{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,19]],"date-time":"2026-09-19T16:32:14Z","timestamp":1789835534440,"version":"4.0.1"},"reference-count":124,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2023,3,9]],"date-time":"2023-03-09T00:00:00Z","timestamp":1678320000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"MBB GAANN","award":["P200A210024"],"award-info":[{"award-number":["P200A210024"]}]},{"name":"MBB GAANN","award":["5T32AI141346"],"award-info":[{"award-number":["5T32AI141346"]}]},{"name":"Microbiology and Infectious Diseases","award":["P200A210024"],"award-info":[{"award-number":["P200A210024"]}]},{"name":"Microbiology and Infectious Diseases","award":["5T32AI141346"],"award-info":[{"award-number":["5T32AI141346"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Microtubules and specialized microtubule-containing structures are assembled from tubulins, an ancient superfamily of essential eukaryotic proteins. Here, we use bioinformatic approaches to analyze features of tubulins in organisms from the phylum Apicomplexa. Apicomplexans are protozoan parasites that cause a variety of human and animal infectious diseases. Individual species harbor one to four genes each for \u03b1- and \u03b2-tubulin isotypes. These may specify highly similar proteins, suggesting functional redundancy, or exhibit key differences, consistent with specialized roles. Some, but not all apicomplexans harbor genes for \u03b4- and \u03b5-tubulins, which are found in organisms that construct appendage-containing basal bodies. Critical roles for apicomplexan \u03b4- and \u03b5-tubulin are likely to be limited to microgametes, consistent with a restricted requirement for flagella in a single developmental stage. Sequence divergence or the loss of \u03b4- and \u03b5-tubulin genes in other apicomplexans appears to be associated with diminished requirements for centrioles, basal bodies, and axonemes. Finally, because spindle microtubules and flagellar structures have been proposed as targets for anti-parasitic therapies and transmission-blocking strategies, we discuss these ideas in the context of tubulin-based structures and tubulin superfamily properties.<\/jats:p>","DOI":"10.3390\/microorganisms11030706","type":"journal-article","created":{"date-parts":[[2023,3,9]],"date-time":"2023-03-09T03:46:40Z","timestamp":1678333600000},"page":"706","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["The Tubulin Superfamily in Apicomplexan Parasites"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8810-3543","authenticated-orcid":false,"given":"Naomi","family":"Morrissette","sequence":"first","affiliation":[{"name":"Molecular Biology and Biochemistry, University of California Irvine, Irvine, CA 92697, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6649-2461","authenticated-orcid":false,"given":"Izra","family":"Abbaali","sequence":"additional","affiliation":[{"name":"Molecular Biology and Biochemistry, University of California Irvine, Irvine, CA 92697, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2277-2373","authenticated-orcid":false,"given":"Chandra","family":"Ramakrishnan","sequence":"additional","affiliation":[{"name":"Institute for Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrian B.","family":"Hehl","sequence":"additional","affiliation":[{"name":"Institute for Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1038\/s41580-021-00399-x","article-title":"Regulation of microtubule dynamics, mechanics and function through the growing tip","volume":"22","author":"Gudimchuk","year":"2021","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Kristensson, M.A. (2021). The Game of Tubulins. Cells, 10.","DOI":"10.3390\/cells10040745"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1006\/jsbi.2001.4386","article-title":"Review: Postchaperonin tubulin folding cofactors and their role in microtubule dynamics","volume":"135","author":"Avila","year":"2001","journal-title":"J. Struct. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1038\/s41594-022-00755-1","article-title":"Snapshots of actin and tubulin folding inside the TRiC chaperonin","volume":"29","author":"Kelly","year":"2022","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2274","DOI":"10.1093\/gbe\/evu187","article-title":"Six subgroups and extensive recent duplications characterize the evolution of the eukaryotic tubulin protein family","volume":"6","author":"Findeisen","year":"2014","journal-title":"Genome Biol. Evol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2723","DOI":"10.1242\/jcs.114.15.2723","article-title":"The extended tubulin superfamily","volume":"114","author":"McKean","year":"2001","journal-title":"J. Cell Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1016\/j.mib.2003.10.016","article-title":"Long-lost relatives reappear: Identification of new members of the tubulin