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Phylogenomic Analysis Restructures the Ulvophyceae1

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Phylogenomic Analysis Restructures the Ulvophyceae1 J. Phycol. *, ***–*** (2021) © 2021 The Authors. Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. DOI: 10.1111/jpy.13168-20-145 PHYLOGENOMIC ANALYSIS RESTRUCTURES THE ULVOPHYCEAE1 Øyvind Sætren Gulbrandsen Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Kristine Bonnevies Hus, Blindernveien 31, 0316 Oslo, Norway Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Centre for Integrative Genetics, Norwegian University of Life Sciences, As, Norway Ina Jungersen Andresen , Anders Kristian Krabberød Centre for Integrative Microbial Evolution (CIME), Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Kristine Bonnevies Hus, Blindernveien 31, 0316 Oslo, Norway Jon Brate 2 Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Kristine Bonnevies Hus, Blindernveien 31, 0316 Oslo, Norway Department of Virology, Norwegian Institute of Public Health, Oslo, Norway and Kamran Shalchian-Tabrizi2 Centre for Integrative Microbial Evolution (CIME), Centre for Epigenetics, Development and Evolution (CEDE), Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Kristine Bonnevies Hus, Blindernveien 31, 0316 Oslo, Norway Here, we present new transcriptome sequencing green algae; phylogeny; Scotinosphaerales; transcrip- data from seven species of Dasycladales tomics; Ulvophyceae (Ulvophyceae) and a phylogenomic analysis of the Abbreviations: Burki250, 250 gene alignment from Chlorophyta with a particular focus on Ulvophyceae. Burki et al. (2016); ML, maximum likelihood; We have focused on a broad selection of green algal MLBS, multilocus bootstrap support; MMETSP, groups and carefully selected genes suitable for Marine Microbial Eukaryote Transcriptome Sequenc- reconstructing deep eukaryote evolutionary histories. ing Project; NPP, Abbreviation for the genera Increasing the taxon sampling of Dasycladales Nephroselmis, Pycnococcus, and Picocystis; UTC, Clade restructures the Ulvophyceae by identifying consisting of the classes Ulvophyceae, Trebouxioph- Dasycladales as closely related to Scotinosphaerales cyeae and Chlorophyceae. and Oltmannsiellopsidales. Contrary to previous studies, we do not find support for a close relationship between Dasycladales and a group with Cladophorales Dasycladales is a group of single-celled green and Trentepohliales. Instead, the latter group is sister algae with an astonishing adaptation to a macro- to the remainder of the Ulvophyceae. Furthermore, scopic lifestyle. Species of Dasycladales consist of our analyses show high and consistent statistical only a single cell, yet they can grow over ten cen- support for a sister relationship between Bryopsidales timeters in size and display highly elaborate mor- and Chlorophyceae in trees generated with both phological structures (Berger 2006). Dasycladales is homogeneous and heterogeneous (heterotachy) part of the class Ulvophyceae which belongs to the evolutionary models. Our study provides a new Chlorophyta. The phylogeny of Chlorophyta has his- framework for interpreting the evolutionary history of torically been subjected to significant changes and Ulvophyceae and the evolution of cellular uncertainties (Fang et al. 2017). In the most recent morphologies. revision of eukaryote systematics (Adl et al. 2019), Key index words: Acetabularia; Bryopsidales; Chloro- Chlorophyta is divided into eleven classes. Among phyta; cytomorphology; Dasycladales; evolution; these, Ulvophyceae, Trebouxiophyceae, Chloro- phyceae, Pedinophyceae, and Chlorodendrophyceae 1Received 19 June 2020. Revised 26 January 2021. Accepted 3 Feb- make up a monophyletic assemblage coined “Core ruary 2021. Chlorophyta” (Leliaert et al. 2016, Fang et al. 2017, 2Author for correspondence: e-mails [email protected] (J.B.); [email protected] (K.S.). Del Cortona et al. 2020). Within the Core Chloro- Editorial Responsibility: H. Verbruggen (Associate Editor) phyta, a large group composed of Ulvophyceae, 1 2 ØYVIND SÆTREN GULBRANDSEN ET AL. Trebouxiophyceae, and Chlorophyceae (the UTC two families, Dasycladaceae and Polyphysaceae, with clade) is especially well studied due to its large spe- species of very different cellular morphologies (Ber- cies diversity and ecological importance. ger 2006), and it is therefore important to increase Ulvophyceae hosts a wide array of different cellular the sampling of taxa across Dasycladales and morphologies (cytomorphologies) and is therefore a include representatives of both families. Another unique model