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http://dx.doi.org/10.12651/JSR.2021.10.2.142

Algal genomics perspective: the pangenome concept beyond traditional molecular phylogeny and taxonomy  

Lee, JunMo (Department of Oceanography, Kyungpook National University)
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Journal of Species Research / v.10, no.2, 2021 , pp. 142-153 More about this Journal
Abstract
Algal genomics approaches provide a massive number of genome/transcriptome sequences and reveal the evolutionary history vis-à-vis primary and serial endosymbiosis events that contributed to the biodiversity of photosynthetic eukaryotes in the eukaryote tree of life. In particular, phylogenomic methods using several hundred or thousands of genes have provided new insights into algal taxonomy and systematics. Using this method, many novel insights into algal species diversity and systematics occurred, leading to taxonomic revisions. In addition, horizontal gene transfers (HGTs) of functional genes have been identified in algal genomes that played essential roles in environmental adaptation and genomic diversification. Finally, algal genomics data can be used to address the pangenome, including core genes shared among all isolates and partially shared strain-specific genes. However, some aspects of the pangenome concept (genome variability of intraspecies level) conflict with population genomics concepts, and the issue is closely related to defining species boundaries using genome variability. This review suggests a desirable future direction to merge algal pangenomics and population genomics beyond traditional molecular phylogeny and taxonomy.
Keywords
algal genomics; biodiversity; genome variability; molecular phylogeny; molecular taxonomy; pangenome;
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1 Keeling, P.J. 2010. The endosymbiotic origin, diversification and fate of plastids. Philosophical Transactions of the Royal Society B: Biological Sciences 365(1541):729-748.   DOI
2 Lhee, D., J.M. Lee, K. Ettahi, C.H. Cho, J.S. Ha, Y.F. Chan, U. Zelzion, T.G. Stephens, D.C. Price, A. Gabr, E.C.M. Nowack, D. Bhattacharya and H.S. Yoon. 2021. Amoeba Genome Reveals Dominant Host Contribution to Plastid Endosymbiosis. Molecular Biology and Evolution 38(2):344-357.   DOI
3 Tang, Q., K. Pang, X. Yuan and S. Xiao. 2020. A one-billion-year-old multicellular chlorophyte. Nature Ecology & Evolution 4(4):543-549.   DOI
4 Theriot, E.C., M. Ashworth, E. Ruck, T. Nakov and R.K. Jansen. 2010. A preliminary multigene phylogeny of the diatoms (Bacillariophyta): challenges for future research. Plant Ecology and Evolution 143(3):278-296.   DOI
5 Timmis, J.N., M.A. Ayliffe, C.Y. Huang and W. Martin. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature Reviews Genetics 5(2):123-135.   DOI
6 Toews, D.P.L. and A. Brelsford. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21(16):3907-3930.   DOI
7 Umen, J. and S. Coelho. 2019. Algal sex determination and the evolution of anisogamy. Annual Review of Microbiology 73:267-291.   DOI
8 Fan, X., H. Qiu, W. Han, Y. Wang, D. Xu, X. Zhang, D. Bhattacharya and N. Ye. 2020. Phytoplankton pangenome reveals extensive prokaryotic horizontal gene transfer of diverse functions. Science Advances 6(18):eaba0111.   DOI
9 Gawryluk, R.M.R., D.V. Tikhonenkov, E. Hehenberger, F. Husnik, A.P., Mylniknov and P.J. Keeling. 2019. Non-photosynthetic predators are sister to red algae. Nature 572(7768):240-243.   DOI
10 Janouskovec, J., S.L. Liu, P.T. Martone, W. Carre, C. Leblanc, J. Collen and P.J. Keeling. 2013. Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. PloS ONE 8(3):e59001.   DOI