superfamily","volume":"6","author":"Dutcher","year":"2003","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"R55","DOI":"10.1016\/S0960-9822(02)01427-6","article-title":"Tubulin superfamily: Giving birth to triplets","volume":"13","author":"Marshall","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.sbi.2020.08.008","article-title":"The structure of the \u03b3-TuRC: A 25-years-old molecular puzzle","volume":"66","author":"Zupa","year":"2021","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1038\/nrm3209","article-title":"Microtubule nucleation by \u03b3-tubulin complexes","volume":"12","author":"Kollman","year":"2011","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"867374","DOI":"10.3389\/fcell.2022.867374","article-title":"The Amazing Evolutionary Complexity of Eukaryotic Tubulins: Lessons from Naegleria and the Multi-tubulin Hypothesis","volume":"10","author":"Fulton","year":"2022","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"jcs259539","DOI":"10.1242\/jcs.259539","article-title":"Tubulin isotypes\u2014Functional insights from model organisms","volume":"135","author":"Nsamba","year":"2022","journal-title":"J. Cell Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"913809","DOI":"10.3389\/fcell.2022.913809","article-title":"Microtubules in Microorganisms: How Tubulin Isotypes Contribute to Diverse Cytoskeletal Functions","volume":"10","author":"Bera","year":"2022","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1002\/bies.950190603","article-title":"Evolution of the multi-tubulin hypothesis","volume":"19","author":"Wilson","year":"1997","journal-title":"Bioessays"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.devcel.2018.08.014","article-title":"Human \u03b2-Tubulin Isotypes Can Regulate Microtubule Protofilament Number and Stability","volume":"47","author":"Ti","year":"2018","journal-title":"Dev. Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1083\/jcb.201603050","article-title":"The structured core of human \u03b2 tubulin confers isotype-specific polymerization properties","volume":"213","author":"Pamula","year":"2016","journal-title":"J. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1002\/dneu.22745","article-title":"\u03b1- and \u03b2-tubulin isotypes are differentially expressed during brain development","volume":"81","author":"Hausrat","year":"2021","journal-title":"Dev. Neurobiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2177","DOI":"10.1016\/j.cub.2015.06.063","article-title":"\u03b6-Tubulin Is a Member of a Conserved Tubulin Module and Is a Component of the Centriolar Basal Foot in Multiciliated Cells","volume":"25","author":"Turk","year":"2015","journal-title":"Curr. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.tcb.2021.03.010","article-title":"\u03b4 and \u03b5 tubulin in mammalian development","volume":"31","author":"Stathatos","year":"2021","journal-title":"Trends Cell Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"6746","DOI":"10.1038\/srep06746","article-title":"Molecular evolution and functional divergence of tubulin superfamily in the fungal tree of life","volume":"4","author":"Zhao","year":"2014","journal-title":"Sci. Rep."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/s13630-016-0041-5","article-title":"Drosophila melanogaster as a model for basal body research","volume":"5","author":"Jana","year":"2016","journal-title":"Cilia"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1407","DOI":"10.1242\/jcs.064873","article-title":"Reconstructing the evolutionary history of the centriole from protein components","volume":"123","author":"Hodges","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Schwarz, A., Sankaralingam, P., O\u2019Connell, K.F., and Muller-Reichert, T. (2018). Revisiting Centrioles in Nematodes-Historic Findings and Current Topics. Cells, 7.","DOI":"10.3390\/cells7080101"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"The Lancet Editors (2022). Malaria in 2022: A year of opportunity. Lancet, 399, 1573.","DOI":"10.1016\/S0140-6736(22)00729-2"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.idc.2008.03.010","article-title":"Human babesiosis","volume":"22","author":"Vannier","year":"2008","journal-title":"Infect. Dis. Clin. North Am."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Yang, Y., Christie, J., Koster, L., Du, A., and Yao, C. (2021). Emerging Human Babesiosis with \u201cGround Zero\u201d in North America. Microorganisms, 9.","DOI":"10.3390\/microorganisms9020440"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Ullah, R., Shams, S., Khan, M.A., Ayaz, S., ul Akbar, N., Din, Q.u., Khan, A., Leon, R., and Zeb, J. (2021). Epidemiology and molecular characterization of Theileria annulata in cattle from central Khyber Pakhtunkhwa, Pakistan. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0249417"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"579929","DOI":"10.3389\/fmicb.2020.579929","article-title":"Population Genetic Analysis of the Theileria annulata Parasites Identified Limited Diversity and Multiplicity of Infection in the Vaccine from India","volume":"11","author":"Roy","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1016\/S1534-5807(04)00135-2","article-title":"Reduction and compaction in the genome of the apicomplexan parasite Cryptosporidium parvum","volume":"6","author":"Keeling","year":"2004","journal-title":"Dev. Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1556\/1886.2019.00019","article-title":"Cryptosporidium Infection: Epidemiology, Pathogenesis and Differential Diagnosis","volume":"9","author":"Gerace","year":"2019","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1645\/GE-3341.1","article-title":"The genus Atoxoplasma (Garnham 1950) as a junior objective synonym of the genus Isospora (Schneider 1881) species infecting birds and resurrection of Cystoisospora (Frenkel 1977) as the correct genus for Isospora species infecting mammals","volume":"91","author":"Barta","year":"2005","journal-title":"J. Parasitol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1490","DOI":"10.1017\/S0031182019000957","article-title":"Cystoisospora belli infections in humans: The past 100 years","volume":"146","author":"Dubey","year":"2019","journal-title":"Parasitology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3389\/fcimb.2020.00043","article-title":"Advances in Cyclosporiasis Diagnosis and Therapeutic Intervention","volume":"10","author":"Li","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"384","DOI":"10.3389\/fvets.2020.00384","article-title":"Overview of Poultry Eimeria Life Cycle and Host-Parasite Interactions","volume":"7","year":"2020","journal-title":"Front. Vet. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Blake, D.P., Worthing, K., and Jenkins, M.C. (2020). Exploring Eimeria Genomes to Understand Population Biology: Recent Progress and Future Opportunities. Genes, 11.","DOI":"10.3390\/genes11091103"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1016\/j.ijpara.2017.08.003","article-title":"Advances in the diagnosis of bovine besnoitiosis: Current options and applications for control","volume":"47","author":"Ferre","year":"2017","journal-title":"Int. J. Parasitol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"551","DOI":"10.4269\/ajtmh.17-0677","article-title":"Toxoplasma gondii Infection in the United States, 2011\u20132014","volume":"98","author":"Jones","year":"2018","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.1016\/S0140-6736(04)16412-X","article-title":"Toxoplasmosis","volume":"363","author":"Montoya","year":"2004","journal-title":"Lancet"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1128\/EC.05161-11","article-title":"SPM1 stabilizes subpellicular microtubules in Toxoplasma gondii","volume":"11","author":"Tran","year":"2012","journal-title":"Eukaryot. Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1091\/mbc.e15-11-0754","article-title":"An ensemble of specifically targeted proteins stabilizes cortical microtubules in the human parasite Toxoplasma gondii","volume":"27","author":"Liu","year":"2016","journal-title":"Mol. Biol. Cell"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1128\/EC.00096-13","article-title":"A SAS-6-like protein suggests that the Toxoplasma conoid complex evolved from flagellar components","volume":"12","author":"Scheumann","year":"2013","journal-title":"Eukaryot. Cell"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"27809","DOI":"10.1038\/srep27809","article-title":"An evolutionarily conserved SSNA1\/DIP13 homologue is a component of both basal and apical complexes of Toxoplasma gondii","volume":"6","author":"Berry","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1038\/nrmicro.2017.86","article-title":"Gliding motility powers invasion and egress in Apicomplexa","volume":"15","author":"Frenal","year":"2017","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"28604","DOI":"10.1038\/srep28604","article-title":"SAS6-like protein in Plasmodium indicates that conoid-associated apical complex proteins persist in invasive stages within the mosquito vector","volume":"6","author":"Wall","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e42669","DOI":"10.7554\/eLife.42669","article-title":"Three F-actin assembly centers regulate organelle inheritance, cell-cell communication and motility in Toxoplasma gondii","volume":"8","author":"Tosetti","year":"2019","journal-title":"eLife"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Cruz-Bustos, T., Feix, A.S., Ruttkowski, B., and Joachim, A. (2021). Sexual Development in Non-Human Parasitic Apicomplexa: Just Biology or Targets for Control?. Animals, 11.","DOI":"10.3390\/ani11102891"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/j.ijpara.2017.03.002","article-title":"Genomics and epigenetics of sexual commitment in Plasmodium","volume":"47","author":"Bechtsi","year":"2017","journal-title":"Int. J. Parasitol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/bs.apar.2016.09.004","article-title":"Targeting the Parasite to Suppress Malaria Transmission","volume":"97","author":"Sinden","year":"2017","journal-title":"Adv. Parasitol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1111\/cmi.12355","article-title":"An essential role of the basal body protein SAS-6 in Plasmodium male gamete development and malaria transmission","volume":"17","author":"Marques","year":"2015","journal-title":"Cell. Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1128\/EC.00225-14","article-title":"Targeting Toxoplasma tubules: Tubulin, microtubules and associated proteins in a human pathogen","volume":"14","author":"Morrissette","year":"2015","journal-title":"Eukaryot. Cell"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/S0169-4758(98)01246-0","article-title":"Microtubule inhibitors as potential antimalarial agents","volume":"14","author":"Bell","year":"1998","journal-title":"Parasitol. Today"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"D898","DOI":"10.1093\/nar\/gkab929","article-title":"VEuPathDB: The eukaryotic pathogen, vector and host bioinformatics resource center","volume":"50","author":"Amos","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1111\/j.1550-7408.2012.00644.x","article-title":"The revised classification of eukaryotes","volume":"59","author":"Adl","year":"2012","journal-title":"J. Eukaryot. Microbiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"D8","DOI":"10.1093\/nar\/gkx1095","article-title":"Database resources of the National Center for Biotechnology Information","volume":"46","author":"Coordinators","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1002\/0471250953.bi0313s48","article-title":"Clustal omega","volume":"48","author":"Sievers","year":"2014","journal-title":"Curr. Protoc. Bioinform."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1002\/pro.3290","article-title":"Clustal Omega for making accurate alignments of many protein sequences","volume":"27","author":"Sievers","year":"2018","journal-title":"Protein Sci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/msb.2011.75","article-title":"Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega","volume":"7","author":"Sievers","year":"2011","journal-title":"Mol. Syst. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/S0168-9525(00)02024-2","article-title":"EMBOSS: The European Molecular Biology Open Software Suite","volume":"16","author":"Rice","year":"2000","journal-title":"Trends Genet."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"6087","DOI":"10.1093\/nar\/gkw536","article-title":"Integrated transcriptomic and proteomic analyses of P. falciparum gametocytes: Molecular insight into sex-specific processes and translational repression","volume":"44","author":"Lasonder","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"40655","DOI":"10.1038\/srep40655","article-title":"Epigenetic regulation of Plasmodium falciparum clonally variant gene expression during development in Anopheles gambiae","volume":"7","author":"Yerbanga","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Lopez-Barragan, M.J., Lemieux, J., Quinones, M., Williamson, K.C., Molina-Cruz, A., Cui, K., Barillas-Mury, C., Zhao, K., and Su, X.Z. (2011). Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genom., 12.","DOI":"10.1186\/1471-2164-12-587"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2951","DOI":"10.1016\/j.celrep.2018.02.075","article-title":"A Specific PfEMP1 Is Expressed in P. falciparum Sporozoites and Plays a Role in Hepatocyte Infection","volume":"22","author":"Zanghi","year":"2018","journal-title":"Cell Rep."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1474","DOI":"10.1038\/s41598-018-37671-8","article-title":"An experimental genetically attenuated live vaccine to prevent transmission of Toxoplasma gondii by cats","volume":"9","author":"Ramakrishnan","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1016\/j.cell.2016.08.019","article-title":"A Genome-wide CRISPR Screen in Toxoplasma Identifies Essential Apicomplexan Genes","volume":"166","author":"Sidik","year":"2016","journal-title":"Cell"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"3991","DOI":"10.1073\/pnas.76.8.3991","article-title":"Mutation in a structural gene for a \u03b2-tubulin specific to testis in Drosophila melanogaster","volume":"76","author":"Kemphues","year":"1979","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/0166-6851(92)90173-H","article-title":"\u03b1-tubulin II is a male-specific protein in Plasmodium falciparum","volume":"56","author":"Rawlings","year":"1992","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/j.ijpara.2007.09.005","article-title":"Isotype expression, post-translational modification and stage-dependent production of tubulins in erythrocytic Plasmodium falciparum","volume":"38","author":"Fennell","year":"2008","journal-title":"Int. J. Parasitol."