Malaria in the ‘Omics Era’
Abstract
:1. Introduction
2. Expanding Horizons: Sequencing Across the Genus Plasmodium
3. The Variable Genome: Genomic Diversity within Plasmodium Species
4. The Dynamic Genome: Methylomics in Plasmodium
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Gardner, M.J.; Hall, N.; Fung, E.; White, O.; Berriman, M.; Hyman, R.W.; Carlton, J.M.; Pain, A.; Nelson, K.E.; Bowman, S.; et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419, 498–511. [Google Scholar] [CrossRef] [PubMed]
- Holt, R.A.; Subramanian, G.M.; Halpern, A.; Sutton, G.G.; Charlab, R.; Nusskern, D.R.; Wincker, P.; Clark, A.G.; Ribeiro, J.C.; Wides, R.; et al. The Genome Sequence of the Malaria Mosquito Anopheles gambiae. Science 2002, 298, 129–149. [Google Scholar] [CrossRef] [PubMed]
- Lander, E.S.; Linton, L.M.; Birren, B.; Nusbaum, C.; Zody, M.C.; Baldwin, J.; Devon, K.; Dewar, K.; Doyle, M.; FitzHugh, W. Initial sequencing and analysis of the human genome. Nature 2001, 409, 860–921. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galen, S.C.; Borner, J.; Martinsen, E.S.; Schaer, J.; Austin, C.C.; West, C.J.; Perkins, S.L. The polyphyly of Plasmodium: Comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. R. Soc. Open Sci. 2018, 5, 171780. [Google Scholar] [CrossRef] [Green Version]
- Sutherland, C.J.; Tanomsing, N.; Nolder, D.; Oguike, M.; Jennison, C.; Pukrittayakamee, S.; Dolecek, C.; Hien, T.T.; Rosário, V.E.D.; Arez, A.P.; et al. Two Nonrecombining Sympatric Forms of the Human Malaria Parasite Plasmodium ovale Occur Globally. J. Infect. Dis. 2010, 201, 1544–1550. [Google Scholar] [CrossRef] [Green Version]
- Auburn, S.; Böhme, U.; Steinbiss, S.; Trimarsanto, H.; Hostetler, J.; Sanders, M.; Gao, Q.; Nosten, F.; Newbold, C.I.; Berriman, M.; et al. A new Plasmodium vivax reference sequence with improved assembly of the subtelomeres reveals an abundance of pir genes. Wellcome Open Res. 2016, 1, 4. [Google Scholar] [CrossRef]
- Otto, T.D.; Böhme, U.; Jackson, A.P.; Hunt, M.; Franke-Fayard, B.; Hoeijmakers, W.A.M.; Religa, A.A.; Robertson, L.; Sanders, M.; Ogun, S.A.; et al. A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol. 2014, 12, 86. [Google Scholar] [CrossRef] [PubMed]
- Pasini, E.M.; Böhme, U.; Rutledge, G.G.; Der Wel, A.V.-V.; Sanders, M.; Berriman, M.; Kocken, C.H.; Otto, T.D. An improved Plasmodium cynomolgi genome assembly reveals an unexpected methyltransferase gene expansion. Wellcome Open Res. 2017, 2, 42. [Google Scholar] [CrossRef] [Green Version]
- Tachibana, S.-I.; Sullivan, S.A.; Kawai, S.; Nakamura, S.; Kim, H.R.; Goto, N.; Arisue, N.; Palacpac, N.M.Q.; Honma, H.; Yagi, M.; et al. Plasmodium cynomolgi genome sequences provide insight into Plasmodium vivax and the monkey malaria clade. Nat. Genet. 2012, 44, 1051–1055. [Google Scholar] [CrossRef] [Green Version]
- Otto, T.D.; Gilabert, A.; Crellen, T.; Böhme, U.; Arnathau, C.; Sanders, M.; Oyola, S.O.; Okouga, A.P.; Boundenga, L.; Willaume, E.; et al. Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria. Nat. Microbiol. 2018, 3, 687–697. [Google Scholar] [CrossRef] [Green Version]
- Carlton, J.M.; Adams, J.H.; Silva, J.C.; Bidwell, S.L.; Lorenzi, H.; Caler, E.; Crabtree, J.; Angiuoli, S.V.; Merino, E.F.; Amedeo, P.; et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008, 455, 757–763. [Google Scholar] [CrossRef] [PubMed]
- Ansari, H.R.; Templeton, T.J.; Subudhi, A.K.; Ramaprasad, A.; Tang, J.; Lu, F.; Naeem, R.; Hashish, Y.; Oguike, M.C.; Benavente, E.D.; et al. Genome-scale comparison of expanded gene families in Plasmodium ovale wallikeri and Plasmodium ovale curtisi with Plasmodium malariae and with other Plasmodium species. Int. J. Parasitol. 2016, 46, 685–696. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gilabert, A.; Otto, T.D.; Rutledge, G.G.; Franzon, B.; Ollomo, B.; Arnathau, C.; Durand, P.; Moukodoum, N.D.; Okouga, A.; Ngoubangoye, B.; et al. Plasmodium vivax—Like genome sequences shed new insights into Plasmodium vivax biology and evolution. PLoS Biol. 2018, 16, e2006035. [Google Scholar] [CrossRef] [PubMed]
- Rutledge, G.G.; Böhme, U.; Sanders, M.; Reid, A.J.; Cotton, J.A.; Maiga-Ascofare, O.; Djimdé, A.A.; Apinjoh, T.O.; Amenga-Etego, L.; Manske, M.; et al. Plasmodium malariae and P. ovale genomes provide insights into malaria parasite evolution. Nature 2017, 542, 101–104. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otto, T.D.; Rayner, J.C.; Böhme, U.; Pain, A.; Spottiswoode, N.; Sanders, M.; Quail, M.; Ollomo, B.; Renaud, F.; Thomas, A.W.; et al. Genome sequencing of chimpanzee malaria parasites reveals possible pathways of adaptation to human hosts. Nat. Commun. 2014, 5, 4754. [Google Scholar] [CrossRef] [Green Version]
- Benavente, E.D.; De Sessions, P.F.; Moon, R.W.; Grainger, M.; Holder, A.A.; Blackman, M.J.; Roper, C.; Drakeley, C.J.; Pain, A.; Sutherland, C.J.; et al. A reference genome and methylome for the Plasmodium knowlesi A1-H.1 line. Int. J. Parasitol. 2018, 48, 191–196. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pain, A.; Böhme, U.; Berry, A.E.; Mungall, K.; Finn, R.; Jackson, A.P.; Mourier, T.; Mistry, J.; Pasini, E.M.; Aslett, M.A.; et al. The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 2008, 455, 799–803. [Google Scholar] [CrossRef]
- Chien, J.-T.; Pakala, S.B.; Geraldo, J.A.; Lapp, S.A.; Humphrey, J.C.; Barnwell, J.W.; Kissinger, J.; Galinski, M.R. High-Quality Genome Assembly and Annotation for Plasmodium coatneyi, Generated Using Single-Molecule Real-Time PacBio Technology. Genome Announc. 2016, 4, e00883-16. [Google Scholar] [CrossRef] [Green Version]
- Brugat, T.; Reid, A.J.; Lin, J.-W.; Cunningham, D.; Tumwine, I.; Kushinga, G.; McLaughlin, S.; Spence, P.; Böhme, U.; Sanders, M.; et al. Antibody-independent mechanisms regulate the establishment of chronic Plasmodium infection. Nat. Microbiol. 2017, 2, 16276. [Google Scholar] [CrossRef] [Green Version]
- Carlton, J.M.; Angiuoli, S.V.; Suh, B.B.; Kooij, T.W.; Pertea, M.; Silva, J.C.; Ermolaeva, M.D.; Allen, J.; Selengut, J.D.; Koo, H.L.; et al. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 2002, 419, 512–519. [Google Scholar] [CrossRef] [Green Version]