11 Guiry, M.D. and G.M. Guiry. 2021. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org; searched on March 2021.
12 Oliveira, M.C., S.I. Repetti, C. Iha, C.J. Jackson, P. Diaz-Tapia, K.M.F. Lubiana, V. Cassano, J.F. Costa, M.C.M. Cremen, V.R. Marcelino and H. Verbruggen. 2018. High-throughput sequencing for algal systematics. European Journal of Phycology 53(3):256-272.   DOI
13 Ponce-Toledo, R., P. Deschamps, P. Lopez-Garcia, Y. Zivanovic, K. Benzerara and D. Moreira. 2017. An early-branching freshwater cyanobacterium at the origin of plastids. Current Biology 27(3):386-391.   DOI
14 Graf, L., E.C. Yang, K.Y. Han, F.C. Kupper, K.M. Benes, J.K. Oyadomari, R.J.H. Herbert, H. Verbruggen, R. Wetherbee, R.A. Andersen and H.S. Yoon. 2020. Multigene phylogeny, morphological observation and re-examination of the literature lead to the description of the Phaeosacciophyceae classis nova and four new species of the Heterokontophyta SI clade. Protist 171(6):125781.   DOI
15 Godfroy, O., A.F. Peters, S.M. Coelho and J.M. Cock. 2015. Genome-wide comparison of ultraviolet and ethyl methanesulphonate mutagenesis methods for the brown alga Ectocarpus. Marine Genomics 24:109-113.   DOI
16 Golicz, A.A., P.E. Bayer, P.L. Bhalla, J. Batley and D. Edwards. 2020. Pangenomics comes of age: from bacteria to plant and animal applications. Trends in Genetics 36(2):132-145.   DOI
17 Gradinger, R. 2009. Sea-ice algae: major contributors to primary production and algal biomass in the Chukchi and Beaufort Seas during May/June 2002. Deep-Sea Research II 56(17):1201-1212.   DOI
18 Graf, L., Y. Shin, J.H. Yang, J.W. Choi, I.K. Hwang, W. Nelson, D. Bhattacharya, F. Viard and H.S. Yoon. 2021. A genome-wide investigation of the effect of farming and human-mediated introduction on the ubiquitous seaweed Undaria pinnatifida. Nature Ecology & Evolution 5(3):360-368.   DOI
19 Gulbrandsen, O.S., I.J. Andresen, A.K. Krabberod, J. Brate and K. Shalchian-Tabrizi. 2021. Phylogenomic analysis restructures the ulvophyceae. Journal of Phycology (accepted article).
20 Hu, Y., W. Xing, Z. Hu and G. Liu. 2020. Phylogenetic analysis and substitution rate estimation of colonial volvocine algae based on mitochondrial genomes. Genes 11(1):115.   DOI
21 Huson, D.H. and D. Bryant. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23(3):254-267.   DOI
22 Pirie, M.D. 2015. Phylogenies from concatenated data: is the end nigh? Taxon 64(3):421-423.   DOI
23 Parfrey, L.W., D.J.G. Lahr, A.H. Knoll and L.A. Katz. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proceedings of the National Academy of Sciences of the USA 108(33):13624-13629.   DOI
24 Maddison, W.P. and L.L. Knowles. 2006. Inferring phylogeny despite incomplete lineage sorting. Systematic Biology 55(1):21-30.   DOI
25 Mao, Y., S. Hou, J. Shi and E.P. Economo. 2020. TREEasy: an automated workflow to infer gene trees, species tress, and phylogenetic networks form multilocus data. Molecular Ecology Resources 20:832-840.   DOI
26 Matteoli, F.P., H. Passarelli-Araujo, F. Pedrosa-Silva, F.L. Olivares and T.M. Venancio. 2020. Population structure and pangenome analysis Enterobacter bugandensis uncover the presence of blaCTX-M-55, blaNDM-5 and blaIMI-1, along with sophisticated iron acquisition strategies. Genomics 112(2):1182-1191.   DOI
27 Matute, D.R. and V.E. Sepulveda. 2019. Fungal species boundaries in the genomics era. Fungal Genetics and Biology 131:103249.   DOI
28 Collen, J., B. Porcel, W. Carre, S.G. Ball, C. Chaparro, T. Tonon, T. Barbeyron, G. Michel, B. Noel, K. Valentin, M. Elias, F. Artiguenave, A. Arun, J.M. Aury, J.F. Barbosa-Neto, J.H. Bothwell, F.Y. Bouget, L. Brillet, F. Cabello-Hurtado, S. Capella-Gutierrez, B. Charrier, L. Cladiere, J.M. Cock, S.M. Coelho, C. Colleoni, M. Czjzek, C.D. Silva, L. Delage, F. Denoeud, P. Deschamps, S.M. Dittami, T. Gabaldon, C.M.M. Gachon, A. Groisillier, C. Herve, K. Jabbari, M. Katinka, B. Kloareg, N. Kowalczyk, K. Labadie, C. Leblanc, P.J. Lopez, D.H. McLachlan, L. Meslet-Cladiere, A. Moustafa, Z. Nehr, P.N. Collen, O. Panaud, F. Partensky, J. Poulain, S.A. Rensing, S. Rousvoal, G. Samson, A. Symeonidi, J. Weissenbach, A. Zambounis, P. Wincker and C. Boyen. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proceedings of the National Academy of Sciences of the USA 110(13):5247-5252.   DOI
29 Simpson, A.G.B., C.H. Slamovits and J.M. Archibald. 2017. Protist diversity and eukaryote phylogeny. In: J.M. Archibald, A.G.B. Simpson and C.H. Slamovits (eds.), Handbook of the protists(2nd ed.), Springer International Publishing, Cham, Switzerland. pp. 1-21.