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Schwank, S., Sutherland, C.J., and Drakeley, C.J. (2010). Promiscuous expression of \u03b1-tubulin II in maturing male and female Plasmodium falciparum gametocytes. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0014470"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.molbiopara.2005.07.003","article-title":"Plasmodium berghei \u03b1-tubulin II: A role in both male gamete formation and asexual blood stages","volume":"144","author":"Kooij","year":"2005","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1126\/science.aaz4352","article-title":"TTC5 mediates autoregulation of tubulin via mRNA degradation","volume":"367","author":"Lin","year":"2020","journal-title":"Science"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"3973","DOI":"10.1091\/mbc.12.12.3973","article-title":"Dominant-lethal \u03b1-tubulin mutants defective in microtubule depolymerization in yeast","volume":"12","author":"Anders","year":"2001","journal-title":"Mol. Biol. Cell"},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Salomaki, E.D., Terpis, K.X., Rueckert, S., Kotyk, M., Varadinova, Z.K., Cepicka, I., Lane, C.E., and Kolisko, M. (2021). Gregarine single-cell transcriptomics reveals differential mitochondrial remodeling and adaptation in apicomplexans. BMC Biol., 19.","DOI":"10.1186\/s12915-021-01007-2"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"e49662","DOI":"10.7554\/eLife.49662","article-title":"Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles","volume":"8","author":"Paskerova","year":"2019","journal-title":"eLife"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0031182015001213","article-title":"Diversity of extracellular proteins during the transition from the \u2018proto-apicomplexan\u2019 alveolates to the apicomplexan obligate parasites","volume":"143","author":"Templeton","year":"2016","journal-title":"Parasitology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"2689","DOI":"10.1093\/molbev\/msn213","article-title":"The Apicomplexan whole-genome phylogeny: An analysis of incongruence among gene trees","volume":"25","author":"Kuo","year":"2008","journal-title":"Mol. Biol. Evol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1007\/978-3-319-53047-5_14","article-title":"The Tubulin Superfamily in Archaea","volume":"84","author":"Aylett","year":"2017","journal-title":"Sub-Cell. Biochem."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1007\/978-1-0716-1661-1_13","article-title":"The Cilioprotist Cytoskeleton, a Model for Understanding How Cell Architecture and Pattern Are Specified: Recent Discoveries from Ciliates and Comparable Model Systems","volume":"2364","author":"Hufnagel","year":"2022","journal-title":"Methods Mol. Biol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13630-016-0022-8","article-title":"Tetrahymena basal bodies","volume":"5","author":"Bayless","year":"2016","journal-title":"Cilia"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1242\/jcs.115.5.1017","article-title":"Disruption of microtubules uncouples budding and nuclear division in Toxoplasma gondii","volume":"115","author":"Morrissette","year":"2002","journal-title":"J. Cell Sci."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1007\/s00709-017-1147-3","article-title":"Kingdom Chromista and its eight phyla: A new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences","volume":"255","year":"2018","journal-title":"Protoplasma"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/BF02198844","article-title":"Evolutionary relationships of eukaryotic kingdoms","volume":"42","author":"Kumar","year":"1996","journal-title":"J. Mol. Evol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/0166-6851(91)90036-6","article-title":"Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates and ciliates","volume":"45","author":"Gajadhar","year":"1991","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"a028076","DOI":"10.1101\/cshperspect.a028076","article-title":"Axoneme Structure from Motile Cilia","volume":"9","author":"Ishikawa","year":"2017","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Valentine, M., and Van Houten, J. (2021). Using Paramecium as a Model for Ciliopathies. Genes, 12.","DOI":"10.3390\/genes12101493"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1038\/s41467-021-20902-4","article-title":"The molecular dynamics of subdistal appendages in multi-ciliated cells","volume":"12","author":"Ryu","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"e53580","DOI":"10.7554\/eLife.53580","article-title":"Super-resolution microscopy reveals coupling between mammalian centriole subdistal appendages and distal appendages","volume":"9","author":"Chong","year":"2020","journal-title":"eLife"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1002\/cphy.c110043","article-title":"The ciliary cytoskeleton","volume":"2","author":"Pedersen","year":"2012","journal-title":"Compr. Physiol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/s13630-017-0053-9","article-title":"The rise and fall of basal bodies in the nematode Caenorhabditis elegans","volume":"6","author":"Nechipurenko","year":"2017","journal-title":"Cilia"},{"key":"ref_89","unstructured":"Chalfie, M. (2006). WormBook, Available online: http:\/\/www.wormbook.org."