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Evolutionary analysis identifies a Golgi pathway and correlates lineage-specific factors with endomembrane organelle emergence in apicomplexans

CM. Klinger, E. Jimenez-Ruiz, T. Mourier, A. Klingl, L. Lemgruber, A. Pain, JB. Dacks, M. Meissner

. 2024 ; 43 (2) : 113740. [pub] 20240215

Jazyk angličtina Země Spojené státy americké

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/bmc24007045

The organelle paralogy hypothesis (OPH) aims to explain the evolution of non-endosymbiotically derived organelles. It predicts that lineage-specific pathways or organelles should result when identity-encoding membrane-trafficking components duplicate and co-evolve. Here, we investigate the presence of such lineage-specific membrane-trafficking machinery paralogs in Apicomplexa, a globally important parasitic lineage. We are able to identify 18 paralogs of known membrane-trafficking machinery, in several cases co-incident with the presence of new endomembrane organelles in apicomplexans or their parent lineage, the Alveolata. Moreover, focused analysis of the apicomplexan Arf-like small GTPases (i.e., ArlX3) revealed a specific post-Golgi trafficking pathway. This pathway appears involved in delivery of proteins to micronemes and rhoptries, with knockdown demonstrating reduced invasion capacity. Overall, our data have identified an unforeseen post-Golgi trafficking pathway in apicomplexans and are consistent with the OPH mechanism acting to produce endomembrane pathways or organelles at various evolutionary stages across the alveolate lineage.

Citace poskytuje Crossref.org

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$a The organelle paralogy hypothesis (OPH) aims to explain the evolution of non-endosymbiotically derived organelles. It predicts that lineage-specific pathways or organelles should result when identity-encoding membrane-trafficking components duplicate and co-evolve. Here, we investigate the presence of such lineage-specific membrane-trafficking machinery paralogs in Apicomplexa, a globally important parasitic lineage. We are able to identify 18 paralogs of known membrane-trafficking machinery, in several cases co-incident with the presence of new endomembrane organelles in apicomplexans or their parent lineage, the Alveolata. Moreover, focused analysis of the apicomplexan Arf-like small GTPases (i.e., ArlX3) revealed a specific post-Golgi trafficking pathway. This pathway appears involved in delivery of proteins to micronemes and rhoptries, with knockdown demonstrating reduced invasion capacity. Overall, our data have identified an unforeseen post-Golgi trafficking pathway in apicomplexans and are consistent with the OPH mechanism acting to produce endomembrane pathways or organelles at various evolutionary stages across the alveolate lineage.
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$a Jimenez-Ruiz, Elena $u Experimental Parasitology, Department of Veterinary Sciences, Faculty of Veterinary Medicine, Ludwig-Maximilians-Universität, LMU, Munich, Germany
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$a Mourier, Tobias $u Pathogen Genomics Laboratory, Bioscience Programme, Biological, and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Kingdom of Saudi Arabia
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$a Klingl, Andreas $u Pflanzliche Entwicklungsbiologie, Biozentrum der Ludwig-Maximilians-Universität, Munich, Germany
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$a Lemgruber, Leandro $u Cellular Analysis Facility, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK
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$a Pain, Arnab $u Pathogen Genomics Laboratory, Bioscience Programme, Biological, and Environmental Sciences and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Kingdom of Saudi Arabia; International Institute for Zoonosis Control, GI-CoRE, Hokkaido University, Sapporo, Japan
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$a Dacks, Joel B $u Division of Infectious Diseases, Department of Medicine and Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada; Women and Children's Health Research Institute, University of Alberta, Edmonton, AB, Canada; Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic; Centre for Life's Origin and Evolution, Department of Genetics, Evolution & Environment, University College London, London, UK. Electronic address: dacks@ualberta.ca
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$a Meissner, Markus $u Experimental Parasitology, Department of Veterinary Sciences, Faculty of Veterinary Medicine, Ludwig-Maximilians-Universität, LMU, Munich, Germany. Electronic address: markus.meissner@lmu.de
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