30 Payo, D.A., F. Leliaert, H. Verbruggen, S. D'hondt, H.P. Calumpong and O. De Clerck. 2013. Extensive cryptic species diversity and fine-scale endemism in the marine red alga Portieria in the Philippines. Proceedings of the Royal Society B: Biological Sciences 280(1753):20122660.   DOI
31 Price, D.C., C.X. Chan, H.S. Yoon, E.C. Yang, H. Qiu, A.P.M. Weber, R. Schwacke, J. Gross, N.A. Blouin, C. Lane, A. Reyes-Prieto, D.G. Durnford, J.A.D. Neilson, B.F. Lang, G. Burger, J.M. Steiner, W. Looffelhardt, J.E. Meuser, M.C. Posewitz, S. Ball, M.C. Arias, B. Henrissat, P.M. Coutinho, S.A. Rensing, A. Symeonidi, H. Doddapaneni, B.R. Green, V.D. Rajah, J. Boore and D. Bhattacharya. 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 355(6070):843-847.
32 Ragan, M.A., C.J. Bird, E.L. Rice, R.R. Gutell, C.A. Murphy and R.K. Singh. 1994. A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proceedings of the National Academy of Sciences of the USA 91(15):7276-7280.   DOI
33 Nowack, E.C.M., M. Melkonian and G. Glockner. 2008. Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Current Biology 18(6):410-418.   DOI
34 Mercado, J.M., S. Salles and D. Cortes. 2020. Ecophysiology of marine algae: factors regulating primary production and growth in natural environments. In: S.K. Kim (ed.), Encyclopedia of marine biotechnology, John Wiley & Sons. pp. 341-357.
35 Munoz-Gomez, S.A., F.G. Mejia-Franco, K. Durnin, M. Colp, C.J. Grisdale, J.M. Archibald and C.H. Slamovits. 2017. The new red algal subphylum Proteorhodophytina comprises the largest and most divergent plastid genomes known. Current Biology 27(11):1677-1684.   DOI
36 Nguyen, L.T., H.A. Schmidt, A. Von Haeseler and B.Q. Minh. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1):268-274.   DOI
37 Ono, J., D. Greig and P.J. Boynton. 2020. Defining and disrupting species boundaries in Saccharomyces. Annual Review of Microbiology 74:477-495.   DOI
38 Keeling, P.J., F. Burki, H.M. Wilcox, B. Allam, E.E. Allen, L.A. Amaral-Zettler, E.V. Armbrust, J.M. Archibald, A.K. Bharti, C.J. Bell, B. Beszteri, K.D. Bidle, C.T. Cameron, L. Campbell, D.A. Caron, R.A. Cattolico, J.L. Collier, K. Coyne, S.K. Davy, P. Deschamps, S.T. Dyhrman, B. Edvardsen, R.D. Gates, C.J. Gobler, S.J. Greenwood, S.M. Guida, J.L. Jacobi, K.S. Jakobsen, E.R. James, B. Jenkins, U. John, M.D. Johnson, A.R. Juhl, A. Kamp, L.A. Katz, R. Kiene, A. Kudryavtsev, B.S. Leander, S. Lin, C. Lovejoy, D. Lynn, A. Marchetti, G. McManus, A.M. Nedelcu, S. Menden-Deuer, C. Miceli, T. Mock, M. Montresor, M.A. Moran, S. Murray, G. Nadathur, S. Nagai, P.B. Ngam, B. Palenik, J. Pawlowski, G. Petroni, G. Piganeau, M.C. Posewitz, K. Rengefors, G. Romano, M.E. Rumpho, T. Rynearson, K.B. Schilling, D.C. Schroeder, A.G.B. Simpson, C.H. Slamovits, D.R. Smith, G.J. Smith, S.R. Smith, H.M. Sosik, P. Stief, E. Theriot, S.N. Twary, P.E. Umale, D. Vaulot, B. Wawrik, G.L. Wheeler, W.H. Wilson, Y. Xu, A. Zingone and A.Z. Worden. 2014. The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PloS Biology 12(6):e1001889.   DOI
39 Reyes-Prieto, A., H.S. Yoon, A. Moustafa, E.C. Yang, R.A. Andersen, S.M. Boo, T. Nakayama, K.I. Ishida and D. Bhattacharya. 2010. Differential gene retention in plastids of common recent origin. Molecular Biology and Evolution 27(7):1530-1537.   DOI