- Fougère, A.; Jackson, A.P.; Paraskevi Bechtsi, D.; Braks, J.A.; Annoura, T.; Fonager, J.; Spaccapelo, R.; Ramesar, J.; Chevalley-Maurel, S.; Klop, O.; et al. Variant Exported Blood-Stage Proteins Encoded by Plasmodium Multigene Families Are Expressed in Liver Stages Where They Are Exported into the Parasitophorous Vacuole. PLoS Pathog. 2016, 12, e1005917. [Google Scholar] [CrossRef]
- Hall, N.; Karras, M.; Raine, J.D.; Carlton, J.M.; Kooij, T.W.; Berriman, M.; Florens, L.; Janssen, C.S.; Pain, A.; Christophides, G.K.; et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 2005, 307, 82–86. [Google Scholar] [CrossRef]
- Böhme, U.; Otto, T.D.; Cotton, J.A.; Steinbiss, S.; Sanders, M.; Oyola, S.O.; Nicot, A.; Gandon, S.; Patra, K.P.; Herd, C.; et al. Complete avian malaria parasite genomes reveal features associated with lineage-specific evolution in birds and mammals. Genome Res. 2018, 28, 547–560. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otto, T.D.; Böhme, U.; Sanders, M.J.; Reid, A.J.; Bruske, E.I.; Duffy, C.W.; Bull, P.C.; Pearson, R.D.; Abdi, A.I.; Dimonte, S.; et al. Long read assemblies of geographically dispersed Plasmodium falciparum isolates reveal highly structured subtelomeres. Wellcome Open Res. 2018, 3, 52. [Google Scholar] [CrossRef] [Green Version]
- Kooij, T.W.; Carlton, J.M.; Bidwell, S.L.; Hall, N.; Ramesar, J.; Janse, C.J.; Waters, A.P. A Plasmodium whole-genome synteny map: Indels and synteny breakpoints as foci for spe-cies-specific genes. PLoS Pathog. 2005, 1, e44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miles, A.; Iqbal, Z.; Vauterin, P.; Pearson, R.; Campino, S.; Theron, M.; Gould, K.; Mead, D.; Drury, E.; O’Brien, J.; et al. Indels, structural variation, and recombination drive genomic diversity in Plasmodium falciparum. Genome Res. 2016, 26, 1288–1299. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cheng, Q.; Cloonan, N.; Fischer, K.; Thompson, J.; Waine, G.; Lanzer, M.; Saul, A. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol. 1998, 97, 161–176. [Google Scholar] [CrossRef]
- Fernandez, V.; Hommel, M.; Chen, Q.; Hagblom, P.; Wahlgren, M. Small, Clonally Variant Antigens Expressed on the Surface of the Plasmodium falciparum–Infected Erythrocyte Are Encoded by the rif Gene Family and Are the Target of Human Immune Responses. J. Exp. Med. 1999, 190, 1393–1404. [Google Scholar] [CrossRef] [PubMed]
- Rubio, J.P.; Thompson, J.K.; Cowman, A.F. The var genes of Plasmodium falciparum are located in the subtelomeric region of most chromosomes. EMBO J. 1996, 15, 4069–4077. [Google Scholar] [CrossRef]
- Su, X.; Heatwole, V.M.; Wertheimer, S.P.; Guinet, F.; Herrfeldt, J.A.; Peterson, D.S.; Ravetch, J.A.; Wellems, T.E. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of plasmodium falciparum-infected erythrocytes. Cell 1995, 82, 89–100. [Google Scholar] [CrossRef] [Green Version]
- Larremore, D.; Sundararaman, S.A.; Liu, W.; Proto, W.R.; Clauset, A.; Loy, D.E.; Speede, S.; Plenderleith, L.J.; Sharp, P.M.; Hahn, B.H.; et al. Ape parasite origins of human malaria virulence genes. Nat. Commun. 2015, 6, 8368. [Google Scholar] [CrossRef]
- Plenderleith, L.J.; Liu, W.; Learn, G.H.; Loy, D.E.; Speede, S.; Sanz, C.M.; Morgan, D.B.; Bertolani, P.; Hart, J.A.; Hart, T.B.; et al. Ancient Introgression between Two Ape Malaria Parasite Species. Genome Biol. Evol. 2019, 11, 3269–3274. [Google Scholar] [CrossRef] [PubMed]
- Sundararaman, S.A.; Plenderleith, L.J.; Liu, W.; Loy, D.E.; Learn, G.H.; Li, Y.; Shaw, K.S.; Ayouba, A.; Peeters, M.; Speede, S.; et al. Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria. Nat. Commun. 2016, 7, 11078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, L.; Lopaticki, S.; Riglar, D.T.; Dekiwadia, C.; Uboldi, A.D.; Tham, W.-H.; O’Neill, M.T.; Richard, D.; Baum, J.; Ralph, S.A.; et al. An EGF-like Protein Forms a Complex with PfRh5 and Is Required for Invasion of Human Erythrocytes by Plasmodium falciparum. PLOS Pathog. 2011, 7, e1002199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dreyer, A.M.; Matile, H.; Papastogiannidis, P.; Kamber, J.; Favuzza, P.; Voss, T.S.; Wittlin, S.; Pluschke, G. Passive Immunoprotection of Plasmodium falciparum-Infected Mice Designates the CyRPA as Candidate Malaria Vaccine Antigen. J. Immunol. 2012, 188, 6225–6237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reddy, K.S.; Amlabu, E.; Pandey, A.K.; Mitra, P.; Chauhan, V.S.; Gaur, D. Multiprotein complex between the GPI-anchored CyRPA with PfRH5 and PfRipr is crucial for Plasmodium falciparum erythrocyte invasion. Proc. Natl. Acad. Sci. USA 2015, 112, 1179–1184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Volz, J.C.; Yap, A.; Sisquella, X.; Thompson, J.K.; Lim, N.T.; Whitehead, L.W.; Chen, L.; Lampe, M.; Tham, W.; Wilson, D.; et al. Essential Role of the PfRh5/PfRipr/CyRPA Complex during Plasmodium falciparum Invasion of Erythrocytes. Cell Host Microbe 2016, 20, 60–71. [Google Scholar] [CrossRef] [Green Version]
- Galaway, F.; Yu, R.; Constantinou, A.; Prugnolle, F.; Wright, G.J. Resurrection of the ancestral RH5 invasion ligand provides a molecular explanation for the origin of P. falciparum malaria in humans. PLoS Biol. 2019, 17, e3000490. [Google Scholar] [CrossRef] [Green Version]
- Wanaguru, M.; Liu, W.; Hahn, B.H.; Rayner, J.C.; Wright, G.J. RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 2013, 110, 20735–20740. [Google Scholar] [CrossRef] [Green Version]
- Wright, K.E.; Hjerrild, K.A.; Bartlett, J.; Douglas, A.D.; Jin, J.; Brown, R.E.; Illingworth, J.J.; Ashfield, R.; Clemmensen, S.B.; de Jongh, W.A.; et al. Structure of malaria invasion protein RH5 with erythrocyte basigin and blocking antibodies. Nature 2014, 515, 427–430. [Google Scholar] [CrossRef] [Green Version]
- Payne, R.O.; Silk, S.E.; Elias, S.; Miura, K.; Diouf, A.; Galaway, F.; De Graaf, H.; Brendish, N.J.; Poulton, I.D.; Griffiths, O.J.; et al. Human vaccination against RH5 induces neutralizing antimalarial antibodies that inhibit RH5 invasion complex interactions. JCI Insight 2017, 2. [Google Scholar] [CrossRef] [PubMed]