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"R516","DOI":"10.1016\/j.cub.2020.02.076","article-title":"Chytrid fungi","volume":"30","author":"Medina","year":"2020","journal-title":"Curr. Biol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/S0169-5347(03)00152-6","article-title":"Morphostasis in alveolate evolution","volume":"18","author":"Leander","year":"2003","journal-title":"Trends Ecol. Evol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1186\/s13630-016-0025-5","article-title":"Basal body structure and composition in the apicomplexans Toxoplasma and Plasmodium","volume":"5","author":"Francia","year":"2015","journal-title":"Cilia"},{"key":"ref_93","doi-asserted-by":"crossref","unstructured":"Zeeshan, M., Brady, D., Markus, R., Vaughan, S., Ferguson, D., Holder, A.A., and Tewari, R. (2022). Plasmodium SAS4: Basal body component of male cell which is dispensable for parasite transmission. Life Sci. Alliance, 5.","DOI":"10.26508\/lsa.202101329"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s13630-016-0032-6","article-title":"Naegleria: A classic model for de novo basal body assembly","volume":"5","author":"Fulton","year":"2016","journal-title":"Cilia"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1083\/jcb.29.1.97","article-title":"Centriole replication. II. Sperm formation in the fern, Marsilea and the cycad, Zamia","volume":"29","author":"Mizukami","year":"1966","journal-title":"J. Cell Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"1701","DOI":"10.1017\/S0031182013000838","article-title":"Sex and Eimeria: A molecular perspective","volume":"140","author":"Walker","year":"2013","journal-title":"Parasitology"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.mib.2010.05.016","article-title":"The flagellum in malarial parasites","volume":"13","author":"Sinden","year":"2010","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1007\/BF01951336","article-title":"Electron microscopical study on gamogony of Sarcocystis suihominis in human tissue cultures","volume":"58","author":"Mehlhorn","year":"1979","journal-title":"Z Parasitenkd"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/S1471-4922(02)02330-9","article-title":"Toxoplasma gondii and sex: Essential or optional extra?","volume":"18","author":"Ferguson","year":"2002","journal-title":"Trends Parasitol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/BF00329535","article-title":"Fine structural changes associated with microgametogenesis of Eimeria acervulina in chickens","volume":"43","author":"Fernando","year":"1973","journal-title":"Z. Parasitenkd."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1293","DOI":"10.1091\/mbc.9.6.1293","article-title":"The UNI3 gene is required for assembly of basal bodies of Chlamydomonas and encodes \u03b4-tubulin, a new member of the tubulin superfamily","volume":"9","author":"Dutcher","year":"1998","journal-title":"Mol. Biol. Cell"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"3859","DOI":"10.1091\/mbc.e02-04-0205","article-title":"\u03b5-tubulin is an essential component of the centriole","volume":"13","author":"Dutcher","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_103","doi-asserted-by":"crossref","unstructured":"Wingfield, J.L., and Lechtreck, K.F. (2018). Chlamydomonas Basal Bodies as Flagella Organizing Centers. Cells, 7.","DOI":"10.3390\/cells7070079"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/0035-9203(67)90054-5","article-title":"Electron microscope studies of motile stages of malaria parasites. V. Exflagellation in Plasmodium, Hepatocystis and Leucocytozoon","volume":"61","author":"Garnham","year":"1967","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1007\/BF00389644","article-title":"Elektronenmikroskopische Untersuchung an Entwicklungsstadien von Theileria annulata (Dschunkowsky, Luhs, 1904) im Darm und in der H\u00e4molymphe von Hyalomma anatolicum excavatum (Koch, 1844)","volume":"48","author":"Mehlhorn","year":"1975","journal-title":"Z. Parasitenkd."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"2966","DOI":"10.1073\/pnas.80.10.2966","article-title":"Sexuality in piroplasms as revealed by electron microscopy in Babesia microti","volume":"80","author":"Rudzinska","year":"1983","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1007\/BF00215696","article-title":"Penetration of the peritrophic membrane of the tick by Babesia microti","volume":"221","author":"Rudzinska","year":"1982","journal-title":"Cell Tissue Res."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/BF00383118","article-title":"Preliminary observations on the ultrastructure of supposed sexual stages of Babesia bigemina (Piroplasmea)","volume":"53","author":"Weber","year":"1977","journal-title":"Z. Parasitenkd."