40 Zhang, Z., C. Qu, K. Zhang, Y. He, X. Zhao, L. Yang, Z. Zheng, X. Ma, X. Wang, W. Wang, K. Wang, D. Li, L. Zhang, X. Zhang, D. Su, X. Chang, M. Zhou, D. Gao, W. Jiang, F. Leliaert, D. Bhattacharya, O. De Clerck, B. Zhong and J. Miao. 2020. Adaptation to extreme Antarctic environments revealed by the genome of a sea ice green alga. Current Biology 30(17):3330-3341.   DOI
41 Rice, D.W. and J.D. Palmer. 2006. An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biology 4:31.   DOI
42 Xi, Z., L. Liu, J.S. Rest and C.C. Davis. 2014. Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. Systematic Biology 63(6):919-932.   DOI
43 Yabuki, A., R. Kamikawa, S.A. Ishikawa, M. Kolisko, E. Kim, A.S. Tanabe, K. Kume, K.I. Ishida and Y. Inagki. 2014. Palpitomonas bilix represents a basal cryptist lineage: insight into the character evolution in Cryptista. Scientific Reports 4:4641.   DOI
44 Yang, E.C., K.M. Kim, S.Y. Kim, J.M. Lee, G.H. Boo, J.H. Lee, W.A. Nelson, G. Yi, W.E. Schmidt, S. Fredericq, S.M. Boo, D. Bhattacharya and H.S. Yoon. 2015. Highly conserved mitochondrial genomes among multicellular red algae of the Florideophyceae. Genome Biology and Evolution 7(8):2394-2406.   DOI
45 Adl, S.M., A.G. Simpson, M.A. Farmer, R. Andersen, O.R. Anderson, J.R. Barta, S.S. Bowser, G. Brugerolle, R.A. Fensome, S. Fredericq, T.Y. James, S. Karpov, P. Kugrens, J. Krug, C.E. Lane, L.A. Lewis, J. Lodge, D.H. Lynn, D.G. Mann, R.M. McCourt, L. Mendoza, O. Moestrup, S.E. Mozley-Standridge, T.A. Nerad, C.A. Shearer, A.V. Smirnov, F.W. Spiegel and M.F. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology 52(5):399-451.   DOI
46 Kim, J.I., C.E. Moore, J.M. Archibald, D. Bhattacharya, G. Yi, H.S. Yoon and W. Shin. 2017. Evolutionary dynamics of cryptophyte plastid genomes. Genome Biology and Evolution 9(7):1859-1872.   DOI
47 Van Etten, J. and D. Bhattacharya. 2020. Horizontal gene transfer in eukaryotes: not if, but how much? Trends in Genetics 36(12):915-925.   DOI
48 Wendel, J.F. and J.J. Doyle. 1998. Phylogenetic incongruence: window into genome history and molecular evolution. In: D.E. Soltis, P.S. Soltis and J.J. Doyle (eds.), Molecular Systematics of Plants II, Springer, Boston, MA. pp. 265-296.
49 Read, B.A., J. Kegel, M.J. Klute, A. Kuo, S.C. Lefebvre, F. Maumus, C. Mayer, J. Miller, A. Monier, A. Salamov, J. Young, M. Aguilar, J.M. Claverie, S. Frickenhaus, K. Gonzalez, E.K. Herman, Y.C. Lin, J. Napier, H. Ogata, A.F. Sarno, J. Shmutz, D. Schroeder, C. de Vargas, F. Verret, P. von Dassow, K. Valentin, Y. Van de Peer, G. Sheeler, Emiliania huxleyi Annotation Consortium, J.B. Dacks, C.F. Delwiche, S.T. Dyhrman, G. Glockner, U. John, T. Richards, A.Z. Worden, X. Zhang and I.V. Grigoriev. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499(7457):209-213.   DOI
50 Dorrell, R.G., G. Gile, G. McCallum, R. Meheust, E.P. Bapteste, C.M. Klinger, L. Brillet-Gueguen, K.D. Freeman, D.J. Richter and C. Bowler. 2017. Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. eLife 6:e23717.   DOI
51 Azarian, T., I.T. Huang and W.P. Hanage. 2020. Structure and dynamics of bacterial populations: pangenome ecology. In: H. Tettelin and D. Medini (eds.), The pangenome: diversity, dynamics and evolution of genomes, Springer, Cham, Switzerland. pp. 115-128.
