014. 10633921
53. Siddall ME, Desser SS (1992) Alternative leech vectors for frog and turtle trypanosomes. J Parasitol 78: 562–563. http://www.ncbi.nlm.nih.gov/pubmed/1597811. Accessed 11 April 2014. 1597811
54. Hamilton PB, Stevens JR, Gidley J, Holz P, Gibson WC (2005) A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). Int J Parasitol 35: 431–443. http://www.sciencedirect.com/science/article/pii/S0020751905000020. Accessed 8 April 2014. 15777919
55. Hamilton PB, Gibson WC, Stevens JR (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Mol Phylogenet Evol 44: 15–25. http://www.sciencedirect.com/science/article/pii/S1055790307000905. Accessed 8 April 2014. 17513135
56. Alves E Silva TL, Vasconcellos LRC, Lopes AH, Souto-Padrón T (2013) The Immune Response of Hemocytes of the Insect Oncopeltus fasciatus against the Flagellate Phytomonas serpens. PLoS One 8: e72076. http://dx.plos.org/10.1371/journal.pone.0072076. Accessed 26 September 2013. doi: 10.1371/journal.pone.0072076 24015207
57. Camargo EP, Kastelein P, Roitman I (1990) Trypanosomatid parasites of plants (phytomonas). Parasitol Today 6: 22–25. http://dx.doi.org/10.1016/0169-4758(90)90388-K. Accessed 17 June 2013. 15463252
58. Brazil RP, Fiorini JE, Silva PMFE (1990) Phytomonas sp., a trypanosomatid parasite of tomato, isolated from salivary glands of Phthia picta (Hemiptera: Coreidae) in southeast Brazil. Mem Inst Oswaldo Cruz 85: 239–240. http://www.cabdirect.org/abstracts/19910881423.html;jsessionid=E654E3491B07A246AEFC3B74997D2B40?freeview=true. Accessed 8 June 2014.
59. Barry J (1998) VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei. Mol Biochem Parasitol 91: 93–105. http://www.sciencedirect.com/science/article/pii/S016668519700193X. Accessed 19 July 2014. 9574928
60. Späth GF, Beverley SM (2001) A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp Parasitol 99: 97–103. http://www.ncbi.nlm.nih.gov/pubmed/11748963. Accessed 6 August 2014. 11748963
61. Späth GF, Epstein L, Leader B, Singer SM, Avila HA, et al. (2000) Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc Natl Acad Sci U S A 97: 9258–9263. http://www.pnas.org/content/97/16/9258.short. Accessed 6 August 2014. 10908670
62. Jankevicius JV, Jankevfcius SI, Campaner M, Conchon I, Madea LA, et al. (1989) Life Cycle and Culturing of Phytomonas serpens (Gibbs), a Trypanosomatid Parasite of Tomatoes. J Protozool 36: 265–271. http://doi.wiley.com/10.1111/j.1550-7408.1989.tb05361.x. Accessed 11 April 2014.
63. Zakai HA, Chance ML, Bates PA (1998) In vitro stimulation of metacyclogenesis in Leishmania braziliensis, L. donovani, L. major and L. mexicana. Parasitology 116 (Pt 4: 305–309. http://www.ncbi.nlm.nih.gov/pubmed/9585932. Accessed 6 August 2014. 9585932
64. Rogers ME, Bates PA (2007) Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. PLoS Pathog 3: e91. http://dx.plos.org/10.1371/journal.ppat.0030091. Accessed 24 January 2014. 17604451
65. Hogenhout SA, Oshima K, Ammar E-D, Kakizawa S, Kingdom HN, et al. (2008) Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 9: 403–423. http://www.ncbi.nlm.nih.gov/pubmed/18705857. Accessed 3 October 2013. doi: 10.1111/j.1364-3703.2008.00472.x 18705857
66. Ienne S, Freschi L, Vidotto VF, DE Souza TA, Purgatto E, et al. (2014) Auxin production by the plant trypanosomatid Phytomonas serpens and auxin homoeostasis in infected tomato fruits. Parasitology 141: 1299–1310. Available: http://journals.cambridge.org/abstract_S0031182014000547. Accessed 31 July 2014. doi: 10.1017/S0031182014000547 24805281
67. Redman CA, Schneider P, Mehlert A, Ferguson MA (1995) The glycoinositol-phospholipids of Phytomonas. Biochem J 311: 495–503. http://www.biochemj.org/bj/311/bj3110495.htm. Accessed 11 April 2014. 7487886
68. 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. http://www.ncbi.nlm.nih.gov/pubmed/16732452. Accessed 21 March 2013. 16732452
