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The JapaneseSocietyJapanese Society forforPlant Plant Systematics ISSNl346-7565 Acta Phytotax, Geobot.56 (l):11-20(2005) Invited article "Plants" Origin andEvolutionof as Deduced fromGenome Information HISAYOSHI NOZAKI Department ofBiologicat Seiences, Gradttate Schoot ofScience, qf' 7bk}'o, Hongo, Bunkyo-ku, 7bkyo 113-O033, JapanUhiversity Phylogenetic re]ationships between three lineages of the primary photosynthetic eukaryotes (red algae, green plants and glaucophytes) seemed to remain unresolved because previous nuclear multigene phylogenies used the incomplete red algal gene sequences. Recently, we canied out phylogenetic analy- ses based on a 1 525-amino-acid sequence of four concatenated nuclear genes from various lineages of only mitochondria-containing eukaryotes, using complete genome sequences from the red alga C}'anidioschyzon tnerolae. This study resolved two large monophyletic greups (groups A and B) and the basal group (Ameebozoa), GrQup A corresponded to the Opisthokonta (Metazoa and Fungi), where- as group B included various primury and secondary plastid-centaining lineages (euglenoids, het- erokonts, and apicomplexans), Ciliophora, Kinetoplastida, and Heterolobosea. The rod aLgae represented the most basal lineage within group B. Sincc the single event of the plastid primary endosymbiosis was strongly suggested by other data, it was considered that the primary plastid endosymbiosis likely eccurred once in the common ancestor of group B, and the primary plastids were subsequently lost in the ancestor(s) of organisms which now ]ack primary plastids within group B. A new concept of "Plantae" was proposed for photetrophic and nonphototrophic organisms belonging to group B, on the basis of the common history of the primary plastid endosymbiosis. nuclear endosymbiosis,secondary endesym- Key words: evelution , genes,phylogeny,plastids,primary biosis "primary Problems in previous nuclear multi- plants, glaucophytes and red algae are eukaryotes", whose may gene phylogeny of the primary photo- photosynthetic plastids synthetic eukaryotes have originated directly from a cyanobacterium- "primary like ancestor via endosymbiosis" (e,g,, The origin and diversity of plastids (chloroplasts) in Bhattacharya & Medlin 1995, Delwiche 1999, eukaryotic cells can be atuibuted to two types of McFadden 2001, Cavalier-Smith 2002a). By con- endosymbiotic events: primary endosymbiosis, and trast, the plastids of other lineages of eukaryotic secondary or tertiary endosymbiosis. The green phototrophs appear to be the result of secondary This article is formed frQm the presentation as one of contributions for the International Symposium 2004,Asian Plant - Diversity and Systernatics, held at Sakura, Chiba, Japan on July 29 August 2, 2004. NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics 12 APG ivbl, 56 or tertiary endosymbiotic events (involving a pho- strated the strong monophyly of red and green totrophic eukaryote and a host cell) because they are plants based on 13 nuclear genes, but they used surrounded by three or four bounding membranes, oomycete beta tubulin sequences and two cryp- and the endosymbiotic remnant of the phetosyn- tomonad nucleomorph (highly reduced red algal thetic eukaryotic nucleus, called the nucleomorph, nucleus after the plastid secondary endosymbio- may be recognized between the bounding mem- sis) sequences for the red aigal OTU, Therefbre, branes (e.g.,Delwiche ]999,McFadden 2001, nuclear gene sequences from free-living red algae, Cavalier-Smith 2002a, Ybon et al. 2002). Cavalier- especially from the Cyanidiophyceae, were needed Smith (1981, 2002b) classified only the primary to reso]ve reliable phylogenetic positions of the "Plantae'". photosynthetic eukaryotes as the kingdom three groups of the primary photosynthetic eukary- All of the plastids in eukaryotes can be considered otes. to be the preduct of a single primary endosymbiosis, basedon the phylogenetic analyses ofplastid-cod- Macrophylogeny using nuclear gene ing genes and the similarity of the plastid genome sequences obtained from the genome organization (e,g,, Morden et al. 1992, Nelissen et project of the red alga Cyanidioscltyzon al. 1995, Bhattacharya & Med]in 1995) and the conserved mosaic origin of Calvin cycle enzymes in Cemplete sequences of all of the three genomes, the red alga (lyanidioscdyzon and green plants (Matsu- mitochondrial (Ohta et aL 1998), plastid (Ohta et al. zaki et at. 2004), 2003) and nuclear (Matsuzaki et al. 2004) genomes, three Recently, phylogenetic studies of con- from Cly,anidiosch),zon merolae (Cyanidiophyceae) catenated amino acid sequences of mu]tiple nuclear were deterrnined for the first time in eukaryotic genes were carTied out (Moreira