- Joste, V.; Bailly, J.; Hubert, V.; Pauc, C.; Gendrot, M.; Guillochon, E.; Madamet, M.; Thellier, M.; Kendjo, E.; Argy, N.; et al. Plasmodium ovale wallikeri and P. ovale curtisi Infections and Diagnostic Approaches to Imported Malaria, France, 2013–2018. Emerg. Infect. Dis. 2021, 27, 372–384. [Google Scholar] [CrossRef]
- Nabarro, L.E.; Nolder, D.; Broderick, C.; Nadjm, B.; Smith, V.; Blaze, M.; Checkley, A.M.; Chiodini, P.L.; Sutherland, C.J.; Whitty, C.J.M. Geographical and temporal trends and seasonal relapse in Plasmodium ovale spp. and Plasmodium mlariae infections imported to the UK between 1987 and 2015. BMC Med. 2018, 16, 218. [Google Scholar] [CrossRef] [PubMed]
- Nolder, D.; Oguike, M.C.; Maxwell-Scott, H.; Niyazi, H.A.; Smith, V.; Chiodini, P.; Sutherland, C.J. An observational study of malaria in British travellers: Plasmodium ovale wallikeri and Plasmodium ovale curtisi differ significantly in the duration of latency. BMJ Open 2013, 3, e002711. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rojo-Marcos, G.; Rubio-Muñoz, J.M.; Angheben, A.; Jaureguiberry, S.; García-Bujalance, S.; Tomasoni, L.R.; Rodríguez-Valero, N.; Ruiz-Giardín, J.M.; Salas-Coronas, J.; Cuadros-González, J.; et al. Prospective comparative multi-centre study on imported Plasmodium ovale wallikeri and Plasmodium ovale curtisi infections. Malar. J. 2018, 17, 399. [Google Scholar] [CrossRef]
- Neafsey, D.E.; Taylor, A.R.; MacInnis, B.L. Advances and opportunities in malaria population genomics. Nat. Rev. Genet. 2021, 1–16. [Google Scholar] [CrossRef]
- Malaria, G.E.N. Plasmodium falciparum Community Project Genomic epidemiology of artemisinin resistant malaria. eLife 2016, 5. [Google Scholar] [CrossRef]
- Pearson, R.D.; Ahouidi, A.; Ali, M.; Almagro-Garcia, J.; Amambua-Ngwa, A.; Amaratunga, C.; Amato, R.; Amenga-Etego, L.; Andagalu, B.; Anderson, T.J.C.; et al. An open dataset of Plasmodium falciparum genome variation in 7000 worldwide samples. Wellcome Open Res. 2021, 6, 42. [Google Scholar] [CrossRef]
- Noviyanti, R.; Miotto, O.; Barry, A.; Marfurt, J.; Siegel, S.; Thuy-Nhien, N.; Quang, H.H.; Anggraeni, N.D.; Laihad, F.; Liu, Y.; et al. Implementing parasite genotyping into national surveillance frameworks: Feedback from control programmes and researchers in the Asia–Pacific region. Malar. J. 2020, 19, 1–20. [Google Scholar] [CrossRef]
- Tessema, S.K.; Raman, J.; Duffy, C.W.; Ishengoma, D.S.; Amambua-Ngwa, A.; Greenhouse, B. Applying next-generation sequencing to track falciparum malaria in sub-Saharan Africa. Malar. J. 2019, 18, 268. [Google Scholar] [CrossRef] [Green Version]
- Liu, W.; Li, Y.; Learn, G.H.; Rudicell, R.S.; Robertson, J.D.; Keele, B.F.; Ndjango, J.-B.N.; Sanz, C.M.; Morgan, D.B.; Locatelli, S.; et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 2010, 467, 420–425. [Google Scholar] [CrossRef] [PubMed]
- Sharp, P.M.; Plenderleith, L.J.; Hahn, B.H. Ape Origins of Human Malaria. Annu. Rev. Microbiol. 2020, 74, 39–63. [Google Scholar] [CrossRef]
- Rich, S.M.; Licht, M.C.; Hudson, R.R.; Ayala, F.J. Malaria’s Eve: Evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 1998, 95, 4425–4430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Neafsey, D.E.; Galinsky, K.; Jiang, R.H.; Young, L.; Sykes, S.M.; Saif, S.; Gujja, S.; Goldberg, J.M.; Young, S.; Zeng, Q.; et al. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat. Genet. 2012, 44, 1046–1050. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anderson, T.J.; Haubold, B.; Williams, J.T.; Estrada-Franco, J.G.; Richardson, L.; Mollinedo, R.; Bockarie, M.; Mokili, J.; Mharakurwa, S.; French, N.; et al. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol. Biol. Evol. 2000, 17, 1467–1482. [Google Scholar] [CrossRef] [Green Version]
- Manske, M.; Miotto, O.; Campino, S.; Auburn, S.; Almagro-Garcia, J.; Maslen, G.; O’Brien, J.; Djimde, A.; Doumbo, O.; Zongo, I.; et al. Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 2012, 487, 375–379. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Amambua-Ngwa, A.; Amenga-Etego, L.; Kamau, E.; Amato, R.; Ghansah, A.; Golassa, L.; Randrianarivelojosia, M.; Ishengoma, D.; Apinjoh, T.; Maïga-Ascofaré, O.; et al. Major subpopulations of Plasmodium falciparum in sub-Saharan Africa. Science 2019, 365, 813–816. [Google Scholar] [CrossRef] [Green Version]
- Baniecki, M.L.; Faust, A.L.; Schaffner, S.F.; Park, D.J.; Galinsky, K.; Daniels, R.F.; Hamilton, E.; Ferreira, M.U.; Karunaweera, N.D.; Serre, D.; et al. Development of a single nucleotide polymorphism barcode to genotype Plasmodium vivax infections. PLoS Negl. Trop. Dis. 2015, 9, e0003539. [Google Scholar] [CrossRef] [PubMed]
- Daniels, R.; Volkman, S.K.; Milner, D.A.; Mahesh, N.; Neafsey, D.E.; Park, D.J.; Rosen, D.; Angelino, E.; Sabeti, P.C.; Wirth, D.F.; et al. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar. J. 2008, 7, 223. [Google Scholar] [CrossRef] [Green Version]
- Preston, M.D.; Campino, S.; Assefa, S.A.; Echeverry, D.F.; Ocholla, H.; Amambua-Ngwa, A.; Stewart, L.B.; Conway, D.; Borrmann, S.; Michon, P.; et al. A barcode of organellar genome polymorphisms identifies the geographic origin of Plasmodium falciparum strains. Nat. Commun. 2014, 5, 4052. [Google Scholar] [CrossRef] [Green Version]
- Albsheer, M.M.A.; Gebremeskel, E.I.; Kepple, D.; Lo, E.; Rougeron, V.; Ibrahim, M.E.; Hamid, M.M.A. Extensive genetic diversity in Plasmodium vivax from Sudan and its genetic relationships with other geographical isolates. BioRxiv 2020. [Google Scholar] [CrossRef]
- Bâ, H.; Duffy, C.W.; Ahouidi, A.D.; Deh, Y.B.; Diallo, M.Y.; Tandia, A.; Conway, D.J. Widespread distribution of Plasmodium vivax malaria in Mauritania on the interface of the Maghreb and West Africa. Malar. J. 2016, 15, 80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ba, H.; Auburn, S.; Jacob, C.G.; Goncalves, S.; Duffy, C.W.; Stewart, L.B.; Price, R.N.; Deh, Y.B.; Diallo, M.Y.; Tandia, A.; et al. Multi-locus genotyping reveals established endemicity of a geographically distinct Plasmodium vivax population in Mauritania, West Africa. PLoS Negl. Trop. Dis. 2020, 14, e0008945. [Google Scholar] [CrossRef] [PubMed]
