Evolution of the Chlorophyta: Insights from Chloroplast Phylogenomic Analyses

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Evolution of the Chlorophyta: Insights from Chloroplast Phylogenomic Analyses Journal of Systematics JSE and Evolution doi: 10.1111/jse.12248 Review Evolution of the Chlorophyta: Insights from chloroplast phylogenomic analyses Ling Fang1, Frederik Leliaert2,3, Zhen-Hua Zhang1, David Penny4, and Bo-Jian Zhong1* 1College of Life Sciences, Nanjing Normal University, Nanjing 210023, China 2Botanic Garden Meise, 1860 Meise, Belgium 3Phycology Research Group, Biology Department, Ghent University, 9000 Ghent, Belgium 4Institute of Fundamental Sciences, Massey University, Palmerston North 4442, New Zealand *Author for correspondence. E-mail: [email protected]. Tel.: 86-25-85891726. Received 6 January 2017; Accepted 4 March 2017; Article first published online 5 May 2017 Abstract Green plants comprise two main clades: the Streptophyta, which include charophyte green algae and the embryophytic land plants, and the Chlorophyta including a wide diversity of marine, freshwater, and terrestrial green algae. Establishing a robust phylogeny is important to provide an evolutionary framework for comparative and functional studies. During the last two decades our understanding of the evolution of green algae has profoundly changed, first by phylogenetic analyses of nuclear ribosomal sequence data (mainly 18S), and more recently by analyses of multi-gene and chloroplast genomic data. The phylogenetic relationships among the main streptophytan lineages have been extensively studied and are now relatively well resolved. Although a lot of progress has been made in the last few years, the phylogenetic relationships in the Chlorophyta are still less well established. Here we review how chloroplast genomic data have contributed to address relationships among the main chlorophytan lineages. We highlight recent progress and conflicts among different studies, and discuss future directions in chloroplast phylogenomics of green algae. Key words: Chlorophyta, chloroplast genome, green algae, model evaluation, phylogenomics. 1 Introduction Neoproterozoic era, where unicellular planktonic algae (known as prasinophytes) diversified in the oceans, and Green algae are morphologically and ecologically diverse and later gave rise to the core chlorophytes that radiated in ubiquitous in marine, freshwater, and terrestrial habitats coastal, freshwater, and terrestrial environments, and today (Graham et al., 2009). They are not a monophyletic group but contain most of the species (Leliaert et al., 2011, 2012). belong to the green plants, an ancient lineage of eukaryotes Extant prasinophytes form a paraphyletic assemblage of comprising two main clades. One clade, the Streptophyta, planktonic unicellular green algae with a wide variety of cell include mostly freshwater green algae (known as charo- shapes, flagellar numbers and behavior, body scale mor- phytes) and the land plants. The other clade, the Chlorophyta, phologies, mitotic processes, and photosynthetic pigments, include marine, freshwater, and terrestrial green algae with a and are living both in oceanic and freshwater environments. wide morphological diversity, ranging from planktonic This wide diversity in conserved phenotypic features unicellular organisms, to colonial, multicellular, and siphonous supports the notion that prasinophytes are ancient lineages. algae. The divergence between the Streptophyta and The core Chlorophyta include three major classes, Chlor- Chlorophyta is estimated to have taken place more than 1 ophyceae,Ulvophyceae,andTrebouxiophyceae,plusthe billion years ago (Leliaert et al., 2011; Moczydłowska et al., two smaller lineages, the Chlorodendrophyceae, comprising 2011). The phylogenetic relationships among the main the scaly quadriflagellates Tetraselmis and Scherffelia from charophyte clades, and especially the relationship with the freshwater, brackish water, marine, and hypersaline habitats land plants, have been extensively investigated and reviewed (Norris et al., 1980; Arora et al., 2013) and Pedinophyceae, (e.g., Cooper, 2014; Delwiche & Cooper, 2015; Zhong et al., which include asymmetric, uniflagellate, mostly naked green 2015). It is now well established that the Zygnematophyceae algae from marine, freshwater, or soil habitats (Marin, 2012) are the sister clade to the land plants (Timme & Delwiche, (Fig. 1). The classes Chlorophyceae, Ulvophyceae, and 2010; Wodniok et al., 2011; Timme et al., 2012; Zhong et al., Trebouxiophyceae are species-rich and morphologically 2013; Wickett et al., 2014). and ecologically diverse. The Chlorophyceae include fresh- The Chlorophyta include ecologically, morphologically, water and terrestrial green algae displaying diverse cell and cytologically diverse green algae. The early evolutionary organizations and variable ultrastructure