The Endosymbiotic Origin, Diversification and Fate of Plastids

Overview

Journal Philos Trans R Soc Lond B Biol Sci

Specialty Biology

Date 2010 Feb 4

PMID 20124341

Citations 239

Authors

Patrick J Keeling

Affiliations

Soon will be listed here.

Abstract

Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.

Citing Articles

Dissecting apicoplast functions through continuous cultivation of Toxoplasma gondii devoid of the organelle.

Chen M, Koszti S, Bonavoglia A, Maco B, von Rohr O, Peng H Nat Commun. 2025; 16(1):2095.

PMID: 40025025 PMC: 11873192. DOI: 10.1038/s41467-025-57302-x.

Modes and mechanisms for the inheritance of mitochondria and plastids in pathogenic protists.

Collier S, Farrell S, Goodman C, McFadden G PLoS Pathog. 2025; 21(1):e1012835.

PMID: 39847585 PMC: 11756805. DOI: 10.1371/journal.ppat.1012835.

Genome-wide changes of protein translation levels for cell and organelle proliferation in a simple unicellular alga.

Mogi Y, Matsuo Y, Kondo Y, Higashiyama T, Inada T, Yoshida Y Proc Jpn Acad Ser B Phys Biol Sci. 2025; 101(1):41-53.

PMID: 39805589 PMC: 11808204. DOI: 10.2183/pjab.101.002.

Auxin promotes chloroplast division by increasing the expression of chloroplast division genes.

Wang Y, Zhou Z, Liu X Plant Cell Rep. 2024; 44(1):20.

PMID: 39741196 DOI: 10.1007/s00299-024-03415-4.

Comparative genomics and phylogenetic analysis of six Malvaceae species based on chloroplast genomes.

Zhong Y, Bai B, Sun Y, Wen K, Qiao Y, Guo L BMC Plant Biol. 2024; 24(1):1245.

PMID: 39722018 PMC: 11670485. DOI: 10.1186/s12870-024-05974-w.

References

Tengs T, Dahlberg O, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche C . Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol. 2000; 17(5):718-29. DOI: 10.1093/oxfordjournals.molbev.a026350. View

Harper J, Keeling P . Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol. 2003; 20(10):1730-5. DOI: 10.1093/molbev/msg195. View

Nassoury N, Cappadocia M, Morse D . Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci. 2003; 116(Pt 14):2867-74. DOI: 10.1242/jcs.00517. View

McFadden G, Gilson P, Douglas S, Cavalier-Smith T, Hofmann C, Maier U . Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet. 1997; 13(2):46-9. DOI: 10.1016/s0168-9525(97)01010-x. View

Rogers M, Watkins R, Harper J, Durnford D, Gray M, Keeling P . A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evol Biol. 2007; 7:89. PMC: 1920508. DOI: 10.1186/1471-2148-7-89. View

Delwiche C, Kuhsel M, Palmer J . Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol. 1995; 4(2):110-28. DOI: 10.1006/mpev.1995.1012. View

Reyes-Prieto A, Moustafa A, Bhattacharya D . Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr Biol. 2008; 18(13):956-62. PMC: 2577054. DOI: 10.1016/j.cub.2008.05.042. View

Rodriguez-Ezpeleta N, Brinkmann H, Burey S, Roure B, Burger G, Loffelhardt W . Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol. 2005; 15(14):1325-30. DOI: 10.1016/j.cub.2005.06.040. View

Fast N, Kissinger J, Roos D, Keeling P . Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol. 2001; 18(3):418-26. DOI: 10.1093/oxfordjournals.molbev.a003818. View

10.

Rice D, Palmer J . An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol. 2006; 4:31. PMC: 1570145. DOI: 10.1186/1741-7007-4-31. View

11.

Xu P, Widmer G, Wang Y, Ozaki L, Alves J, Serrano M . The genome of Cryptosporidium hominis. Nature. 2004; 431(7012):1107-12. DOI: 10.1038/nature02977. View

12.

Abrahamsen M, Templeton T, Enomoto S, Abrahante J, Zhu G, Lancto C . Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004; 304(5669):441-5. DOI: 10.1126/science.1094786. View

13.

Moreira D, Le Guyader H, Philippe H . The origin of red algae and the evolution of chloroplasts. Nature. 2000; 405(6782):69-72. DOI: 10.1038/35011054. View

14.

Patron N, Waller R, Keeling P . A tertiary plastid uses genes from two endosymbionts. J Mol Biol. 2006; 357(5):1373-82. DOI: 10.1016/j.jmb.2006.01.084. View

15.

Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng L . The highly reduced genome of an enslaved algal nucleus. Nature. 2001; 410(6832):1091-6. DOI: 10.1038/35074092. View

16.

Cuvelier M, Ortiz A, Kim E, Moehlig H, Richardson D, Heidelberg J . Widespread distribution of a unique marine protistan lineage. Environ Microbiol. 2008; 10(6):1621-34. PMC: 2408648. DOI: 10.1111/j.1462-2920.2008.01580.x. View

17.

Sommer M, Gould S, Lehmann P, Gruber A, Przyborski J, Maier U . Der1-mediated preprotein import into the periplastid compartment of chromalveolates?. Mol Biol Evol. 2007; 24(4):918-28. DOI: 10.1093/molbev/msm008. View

18.

Barrett C, Freudenstein J . Molecular evolution of rbcL in the mycoheterotrophic coralroot orchids (Corallorhiza Gagnebin, Orchidaceae). Mol Phylogenet Evol. 2008; 47(2):665-79. DOI: 10.1016/j.ympev.2008.02.014. View

19.

Hirakawa Y, Kofuji R, Ishida K . TRANSIENT TRANSFORMATION OF A CHLORARACHNIOPHYTE ALGA, LOTHARELLA AMOEBIFORMIS (CHLORARACHNIOPHYCEAE), WITH uidA AND egfp REPORTER GENES(1). J Phycol. 2016; 44(3):814-20. DOI: 10.1111/j.1529-8817.2008.00513.x. View

20.

Slamovits C, Keeling P . Evolution of ultrasmall spliceosomal introns in highly reduced nuclear genomes. Mol Biol Evol. 2009; 26(8):1699-705. DOI: 10.1093/molbev/msp081. View