et al, 2000, Baldauf algae. Nozaki et aL (2003a) thus used complete et al. 2000, Bapteste et at. 2002), However, these sequences of the nuclear genes from C. merolae studies included only a single red algal OTU main- for deducing the natural phylogenetic relationships ly derivedfrom Porphyra. Although the red algae between the three primary photosynthetic eukary- were traditionally assigned to the single class otes. The alignment of four nuclear genes used by Rhodophyceae comprised of two subclasses, the Baldauf et al. (2000) was used, but nucleomorph Bangiophycidae (includin.u Potph.yra and C>'ani- sequences and amitochondrial sequences were dioschyzon)and the Florideophycidae (e. g. Bold & excluded because these highly divergent gene recent Wynne 19g5), molecular phylogenetic analy- sequences seem te exhibit unusual substitutions, ses demonstrated that the Bangiophycidae are para- which can cause long-branch attraction or unnatur- phyletic, and the red algae are composed of two sis- al phylogenetic resolution (see Van de Peer et at. ter clades (e,g., Ciniglia et at, 2004), which can be 1996, Stiller et al. 2001). Therefore, only mito- assigned to the Rhodophyceae (including Perphyra ehondria-containing eukaryotes were ana]yzed and Florideophyceae) and Cyanidophyceae (includ-(Nozaki et aL 2003a). ing Cyanidioschyzon and other acid hot spring red Since it was generally considered that the ami- algae). Baldauf et al. (2000) used four nuclear tochondrial eukaryotes represent the most basal genes of a 1arge number of OTUs from various eukaryotes (see Cavalier-Smith 1998) (Fig. 1), eukaryotes. However, the phylogenetic position exclusion of such organisms from eukaryotic macro- of the red alga was ambiguous, possibly because phylogenies seemed to result in dithculty for des- only a single OTU was analyzed and its sequences ignating the outgroup. In order to resolve basal were incomplete. Moreira et al. (2000) demon- mitochondria-centaining eukaryotes, however, NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics "plants" April 2005 NOZAKI: Origin and evolution of 13 r Secondary phototrophs tt/ FIG. 1. Diagrams of plastid and mitochondriaE endosymbioses and evo]ution of eukaryotes (based on Cavalier-Smith 1998), N, nuc]e- us; m, mitochondrien. Nozaki et al. (2003a) canied out the paralogous from 40 mitochondria-containing organisms with comparison of the combined data set from alpha- those of reversibly concatenated alpha- and beta- and beta-tubulin sequences. The alpha- and beta- tubulin genes from the same 40 organisms. The tubuiin genes may have originated from gene dupli- alignment was carried out according to McKean cation, after the origin of eukaryotes (Edlind et at. et aL (2001). After removing the gaps, 560 amino 1996, Keeling & Doolittle 1 996). Therefore, basal acids from 80 OTUs, in total, were used fbr phylo- eukaryotic organisms can be deduced from a phy- genetic analyses (Nozaki et al. 2003a). Figure 2 logenetic comparison of these two genes Csee Iwabe shows the phylogenetic tree constructed using the et al. 1989). In erder to increase the phylogenetic concatenated amino acid sequences of the alpha- and information, Nozaki et at, (2003a) aligned con- beta-tubulin genes, [[iwo identical subtrees are the- catenated sequences of these two paralogous genes oretically resolved. High bootstrap values resolyed NII-Electronic Library Service The JapaneseSocietyJapanese Society for Plant Systematics 14 APG Vbl.56 Hemo Danio 9971 :t;sMso:IZila thenorhabditis S6 62 Histriculus iVeurospora stndidb ccharenryces * 86 " Sbhizosaccharompees 6 Ps'le#f,m.oewtistum * PhaeoRoant:iiZSscltyzon eae Red algae Arabidopsis 4(796 veagaenlarrEpdomonas Yblvex 56- ptosporidium 53{-) de pfbsmS}IIum Eimeria .7bpX lalasma a-tueMilin B-tubulin t denuis m m rmophila . meetum 70 8185 eizxep es A9,X.Y,i･,richidae Mffglat.e."t.'" lee{loe)94 7fi(.) Lelshmania lppanosomabrucgicruu pig,sarum-itmpanosoma 84(99) D.c-fe:$s:iae'z,. Cellular s]ime molds 99 Acytostelium Hbmo Danio gg gg S9.M,em ila 7bethothenorhabditis 86 e4 IVle"rospera Htstricutttskecharofiij,ees Chndide S6 68 Pneumt ± :g/Z/utttZOSaCCharontyces Phaeop -Red bygn zon algae Arahidurp SISwr.e,a,fa,Schizop 92-6 9z/:acalaaydbmen"s 52 Fbtvox PlasmM mtOsporidium su Eimeria lbxoplasma B-tubulin a-tufutiei:a Cbipvda . m t 7e 82 !ll.lz'`.for:'eeM,/f/t.ta 85 E otesO richidae 7 .)ilS!glena Leishmania de !}l&1'."."re,M.".b.r.".C:ef,' Acrasis fVlaegtaeria --10changes Pijysarum 2 9999 ttSKzti-.eLi,ulynti'..Cel]ular s]ime molds Acytostetiumm FiG. 2. 0ne of the four most parsimonious tiees ofconcatenated paralogous genes (alpha- and beta-tubulin genes) from 40 mitochonchia- containing organisms based on the unamblguously aligned 560 amino acids, with reversibly concatenated alpha- and