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Red and Green Algal Monophyly and Extensive Gene Sharing Found in a Rich Repertoire of Red Algal Genes

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Red and Green Algal Monophyly and Extensive Gene Sharing Found in a Rich Repertoire of Red Algal Genes Current Biology 21, 328–333, February 22, 2011 ª2011 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2011.01.037 Report Red and Green Algal Monophyly and Extensive Gene Sharing Found in a Rich Repertoire of Red Algal Genes Cheong Xin Chan,1,5 Eun Chan Yang,2,5 Titas Banerjee,1 sequences in our local database, in which we included the Hwan Su Yoon,2,* Patrick T. Martone,3 Jose´ M. Estevez,4 23,961 predicted proteins from C. tuberculosum (see Table and Debashish Bhattacharya1,* S1 available online). Of these hits, 9,822 proteins (72.1%, 1Department of Ecology, Evolution, and Natural Resources including many P. cruentum paralogs) were present in C. tuber- and Institute of Marine and Coastal Sciences, Rutgers culosum and/or other red algae, 6,392 (46.9%) were shared University, New Brunswick, NJ 08901, USA with C. merolae, and 1,609 were found only in red algae. A total 2Bigelow Laboratory for Ocean Sciences, West Boothbay of 1,409 proteins had hits only to red algae and one other Harbor, ME 04575, USA phylum. Using this repertoire, we adopted a simplified recip- 3Department of Botany, University of British Columbia, 6270 rocal BLAST best-hits approach to study the pattern of exclu- University Boulevard, Vancouver, BC V6T 1Z4, Canada sive gene sharing between red algae and other phyla (see 4Instituto de Fisiologı´a, Biologı´a Molecular y Neurociencias Experimental Procedures). We found that 644 proteins showed (IFIBYNE UBA-CONICET), Facultad de Ciencias Exactas y evidence of exclusive gene sharing with red algae. Of these, Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, 145 (23%) were found only in red + green algae (hereafter, Argentina RG) and 139 (22%) only in red + Alveolata (Figure 1A). In comparison, we found only 34 (5%) proteins in red + Glauco- phyta, likely as a result of the limited availability of glaucophyte Summary data in the database. As we restricted this search by requiring a larger number of hits per query (x) from both phyla, the The Plantae comprising red, green (including land plants), proportion of RG proteins increased relative to other taxa. and glaucophyte algae are postulated to have a single For instance, the number of red + Alveolata and red + Metazoa common ancestor that is the founding lineage of photosyn- proteins was reduced from 139/1/0 and from 55/3/ thetic eukaryotes [1, 2]. However, recent multiprotein 0 when x R 2 (644 proteins), x R 10 (96 proteins), and x R 20 phylogenies provide little [3, 4]orno[5, 6] support for this (22 proteins), respectively (Figures 1A–1C). This BLASTp hypothesis. This may reflect limited complete genome data analysis is based on the implicit assumption that significant available for red algae, currently only the highly reduced similarity among a group of sequences indicates a putative genome of Cyanidioschyzon merolae [7], a reticulate gene homologous relationship (i.e., a shared common ancestry). ancestry [5], or variable gene divergence rates that mislead This approach could potentially be misled by convergence at phylogenetic inference [8]. Here, using novel genome data the amino acid level that results in high similarity among non- from the mesophilic Porphyridium cruentum and Calliar- homologous sequences (i.e., homoplasy [9, 10]). Alternatively, thron tuberculosum, we analyze 60,000 novel red algal genes because RG are primarily photoautotrophs, exclusive gene to test the monophyly of red + green (RG) algae and their sharing could be explained by these lineages having retained extent of gene sharing with other lineages. Using a gene- a common set of ancestral genes that were lost in other eukary- by-gene approach, we find an emerging signal of RG otes. With these potential issues in mind, we suggest that monophyly (supported by w50% of the examined protein exclusive gene sharing (as defined by significant reciprocal phylogenies) that increases with the number of distinct BLASTp hits) provisionally favors the RG grouping. phyla and terminal taxa in the analysis. A total of 1,808 phylogenies show evidence of gene sharing between Gene Sharing between RG and Other Lineages Plantae and other lineages. We demonstrate that a rich meso- Using a phylogenomic approach, we generated maximum- philic red algal gene repertoire is crucial for testing contro- likelihood (ML) trees for each of the 13,632 P. cruentum versial issues in eukaryote evolution and for understanding proteins with significant hits to the local database. One of the complex patterns of gene inheritance in protists. the major confounding issues in phylogenomic analysis is inadequate and/or biased taxon sampling. To reduce such biases in our inference of