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Rates and Patterns of Bryophyte Molecular Evolution Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1850 Rates and patterns of bryophyte molecular evolution ANNA-MALIN LINDE ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-0740-4 UPPSALA urn:nbn:se:uu:diva-392462 2019 Dissertation presented at Uppsala University to be publicly examined in Zootissalen, EBC, Villavägen 9, Uppsala, Wednesday, 23 October 2019 at 10:00 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Professor Jonathan Shaw (Duke University). Abstract Linde, A.-M. 2019. Rates and patterns of bryophyte molecular evolution. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1850. 42 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0740-4. Plants have been growing on land for at least 450 million years. The bryophytes comprising the three phyla liverworts, mosses and hornworts, are considered to be the closest extant relatives to the plants that colonized land. Bryophytes has been described as evolutionary “unchanging sphinxes of the past” regarding both morphological and genetic potential. This suggestion has some support in limited studies of molecular evolution within bryophytes, but has also been questioned based on e.g., studies of species diversification rates. To shed more light on this controversy, the overall aim of this thesis is to investigate rates and patterns of bryophyte molecular evolution. Our data suggest that the per nucleotide mutation rates in bryophytes are lower than those in angiosperms. Likewise, angiosperms are also more dynamic in terms of genome size, structural rearrangements, genome duplications and transposon activity. However, our data show that mutation rates of bryophytes are higher or at least on par with those of gymnosperms. Genome evolution in bryophytes is actually, in many aspects, similar to that of gymnosperms. Gymnosperms and bryophytes are both characterized by a low speciation rate, a low nucleotide mutation rate, low variation in chromosome numbers and relatively stable genome sizes. Studies have also suggested that macrosynteny is better conserved between conifer species compared with angiosperms, just as this study shows for bryophytes. Hybridization and introgression has been suggested to affect speciation and evolution. Recent genomic data shows that hybridization and introgression in angiosperms is more common then previously thought, but the question is less well studied in bryophytes. The present study gave some support to the occurrence of introgression between Marchantia polymorpha subspecies, but refute a previous hypothesis that M. polymorpha subsp. ruderalis is a new stabilized hybrid between M. polymorpha montivagans and polymorpha. An additional aspect of genome evolution and complexity is changes in gene regulatory networks. Gene regulatory networks generally appear more complex in angiosperms compared with bryophytes; also reflected in the circadian clock; with more gene components and more duplicated paralogous members, with possibly overlapping function, allowing a more robust and flexible system. Our studies of the plant circadian clock revealed that orthologs of most genes of the A. thaliana clock were present already in charophycean algae. Although gene numbers and complexity have generally increased during plant circadian clock evolution, our results suggest that gene loss has also been important in shaping the circadian clocks in the three bryophyte groups. Anna-Malin Linde, Department of Ecology and Genetics, Plant Ecology and Evolution, Norbyvägen 18 D, Uppsala University, SE-752 36 Uppsala, Sweden. © Anna-Malin Linde 2019 ISSN 1651-6214 ISBN 978-91-513-0740-4 urn:nbn:se:uu:diva-392462 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-392462) List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Linde, A-M., Sawangproh, W., Cronberg, N., Szövényi, P., & Lagercrantz, U. Evolutionary history of the Marchantia polymorpha complex. Manuscript II Linde, A-M., Eklund, D.M., Cronberg, N., Lagercrantz, U. Rates and patterns of molecular evolution in liverwort genomes, with fo- cus of Marchantiopsida. Manuscript III Linde, A-M., Eklund, D.M., Cronberg, N., Lagercrantz, U. Rates of structural changes in bryophyte genomes; exemplified by Marchan- tiopsida. Manuscript IV Linde, A-M., Eklund, D.M., Kubota, A., Pederson, E, Holm, K., Gyllenstrand, N., Nishihama, R., Cronberg, N., Muranaka, T., Oya- ma, T., Kohchi, T., & Lagercrantz, U. (2017) Early evolution of the land plant circadian clock. New Phytologist, 216(2) 576-590 Reprints were made with permission from the respective publishers. Contents Introduction ..................................................................................................... 7 Bryophyte phylogeny and evolution ........................................................... 8 The Marchantia polymorpha species complex ...................................... 8 Plant Genome Evolution ........................................................................... 10 Mutation and substitution rates ............................................................ 11 Transposable elements ......................................................................... 11 Gene and genome duplications ............................................................ 12 Genome size dynamics ........................................................................ 12 Hybridization, from a bryophyte perspective ...................................... 15 The Evolution of Gene Regulatory Networks .......................................... 16 The evolution of a specific functional network of genes: The circadian clock ..................................................................................... 16 Aims of the thesis .......................................................................................... 18 Materials and Methods .................................................................................. 19 Gene annotation of Marchantia sp. and Lunularia cruciata assemblies (Papers I, II, III) ..................................................................................... 19 Genetic variation analysis of Marchantia polymorpha L (Paper I) ......... 19 Rate calculations and associations (Paper II) .......................................... 20 TE landscape, gene statistics and synteny (Paper III) ............................ 20 Homolog search and functional analyses of clock genes in bryophyte and charophytes genomes (Paper IV) .................................... 21 Results and Discussion .................................................................................. 22 The phylogenetic relationship between the three subspecies of Marchantia polymorpha (Paper I) ........................................................... 22 Bryophytes do not have a uniquely low mutation rate (Paper II) ........... 23 Slow structural evolution of liverwort genomes (Paper III) .............. 26 Most components of the plant circadian clock are present in liverworts and in charophytes (Paper IV) ............................................... 28 Svensk sammanfattning ................................................................................. 30 Acknowledgement ......................................................................................... 34 References ..................................................................................................... 36 Introduction Based on spores found in the fossil record, plants have been living on land at least since Middle Ordovician, approximately 460 million years ago (Kenrick and Crane 1997). Land plants belong to the Embryophyta, whose members primarily live in terrestrial habitats and show a great variety of appearances. Now living embryophytes include hornworts, mosses, ferns, lycophytes, gymnosperms and angiosperms (flowering plants) (Figure 1). Together with some of the green algal lineages (Charophycean algae) they form the group streptophytes. All green algae and lands plants together com- prise the clade Viridiplantae (“green plants”), which is the collective name of streptophytes and chlorophytes. Land plants form a monophyletic group which nests within the freshwater Charophycean algal clade, making it likely that land plant evolved from an ancestral freshwater or terrestrial alga (Bowman 2013; Harholt et al. 2016). It has been suggested that adaptations to land already evolved in early terrestrial charophytes (Delwiche and Cooper 2015; Harholt et al. 2016). Figure 1. The phylogenetic relationship of plants, rooted with a charophytes algae. The phylogenetic order is adopted from Puttick et al. (2018). The branch lengths are not informative. 7 Bryophyte phylogeny and evolution The plants called “bryophytes” belong to three phyla, the liverworts (Marchantiopsida), mosses (Bryopsida) and hornworts (Antheroceropsida). Although these lineages represent a large fraction of the earth’s flora, exist on all continents and have significant ecological importance, they are often overlooked in the research of land plants. Traits they have in common in- clude small size, comparatively small genomes, a predominant haploid gam- etophytic life phase and a reduced sporophytic phase (Shaw et al. 2011; Bowman et al. 2017; Rensing et al. 2008). The bryophytes are considered to be the closest extant relatives of the plants that first colonized
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