- Dewasurendra, R.L.; Baniecki, M.L.; Schaffner, S.; Siriwardena, Y.; Moon, J.; Doshi, R.; Gunawardena, S.; Daniels, R.F.; Neafsey, D.; Volkman, S.; et al. Use of a Plasmodium vivax genetic barcode for genomic surveillance and parasite tracking in Sri Lanka. Malar. J. 2020, 19, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Diez Benavente, E.; Campos, M.; Phelan, J.; Nolder, D.; Dombrowski, J.G.; Marinho, C.R.F.; Sriprawat, K.; Taylor, A.R.; Watson, J.; Roper, C.; et al. A molecular barcode to inform the geographical origin and transmission dynamics of Plasmodium vivax malaria. PLoS Genet. 2020, 16, e1008576. [Google Scholar] [CrossRef] [Green Version]
- Fola, A.A.; Kattenberg, E.; Razook, Z.; Lautu-Gumal, D.; Lee, S.; Mehra, S.; Bahlo, M.; Kazura, J.; Robinson, L.J.; Laman, M.; et al. SNP barcodes provide higher resolution than microsatellite markers to measure Plasmodium vivax population genetics. Malar. J. 2020, 19, 1–15. [Google Scholar] [CrossRef]
- Rougeron, V.; Elguero, E.; Arnathau, C.; Hidalgo, B.A.; Durand, P.; Houze, S.; Berry, A.; Zakeri, S.; Haque, R.; Alam, M.S.; et al. Human Plasmodium vivax diversity, population structure and evolutionary origin. PLOS Negl. Trop. Dis. 2020, 14, e0008072. [Google Scholar] [CrossRef] [Green Version]
- Price, R.N.; Commons, R.J.; Battle, K.E.; Thriemer, K.; Mendis, K. Plasmodium vivax in the Era of the Shrinking P. falciparum Map. Trends Parasitol. 2020, 36, 560–570. [Google Scholar] [CrossRef] [PubMed]
- Jennison, C.; Arnott, A.; Tessier, N.; Tavul, L.; Koepfli, C.; Felger, I.; Siba, P.M.; Reeder, o.C.; Bahlo, M.; Mueller, I.; et al. Plasmodium vivax populations are more genetically diverse and less structured than sympatric Plasmodium falciparum populations. PLoS Negl. Trop. Dis. 2015, 9, e0003634. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Orjuela-Sánchez, P.; Sá, J.M.; Brandi, M.C.; Rodrigues, P.T.; Bastos, M.S.; Amaratunga, C.; Duong, S.; Fairhurst, R.M.; Ferreira, M.U. Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Exp. Parasitol. 2013, 134, 318–326. [Google Scholar] [CrossRef] [Green Version]
- Parobek, C.M.; Lin, J.T.; Saunders, D.L.; Barnett, E.J.; Lon, C.; Lanteri, C.A.; Balasubramanian, S.; Brazeau, N.; DeConti, D.K.; Garba, D.L.; et al. Selective sweep suggests transcriptional regulation may underlie Plasmodium vivax resilience to malaria control measures in Cambodia. Proc. Natl. Acad. Sci. USA 2016, 113, E8096–E8105. [Google Scholar] [CrossRef] [Green Version]
- Ferreira, M.U.; Karunaweera, N.D.; da Silva-Nunes, M.; Da Silva, N.S.; Wirth, D.F.; Hartl, D.L. Population structure and transmission dynamics of Plasmodium vivax in rural Amazonia. J. Infect. Dis. 2007, 195, 1218–1226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Imwong, M.; Nair, S.; Pukrittayakamee, S.; Sudimack, D.; Williams, J.T.; Mayxay, M.; Newton, P.N.; Kim, J.R.; Nandy, A.; Osorio, L.; et al. Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int. J. Parasitol. 2007, 37, 1013–1022. [Google Scholar] [CrossRef] [PubMed]
- Taylor, J.E.; Pacheco, M.A.; Bacon, D.J.; Beg, M.A.; Machado, R.L.; Fairhurst, R.M.; Herrera, S.; Kim, J.; Menard, D.; Póvoa, M.M.; et al. The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: Parasite genetic diversity in the Americas. Mol. Biol. Evol. 2013, 30, 2050–2064. [Google Scholar] [CrossRef] [Green Version]
- Eede, P.V.D.; Van Der Auwera, G.; Delgado, C.; Huyse, T.; Soto-Calle, V.E.; Gamboa, D.; Grande, T.; Rodriguez, H.; Llanos, A.; Anné, J.; et al. Multilocus genotyping reveals high heterogeneity and strong local population structure of the Plasmodium vivax population in the Peruvian Amazon. Malar. J. 2010, 9, 151. [Google Scholar] [CrossRef] [Green Version]
- Gunawardena, S.; Wirth, D.F.; Konradsen, F.; Ferreira, M.U.; Abeyasinghe, R.R.; Alifrangis, M.; Schousboe, M.L.; Amerasinghe, P.H.; Hartl, D.L.; Phone-Kyaw, M.; et al. Geographic Structure of Plasmodium vivax: Microsatellite Analysis of Parasite Populations from Sri Lanka, Myanmar, and Ethiopia. Am. J. Trop. Med. Hyg. 2010, 82, 235–242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gray, K.-A.; Dowd, S.; Bain, L.; Bobogare, A.; Wini, L.; Shanks, G.D.; Cheng, Q. Population genetics of Plasmodium falciparum and Plasmodium vivax and asymptomatic malaria in Temotu Province, Solomon Islands. Malar. J. 2013, 12, 429. [Google Scholar] [CrossRef] [Green Version]
- Koepfli, C.; Timinao, L.; Antao, T.; Barry, A.E.; Siba, P.; Mueller, I.; Felger, I. A Large Plasmodium vivax Reservoir and Little Population Structure in the South Pacific. PLoS ONE 2013, 8, e66041. [Google Scholar] [CrossRef] [Green Version]
- Twohig, K.A.; Pfeffer, D.A.; Baird, J.K.; Price, R.N.; Zimmerman, P.A.; Hay, S.I.; Gething, P.W.; Battle, K.E.; Howes, R.E. Growing evidence of Plasmodium vivax across malaria-endemic Africa. PLOS Neglected Trop. Dis. 2019, 13, e0007140. [Google Scholar] [CrossRef] [Green Version]
- Gunalan, K.; Niangaly, A.; Thera, M.A.; Doumbo, O.K.; Miller, L.H. Plasmodium vivax Infections of Duffy-Negative Erythrocytes: Historically Undetected or a Recent Adaptation? Trends Parasitol. 2018, 34, 420–429. [Google Scholar] [CrossRef]
- Battle, K.E.; Lucas, T.C.D.; Nguyen, M.; Howes, R.E.; Nandi, A.K.; Twohig, K.A.; Pfeffer, D.A.; Cameron, E.; Rao, P.C.; Casey, D.; et al. Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000–2017: A spatial and temporal modelling study. Lancet 2019, 394, 332–343. [Google Scholar] [CrossRef] [Green Version]
- De Oliveira, T.C.; Corder, R.M.; Early, A.; Rodrigues, P.T.; Ladeia-Andrade, S.; Alves, J.M.P.; Neafsey, D.E.; Ferreira, M.U. Population genomics reveals the expansion of highly inbred Plasmodium vivax lineages in the main malaria hotspot of Brazil. PLOS Negl. Trop. Dis. 2020, 14, e0008808. [Google Scholar] [CrossRef] [PubMed]
- Gunawardena, S.; Ferreira, M.U.; Kapilananda GM, G.; Wirth, D.F.; Karunaweera, N.D. The Sri Lankan paradox: High genetic diversity in Plasmodium vivax populations despite de-creasing levels of malaria transmission. Parasitology 2014, 141, 880–890. [Google Scholar] [CrossRef] [PubMed]
