Table of Contents Author Guidelines Submit a Manuscript
International Journal of Genomics
Volume 2017 (2017), Article ID 1707231, 9 pages
https://doi.org/10.1155/2017/1707231
Research Article

Evolution of the Apicomplexan Sugar Transporter Gene Family Repertoire

1Department of Genetics, University of Georgia, Athens, GA 30602, USA
2Center for Tropical and Emerging Global Diseases, University of Georgia, Athens, GA 30602, USA
3Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA

Correspondence should be addressed to Jessica C. Kissinger; ude.agu@gnissikj

Received 17 January 2017; Accepted 30 March 2017; Published 7 May 2017

Academic Editor: Marco Gerdol

Copyright © 2017 Ousman Mahmud and Jessica C. Kissinger. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. S. Reddy, M. A. Shlykov, R. Castillo, E. I. Sun, and M. H. Saier Jr., “The major facilitator superfamily (MFS) revisited,” The FEBS Journal, vol. 279, no. 11, pp. 2022–2035, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. M. D. Marger and M. H. Saier Jr., “A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport,” Trends in Biochemical Sciences, vol. 18, no. 1, pp. 13–20, 1993. View at Publisher · View at Google Scholar · View at Scopus
  3. E. M. Quistgaard, C. Low, F. Guettou, and P. Nordlund, “Understanding transport by the major facilitator superfamily (MFS): structures pave the way,” Nature Reviews. Molecular Cell Biology, vol. 17, no. 2, pp. 123–132, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Afoufa-Bastien, A. Medici, J. Jeauffre et al., “The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling,” BMC Plant Biology, vol. 10, no. 1, p. 245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Buttner, “The monosaccharide transporter(-like) gene family in Arabidopsis,” FEBS Letters, vol. 581, no. 12, pp. 2318–2324, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. WHO, World Malaria Report 2015, World Health Organization Global Malaria Programme, Geneva, Switzerland, 2015.
  7. A. A. Escalante and F. J. Ayala, “Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 13, pp. 5793–5797, 1995. View at Publisher · View at Google Scholar · View at Scopus
  8. H. D. Nguyen, M. Yoshihama, and N. Kenmochi, “The evolution of spliceosomal introns in alveolates,” Molecular Biology and Evolution, vol. 24, no. 5, pp. 1093–1096, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. O. S. Harb and D. S. Roos, “The eukaryotic pathogen databases: a functional genomic resource integrating data from human and veterinary parasites,” Methods in Molecular Biology, vol. 1201, pp. 1–18, 2015. View at Publisher · View at Google Scholar
  10. J. C. Kissinger and J. DeBarry, “Genome cartography: charting the apicomplexan genome,” Trends in Parasitology, vol. 27, no. 8, pp. 345–354, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Blazejewski, N. Nursimulu, V. Pszenny et al., “Systems-based analysis of the Sarcocystis neurona genome identifies pathways that contribute to a heteroxenous life cycle,” MBio, vol. 6, no. 1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Joet, L. Holterman, T. T. Stedman et al., “Comparative characterization of hexose transporters of Plasmodium knowlesi, Plasmodium yoelii and Toxoplasma gondii highlights functional differences within the apicomplexan family,” The Biochemical Journal, vol. 368, Part 3, pp. 923–929, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Blume, D. Rodriguez-Contreras, S. Landfear et al., “Host-derived glucose and its transporter in the obligate intracellular pathogen Toxoplasma gondii are dispensable by glutaminolysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 31, pp. 12998–13003, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. E. T. Derbyshire, F. J. Franssen, E. de Vries et al., “Identification, expression and characterisation of a Babesia bovis hexose transporter,” Molecular and Biochemical Parasitology, vol. 161, no. 2, pp. 124–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Slavic, U. Straschil, L. Reininger et al., “Life cycle studies of the hexose transporter of Plasmodium species and genetic validation of their essentiality,” Molecular Microbiology, vol. 75, no. 6, pp. 1402–1413, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Joet, K. Chotivanich, K. Silamut, A. P. Patel, C. Morin, and S. Krishna, “Analysis of Plasmodium vivax hexose transporters and effects of a parasitocidal inhibitor,” The Biochemical Journal, vol. 381, Part 3, pp. 905–909, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Joet, U. Eckstein-Ludwig, C. Morin, and S. Krishna, “Validation of the hexose transporter of Plasmodium falciparum as a novel drug target,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 13, pp. 7476–7479, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. H. Woo, H. Ansari, T. D. Otto et al., “Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites,” eLife, vol. 4, article e06974, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Li, C. J. Stoeckert Jr., and D. S. Roos, “OrthoMCL: identification of ortholog groups for eukaryotic genomes,” Genome Research, vol. 13, no. 9, pp. 2178–2189, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. R. D. Finn, A. Bateman, J. Clements et al., “Pfam: the protein families database,” Nucleic Acids Research, vol. 42, Database issue, pp. D222–D230, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. S. R. Eddy, “Accelerated profile HMM searches,” PLoS Computational Biology, vol. 7, no. 10, article e1002195, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. S. F. Altschul, W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, “Basic local alignment search tool,” Journal of Molecular Biology, vol. 215, no. 3, pp. 403–410, 1990. View at Publisher · View at Google Scholar
