Abstract
A substantial portion of eukaryote diversity consists of algae with complex plastids, i.e., plastids originating from eukaryote-to-eukaryote endosymbioses. These plastids are characteristic by a deviating number of envelope membranes (higher than two), and sometimes a remnant nucleus of the endosymbiont alga, termed the nucleomorph, is present. Complex plastid-bearing algae are therefore much like living matryoshka dolls, eukaryotes within eukaryotes. In comparison, primary plastids of Archaeplastida (plants, green algae, red algae, and glaucophytes) arose upon a single endosymbiosis event with a cyanobacterium and are surrounded by two membranes. Complex plastids were acquired several times by unrelated groups nested within eukaryotic heterotrophs, suggesting complex plastids are somewhat easier to obtain than primary plastids. This is consistent with the existence of higher-order and serial endosymbioses, i.e., engulfment of complex plastid-bearing algae by (tertiary) eukaryotic hosts and functional plastid replacements, respectively. Plastid endosymbiosis is typical by a massive transfer of genetic material from the endosymbiont to the host nucleus and metabolic rearrangements related to the trophic switch to phototrophy; this is necessary to establish metabolic integration of the plastid and control over its division. Although photosynthesis is the main advantage of plastid acquisition, algae that lost photosynthesis often maintain complex plastids, suggesting their roles beyond photosynthesis. This chapter summarizes basic knowledge on acquisition and functions of complex plastid.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64:583–607. https://doi.org/10.1146/annurev-arplant-050312-120144
Armbrust EV, Berges JA, Bowler C et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86. https://doi.org/10.1126/science.1101156
Nowack ECM, Melkonian M, Glöckner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410–418. https://doi.org/10.1016/j.cub.2008.02.051
Oborník M, Lukeš J (2015) The organellar genomes of Chromera and Vitrella, the phototrophic relatives of apicomplexan parasites. Annu Rev Microbiol 69:129–144. https://doi.org/10.1146/annurev-micro-091014-104449
Dorrell R, Howe C (2015) Integration of plastids with their hosts: lessons learned from dinoflagellates. Proc Natl Acad Sci U S A 112:201421380. https://doi.org/10.1073/pnas.1421380112
Burki F, Kaplan M, Tikhonenkov DV et al (2016) Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc R Soc B Biol Sci 283:20152802. https://doi.org/10.1098/rspb.2015.2802
Petersen J, Ludewig AK, Michael V et al (2014) Chromera velia, endosymbioses and the rhodoplex hypothesis— plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol 6:666–684. https://doi.org/10.1093/gbe/evu043
Derelle R, Torruella G, Klimeš V et al (2015) Bacterial proteins pinpoint a single eukaryotic root. Proc Natl Acad Sci U S A 112:E693–E699. https://doi.org/10.1073/pnas.1420657112
Hurst GDD (2017) Extended genomes: symbiosis and evolution. Interface Focus 7:20170001. https://doi.org/10.1098/rsfs.2017.0001
Sibbald SJ, Cenci U, Colp M et al (2017) Diversity and evolution of Paramoeba spp. and their kinetoplastid endosymbionts. J Eukaryot Microbiol 64(5):598–607. https://doi.org/10.1111/jeu.12394
Stiller JW (2014) Toward an empirical framework for interpreting plastid evolution. J Phycol 50(3):462–471. https://doi.org/10.1111/jpy.12178
Curtis BA, Tanifuji G, Burki F et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65. https://doi.org/10.1038/nature11681
Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366. https://doi.org/10.1111/j.1550-7408.1999.tb04614.x
Füssy Z, Oborník M (2017) Chromerids and their plastids. In: Hirakawa Y (ed) Advances in botanical research, vol 84. Academic Press, Massachusetts in press
Dorrell RG, Bowler C (2017) Secondary plastids of stramenopiles. In: Hirakawa Y (ed) Advances in botanical research, vol 84. Academic Press, Massachusetts in press
Falkowski PG, Katz ME, Knoll AH et al (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360. https://doi.org/10.1126/science.1095964
Baurain D, Brinkmann H, Petersen J et al (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 27:1698–1709. https://doi.org/10.1093/molbev/msq059
Parfrey LW, Lahr DJG, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A 108:13624–13629. https://doi.org/10.1073/pnas.1110633108
Cihlář J, Füssy Z, Horák A, Oborník M (2016) Evolution of the tetrapyrrole biosynthetic pathway in secondary algae: conservation, redundancy and replacement. PLoS One 11:e0166338. https://doi.org/10.1371/journal.pone.0166338
Janouškovec J, Horák A, Oborník M et al (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 107:10949–10954. https://doi.org/10.1073/pnas.1003335107
Ševčíková T, Horák A, Klimeš V et al (2015) Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci Rep 5:10134. https://doi.org/10.1038/srep10134