- Divis, P.C.; Singh, B.; Anderios, F.; Hisam, S.; Matusop, A.; Kocken, C.H.; Assefa, S.A.; Duffy, C.W.; Conway, D.J. Admixture in Humans of Two Divergent Plasmodium knowlesi Populations Associated with Different Macaque Host Species. PLoS Pathog. 2015, 11, e1004888. [Google Scholar] [CrossRef] [Green Version]
- Benavente, E.D.; Gomes, A.R.; De Silva, J.R.; Grigg, M.; Walker, H.; Barber, B.E.; William, T.; Yeo, T.W.; De Sessions, P.F.; Ramaprasad, A.; et al. Whole genome sequencing of amplified Plasmodium knowlesi DNA from unprocessed blood reveals genetic exchange events between Malaysian Peninsular and Borneo subpopulations. Sci. Rep. 2019, 9, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benavente, E.D.; de Sessions, P.F.; Moon, R.W.; Holder, A.A.; Blackman, M.J.; Roper, C.; Drakeley, C.J.; Pain, A.; Sutherland, C.J.; Hibberd, M.L.; et al. Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations. PLoS Genet. 2017, 13, e1007008. [Google Scholar] [CrossRef] [Green Version]
- Divis, P.C.S.; Duffy, C.W.; Kadir, K.A.; Singh, B.; Conway, D.J. Genome-wide mosaicism in divergence between zoonotic malaria parasite subpopulations with separate sympatric transmission cycles. Mol. Ecol. 2018, 27, 860–870. [Google Scholar] [CrossRef] [Green Version]
- Pinheiro, M.M.; Ahmed, M.A.; Millar, S.B.; Sanderson, T.; Otto, T.D.; Lu, W.C.; Krishna, S.; Rayner, J.C.; Cox-Singh, J. Plasmodium knowlesi genome sequences from clinical isolates reveal extensive genomic dimorphism. PLoS ONE 2015, 10, e0121303. [Google Scholar] [CrossRef] [Green Version]
- Divis, P.C.; Lin, L.C.; Rovie-Ryan, J.J.; Kadir, K.A.; Anderios, F.; Hisam, S.; Sharma, R.S.; Singh, B.; Conway, D.J. Three Divergent Subpopulations of the Malaria Parasite Plasmodium knowlesi. Emerg. Infect. Dis. 2017, 23, 616–624. [Google Scholar] [CrossRef] [Green Version]
- Hocking, S.E.; Divis, P.C.; Kadir, K.A.; Singh, B.; Conway, D.J. Population Genomic Structure and Recent Evolution of Plasmodium knowlesi, Peninsular Malaysia. Emerg. Infect. Dis. 2020, 26, 1749–1758. [Google Scholar] [CrossRef] [PubMed]
- Yusof, R.; Ahmed, A.; Jelip, J.; Ngian, H.U.; Mustakim, S.; Hussin, H.M.; Fong, M.Y.; Mahmud, R.; Sitam, F.A.T.; Japning, J.R.-R.; et al. Phylogeographic Evidence for 2 Genetically Distinct Zoonotic Plasmodium knowlesi Parasites, Malaysia. Emerg. Infect. Dis. 2016, 22, 1371–1380. [Google Scholar] [CrossRef] [Green Version]
- Weedall, G.D.; Conway, D.J. Detecting signatures of balancing selection to identify targets of anti-parasite im-munity. Trends Parasitol. 2010, 26, 363–369. [Google Scholar] [CrossRef] [PubMed]
- Nwakanma, D.C.; Duffy, C.W.; Amambua-Ngwa, A.; Oriero, E.C.; Bojang, K.A.; Pinder, M.; Drakeley, C.J.; Sutherland, C.J.; Milligan, P.J.; MacInnis, B.; et al. Changes in Malaria Parasite Drug Resistance in an Endemic Population Over a 25-Year Period With Resulting Genomic Evidence of Selection. J. Infect. Dis. 2013, 209, 1126–1135. [Google Scholar] [CrossRef] [Green Version]
- Ravenhall, M.; Benavente, E.D.; Mipando, M.; Jensen, A.T.; Sutherland, C.J.; Roper, C.; Sepúlveda, N.; Kwiatkowski, D.P.; Montgomery, J.; Phiri, K.S.; et al. Characterizing the impact of sustained sulfadoxine/pyrimethamine use upon the Plasmodium falciparum population in Malawi. Malar. J. 2016, 15, 575. [Google Scholar] [CrossRef] [Green Version]
- Hupalo, D.N.; Luo, Z.; Melnikov, A.; Sutton, P.L.; Rogov, P.; Escalante, A.; Vallejo, A.F.; Herrera, S.; Arévalo-Herrera, M.; Fan, Q.; et al. Population genomics studies identify signatures of global dispersal and drug resistance in Plasmodium vivax. Nat. Genet. 2016, 48, 953–958. [Google Scholar] [CrossRef] [PubMed]
- Pearson, R.D.; Amato, R.; Auburn, S.; Miotto, O.; Almagro-Garcia, J.; Amaratunga, C.; Suon, S.; Mao, S.; Noviyanti, R.; Trimarsanto, H.; et al. Genomic analysis of local variation and recent evolution in Plasmodium vivax. Nat. Genet. 2016, 48, 959–964. [Google Scholar] [CrossRef] [PubMed]
- Winter, D.J.; Pacheco, M.A.; Vallejo, A.F.; Schwartz, R.S.; Arevalo-Herrera, M.; Herrera, S.; Cartwright, R.A.; Escalante, A.A. Whole Genome Sequencing of Field Isolates Reveals Extensive Genetic Diversity in Plasmodium vivax from Colombia. PLoS Negl. Trop. Dis. 2015, 9, e0004252. [Google Scholar] [CrossRef] [Green Version]
- Costa, G.L.; Amaral, L.C.; Fontes, C.J.F.; Carvalho, L.H.; De Brito, C.F.A.; De Sousa, T.N. Assessment of copy number variation in genes related to drug resistance in Plasmodium vivax and Plasmodium falciparum isolates from the Brazilian Amazon and a systematic review of the literature. Malar. J. 2017, 16, 152. [Google Scholar] [CrossRef] [Green Version]
- Lin, J.T.; Patel, J.C.; Kharabora, O.; Sattabongkot, J.; Muth, S.; Ubalee, R.; Schuster, A.L.; Rogers, W.O.; Wongsrichanalai, C.; Juliano, J.J. Plasmodium vivax Isolates from Cambodia and Thailand Show High Genetic Complexity and Distinct Patterns of P. vivax Multidrug Resistance Gene 1 (pvmdr1) Polymorphisms. Am. J. Trop. Med. Hyg. 2013, 88, 1116–1123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Auburn, S.; Getachew, S.; Pearson, R.D.; Amato, R.; Miotto, O.; Trimarsanto, H.; Zhu, S.J.; Rumaseb, A.; Marfurt, J.; Noviyanti, R.; et al. Genomic Analysis of Plasmodium vivax in Southern Ethiopia Reveals Selective Pressures in Multiple Parasite Mechanisms. J. Infect. Dis. 2019, 220, 1738–1749. [Google Scholar] [CrossRef] [Green Version]
- Ashley, E.A.; Dhorda, M.; Fairhurst, R.M.; Amaratunga, C.; Lim, P.; Suon, S.; Sreng, S.; Anderson, J.M.; Mao, S.; Sam, B.; et al. Spread of Artemisinin Resistance in Plasmodium falciparum Malaria. N. Engl. J. Med. 2014, 371, 411–423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dondorp, A.M.; Nosten, F.; Yi, P.; Das, D.; Phyo, A.P.; Tarning, J.; Lwin, K.M.; Ariey, F.; Hanpithakpong, W.; Lee, S.J.; et al. Artemisinin Resistance in Plasmodium falciparum Malaria. N. Engl. J. Med. 2009, 361, 455–467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Noedl, H.; Se, Y.; Schaecher, K.; Smith, B.L.; Socheat, D.; Fukuda, M.M. Evidence of Artemisinin-Resistant Malaria in Western Cambodia. N. Engl. J. Med. 2008, 359, 2619–2620. [Google Scholar] [CrossRef]
