A contemplation on the secondary origin of green algal and plant plastids

Eunsoo Kim, Shinichiro Maruyama

Abstract


A single origin of plastids and the monophyly of three “primary” plastid-containing groups – the Chloroplastida (or Viridiplantae; green algae+land plants), Rhodophyta, and Glaucophyta – are widely accepted, mainstream hypotheses that form the basis for many comparative evolutionary studies. This “Archaeplastida” hypothesis, however, thus far has not been unambiguously confirmed by phylogenetic studies based on nucleocytoplasmic markers. In view of this as well as other lines of evidence, we suggest the testing of an alternate hypothesis that plastids of the Chloroplastida are of secondary origin. The new hypothesis is in agreement with, or perhaps better explains, existing data, including both the plastidal and nucleocytoplasmic characteristics of the Chloroplastida in comparison to those of other groups.

Keywords


Archaeplastida; Chloroplastida; glaucophytes; green algae; plastids; primary plastids; red algae; secondary plastids; Viridiplantae

Full Text:

PDF

References


Archibald JM. The puzzle of plastid evolution. Curr Biol. 2009;19(2):R81–R88. http://dx.doi.org/10.1016/j.cub.2008.11.067

Graham LE. Algae. 2nd ed. San Francisco, CA: Pearson/Benjamin Cummings; 2009.

Palmer JD. The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol. 2003;39(1):4–12. http://dx.doi.org/10.1046/j.1529-8817.2003.02185.x

Howe C, Barbrook A, Nisbet RE, Lockhart P, Larkum AW. The origin of plastids. Philos Trans R Soc Lond B Biol Sci. 2008;363(1504):2675–2685. http://dx.doi.org/10.1098/rstb.2008.0050

Cavalier-Smith T. Kingdom protozoa and its 18 phyla. Microbiol Rev. 1993;57(4):953–994.

Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, et al. The revised classification of eukaryotes. J Eukaryot Microbiol. 2012;59(5):429–514. http://dx.doi.org/10.1111/j.1550-7408.2012.00644.x

Minge MA, Shalchian-Tabrizi K, Tørresen OK, Takishita K, Probert I, Inagaki Y, et al. A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evol Biol. 2010;10(1):191. http://dx.doi.org/10.1186/1471-2148-10-191

Sanchez-Puerta MV, Bachvaroff TR, Delwiche CF. Sorting wheat from chaff in multi-gene analyses of chlorophyll c-containing plastids. Mol Phylogenet Evol. 2007;44(2):885–897. http://dx.doi.org/10.1016/j.ympev.2007.03.003

Petersen J, Ludewig AK, Michael V, Bunk B, Jarek M, Baurain D, et al. Chromera velia, endosymbioses and the rhodoplex hypothesis – plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol. 2014;6(3):666–684. http://dx.doi.org/10.1093/gbe/evu043

Parfrey LW, Lahr DJG, Knoll AH, Katz LA. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA. 2011;108(33):13624–13629. http://dx.doi.org/10.1073/pnas.1110633108

Burki F, Okamoto N, Pombert JF, Keeling PJ. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc Biol Sci. 2012;279(1736):2246–2254. http://dx.doi.org/10.1098/rspb.2011.2301

Stiller JW, Hall BD. The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci USA. 1997;94(9):4520–4525.

Stiller JW. Toward an empirical framework for interpreting plastid evolution. J Phycol. 2014;50(3):462–471. http://dx.doi.org/10.1111/jpy.12178

Douglas SE, Turner S. Molecular evidence for the origin of plastids from a cyanobacterium-like ancestor. J Mol Evol. 1991;33(3):267–273. http://dx.doi.org/10.1007/BF02100678

Morden CW, Delwiche CF, Kuhsel M, Palmer JD. Gene phylogenies and the endosymbiotic origin of plastids. Biosystems. 1992;28(1–3):75–90. http://dx.doi.org/10.1016/0303-2647(92)90010-V

Criscuolo A, Gribaldo S. Large-scale phylogenomic analyses indicate a deep origin of primary plastids within cyanobacteria. Mol Biol Evol. 2011;28(11):3019–3032. http://dx.doi.org/10.1093/molbev/msr108

Price DC, Chan CX, Yoon HS, Yang EC, Qiu H, Weber APM, et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science. 2012;335(6070):843–847. http://dx.doi.org/10.1126/science.1213561

Baldauf SL. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science. 2000;290(5493):972–977. http://dx.doi.org/10.1126/science.290.5493.972

Moreira D, Le Guyader H, Philippe H. The origin of red algae and the evolution of chloroplasts. Nature. 2000;405(6782):69–72. http://dx.doi.org/10.1038/35011054

Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, et al. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol. 2005;15(14):1325–1330. http://dx.doi.org/10.1016/j.cub.2005.06.040