  23. M. V. Han, G. W. Thomas, J. Lugo-Martinez, and M. W. Hahn, “Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3,” Molecular Biology and Evolution, vol. 30, no. 8, pp. 1987–1997, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. I. M. Wallace, O. O'Sullivan, D. G. Higgins, and C. Notredame, “M-Coffee: combining multiple sequence alignment methods with T-Coffee,” Nucleic Acids Research, vol. 34, no. 6, pp. 1692–1699, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. A. M. Waterhouse, J. B. Procter, D. M. Martin, M. Clamp, and G. J. Barton, “Jalview version 2—a multiple sequence alignment editor and analysis workbench,” Bioinformatics (Oxford, England), vol. 25, no. 9, pp. 1189–1191, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Whelan and N. Goldman, “A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach,” Molecular Biology and Evolution, vol. 18, no. 5, pp. 691–699, 2001. View at Publisher · View at Google Scholar
  27. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Dereeper, V. Guignon, G. Blanc et al., “Phylogeny.fr: robust phylogenetic analysis for the non-specialist,” Nucleic Acids Research, vol. 36, no. Web Server issue, pp. W465–W469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. J. Drummond, M. A. Suchard, D. Xie, and A. Rambaut, “Bayesian phylogenetics with BEAUti and the BEAST 1.7,” Molecular Biology and Evolution, vol. 29, no. 8, pp. 1969–1973, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. O. Emanuelsson, S. Brunak, G. von Heijne, and H. Nielsen, “Locating proteins in the cell using TargetP, SignalP and related tools,” Nature Protocols, vol. 2, no. 4, pp. 953–971, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. J. D. DeBarry and J. C. Kissinger, “Jumbled genomes: missing Apicomplexan synteny,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2855–2871, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Cornillot, K. Hadj-Kaddour, A. Dassouli et al., “Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti,” Nucleic Acids Research, vol. 40, no. 18, pp. 9102–9114, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Criado, J. Martinez, A. Buling et al., “New data on epizootiology and genetics of piroplasms based on sequences of small ribosomal subunit and cytochrome b genes,” Veterinary Parasitology, vol. 142, no. 3–4, pp. 238–247, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Concannon, K. Wynn-Owen, V. R. Simpson, and R. J. Birtles, “Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK,” Parasitology, vol. 131, Part 4, pp. 489–496, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. B. L. Penzhorn, “Babesiosis of wild carnivores and ungulates,” Veterinary Parasitology, vol. 138, no. 1–2, pp. 11–21, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Laliberte and V. B. Carruthers, “Host cell manipulation by the human pathogen Toxoplasma gondii,” Cellular and Molecular Life Sciences, vol. 65, no. 12, pp. 1900–1915, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Peng, X. Gu, L. J. Xue, J. H. Leebens-Mack, and C. J. Tsai, “Bayesian phylogeny of sucrose transporters: ancient origins, differential expansion and convergent evolution in monocots and dicots,” Frontiers in Plant Science, vol. 5, p. 615, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. O. Lespinet, Y. I. Wolf, E. V. Koonin, and L. Aravind, “The role of lineage-specific gene family expansion in the evolution of eukaryotes,” Genome Research, vol. 12, no. 7, pp. 1048–1059, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. N. S. Morrissette and L. D. Sibley, “Cytoskeleton of apicomplexan parasites,” Microbiology and Molecular Biology Reviews, vol. 66, no. 1, pp. 21–38, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. K. E. Swearingen, S. E. Lindner, L. Shi et al., “Interrogating the Plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics,” PLoS Pathogens, vol. 12, no. 4, article e1005606, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Yu, H. Zhang, and G. Zhu, “Plant-type trehalose synthetic pathway in Cryptosporidium and some other apicomplexans,” PloS One, vol. 5, no. 9, article e12593, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Zhang, F. Guo, H. Zhou, and G. Zhu, “Transcriptome analysis reveals unique metabolic features in the Cryptosporidium parvum oocysts associated with environmental survival and stresses,” BMC Genomics, vol. 13, no. 1, p. 647, 2012. View at Publisher · View at Google Scholar · View at Scopus