of the flagellar history of the clade likely took place in the Meso- and apparatus (Lewis & McCourt, 2004). The Ulvophyceae © 2017 Institute of Botany, Chinese Academy of Sciences July 2017 | Volume 55 | Issue 4 | 322–332 Chloroplast phylogenomics of the Chlorophyta 323 Chlorophyceae Ulvophyceae Core Trebouxiophyceae Trebouxiophyceae Chlorellales Chlorodendrophyceae Core Chloropyhta Chloropyhta Pedinophyceae Prasinophytes Charophyte Green Algae and Land Plants Fig. 1. Phylogeny of Chlorophyta inferred from chloroplast genomic data. Dashed and solid lines indicate uncertain and established relationships, respectively. include mostly macroscopic, multicellular, or siphonous phylogenomic studies aiming to resolve ancient relation- species from coastal habitats, but also many microscopic ships in land plants (Wu et al., 2013; Ruhfel et al., 2014; Lu unicellular or multicellular species from marine, freshwater, et al., 2015). In addition, more realistic substitution models and terrestrial environments (Cocquyt et al., 2010). The of sequence evolution are applied for chloroplast phyloge- Trebouxiophyceae, a class that was circumscribed mainly nomic analyses. For example, in the streptophytan lineage, based on ultrastructural features and nuclear ribosomal DNA Cox et al. (2014) reported the monophyletic phylogeny of sequence data (Mattox & Stewart, 1984; Kantz et al., 1990), the bryophytes (an early diverging land plant lineage) using encompass motile and non-motile unicellular, colonial, and the chloroplast genomes by correcting the phylogenetic multicellular green algae from freshwater, terrestrial, and artifacts, which is caused by mutation-driven compositional sometimes marine habitats, with several species engaging in biases and synonymous substitutions. Zhong et al. (2014) symbiosis with a diversity of eukaryotes (Lewis & McCourt, analyzed the chloroplast genomes of land plants and 2004; Leliaert et al., 2012). charophytes, and phylogenomic analyses supported that A reliable phylogenetic tree of Chlorophyta is important to Zygnematophyceae are the closest relatives to the land understand the early evolution of green algae. However, plants, which is congruent with recent large-scale phylo- resolving the phylogenetic relationships among the major transcriptomic analyses (Wodniok et al., 2011; Timme et al., clades of the Chlorophyta has been shown to be a difficult 2012; Wickett et al., 2014). task, because these ancient lineages radiated rapidly, and In this review, we summarize recent progress in chloroplast possible multiple extinction events occurred from ancient phylogenomic analyses of Chlorophyta, discuss potential lineages (Cocquyt et al., 2010). Ultrastructural data, and errors/biases limiting the resolution of phylogenomic infer- nuclear ribosomal, chloroplast, and mitochondrial sequence ence, and provide further directions to improve the data have yielded ambivalent results (reviewed in Leliaert phylogenetic accuracy of Chlorophyta both by adding critical et al., 2012). Adding to the complexity, the monophyly of the taxa and using more appropriate evolutionary models. Ulvophyceae and Trebouxiophyceae has been questioned. Initial molecular phylogenetic studies investigated the rela- tionships among green algal lineages using a single gene, 2 Chloroplast Phylogenomics of Chloro- mostly the nuclear small subunit ribosomal RNA gene (18S) (Fawley et al., 2000; Krienitz et al., 2001; Muller€ et al., 2004; phyta Bock et al., 2013). It is now apparent that multiple genes from 2.1 Phylogenetic relationship of the prasinophytes many species are the premise to fully resolve ancient Approximately 10 clades of the prasinophytes have been phylogenetic relationships (Philippe & Telford, 2006; Philippe identified based on 18S rDNA sequences (Leliaert et al., 2011). et al., 2011). Although 18S data clearly showed that prasinophytes Chloroplast genomes are particularly useful for phyloge- comprise the earliest diverging lineages of the Chlorophyta, netic reconstruction because of their highly conserved and the affinities among prasinophyte clades are difficult to condensed gene content and their typical mode of resolve (Fawley et al., 2000; Guillou et al., 2004; Marin & uniparental inheritance. Moreover, chloroplast genes are Melkonian, 2010). typically single-copy, in contrast to nuclear genes that are Chloroplast genomic data and increased taxon sampling multi-copy in nature, which can mislead phylogenetic of prasinophytes have greatly improved our understanding inference. Another advantage is that chloroplast genes of early chlorophytan relationships (Turmel et al., 2009a; lack the multiple and often long introns typically found in Lemieux et al., 2014a; Leliaert et al., 2016). Current nuclear genes. Chloroplast genomic data is dramatically understanding of phylogenetic relationships and uncertainties
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