system for studying morphological reason is the long and independent evolutionary and cytomorphological diversification (Verbruggen histories of the different lineages within Ulvo- et al. 2009). Among the Ulvophyceae, cytomorpholo- phyceae, exhibiting a pattern of rapid and ancient gies range from small unicellular species, such as radiations (Del Cortona et al. 2020), possibly also Scotinosphaerales, to large multicellular species, such followed by several extinction events (Berger et al. as the sea lettuce Ulva, to the gigantic single-celled 2003, Fang et al. 2017). For these reasons, most species (up to meters in size) of Bryopsidales and ulvophycean groups have very long branches in Dasycladales. However, the evolutionary relationships molecular phylogenies, making them prone to long- between the different groups of Ulvophyceae are branch attraction artifacts. uncertain, and even the monophyly of the entire To shed light on the evolution of macroscopic class has recently been contested (Leebens-Mack cytomorphologies in Ulvophyceae, the main aim of et al. 2019, Del Cortona et al. 2020). this study was to resolve the phylogeny of the whole Notably, the position of Dasycladales and their group, with a particular focus on the position of most closely related lineages within Ulvophyceae has Dasycladales and Bryopsidales. To address this, we never been fully resolved. Dasycladales have tradi- have improved the representation of Dasycladales by tionally been regarded as closely related to Bryopsi- sequencing the transcriptomes of seven species from dales because of shared cytomorphological traits five different genera covering both the families Poly- such as extremely large, single-celled siphonous spe- physaceae and Dasycladaceae. And to overcome the cies (i.e., macroscopic, single-celled organisms with challenges posed by the long, independent evolu- cytoplasmic streaming and sometimes multiple tionary histories of the chlorophyte classes, we have nuclei; e.g., Verbruggen et al. 2009, Coneva and elected for a conservative approach where we Chitwood 2015). A sister relationship between these selected only slowly evolving single-copy eukaryote two groups would imply that the single-celled genes, removed fast-evolving sites, and minimized macroscopic cytomorphology has only originated the amount of missing data. once within Ulvophyceae (Cocquyt et al. 2010b). However, several chloroplast and nuclear gene phy- logenies over the past decade have shown dis- METHODS crepant placements of Bryopsidales, questioning Dasycladales cultures. Seven species of Dasycladales their sister relationship to Dasycladales and their (Table 1) were kept in culture at the Institute of Biosciences, position within the UTC (Fucıkova et al. 2014, Leli- University of Oslo, in Dasycladales seawater medium prepared aert and Lopez-Bautista 2015, Leliaert et al. 2016, after the recipe of UTEX Culture Collection of Algae. Cul- tures were kept in incubators with a 12:12 h light:dark cycle Turmel et al. 2017). A deeper position within UTC, at a temperature of 20°C, and a light intensity of 2,500 lux. as seen recently (Leebens-Mack et al. 2019, Del Cor- tona et al. 2020), would instead suggest indepen- dent origins of the macroscopic cytomorphologies TABLE 1. Species of Dasycladales investigated in this study. of Dasycladales and Bryopsidales. Furthermore, several ulvophycean lineages are Species UTEXID Family Order unstable in molecular trees, such as the Ignatiales, — Oltmannsiellopsidales, and the Cladophorales/Tren- Acetabularia Polyphysaceae Dasycladales acetabulum tepohliales clade (Fucıkova et al. 2014, Del Cortona Acetabularia crenulata — Polyphysaceae Dasycladales et al. 2020). As a consequence, it is difficult to infer Acetabularia peniculus — Polyphysaceae Dasycladales the ancestral cytomorphology of Ulvophyceae and Parvocaulis LB Polyphysaceae Dasycladales a the cytomorphological origins of Dasycladales. polyphysoides 2707 Bornetella oligospora LB Dasycladaceae Dasycladales Resolving the uncertainties regarding the exact posi- 2689 tion of Dasycladales and its sister groups among Chloroclados LB Dasycladaceae Dasycladales Ulvophyceae, as well as the position of Bryopsidales australasicus 2686 in relation to Ulvophyceae, is a key to understand Neomeris dumetosa LB Dasycladaceae Dasycladales the evolution of large, siphonous cell forms and the 2691 different adaptations to a macroscopic lifestyle Except for the Acetabularia species (identified and provided among green algae. by Prof. W. Martin of the University of Dusseldorf),€ the spe- One reason
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