Rodríguez-Ezpeleta N, Brinkmann H, Burger G, Roger AJ, Gray MW, Philippe H, et al. Toward resolving the eukaryotic tree: the phylogenetic positions of jakobids and cercozoans. Curr Biol. 2007;17(16):1420–1425. http://dx.doi.org/10.1016/j.cub.2007.07.036

Burki F, Shalchian-Tabrizi K, Minge M, Skjæveland Å, Nikolaev SI, Jakobsen KS, et al. Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE. 2007;2(8):e790. http://dx.doi.org/10.1371/journal.pone.0000790

Nozaki H, Iseki M, Hasegawa M, Misawa K, Nakada T, Sasaki N, et al. Phylogeny of primary photosynthetic eukaryotes as deduced from slowly evolving nuclear genes. Mol Biol Evol. 2007;24(8):1592–1595. http://dx.doi.org/10.1093/molbev/msm091

Burki F, Shalchian-Tabrizi K, Pawlowski J. Phylogenomics reveals a new “megagroup” including most photosynthetic eukaryotes. Biol Lett. 2008;4(4):366–369. http://dx.doi.org/10.1098/rsbl.2008.0224

Burki F, Inagaki Y, Brate J, Archibald JM, Keeling PJ, Cavalier-Smith T, et al. Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, telonemia and centroheliozoa, are related to photosynthetic chromalveolates. Genome Biol Evol. 2010;1:231–238. http://dx.doi.org/10.1093/gbe/evp022

Nozaki H, Maruyama S, Matsuzaki M, Nakada T, Kato S, Misawa K. Phylogenetic positions of Glaucophyta, green plants (Archaeplastida) and Haptophyta (Chromalveolata) as deduced from slowly evolving nuclear genes. Mol Phylogenet Evol. 2009;53(3):872–880. http://dx.doi.org/10.1016/j.ympev.2009.08.015

Brown MW, Kolisko M, Silberman JD, Roger AJ. Aggregative multicellularity evolved independently in the eukaryotic supergroup rhizaria. Curr Biol. 2012;22(12):1123–1127. http://dx.doi.org/10.1016/j.cub.2012.04.021

Zhao S, Burki F, Brate J, Keeling PJ, Klaveness D, Shalchian-Tabrizi K. Collodictyon – an ancient lineage in the tree of eukaryotes. Mol Biol Evol. 2012;29(6):1557–1568. http://dx.doi.org/10.1093/molbev/mss001

Brown MW, Sharpe SC, Silberman JD, Heiss AA, Lang BF, Simpson AGB, et al. Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc Biol Sci. 2013;280(1769):20131755. http://dx.doi.org/10.1098/rspb.2013.1755

Burki F, Corradi N, Sierra R, Pawlowski J, Meyer GR, Abbott CL, et al. Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in rhizaria. Curr Biol. 2013;23(16):1541–1547. http://dx.doi.org/10.1016/j.cub.2013.06.033

Yabuki A, Kamikawa R, Ishikawa SA, Kolisko M, Kim E, Tanabe AS, et al. Palpitomonas bilix represents a basal cryptist lineage: insight into the character evolution in Cryptista. Sci Rep. 2014;4:4641. http://dx.doi.org/10.1038/srep04641

Jackson CJ, Reyes-Prieto A. The mitochondrial genomes of the glaucophytes Gloeochaete wittrockiana and Cyanoptyche gloeocystis: multilocus phylogenetics suggests a monophyletic Archaeplastida. Genome Biol Evol. 2014;6(10):2774–2785. http://dx.doi.org/10.1093/gbe/evu218

Stiller JW, Riley J, Hall BD. Are red algae plants? A critical evaluation of three key molecular data sets. J Mol Evol. 2001;52(6):527–539. http://dx.doi.org/10.1007/s002390010183

Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR. Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics. 2007;277(4):427–439. http://dx.doi.org/10.1007/s00438-006-0199-4

Kim E, Lane CE, Curtis BA, Kozera C, Bowman S, Archibald JM. Complete sequence and analysis of the mitochondrial genome of Hemiselmis andersenii CCMP644 (Cryptophyceae). BMC Genomics. 2008;9(1):215. http://dx.doi.org/10.1186/1471-2164-9-215

Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, et al. Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol. 2011;21(4):328–333. http://dx.doi.org/10.1016/j.cub.2011.01.037

Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol. 2005;52(5):399–451. http://dx.doi.org/10.1111/j.1550-7408.2005.00053.x

Cavalier-Smith T. Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. J Eukaryot Microbiol. 2009;56(1):26–33. http://dx.doi.org/10.1111/j.1550-7408.2008.00373.x

Roger AJ, Simpson AGB. Evolution: revisiting the root of the eukaryote tree. Curr Biol. 2009;19(4):R165–R167. http://dx.doi.org/10.1016/j.cub.2008.12.032