- Ghorbal, M.; Gorman, M.; Macpherson, C.R.; Martins, R.M.; Scherf, A.; Lopez-Rubio, J.J. Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nature Biotechnol. 2014, 32, 819–821. [Google Scholar] [CrossRef] [PubMed]
- Miotto, O.; Amato, R.; Ashley, E.A.; MacInnis, B.; Almagro-Garcia, J.; Amaratunga, C.; Lim, P.; Mead, D.; Oyola, S.O.; Dhorda, M.; et al. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat. Genet. 2015, 47, 226–234. [Google Scholar] [CrossRef] [Green Version]
- Straimer, J.; Gnädig, N.F.; Witkowski, B.; Amaratunga, C.; Duru, V.; Ramadani, A.P.; Dacheux, M.; Khim, N.; Zhang, L.; Lam, S.; et al. K13-propeller mutations confer artemisinin resistance in Plasmodium falciparum clinical isolates. Science 2015, 347, 428–431. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takala-Harrison, S.; Jacob, C.G.; Arze, C.; Cummings, M.P.; Silva, J.C.; Dondorp, A.M.; Fukuda, M.M.; Hien, T.T.; Mayxay, M.; Noedl, H.; et al. Independent Emergence of Artemisinin Resistance Mutations Among Plasmodium falciparum in Southeast Asia. J. Infect. Dis. 2015, 211, 670–679. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ménard, D.; Khim, N.; Beghain, J.; Adegnika, A.A.; Shafiul-Alam, M.; Amodu, O.; Rahim-Awab, G.; Barnadas, C.; Berry, A.; Boum, Y.; et al. A Worldwide Map of Plasmodium falciparum K13-Propeller Polymorphisms. N. Engl. J. Med. 2016, 374, 2453–2464. [Google Scholar] [CrossRef]
- Muwanguzi, J.; Henriques, G.; Sawa, P.; Bousema, T.; Sutherland, C.J.; Beshir, K.B. Lack of K13 mutations in Plasmodium falciparum persisting after artemisinin combination therapy treatment of Kenyan children. Malar. J. 2016, 15, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Dogovski, C.; Xie, S.C.; Burgio, G.; Bridgford, J.; Mok, S.; McCaw, J.; Chotivanich, K.; Kenny, S.; Gnädig, N.; Straimer, J.; et al. Targeting the Cell Stress Response of Plasmodium falciparum to Overcome Artemisinin Resistance. PLoS Biol. 2015, 13, e1002132. [Google Scholar] [CrossRef] [Green Version]
- Mok, S.; Ashley, E.A.; Ferreira, P.E.; Zhu, L.; Lin, Z.; Yeo, T.; Chotivanich, K.; Imwong, M.; Pukrittayakamee, S.; Dhorda, M.; et al. Drug resistance. Population transcriptomics of human malaria parasites reveals the mechanism of arte-misinin resistance. Science 2015, 347, 431–435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mok, S.; Stokes, B.H.; Gnädig, N.F.; Ross, L.S.; Yeo, T.; Amaratunga, C.; Allman, E.; Solyakov, L.; Bottrill, A.R.; Tripathi, J.; et al. Artemisinin-resistant K13 mutations rewire Plasmodium falciparum’s intra-erythrocytic metabolic pro-gram to enhance survival. Nat. Commun. 2021, 12, 530. [Google Scholar] [CrossRef] [PubMed]
- Rocamora, F.; Zhu, L.; Liong, K.Y.; Dondorp, A.; Miotto, O.; Mok, S.; Bozdech, Z. Oxidative stress and protein damage responses mediate artemisinin resistance in malaria parasites. PLOS Pathog. 2018, 14, e1006930. [Google Scholar] [CrossRef] [PubMed]
- Duffy, C.W.; Amambua-Ngwa, A.; Ahouidi, A.D.; Diakite, M.; Awandare, G.A.; Ba, H.; Tarr, S.J.; Murray, L.; Stewart, L.B.; D’Alessandro, U.; et al. Multi-population genomic analysis of malaria parasites indicates local selection and differentiation at the gdv1 locus regulating sexual development. Sci. Rep. 2018, 8, 15763. [Google Scholar] [CrossRef] [PubMed]
- Mobegi, V.A.; Duffy, C.W.; Amambua-Ngwa, A.; Loua, K.M.; Laman, E.; Nwakanma, D.; MacInnis, B.; Aspeling-Jones, H.; Murray, L.; Clark, T.; et al. Genome-Wide Analysis of Selection on the Malaria Parasite Plasmodium falciparum in West African Populations of Differing Infection Endemicity. Mol. Biol. Evol. 2014, 31, 1490–1499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tagliamonte, M.S.; Yowell, C.A.; ElBadry, M.A.; Boncy, J.; Raccurt, C.P.; Okech, B.A.; Goss, E.M.; Salemi, M.; Dame, J.B. Genetic Markers of Adaptation of Plasmodium falciparum to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America. mSphere 2020, 5. [Google Scholar] [CrossRef]
- Bozdech, Z.; Llinás, M.; Pulliam, B.L.; Wong, E.D.; Zhu, J.; DeRisi, J.L. The Transcriptome of the Intraerythrocytic Developmental Cycle of Plasmodium falciparum. PLoS Biol. 2003, 1, e5. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chappell, L.; Ross, P.; Orchard, L.; Russell, T.J.; Otto, T.D.; Berriman, M.; Rayner, J.C.; Llinás, M. Refining the transcriptome of the human malaria parasite Plasmodium falciparum using amplifica-tion-free RNA-seq. BMC Genom. 2020, 21, 395. [Google Scholar] [CrossRef]
- Le Roch, K.G.; Zhou, Y.; Blair, P.L.; Grainger, M.; Moch, J.K.; Haynes, J.D.; De La Vega, P.; Holder, A.; Batalov, S.; Carucci, D.J.; et al. Discovery of Gene Function by Expression Profiling of the Malaria Parasite Life Cycle. Science 2003, 301, 1503–1508. [Google Scholar] [CrossRef] [Green Version]
- Llinás, M.; Bozdech, Z.; Wong, E.D.; Adai, A.T.; DeRisi, J.L. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 2006, 34, 1166–1173. [Google Scholar] [CrossRef]
- Otto, T.D.; Wilinski, D.; Assefa, S.; Keane, T.M.; Sarry, L.R.; Böhme, U.; Lemieux, J.; Barrell, B.; Pain, A.; Berriman, M.; et al. New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol. Microbiol. 2010, 76, 12–24. [Google Scholar] [CrossRef] [Green Version]
- Painter, H.J.; Chung, N.C.; Sebastian, A.; Albert, I.; Storey, J.; Llinás, M. Genome-wide real-time in vivo transcriptional dynamics during Plasmodium falciparum blood-stage development. Nat. Commun. 2018, 9, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Bechtsi, D.P.; Waters, A.P. Genomics and epigenetics of sexual commitment in Plasmodium. Int. J. Parasitol. 2017, 47, 425–434. [Google Scholar] [CrossRef] [PubMed]
- Cortés, A.; Deitsch, K.W. Malaria Epigenetics. Cold Spring Harb. Perspect. Med. 2017, 7, a025528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gupta, A.P.; Bozdech, Z. Epigenetic landscapes underlining global patterns of gene expression in the human malaria parasite, Plasmodium falciparum. Int. J. Parasitol. 2017, 47, 399–407. [Google Scholar] [CrossRef] [PubMed]