gene phylogeny, we restricted our Results and Discussion analysis to trees that contain R3 phyla (per tree) and analyzed these phylogenies based on the minimum number of terminal Assessing Red and Green Algal Monophyly Based taxa per tree (n), ranging from 4 to 40 (Figure 1D). The expec- on Exclusive Gene Sharing tation was that the impact of inadequate taxon sampling Here, with 36,167 expressed sequence-tagged (EST) unigenes on our interpretation of the data would be minimal in trees from Porphyridium cruentum and 23,961 predicted proteins with large n. Applying these restrictions, n R 4 returned from Calliarthron tuberculosum, we report analyses of 1,367 trees that contained red algae positioned within >60,000 novel genes from mesophilic red algae. Of the 36,167 a strongly supported (bootstrap R 90%) monophyletic clade P. cruentum unigenes (6.7-fold greater than the gene number (Figure 1D); the majority of these trees (1,129 of 1,367; 83%) [5,331] from Cyanidioschyzon merolae [7]), 13,632 encode had n R 10. Among the 1,367 trees, 329 showed exclusive proteins with significant BLASTp hits (e value % 10210)to RG monophyly, of which 53 trees defined RG + glaucophytes (i.e., were putatively Plantae-specific). The number of trees *Correspondence: [email protected] (H.S.Y.), bhattacharya@aesop. that recovered the RG remained similar between cases of rutgers.edu (D.B.) n R 4 and n R 10, with only 71 trees having n between 4 and 5These authors contributed equally to this work 9. As n increased, the proportion of RG groupings remained Assessing Red and Green Algal Monophyly 329 Rhodophyta-Cyanidioschyzon merolae CMT191C A A 81 Rhodophyta-Cyanidioschyzon merolae CMT574C Rhodophyta-Calliarthron tuberculosum g9362t1 Viridiplantae-Chlamydomonas reinhardtii gi159472571 100 Viridiplantae-Chlorella NC64A jgi20786 100 Viridiplantae-Chlorella NC64A jgi23974 Viridiplantae-Chlorella vulgaris jgi77486 Viridiplantae-Physcomitrella patens subsp patens gi168035809 68 Viridiplantae-Oryza sativa Japonica Group gi115459498 Viridiplantae-Zea mays gi226491452 97 Viridiplantae-Sorghum bicolor gi242073740 Viridiplantae-Ricinus communis gi255577977 100 100 Viridiplantae-Sorghum bicolor gi242043424 Viridiplantae-Oryza sativa Japonica Group gi115471329 Viridiplantae-Vitis vinifera gi225440504 100 Viridiplantae-Arabidopsis thaliana gi79324637 Viridiplantae-Arabidopsis lyrata jgi482793 92 100 Viridiplantae-Vitis vinifera gi225436365 Viridiplantae-Populus trichocarpa gi224103009 B Viridiplantae-Arabidopsis lyrata jgi326573 97 Viridiplantae-Arabidopsis thaliana gi15242979 98 Viridiplantae-Chlamydomonas reinhardtii gi159473677 96 Viridiplantae-Volvox carteri jgi106345 72 Viridiplantae-Chlorella vulgaris jgi72495 61 Viridiplantae-Chlorella NC64A jgi137672 Viridiplantae-Ostreococcus tauri gi116055893 Viridiplantae-Chlorella vulgaris jgi84560 93 92 Viridiplantae-Micromonas pusilla CCMP1545 gi303278506 100 Viridiplantae-Micromonas sp. RCC299 gi255076153 Viridiplantae-Ostreococcus lucimarinus CCE9901 gi145349444 Glaucophyta-Cyanophora paradoxa Contig638 4 Rhodophyta-Cyanidioschyzon merolae CMM247C 67 Viridiplantae-Physcomitrella patens subsp. patens gi168028204 Viridiplantae-Physcomitrella patens subsp. patens gi168034841 63 Viridiplantae-Ricinus communis gi255553448 C Viridiplantae-Populus trichocarpa gi224059600 99 Viridiplantae-Vitis vinifera gi225435391 100 Viridiplantae-Arabidopsis thaliana gi18416870 69 Viridiplantae-Arabidopsis lyrata jgi909228 92 Viridiplantae-Populus trichocarpa gi224104171 91Viridiplantae-Populus trichocarpa gi224059548 93 82 Viridiplantae-Ricinus communis gi255544908 100 Viridiplantae-Sorghum bicolor gi242087801 100 Viridiplantae-Zea mays gi226529786 Viridiplantae-Oryza sativa Japonica Group gi115463661 62 93 100 Viridiplantae-Zea mays gi226533441 Viridiplantae-Sorghum bicolor gi242059969 D 98 Viridiplantae-Oryza sativa Japonica Group gi115442333 90 Viridiplantae-Vitis vinifera gi225450009 100 Viridiplantae-Chlamydomonas reinhardtii gi159490938 100 Viridiplantae-Volvox carteri jgi79235 Viridiplantae-Chlorella vulgaris jgi81458 91 Viridiplantae-Arabidopsis thaliana gi22331818 90 100 Viridiplantae-Arabidopsis lyrata jgi483095 87 Viridiplantae-Zea mays gi212274441 Viridiplantae-Physcomitrella patens jgi20837 Glaucophyta-Glaucocystis nostochinearum GNL00002567 1 66 Rhodophyta-Porphyridium cruentum Contig9125 2 97 Rhodophyta-Cyanidioschyzon merolae CMX001C 91 Rhodophyta-Calliarthron tuberculosum g6851t1 Rhodophyta-Porphyra haitanensis 61663183 2 0.5 substitutions/site 60 Phaeodactylum tricornutum gi219125311 100 Thalassiosira pseudonana gi219125311 STRAMENOPILES B 91 Fragilariopsis cylindrus jgi206207 96 88 Rhodophyta-Galdieria sulphuraria Gs42470.1 69 Rhodophyta-Cyanidioschyzon merolae CMT608C Glaucophyta-Cyanophora paradoxa Contig23 4 95 Viridiplantae-Sorghum bicolor gi242062504 Viridiplantae-Zea mays gi226496273 98 Viridiplantae-Arabidopsis thaliana gi15223439
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