52 Barth, J.M.I., C. Gubili, M. Matschiner, O.K. Torresen, S. Watanabe, B. Egger, Y.S. Han, E. Feunteun, R. Sommaruga, R. Jehle and R. Schabetsberger. 2020. Stable species boundaries despite ten million years of hybridization in tropical eels. Nature Communications 11:1433.   DOI
53 Bengtson, S., T. Sallstedt, V. Belivanova and M. Whitehouse. 2017. Three-dimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PloS Biology 15(3):e2000735.   DOI
54 Yoon, H.S., J.D. Hackett, C. Ciniglia, G. Pinto and D. Bhattacharya. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution 21(5):809-818.   DOI
55 Yoon, H.S., K.M. Muller, R.G. Sheath, F.D. Ott and D. Bhattacharya. 2006. Defining the major lineages of red algae (Rhodophyta). Journal of Phycology 42(2):482-492.   DOI
56 Brodie, J., S.G. Ball, F.Y. Bouget, C.X. Chan, O. De Clerck, J.M. Cock, C. Gachon, A.R. Grossman, T. Mock, J.A. Raven, M. Saha, A.G. Smith, A. Vardi, H.S. Yoon and D. Bhattacharya. 2017. Biotic interactions as drivers of algal origin and evolution. New Phytologist 216(3):670-681.   DOI
57 Bhattacharya, D., H.S. Yoon and J.D. Hackett. 2004. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26:50-60.   DOI
58 Bobay, L.M. 2020. The prokaryotic species concept and challenges. In: H. Tettelin and D. Medini (eds.), The pangenome: diversity, dynamics and evolution of genomes, Springer, Cham, Switzerland. pp. 21-49.
59 Brawley, S.H., N.A. Blouin, E. Ficko-Blean, G.L. Wheeler, M. Lohr, H.V. Goodson, J.W. Jenkins, C.E. Blaby-Haas, K.E. Helliwell, C.X. Chan, T.N. Marriage, D. Bhattacharya, A.S. Klein, Y. Badis, J. Brodie, Y. Cao, J. Collen, S.M. Dittami, C.M.M. Gachon, B.R. Green, S.J. Karpowicz, J.W. Kim, U.J. Kudahl, S. Lin, G. Michel, M. Mittag, B.J.S.C. Olson, J.L. Pangilinan, Y. Peng, H. Qiu, S. Shu, J.T. Singer, A.G. Smith, B.N. Sprecher, V. Wagner, W. Wang, Z.Y. Wang, J. Yan, C. Yarish, C. Zauner-Riek, Y. Zhuang, Y. Zou, E.A. Lindquist, J. Grimwood, K.W. Barry, D.S. Rokhsar, J. Schmutz, J.W. Stiller, A.R. Grossman and S.E. Prochnik. 2017. Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proceedings of the National Academy of Sciences of the USA 114(31): E6361-6370.   DOI
60 Bryand, D.A. and D.P. Canniffe. 2018. How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. Journal of Physics B: Atomic, Molecular and Optical Physics 51(3):033001.   DOI
61 Bennetzen, J.L. and H. Wang. 2014. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annual Review of Plant Biology 65:505-530.   DOI
62 Rossoni, A.W., D.C. Price, M. Seger, D. Lyska, P. Lammers, D. Bhattacharya and A.P.M. Weber. 2019. The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions. eLife 8:e45017.   DOI
63 Richard, G.F. 2020. Eukaryotic pangenomes. In: H. Tettelin and D. Medini(eds.), The pangenome: diversity, dynamics and evolution of genomes, Springer, Cham, Switzerland. pp. 253-291.
64 Rodriguez-Ezpeleta, N., H. Brinkmann, S.C. Burey, B. Roure, G. Burger, W. Loffelhardt, H.J. Bohnert, H. Philippe and B.F. Lang. 2005. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Current Biology 15(14):1325-1330.   DOI
65 Rokas, A., B.L. Williams, N. King and S.B. Carroll. 2003. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425(6960):798-804.   DOI
66 Rudd, S. 2003. Expressed sequence tags: alternative or complement to whole genome sequences? Trends in Plant Science 8(7):1360-1385.   DOI
67 Russell, S., C. Jackson and A. Reyes-Prieto. 2021. High sequence divergence but limited architectural rearrangements in organelle genomes of Cyanophora (Glaucophyta) species. Journal of Eukaryotic Microbiology 68:e12831.
68 Sanchez-Baracaldo, P., J.A. Raven, D. Pisani and A.H. Knoll. 2017. Early photosynthetic eukaryotes inhabited low-salinity habitats. Proceedings of the National Academy of Sciences of the USA 114(37):E7737-7745.   DOI
69 Burki, F., N. Okamoto, J.F. Pombert and P.J. Keeling. 2012. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proceedings of the Royal Society B: Biological Sciences 279(1736):2246-2254.   DOI
70 Burki, F., A.J. Roger, M.W. Brown and A.G.B. Simpson. 2019. The new tree of eukaryotes. Trends in Ecology & Evolution 31(1):43-55.