Moore RB, Oborník M, Janouškovec J et al (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963. https://doi.org/10.1038/nature06635
Oborník M, Modrý D, Lukeš M et al (2012) Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the great barrier reef. Protist 163:306–323. https://doi.org/10.1016/j.protis.2011.09.001
Waller RF, Kořený L (2017) Plastid complexity in dinoflagellates: a picture of gains, losses, replacements and revisions. In: Hirakawa Y (ed) Advances in botanical research, vol 84. Academic Press, Massachusetts in press
Park MG, Kim M, Kim S (2014) The acquisition of plastids/phototrophy in heterotrophic dinoflagellates. Acta Protozool 53:39–50. https://doi.org/10.4467/16890027AP.14.005.1442
Yamada N, Sym SD, Horiguchi T (2017) Identification of highly divergent diatom-derived chloroplasts in dinoflagellates, including a description of Durinskia kwazulunatalensis sp. nov. (Peridiniales, Dinophyceae). Mol Biol Evol 34:1335–1351. https://doi.org/10.1093/molbev/msx054
Dorrell RG, Howe CJ (2012) What makes a chloroplast? Reconstructing the establishment of photosynthetic symbioses. J Cell Sci 125:1865–1875. https://doi.org/10.1242/jcs.102285
McFadden GI, Guy L, Saw JH et al (2014) Origin and evolution of plastids and photosynthesis in eukaryotes. Cold Spring Harb Perspect Biol 6(4):a016105. https://doi.org/10.1101/cshperspect.a016105
Zimorski V, Ku C, Martin WF, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48. https://doi.org/10.1016/j.mib.2014.09.008
Gross J, Bhattacharya D (2009) Mitochondrial and plastid evolution in eukaryotes: an outsiders’ perspective. Nat Rev Genet 10:495–505. https://doi.org/10.1038/nrg2649
Tyra HM, Linka M, Weber APM, Bhattacharya D (2007) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8(10):R212. https://doi.org/10.1186/gb-2007-8-10-r212
Basak I, Moeller SG (2013) Emerging facets of plastid division regulation. Planta 237:389–398. https://doi.org/10.1007/s00425-012-1743-6
Archibald JM (2015) Genomic perspectives on the birth and spread of plastids. Proc Natl Acad Sci U S A 112:10147–10153. https://doi.org/10.1073/pnas.1421374112
Collén J, Porcel B, Carré W et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A 110:5247–5252. https://doi.org/10.1073/pnas.1221259110
Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. BioEssays 29:1048–1058. https://doi.org/10.1002/bies.20638
Fristedt R (2017) Chloroplast function revealed through analysis of GreenCut2 genes. J Exp Bot 68:2111–2120. https://doi.org/10.1093/jxb/erx082
Terashima M, Specht M, Hippler M (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57:151–168. https://doi.org/10.1007/s00294-011-0339-1
Gruber A, Rocap G, Kroth PG et al (2015) Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage. Plant J 81:519–528. https://doi.org/10.1111/tpj.12734
Cavalier-Smith T (2000) Membrane heredity and early chloroplast evolution. Trends Plant Sci 5:174–182. https://doi.org/10.1016/S1360-1385(00)01598-3
Patron NJ, Waller RF, Archibald JM, Keeling PJ (2005) Complex protein targeting to dinoflagellate plastids. J Mol Biol 348:1015–1024. https://doi.org/10.1016/j.jmb.2005.03.030
Durnford DG, Gray MW (2006) Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot Cell 5:2079–2091. https://doi.org/10.1128/EC.00222-06
Felsner G, Sommer MS, Gruenheit N et al (2011) ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane. Genome Biol Evol 3:140–150. https://doi.org/10.1093/gbe/evq074
Hehenberger E, Burki F, Kolisko M, Keeling PJ (2016) Functional relationship between a dinoflagellate host and its diatom endosymbiont. Mol Biol Evol 33:2376–2390. https://doi.org/10.1093/molbev/msw109
Facchinelli F, Weber APM (2011) The metabolite transporters of the plastid envelope: an update. Front Plant Sci 2:1–18. https://doi.org/10.3389/fpls.2011.00050
Mulkidjanian AY, Koonin EV, Makarova KS et al (2006) The cyanobacterial genome core and the origin of photosynthesis. Proc Natl Acad Sci U S A 103:13126–13131. https://doi.org/10.1073/pnas.0605709103
Smith SR, Gillard JTF, Kustka AB et al (2016) Transcriptional orchestration of the global cellular response of a model pennate diatom to diel light cycling under iron limitation. PLoS Genet 12:e1006490. https://doi.org/10.1371/journal.pgen.1006490
Bailleul B, Berne N, Murik O et al (2015) Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524:366–369. https://doi.org/10.1038/nature14599
Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311. https://doi.org/10.1016/S0168-9525(98)01494-2
Larkum AWD, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–195. https://doi.org/10.1016/j.tplants.2007.03.011
Oborník M, Green BR (2005) Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol 22:2343–2353. https://doi.org/10.1093/molbev/msi230
Martin W, Schnarrenberger C (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 32:1–18. https://doi.org/10.1007/s002940050241
