Invited paper from Symposium, during a joint meeting of the Society of Protozoologists, American Phycological Society, and the International Society of Evolutionary Protistology, Flagstaff, AR, August 7, 1998.
Article first published online: 2 MAY 2007
Journal of Eukaryotic Microbiology
Volume 46, Issue 4, pages 347–366, July 1999
How to Cite
CAVALIER-SMITH, T. (1999), Principles of Protein and Lipid Targeting in Secondary Symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan Plastid Origins and the Eukaryote Family Tree,. Journal of Eukaryotic Microbiology, 46: 347–366. doi: 10.1111/j.1550-7408.1999.tb04614.x
Address effective August 1999: Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK.
- Issue published online: 2 MAY 2007
- Article first published online: 2 MAY 2007
- plastid envelope;
- protein targeting;
The biggest unsolved problems in chloroplast evolution are the origins of dinoflagellate and euglenoid chloroplasts, which have envelopes of three membranes not two like plants and chromists, and of the sporozoan plastid, bounded by four smooth membranes. I review evidence that all three of these protozoan plastid types originated by secondary symbiogenesis from eukaryotic endosymbionts. Instead of separate symbiogenetic events, I argue that dinoflagellate and sporozoan plastids are directly related and that the common ancestor of dinoflagellates and Sporozoa was photosynthetic. I suggest that the last common ancestor of all Alveolata was photosynthetic and acquired its chlorophyll c-containing plastids in the same endosymbiogenetic event as those of Chromista. Chromista and Alveolata are postulated to be a clade designated chromalveolates. I propose that euglenoids obtained their plastids from the same (possibly ulvophycean) green alga as chlorarachneans and that Discicristata (Euglenozoa plus Percolozoa) and Cercozoa (the group including chlorarachneans) form a clade designated cabozoa (protozoa with chlorophyll a + b). If both theories are correct, there were only two secondary symbiogenetic events (witnessed by the chlorarachnean and cryptomonad nucleomorphs) in the history of life, not seven as commonly assumed. This greatly reduces the postulated number of independent origins of chloroplast protein-targeting machinery and of gene transfers from endosymbiont to host nuclei. I discuss the membrane and plastid losses and innovations in protein targeting implied by these theories, the comparative evidence for them, and their implications for eukaryote megaphylogeny. The principle of evolutionary conservatism leads to a novel theory for the function of periplastid vesicles in membrane biogenesis of chlorarachneans and chromists and of the key steps in secondary symbiogenesis. Protozoan classification is also slightly revised by abandoning the probably polyphyletic infrakingdom Actinopoda, grouping Foraminifera and Radiolaria as a new infrakingdom Retaria, placing Heliozoa within a revised infrakingdom Sarcomastigota, establishing a new flagellate phylum Loukozoa for Jakobea plus Anaeromonadea within an emended subkingdom Eozoa, and ranking Archezoa as an infrakingdom within Eozoa.