71 Yoon, H.S., D.C. Price, R. Stepanauskas, V.D. Rajah, M.E. Sieracki, W.H. Wilson, E.C. Yang, S. Duffy and D. Bhattacharya. 2011. Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332(6030):714-717.   DOI
72 Butterfield, N.J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26(3):386-404.   DOI
73 Iha, C., C.J. Grassa, G.D.M. Lyra, C.C. Davis, H. Verbruggen and M.C. Oliveira. 2018. Organellar genomics: a useful tool to study evolutionary relationships and molecular evolution in Gracilariaceae (Rhodophyta). Journal of Phycology 54(6):775-787.   DOI
74 Jain, C., L.M. Rodriguez-R, A.M. Phillippy, K.T. Konstantinidis and S. Aluru. 2018. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications 9:5114.   DOI
75 Zuccarello, G.C. and J.A. West. 2003. Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans/B. moritziana complex (Rhodomelaceae, Rhodophyta) with focus on North American isolates. Journal of Phycology 39(5):948-959.   DOI
76 Costa, J.F., S.M. Lin, E.C. Macaya, C. Fernandez-Garcia and H. Verbruggen. 2016. Chloroplast genomes as a tool to resolve red algal phylogenies: a case study in the Nemaliales. BMC Evolutionary Biology 16:205.   DOI
77 Keeling, P.J. and F. Burki. 2019. Progress towards the tree of eukaryotes. Current Biology 29(16):R808-R817.   DOI
78 Kumar, V., F. Lammers, T. Bidon, M. Pfenninger, L. Kolter, M.A. Nilsson and A. Janke. 2017. The evolutionary history of bears is characterized by gene flow across species. Scientific Reports 7:46487.   DOI
79 Lee, J.M., C.H. Cho, S.I. Park, J.W. Choi, H.S. Song, J.A. West, D. Bhattacharya and H.S. Yoon. 2016a. Parallel evolution of highly conserved plastid genome architecture in red seaweeds and seed plants. BMC Biology 14:75.   DOI
80 Cummins, C.A. and J.O. Mclnerney. 2011. A method for inferring the rate of evolution of homologous characters that can potentially improve phylogenetic inference, resolve deep divergence and correct systematic biases. Systematic Biology 60(6):833-844.   DOI
81 de Vries, J., A. Stanton, J.M. Archibald and S.B. Gould. 2016. Streptophyte terrestrialization in light of plastid evolution. Trends in Plant Science 21(6):467-476.   DOI
82 de Vries, J. and S.B. Gould. 2018. The monoplastidic bottleneck in algae and plant evolution. Journal of Cell Science 131(2):jcs203414.   DOI
83 Schliep, K., A.J. Potts, D.A. Morrison and G.W. Grimm. 2017. Intertwining phylogenetic trees and networks. Methods in Ecology and Evolution 8(10):1212-1220.   DOI
84 Diaz-Tapia, P., C.A. Maggs, J.A. West and H. Verbruggen. 2017. Analysis of chloroplast genomes and a supermatrix inform reclassification of the Rhodomelaceae (Rhodophyta). Journal of Phycology 53(5):920-937.   DOI
85 Yoon, H.S., G.C. Zuccarello and D. Bhattacharya. 2010. Evolutionary history and taxonomy of red algae. In: J. Seckbach and D.J. Chapman (eds.), Red algae in the genomic age, Springer, Dordrecht. pp. 27-42.