Wolf YI, Koonin EV (2013) Genome reduction as the dominant mode of evolution. BioEssays 35:829–837. https://doi.org/10.1002/bies.201300037
Aury J, Jaillon O, Duret L et al (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178. https://doi.org/10.1038/nature05230
Dagan T, Blekhman R, Graur D (2006) The “domino theory” of gene death: gradual and mass gene extinction events in three lineages of obligate symbiotic bacterial pathogens. Mol Biol Evol 23:310–316. https://doi.org/10.1093/molbev/msj036
Howe CJ, Barbrook AC, Koumandou VL et al (2003) Evolution of the chloroplast genome. Philos Trans R Soc Lond Ser B Biol Sci 358:99–106-107. https://doi.org/10.1098/rstb.2002.1176
Kořený L, Oborník M (2011) Sequence evidence for the presence of two tetrapyrrole pathways in Euglena gracilis. Genome Biol Evol 3:359–364. https://doi.org/10.1093/gbe/evr029
Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517. https://doi.org/10.1146/annurev.arplant.59.032607.092915
Waller RF, Gornik SG, Kořený L, Pain A (2016) Metabolic pathway redundancy within the apicomplexan-dinoflagellate radiation argues against an ancient chromalveolate plastid. Commun Integr Biol 9:e1116653. https://doi.org/10.1080/19420889.2015.1116653
Nuismer SL, Otto SP (2004) Host-parasite interactions and the evolution of ploidy. Proc Natl Acad Sci U S A 101:11036–11039. https://doi.org/10.1073/pnas.0403151101
Blouin N, Lane C (2015) Red algae provide fertile ground for exploring parasite evolution. Perspect Phycol 3:11–19. https://doi.org/10.1127/pip/2015/0027
Figueroa-Martinez F, Nedelcu AM, Smith DR, Reyes-Prieto A (2015) When the lights go out: the evolutionary fate of free-living colorless green algae. New Phytol 206:972–982
Krause K (2008) From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet 54:111–121. https://doi.org/10.1007/s00294-008-0208-8
Záhonová K, Füssy Z, Oborník M et al (2016) RuBisCO in non-photosynthetic alga Euglena longa: divergent features, transcriptomic analysis and regulation of complex formation. PLoS One 11:1–15. https://doi.org/10.1371/journal.pone.0158790
Abrahamsen MS, Templeton TJ, Enomoto S et al (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441–445. https://doi.org/10.1126/science.1094786
Toso MA, Omoto CK (2007) Gregarina niphandrodes may lack both a plastid genome and organelle. J Eukaryot Microbiol 54:66–72. https://doi.org/10.1111/j.1550-7408.2006.00229.x
Gornik SG, Febrimarsa CAM et al (2015) Endosymbiosis undone by stepwise elimination of the plastid in a parasitic dinoflagellate. Proc Natl Acad Sci U S A 112:5767–5772. https://doi.org/10.1073/pnas.1423400112
Lim L, McFadden GI (2010) The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond Ser B Biol Sci 365:749–763. https://doi.org/10.1098/rstb.2009.0273
Janouškovec J, Tikhonenkov DV, Burki F et al (2015) Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc Natl Acad Sci U S A 112:10200–10207. https://doi.org/10.1073/pnas.1423790112
Janouškovec J, Gavelis GS, Burki F et al (2017) Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics. Proc Natl Acad Sci U S A 114:E171–E180. https://doi.org/10.1073/pnas.1614842114
McFadden GI, Reith ME, Munholland J, Lang-Unnasch N (1996) Plastid in human parasites. Nature 381:482–482. https://doi.org/10.1038/381482a0
Mukherjee A, Sadhukhan GC (2016) Anti-malarial drug design by targeting apicoplasts: new perspectives. J Pharmacopuncture 19:7–15. https://doi.org/10.3831/KPI.2016.19.001
Kořený L, Sobotka R, Kovářová J et al (2012) Aerobic kinetoplastid flagellate Phytomonas does not require heme for viability. Proc Natl Acad Sci U S A 109:3808–3813. https://doi.org/10.1073/pnas.1201089109
Sanchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF (2007) Plastid genes in a non-photosynthetic dinoflagellate. Protist 158:105–117. https://doi.org/10.1016/j.protis.2006.09.004
Slamovits CH, Keeling PJ (2008) Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Mol Biol Evol 25:1297–1306. https://doi.org/10.1093/molbev/msn075
Pradel G, Schlitzer M (2010) Antibiotics in malaria therapy and their effect on the parasite apicoplast. Curr Mol Med 10:335–349. https://doi.org/10.2174/156652410791065273
Acknowledgment
Authors are supported by a grant from the Czech Science Foundation (grant no: 16-24027S).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Science+Business Media, LLC, part of Springer Nature
About this protocol
Cite this protocol
Füssy, Z., Oborník, M. (2018). Complex Endosymbioses I: From Primary to Complex Plastids, Multiple Independent Events. In: Maréchal, E. (eds) Plastids. Methods in Molecular Biology, vol 1829. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-8654-5_2
Download citation
DOI: https://doi.org/10.1007/978-1-4939-8654-5_2
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-8653-8
Online ISBN: 978-1-4939-8654-5
eBook Packages: Springer Protocols