69. 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. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3650584&tool=pmcentrez&rendertype=abstract. Accessed 30 April 2013. doi: 10.1016/j.ympev.2013.01.002 23337175
70. Jaffe CL, Dwyer DM (2003) Extracellular release of the surface metalloprotease, gp63, from Leishmania and insect trypanosomatids. Parasitol Res 91: 229–237. http://www.ncbi.nlm.nih.gov/pubmed/12923634. Accessed 16 January 2014. 12923634
71. Santos ALS, d’Avila-Levy CM, Elias CGR, Vermelho AB, Branquinha MH (2007) Phytomonas serpens: immunological similarities with the human trypanosomatid pathogens. Microbes Infect 9: 915–921. 17556002
72. Elias CGR, Pereira FM, Dias FA, Silva TLA, Lopes AHCS, et al. (2008) Cysteine peptidases in the tomato trypanosomatid Phytomonas serpens: influence of growth conditions, similarities with cruzipain and secretion to the extracellular environment. Exp Parasitol 120: 343–352. http://www.ncbi.nlm.nih.gov/pubmed/18793639. Accessed 21 March 2013. doi: 10.1016/j.exppara.2008.08.011 18793639
73. Beneteau J, Renard D, Marché L, Douville E, Lavenant L, et al. (2010) Binding properties of the N-acetylglucosamine and high-mannose N-glycan PP2-A1 phloem lectin in Arabidopsis. Plant Physiol 153: 1345–1361. http://www.plantphysiol.org/content/153/3/1345.abstract. Accessed 28 May 2014. doi: 10.1104/pp.110.153882 20442276
74. Gaupels F, Ghirardo A (2013) The extrafascicular phloem is made for fighting. Front Plant Sci 4: 187. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3678090&tool=pmcentrez&rendertype=abstract. Accessed 6 June 2014. doi: 10.3389/fpls.2013.00187 23781225
75. Elias CGR, Chagas MG, Souza-Gonçalves AL, Pascarelli BMO, 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. http://www.ncbi.nlm.nih.gov/pubmed/22033075. Accessed 21 March 2013. doi: 10.1016/j.exppara.2011.10.005 22033075
76. Späth GF, Garraway LA, Turco SJ, Beverley SM (2003) The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc Natl Acad Sci U S A 100: 9536–9541. http://www.pnas.org/content/100/16/9536. Accessed 23 May 2014. 12869694
77. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323–329. http://dx.doi.org/10.1038/nature05286. Accessed 21 May 2013. 17108957
78. El-On J, Bradley DJ, Freeman JC (1980) Leishmania donovani: action of excreted factor on hydrolytic enzyme activity of macrophages from mice with genetically different resistance to infection. Exp Parasitol 49: 167–174. http://www.ncbi.nlm.nih.gov/pubmed/6767620. Accessed 17 September 2014. 6767620
79. McNeely TB, Turco SJ (1990) Requirement of lipophosphoglycan for intracellular survival of Leishmania donovani within human monocytes. J Immunol 144: 2745–2750. http://www.ncbi.nlm.nih.gov/pubmed/2319134. Accessed 17 September 2014. 2319134
80. Barbieri L, Falasca A, Franceschi C, Licastro F, Rossi CA, et al. (1983) Purification and properties of two lectins from the latex of the euphorbiaceous plants Hura crepitans L. (sand-box tree) and Euphorbia characias L. (Mediterranean spurge). Biochem J 215: 433–439. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1152420&tool=pmcentrez&rendertype=abstract. Accessed 5 May 2014. 6661180
81. Sanchez-Moreno M, Fernandez-Becerra C, Mascaro C, Rosales MJ, Dollet M, et al. (1995) Isolation, in vitro culture, ultrastructure study, and characterization by lectin-agglutination tests of Phytomonas isolated from tomatoes (Lycopersicon esculentum) and cherimoyas (Anona cherimolia) in southeastern Spain. Parasitol Res 81: 575–581. http://link.springer.com/10.1007/BF00932024. Accessed 22 April 2014. 7479649
82. Da Silva R V, Malvezi AD, Augusto L da S, Kian D, Tatakihara VLH, et al. (2013) Oral exposure to Phytomonas serpens attenuates thrombocytopenia and leukopenia during acute infection with Trypanosoma cruzi. PLoS One 8: e68299. http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068299;jsessionid=973A60CAB98EA0D186580F375A605096. Accessed 31 January 2014. doi: 10.1371/journal.pone.0068299 23844182