86 Seeleuthner, Y., S. Mondy, V. Lombard, Q. Carradec, E. Pelletier, M. Wessner, J. Leconte, J.F. Mangot, J. Poulain, K. Labadie, R. Logares, S. Sunagawa, V. de Berardinis, M. Salanoubat, C. Dimier, S. Kandels-Lewis, M. Picheral, S. Searson, Tara Oceans Coordinators, S. Pesant, N. Poulton, R. Stepanauskas, P. Bork, C. Bowler, P. Hingamp, M.B. Sullivan, D. Iudicone, R. Massana, J.M. Aury, B. Henrissat, E. Karsenti, O. Jaillon, M. Sieracki, C. de Vargas and P. Wincker. 2018. Single-cell genomics of multiple uncultured stramenopiles reveals underestimated functional diversity across oceans. Nature Communications 9:310.   DOI
87 Shaw, K.L. 2002. Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proceedings of the National Academy of Sciences of the USA 99(25):16122-16127.   DOI
88 Sibbald, S.J. and J.M. Archibald. 2020. Genomic insights into plastid evolution. Genome Biology and Evolution 12(7): 978-990.   DOI
89 Diaz-Tapia, P., M.M. Pasella, H. Verbruggen and C.A. Maggs. 2019. Morphological evolution and classification of the red algal order Ceramiales inferred using plastid phylogenomics. Molecular Phylogenetics and Evolution 137:76-85.   DOI
90 Diaz-Tapia, P., C.A. Maggs, E.C. Macaya and H. Verbruggen. 2018. Widely distributed red aglae often represent hidden introductions, complexes of cryptic species or species with strong phylogeographic structure. Journal of Phycology 54(6):829-839.   DOI
91 Edge, M.D. and G. Coop. 2019. Reconstructing the history of polygenic scores using coalescent trees. Genetics 211:235-262.   DOI
92 Fehrer, J., B. Gemeinholzer and J.B.S. Chrtek. 2007. Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Molecular Phylogenetics and Evolution 42(2):347-361.   DOI
93 Tettelin, H., V. Masignani, M.J. Cieslewicz, C. Donati, D. Medini, N.L. Ward, S.V. Angiuoli, J. Crabtree, A.L. Jones, A.S. Durkin, R.T. DeBoy, T.M. Davidsen, M. Mora, M. Scarselli, I.M. Ros, J.D. Peterson, C.R. Hauser, J.P. Sundaram, W.C. Nelson, R. Madupu, L.M. Brinkac, R.J. Dodson, M.J. Rosovitz, S.A. Sullivan, S.C. Daugherty, D.H. Haft, J. Selengut, M.L. Gwinn, L. Zhou, N. Zafar, H. Khouri, D. Radune, G. Dimitrov, K. Watkins, K.J.B. O'Connor, S. Smith, J.L. Telford, M.R. Wessels, R. Rappuoli and C.M. Fraser. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proceedings of the National Academy of Sciences of the USA 102(39):13950-13955.   DOI
94 Jarvis, E.D., S. Mirarab, A.J. Aberer, B. Li, P. Houde, C. Li, S.Y.W. Ho, B.C. Faircloth, B. Nabholz, J.T. Howard, A. Suh, C.C. Weber, R.R. da Fonseca, J. Li, F. Zhang, H. Li, L. Zhou, N. Narula, L. Liu, G. Ganapathy, B. Boussau, M.S. Bayzid, V. Zavidovych, S. Subramanian, T. Gabaldon, S. Capella-Gutierrez, J. Huerta-Cepas, B. Rekepalli, K. Munch, M. Schierup, B. Lindow, W.C. Warren, D. Ray, R.E. Green, M.W. Bruford, X. Zhan, A. Dixon, S. Li, N. Li, Y. Huang, E.P. Derryberry, M.F. Bertelsen, F.H. Sheldon, R.T. Brumfield, C.V. Mello, P.V. Lovell, M. Wirthlin, M.P.C. Schneider, F. Prosdocimi, J.A. Samaniego, A.M.V. Velazquez, A. Alfaro-Nunez, P.F. Compos, B. Petersen, T. Sicheritz-Ponten, A. Pas, T. Bailey, P. Scofield, M. Bunce, D.M. Lambert, Q. Zhou, P. Perelman, A.C. Driskell, B. Shapiro, Z. Xiong, Y. Zeng, S. Liu, Z. Li, B. Liu, K. Wu, J. Xiao, X. Yinqi, Q. Zheng, Y. Zhang, H. Yang, J. Wang, L. Smeds, F.E. Rheindt, M. Braun, J. Fjeldsa, L. Orlando, F.K. Barker, K.A. Jonsson, W. Johnson, K.P. Keopfli, S. O'Brien, D. Haussler, O.A. Ryder, C. Rahbek, E. Willerslev, G.R. Graves, T.C. Glenn, J. McCormack, D. Burt, H. Ellegren, P. Alstrom, S.V. Edwards, A. Stamatakis, D.P. Mindell, J. Cracraft, E.L. Braun, T. Warnow, W. Jun, M.T.P. Gilbert and G. Zhang. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346(6215):1320-1331.   DOI
95 Freshwater, D.W., S. Fredericq, B.S. Butler, M.H. Hommersand and M.W. Chase. 1994. A gene phylogeny of the red algae (Rhodophyta) based on plastid rbcL. Proceedings of the National Academy of Sciences of the USA 91(15): 7281-7285.   DOI
96 Gabrielson, P.W., D.J. Garbary and R.F. Scagel. 1985. The nature of the ancestral red alga: inferences from a cladistic analysis. BioSystems 18(3-4):335-346.   DOI
97 Gibson, T.M., P.M. Shih, V.M. Cumming, W.W. Fischer, P.W. Crockford, M.S.W. Hodgskiss, S. Worndle, R.A. Creaser, R.H. Rainbird, T.M. Skulski and G.P. Halverson. 2018. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46(2):135-138.   DOI
98 Medlin, L.K., K. Metfies, U. John and J.L. Olsen. 2007. Algal molecular systematics: a review of the past and prospects for the future. In: J. Brodie and J. Lewis (eds.), Unravelling the algae: the past, present, and future of algal systematics, Taylor and Francis, Boca Raton, Florida. pp. 341-353.