Walker G, Dorrell RG, Schlacht A, Dacks JB. Eukaryotic systematics: a user’s guide for cell biologists and parasitologists. Parasitology. 2011;138(13):1638–1663. http://dx.doi.org/10.1017/S0031182010001708

Deschamps P, Moreira D. Signal conflicts in the phylogeny of the primary photosynthetic eukaryotes. Mol Biol Evol. 2009;26(12):2745–2753. http://dx.doi.org/10.1093/molbev/msp189

Maddison W, Knowles L. Inferring phylogeny despite incomplete lineage sorting. Syst Biol. 2006;55(1):21–30. http://dx.doi.org/10.1080/10635150500354928

Laurin-Lemay S, Brinkmann H, Philippe H. Origin of land plants revisited in the light of sequence contamination and missing data. Curr Biol. 2012;22(15):R593–R594. http://dx.doi.org/10.1016/j.cub.2012.06.013

O’Kelly CJ. Relationships of eukaryotic algal groups to other protists. In: Berner T, editor. Ultrastructure of microalgae. Boca Raton, FL: CRC Press; 1993. p. 269–293.

Stiller JW. Plastid endosymbiosis, genome evolution and the origin of green plants. Trends Plant Sci. 2007;12(9):391–396. http://dx.doi.org/10.1016/j.tplants.2007.08.002

Ball SG, Subtil A, Bhattacharya D, Moustafa A, Weber APM, Gehre L, et al. Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell. 2013;25(1):7–21. http://dx.doi.org/10.1105/tpc.112.101329

Rujan T, Martin W. How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trends Genet. 2001;17(3):113–120. http://dx.doi.org/10.1016/S0168-9525(00)02209-5

Deschamps P, Haferkamp I, Dauvillee D, Haebel S, Steup M, Buleon A, et al. Nature of the periplastidial pathway of starch synthesis in the cryptophyte Guillardia theta. Eukaryot. Cell. 2006;5(6):954–963. http://dx.doi.org/10.1128/EC.00380-05

Dagan T, Martin W. The tree of one percent. Genome Biol. 2006;7(10):118. http://dx.doi.org/10.1186/gb-2006-7-10-118

Rumpho ME. Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 2000;123(1):29–38. http://dx.doi.org/10.1104/pp.123.1.29

Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, et al. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA. 2002;99(19):12246–12251. http://dx.doi.org/10.1073/pnas.182432999

Bodył A. Do plastid-related characters support the chromalveolate hypothesis? J Phycol. 2005;41(3):712–719. http://dx.doi.org/10.1111/j.1529-8817.2005.00091.x

Cenci U, Nitschke F, Steup M, Minassian BA, Colleoni C, Ball SG. Transition from glycogen to starch metabolism in Archaeplastida. Trends Plant Sci. 2014;19(1):18–28. http://dx.doi.org/10.1016/j.tplants.2013.08.004

Deschamps P, Haferkamp I, d’ Hulst C, Neuhaus HE, Ball SG. The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci. 2008;13(11):574–582. http://dx.doi.org/10.1016/j.tplants.2008.08.009

Flannagan RS, Jaumouillé V, Grinstein S. The cell biology of phagocytosis. Annu Rev Pathol. 2012;7(1):61–98. http://dx.doi.org/10.1146/annurev-pathol-011811-132445

Raven JA, Beardall J, Flynn KJ, Maberly SC. Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin’s insectivorous plants. J Exp Bot. 2009;60(14):3975–3987. http://dx.doi.org/10.1093/jxb/erp282

Raven JA. Phagotrophy in phototrophs. Limnol Ocean. 1997;42(1):198–205. http://dx.doi.org/10.4319/lo.1997.42.1.0198

Yamaguchi A, Yubuki N, Leander BS. Morphostasis in a novel eukaryote illuminates the evolutionary transition from phagotrophy to phototrophy: description of Rapaza viridis n. gen. et sp. (Euglenozoa, Euglenida). BMC Evol Biol. 2012;12(1):29. http://dx.doi.org/10.1186/1471-2148-12-29

Maruyama S, Kim E. A modern descendant of early green algal phagotrophs. Curr Biol. 2013;23(12):1081–1084. http://dx.doi.org/10.1016/j.cub.2013.04.063

McKie-Krisberg ZM, Sanders RW. Phagotrophy by the picoeukaryotic green alga Micromonas: implications for Arctic Oceans. ISME J. 2014;8(10):1953–1961. http://dx.doi.org/10.1038/ismej.2014.16

Baurain D, Brinkmann H, Petersen J, Rodriguez-Ezpeleta N, Stechmann A, Demoulin V, et al. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol. 2010;27(7):1698–1709. http://dx.doi.org/10.1093/molbev/msq059




DOI: https://doi.org/10.5586/asbp.2014.040

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society