83. Franchini G (1922) Essais d’inoculation aux souris blanches du latex parasite de differentes especes d’euphorbes. Ann l’instutut Pasteur 36: 873–881. doi: 10.1167/iovs.14-15247 25190660
84. Carrari F, Baxter C, Usadel B, Urbanczyk-Wochniak E, Zanor M- I, et al. (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol 142: 1380–1396. http://www.plantphysiol.org/content/142/4/1380. Accessed 29 April 2014. 17071647
85. Oliveira AP, Silva LR, Andrade PB, Valentão P, Silva BM, et al. (2010) Further insight into the latex metabolite profile of Ficus carica. J Agric Food Chem 58: 10855–10863. http://dx.doi.org/10.1021/jf1031185. Accessed 28 April 2014. doi: 10.1021/jf1031185 20923221
86. Maslov D, Nawathean P, Scheel J (1999) Partial kinetoplast-mitochondrial gene organization and expression in the respiratory deficient plant trypanosomatid Phytomonas serpens. Mol Biochem Parasitol 99: 207–221. Available: http://www.sciencedirect.com/science/article/pii/S0166685199000286. Accessed 1 August 2014. 10340485
87. 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. doi: 10.1007/s002940000135 10975258
88. Bringaud F, Rivière L, Coustou V (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol. http://www.sciencedirect.com/science/article/pii/S0166685106001150. Accessed 1 August 2014.
89. Chaumont F, Schanck A, Blum JJ, Opperdoes FR (1994) Aerobic and anaerobic glucose metabolism of Phytomonas sp. isolated from Euphorbia characias. Mol Biochem Parasitol 67: 321–331. http://dx.doi.org/10.1016/0166-6851(94)00141-3. Accessed 17 June 2013. 7870136
90. 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. http://www.sciencedirect.com/science/article/pii/016668519290111V. Accessed 1 August 2014. 1435859
91. Frankenberg N, Moser J, Jahn D (2003) Bacterial heme biosynthesis and its biotechnological application. Appl Microbiol Biotechnol 63: 115–127. http://www.ncbi.nlm.nih.gov/pubmed/13680202. Accessed 13 July 2014. 13680202
92. Molinas SM, Altabe SG, Opperdoes FR, Rider MH, Michels PAM, 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. http://www.ncbi.nlm.nih.gov/pubmed/12853449. Accessed 1 August 2014. 12853449
93. Uttaro AD, Opperdoes FR (1997) Purification and characterisation of a novel iso-propanol dehydrogenase from Phytomonas sp. Mol Biochem Parasitol 85: 213–219. http://www.ncbi.nlm.nih.gov/pubmed/9106194. Accessed 1 August 2014. 9106194
94. 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. http://www.ncbi.nlm.nih.gov/pubmed/9297700. Accessed 6 August 2014. 9297700
95. 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: D457–62. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2808979&tool=pmcentrez&rendertype=abstract. Accessed 27 May 2014. doi: 10.1093/nar/gkp851 19843604
96. Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=403725&tool=pmcentrez&rendertype=abstract. Accessed 26 May 2014. 12952885
97. Collingridge PW, Kelly S (2012) MergeAlign: improving multiple sequence alignment performance by dynamic reconstruction of consensus multiple sequence alignments. BMC Bioinformatics 13: 117. http://www.biomedcentral.com/1471-2105/13/117. Accessed 3 June 2014. doi: 10.1186/1471-2105-13-117 22646090
98. Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26: 1641–1650. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2693737&tool=pmcentrez&rendertype=abstract. Accessed 27 May 2014. doi: 10.1093/molbev/msp077 19377059
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2015 Číslo 1
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Infections in Humans and Animals: Pathophysiology, Detection, and Treatment
- The Phylogenetically-Related Pattern Recognition Receptors EFR and XA21 Recruit Similar Immune Signaling Components in Monocots and Dicots
- Specificity and Dynamics of Effector and Memory CD8 T Cell Responses in Human Tick-Borne Encephalitis Virus Infection
- Viral Activation of MK2-hsp27-p115RhoGEF-RhoA Signaling Axis Causes Cytoskeletal Rearrangements, P-body Disruption and ARE-mRNA Stabilization