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"2226","DOI":"10.1038\/s41564-019-0539-x","article-title":"Life cycle progression and sexual development of the apicomplexan parasite Cryptosporidium parvum","volume":"4","author":"Tandel","year":"2019","journal-title":"Nat. Microbiol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1016\/j.cell.2005.03.027","article-title":"Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology","volume":"121","author":"Khan","year":"2005","journal-title":"Cell"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1074\/mcp.M116.061804","article-title":"Sex-Specific Biology of the Human Malaria Parasite Revealed from the Proteomes of Mature Male and Female Gametocytes","volume":"16","author":"Miao","year":"2017","journal-title":"Mol. Cell. Proteom."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"608291","DOI":"10.3389\/fcimb.2020.608291","article-title":"The Structural and Molecular Underpinnings of Gametogenesis in Toxoplasma gondii","volume":"10","author":"Tomasina","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"Straschil, U., Talman, A.M., Ferguson, D.J.P., Bunting, K.A., Xu, Z., Bailes, E., Sinden, R.E., Holder, A.A., Smith, E.F., and Coates, J.C. (2010). The Armadillo Repeat Protein PF16 Is Essential for Flagellar Structure and Function in Plasmodium Male Gametes. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0012901"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"3753","DOI":"10.1242\/jeb.00653","article-title":"Antimalarial compounds: From bench to bedside","volume":"206","author":"Olliaro","year":"2003","journal-title":"J. Exp. Biol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"1947","DOI":"10.2165\/00003495-200767130-00015","article-title":"Nitazoxanide: A review of its use in the treatment of gastrointestinal infections","volume":"67","author":"Anderson","year":"2007","journal-title":"Drugs"},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/0002-9343(88)90014-9","article-title":"Treatment of central nervous system toxoplasmosis with pyrimethamine\/sulfadiazine combination in 35 patients with the acquired immunodeficiency syndrome. Efficacy of long-term continuous therapy","volume":"84","author":"Leport","year":"1988","journal-title":"Am. J. Med."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"21160","DOI":"10.1073\/pnas.1908239116","article-title":"Genetic ablation of purine salvage in Cryptosporidium parvum reveals nucleotide uptake from the host cell","volume":"116","author":"Pawlowic","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1099\/ijs.0.02328-0","article-title":"Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage","volume":"53","author":"Saldarriaga","year":"2003","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1111\/j.1550-7408.2002.tb00336.x","article-title":"Re-examining alveolate evolution using multiple protein molecular phylogenies","volume":"49","author":"Fast","year":"2002","journal-title":"J. Eukaryot. Microbiol."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"1297","DOI":"10.1093\/oxfordjournals.molbev.a025576","article-title":"\u03b1-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family","volume":"13","author":"Keeling","year":"1996","journal-title":"Mol. Biol. Evol."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"e13818","DOI":"10.15252\/emmm.202013818","article-title":"Inhibiting parasite proliferation using a rationally designed anti-tubulin agent","volume":"13","author":"Gaillard","year":"2021","journal-title":"EMBO Mol. Med."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.1021\/acsinfecdis.0c00122","article-title":"An Antiparasitic Compound from the Medicines for Malaria Venture Pathogen Box Promotes Leishmania Tubulin Polymerization","volume":"6","author":"Ullah","year":"2020","journal-title":"ACS Infect. Dis."},{"key":"ref_123","doi-asserted-by":"crossref","unstructured":"Parker, A.L., Teo, W.S., McCarroll, J.A., and Kavallaris, M. (2017). An Emerging Role for Tubulin Isotypes in Modulating Cancer Biology and Chemotherapy Resistance. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18071434"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1960","DOI":"10.1091\/mbc.e03-07-0530","article-title":"Dinitroanilines bind \u03b1-tubulin to disrupt microtubules","volume":"15","author":"Morrissette","year":"2004","journal-title":"Mol. Biol. Cell"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/3\/706\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:51:43Z","timestamp":1760122303000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/3\/706"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,9]]},"references-count":124,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["microorganisms11030706"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11030706","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,9]]}}}