- Hammam, E.; Ananda, G.; Sinha, A.; Scheidig-Benatar, C.; Bohec, M.; Preiser, P.R.; Dedon, P.C.; Scherf, A.; Vembar, S.S. Discovery of a new predominant cytosine DNA modification that is linked to gene expression in malaria parasites. Nucleic Acids Res. 2020, 48, 184–199. [Google Scholar] [CrossRef] [Green Version]
- McInroy, G.R.; Beraldi, D.; Raiber, E.-A.; Modrzynska, K.; Van Delft, P.; Billker, O.; Balasubramanian, S. Enhanced Methylation Analysis by Recovery of Unsequenceable Fragments. PLoS ONE 2016, 11, e0152322. [Google Scholar] [CrossRef] [Green Version]
- Ponts, N.; Fu, L.; Harris, E.Y.; Zhang, J.; Chung, D.-W.D.; Cervantes, M.C.; Prudhomme, J.; Atanasova-Penichon, V.; Zehraoui, E.; Bunnik, E.; et al. Genome-wide Mapping of DNA Methylation in the Human Malaria Parasite Plasmodium falciparum. Cell Host Microbe 2013, 14, 696–706. [Google Scholar] [CrossRef] [Green Version]
- Lopez-Rubio, J.-J.; Mancio-Silva, L.; Scherf, A. Genome-wide analysis of heterochromatin associates clonally var-iant gene regulation with perinuclear repressive centers in malaria parasites. Cell Host Microbe 2009, 5, 179–190. [Google Scholar] [CrossRef] [Green Version]
- Salcedo-Amaya, A.M.; van Driel, M.A.; Alako, B.T.; Trelle, M.B.; van den Elzen, A.M.; Cohen, A.M.; Janssen-Megens, E.M.; van de Vegte-Bolmer, M.; Selzer, R.R.; Iniguez, A.L.; et al. Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 2009, 106, 9655–9660. [Google Scholar] [CrossRef] [Green Version]
- Baum, J.; Papenfuss, A.T.; Mair, G.R.; Janse, C.J.; Vlachou, D.; Waters, A.P.; Cowman, A.F.; Crabb, B.S.; De Koning-Ward, T.F. Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res. 2009, 37, 3788–3798. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miao, F.; Li, S.; Chavez, V.; Lanting, L.; Natarajan, R. Coactivator-associated arginine methyltransferase-1 enhances nuclear factor-kappaB-mediated gene transcription through methylation of histone H3 at arginine 17. Mol. Endocrinol. 2006, 20, 1562–1573. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Deobagkar, D. Epigenetics with special reference to the human X chromosome inactivation and the enigma of Drosophila DNA methylation. J. Genet. 2018, 97, 371–378. [Google Scholar] [CrossRef] [PubMed]
- Albalat, R.; Martí-Solans, J.; Cañestro, C. DNA methylation in amphioxus: From ancestral functions to new roles in vertebrates. Briefings Funct. Genom. 2012, 11, 142–155. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Mendoza, A.; Lister, R.; Bogdanovic, O. Evolution of DNA Methylome Diversity in Eukaryotes. J. Mol. Biol. 2020, 432, 1687–1705. [Google Scholar] [CrossRef] [PubMed]
- Borodinova, A.A.; Balaban, P.M. Epigenetic Regulation as a Basis for Long-Term Changes in the Nervous Sys-tem: In Search of Specificity Mechanisms. Biochem. Biokhimiia 2020, 85, 994–1010. [Google Scholar] [CrossRef]
- Nikolic, D.; Jankovic, M.; Petrovic, B.; Novakovic, I. Genetic Aspects of Inflammation and Immune Response in Stroke. Int. J. Mol. Sci. 2020, 21, 7409. [Google Scholar] [CrossRef]
- Rossnerova, A.; Izzotti, A.; Pulliero, A.; Bast, A.; Rattan, S.; Rossner, P. The Molecular Mechanisms of Adaptive Response Related to Environmental Stress. Int. J. Mol. Sci. 2020, 21, 7053. [Google Scholar] [CrossRef]
- Thamban, T.; Agarwaal, V.; Khosla, S. Role of genomic imprinting in mammalian development. J. Biosci. 2020, 45, 1–21. [Google Scholar] [CrossRef]
- Choi, S.-W.; Keyes, M.K.; Horrocks, P. LC/ESI-MS demonstrates the absence of 5-methyl-2′-deoxycytosine in Plasmodium falciparum genomic DNA. Mol. Biochem. Parasitol. 2006, 150, 350–352. [Google Scholar] [CrossRef]
- Gissot, M.; Choi, S.-W.; Thompson, R.F.; Greally, J.M.; Kim, K. Toxoplasma gondii and Cryptosporidium parvum Lack Detectable DNA Cytosine Methylation. Eukaryot. Cell 2008, 7, 537–540. [Google Scholar] [CrossRef] [Green Version]
- Pollack, Y.; Kogan, N.; Golenser, J. Plasmodium falciparum: Evidence for a DNA methylation pattern. Exp. Parasitol. 1991, 72, 339–344. [Google Scholar] [CrossRef]
- Krueger, F.; Kreck, B.; Franke, A.; Andrews, S.R. DNA methylome analysis using short bisulfite sequencing data. Nat. Methods 2012, 9, 145–151. [Google Scholar] [CrossRef]
- Tahiliani, M.; Koh, K.P.; Shen, Y.; Pastor, W.A.; Bandukwala, H.; Brudno, Y.; Agarwal, S.; Iyer, L.M.; Liu, D.R.; Aravind, L.; et al. Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1. Science 2009, 324, 930–935. [Google Scholar] [CrossRef] [Green Version]
- Lyko, F. The DNA methyltransferase family: A versatile toolkit for epigenetic regulation. Nat. Rev. Genet. 2018, 19, 81–92. [Google Scholar] [CrossRef]
- Pastor, W.A.; Aravind, L.; Rao, A. TETonic shift: Biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol. 2013, 14, 341–356. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rausch, C.; Hastert, F.D.; Cardoso, M.C. DNA Modification Readers and Writers and Their Interplay. J. Mol. Biol. 2020, 432, 1731–1746. [Google Scholar] [CrossRef]
- Wu, X.; Zhang, Y. TET-mediated active DNA demethylation: Mechanism, function and beyond. Nat. Rev. Genet. 2017, 18, 517–534. [Google Scholar] [CrossRef] [PubMed]
- Kohli, R.M.; Zhang, Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 2013, 502, 472–479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peng, J.; Xia, B.; Yi, C. Single-base resolution analysis of DNA epigenome via high-throughput sequencing. Sci. China Life Sci. 2016, 59, 219–226. [Google Scholar] [CrossRef] [Green Version]
- Tost, J. Current and Emerging Technologies for the Analysis of the Genome-Wide and Locus-Specific DNA Methylation Patterns. Adv. Exp. Med. Biol. 2016, 945, 343–430. [Google Scholar] [PubMed]
- Williams, K.; Christensen, J.; Pedersen, M.T.; Johansen, J.V.; Cloos, P.; Rappsilber, J.; Helin, K. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011, 473, 343–348. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Wu, F.; Tan, L.; Kong, L.; Xiong, L.; Deng, J.; Barbera, A.J.; Zheng, L.; Zhang, H.; Huang, S.; et al. Genome-wide Regulation of 5hmC, 5mC, and Gene Expression by Tet1 Hydroxylase in Mouse Embryonic Stem Cells. Mol. Cell 2011, 42, 451–464. [Google Scholar] [CrossRef] [Green Version]