99 Saunders, G.W. and K.V. Lehmkuhl. 2005. Molecular divergence and morphological diversity among four cryptic species of Plocamium (Plocamiales, Florideophyceae) in norther Europe. European Journal of Phycology 40(3):293-312.   DOI
100 Shapiro, B.J. 2017. The population genetics of pangenomes. Nature Microbiology 2(12):1574-1574.   DOI
101 Willis, A. and J.N. Woodhouse. 2020. Defining cyanobacterial species: diversity and description through genomics. Critical Reviews in Plant Science 39(2):101-124.   DOI
102 Lee, J.M., D. Kim, D. Bhattacharya and H.S. Yoon. 2019. Expansion of phycobilisome linker gene families in mesophilic red algae. Nature Communications 10:4823.   DOI
103 Giovagnetti, V. and A.V. Ruban. 2018. The evolution of the photoprotective antenna proteins in oxygenic photosynthetic eukaryotes. Biochemical Society Transaction 46(5): 1263-1277.   DOI
104 Lee, J.M., K.M. Kim, E.C. Yang, K.A. Miller, S.M. Boo, D. Bhattacharya and H.S. Yoon. 2016b. Reconstructing the complex evolutionary history of mobile plasmids in red algal genomes. Scientific Reports 6:23744.   DOI
105 Lee, J.M., E.C. Yang, L. Graf, J.H. Yang, H. Qiu, U. Zelzion, C.X. Chan, T.G. Stephens, A.P.M. Weber, G.H. Boo, S.M. Boo, K.M. Kim, Y. Shin, M. Jung, S.J. Lee, H.S. Yim, J.H. Lee, D. Bhattacharya and H.S. Yoon. 2018b. Analysis of the draft genome of the red seaweed Gracilariopsis chorda provides insights into genome size evolution in Rhodophyta. Molecular Biology and Evolution 35(8):1869-1886.   DOI
106 Song, H.J., J.M. Lee, L. Graf, M. Rho, H. Qiu, D. Bhattacharya and H.S. Yoon. 2016. A novice's guide to analyzing NGS-derived organelle and metagenome data. Algae 31(2):137-154.   DOI
107 Strassert, J.F.H., M. Jamy, A.P. Mylnikov, D.V. Tikhonenkov and F. Burki. 2019. New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life. Molecular Biology and Evolution 36(4):757-765.   DOI
108 Strassert, J.F.H., I. Irisarri, T.A. Williams and F. Burki. 2021. A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids. Nature Communications 12:1879.   DOI
109 Sun, M., D.E. Soltis, P.S. Solits, X. Zhu, J.G. Burleigh and Z. Chen. 2015. Deep phylogenetic incongruence in the angiosperm clade Rosidae. Molecular Phylogenetics and Evolution 83:156-166.   DOI
110 Yoon, H.S., J.D. Hackett and D. Bhattacharya. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proceedings of the National Academy of Sciences of the USA 99(18):11724-11729.   DOI
111 Lee, J.M., H.J. Song, S.I. Park, Y.M. Lee, S.Y. Jeong, T.O. Cho, J.H. Kim, H.G. Choi, C.G. Choi, W.A. Nelson, S. Fredericq, D. Bhattacharya and H.S. Yoon. 2018a. Mitochondrial and plastid genomes from coralline red algae provide insights into the incongruent evolutionary histories of organelles. Genome Biology and Evolution 10(11):2961-2972.   DOI
112 MacGuigan, D.J., A.J. Geneva and R.E. Glor. 2017. A genomic assessment of species boundaries and hybridization in a group of highly polymorphic anoles(distichus species complex). Ecology and Evolution 7(11):3657-3671.   DOI
113 Bhattacharya, D. and D.C. Price. 2020. The algal tree of life from a genomics perspective. In: A.W.D. Larkum, A.R. Grossman and J.A. Raven (eds.), Photosynthesis in algae: biochemical and physiological mechanisms, Springer, Cham, Switzerland. pp. 11-24.
114 Chan, C.X., E.C. Yang, T. Banerjee, H.S. Yoon, P.T. Martone, J.M. Estevez and D. Bhattacharya. 2011. Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Current Biology 21(4): 328-333.   DOI