- Laurent, L.; Wong, E.; Li, G.; Huynh, T.; Tsirigos, A.; Ong, C.T.; Low, H.M.; Sung, W.-K.; Rigoutsos, I.; Loring, J.; et al. Dynamic changes in the human methylome during differentiation. Genome Res. 2010, 20, 320–331. [Google Scholar] [CrossRef] [Green Version]
- Zilberman, D.; Gehring, M.; Tran, R.K.; Ballinger, T.; Henikoff, S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 2006, 39, 61–69. [Google Scholar] [CrossRef]
- Gaiti, F.; Jindrich, K.; Fernandez-Valverde, S.L.; Roper, K.E.; Degnan, B.M.; Tanurdžić, M. Landscape of histone modifications in a sponge reveals the origin of animal cis-regulatory complexity. eLife 2017, 6. [Google Scholar] [CrossRef] [Green Version]
- Guo, X.; Wang, L.; Li, J.; Ding, Z.; Xiao, J.; Yin, X.; He, S.; Shi, P.; Dong, L.; Li, G.; et al. Structural insight into autoinhibition and histone H3-induced activation of DNMT3A. Nature 2015, 517, 640–644. [Google Scholar] [CrossRef] [PubMed]
- Raddatz, G.; Guzzardo, P.M.; Olova, N.; Fantappie, M.R.; Rampp, M.; Schaefer, M.; Reik, W.; Hannon, G.J.; Lyko, F. Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proc. Natl. Acad. Sci. USA 2013, 110, 8627–8631. [Google Scholar] [CrossRef] [Green Version]
- Govindaraju, G.; Jabeena, C.; Sethumadhavan, D.V.; Rajaram, N.; Rajavelu, A. DNA methyltransferase homologue TRDMT1 in Plasmodium falciparum specifically methylates endogenous aspartic acid tRNA. Biochim. Biophys. Acta (BBA)—Bioenerg. 2017, 1860, 1047–1057. [Google Scholar] [CrossRef]
- Bewick, A.J.; Hofmeister, B.T.; Powers, R.A.; Mondo, S.J.; Grigoriev, I.V.; James, T.Y.; Stajich, J.E.; Schmitz, R.J. Diversity of cytosine methylation across the fungal tree of life. Nat. Ecol. Evol. 2019, 3, 479–490. [Google Scholar] [CrossRef]
- Huff, J.T.; Zilberman, D. Dnmt1-Independent CG Methylation Contributes to Nucleosome Positioning in Diverse Eukaryotes. Cell 2014, 156, 1286–1297. [Google Scholar] [CrossRef] [Green Version]
- Yaari, R.; Katz, A.; Domb, K.; Harris, K.D.; Zemach, A.; Ohad, N. RdDM-independent de novo and heterochromatin DNA methylation by plant CMT and DNMT3 orthologs. Nat. Commun. 2019, 10, 1613. [Google Scholar] [CrossRef] [Green Version]
- Gabel, H.W.; Kinde, B.Z.; Stroud, H.; Gilbert, C.S.; Harmin, D.A.; Kastan, N.R.; Hemberg, M.; Ebert, D.H.; Greenberg, M.E. Disruption of DNA-methylation-dependent long gene repression in Rett syndrome. Nature 2015, 522, 89–93. [Google Scholar] [CrossRef] [Green Version]
- Guo, J.U.; Su, Y.; Shin, J.H.; Shin, J.; Li, H.; Xie, B.; Song, H. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat. Neurosci. 2014, 17, 215–222. [Google Scholar] [CrossRef] [Green Version]
- Liu, K.; Xu, C.; Lei, M.; Yang, A.; Loppnau, P.; Hughes, T.R.; Min, J. Structural basis for the ability of MBD domains to bind methyl-CG and TG sites in DNA. J. Biol. Chem. 2018, 293, 7344–7354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sperlazza, M.J.; Bilinovich, S.M.; Sinanan, L.M.; Javier, F.R.; Williams, D.C., Jr. Structural Basis of MeCP2 Distribution on Non-CpG Methylated and Hydroxymethylated DNA. J. Mol. Biol. 2017, 429, 1581–1594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ludwig, A.K.; Zhang, P.; Cardoso, M.C. Modifiers and Readers of DNA Modifications and Their Impact on Genome Structure, Expression, and Stability in Disease. Front. Genet. 2016, 7, 115. [Google Scholar] [CrossRef] [Green Version]
- Hashimoto, H.; Zhang, X.; Cheng, X. Excision of thymine and 5-hydroxymethyluracil by the MBD4 DNA glyco-sylase domain: Structural basis and implications for active DNA demethylation. Nucleic Acids Res. 2012, 40, 8276–8284. [Google Scholar] [CrossRef] [PubMed]
- Booth, M.J.; Branco, M.R.; Ficz, G.; Oxley, D.; Krueger, F.; Reik, W.; Balasubramanian, S. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 2012, 336, 934–937. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ficz, G.; Branco, M.R.; Seisenberger, S.; Santos, F.; Krueger, F.; Hore, T.; Marques, C.J.; Andrews, S.; Reik, W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011, 473, 398–402. [Google Scholar] [CrossRef] [PubMed]
- Jin, S.-G.; Wu, X.; Li, A.X.; Pfeifer, G.P. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res. 2011, 39, 5015–5024. [Google Scholar] [CrossRef] [PubMed]
- Pastor, W.A.; Pape, U.J.; Huang, Y.; Henderson, H.R.; Lister, R.; Ko, M.; McLoughlin, E.M.; Brudno, Y.; Mahapatra, S.; Kapranov, P.; et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011, 473, 394–397. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Neri, F.; Incarnato, D.; Krepelova, A.; Rapelli, S.; Anselmi, F.; Parlato, C.; Medana, C.; Bello, F.; Oliviero, S. Single-Base Resolution Analysis of 5-Formyl and 5-Carboxyl Cytosine Reveals Promoter DNA Methylation Dynamics. Cell Rep. 2015, 10, 674–683. [Google Scholar] [CrossRef] [Green Version]
- Raiber, E.A.; Beraldi, D.; Ficz, G.; Burgess, H.E.; Branco, M.R.; Murat, P.; Oxley, D.; Booth, M.J.; Reik, W.; Balasubramanian, S. Genome-wide distribution of 5-formylcytosine in embryonic stem cells is associated with transcrip-tion and depends on thymine DNA glycosylase. Genome Biol. 2012, 13, R69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, C.-X.; Szulwach, K.E.; Dai, Q.; Fu, Y.; Mao, S.-Q.; Lin, L.; Street, C.; Li, Y.; Poidevin, M.; Wu, H.; et al. Genome-wide Profiling of 5-Formylcytosine Reveals Its Roles in Epigenetic Priming. Cell 2013, 153, 678–691. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pegoraro, M.; Weedall, G.D. Malaria in the ‘Omics Era’. Genes 2021, 12, 843. https://doi.org/10.3390/genes12060843
Pegoraro M, Weedall GD. Malaria in the ‘Omics Era’. Genes. 2021; 12(6):843. https://doi.org/10.3390/genes12060843
Chicago/Turabian StylePegoraro, Mirko, and Gareth D. Weedall. 2021. "Malaria in the ‘Omics Era’" Genes 12, no. 6: 843. https://doi.org/10.3390/genes12060843
APA StylePegoraro, M., & Weedall, G. D. (2021). Malaria in the ‘Omics Era’. Genes, 12(6), 843. https://doi.org/10.3390/genes12060843