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Early evolution of the land plant circadian clock
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Linnean Ctr Plant Biol Uppsala, Uppsala, Sweden.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Linnean Ctr Plant Biol Uppsala, Uppsala, Sweden.ORCID iD: 0000-0002-0576-7636
Kyoto Univ, Grad Sch Biostudies, Kyoto 6068502, Japan.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution. Linnean Ctr Plant Biol Uppsala, Uppsala, Sweden.
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2017 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 216, no 2, p. 576-590Article in journal (Refereed) Published
Abstract [en]

While angiosperm clocks can be described as an intricate network of interlocked transcriptional feedback loops, clocks of green algae have been modelled as a loop of only two genes. To investigate the transition from a simple clock in algae to a complex one in angiosperms, we performed an inventory of circadian clock genes in bryophytes and charophytes. Additionally, we performed functional characterization of putative core clock genes in the liverwort Marchantia polymorpha and the hornwort Anthoceros agrestis. Phylogenetic construction was combined with studies of spatiotemporal expression patterns and analysis of M. polymorpha clock gene mutants. Homologues to core clock genes identified in Arabidopsis were found not only in bryophytes but also in charophytes, albeit in fewer copies. Circadian rhythms were detected for most identified genes in M. polymorpha and A. agrestis, and mutant analysis supports a role for putative clock genes in M. polymorpha. Our data are in line with a recent hypothesis that adaptation to terrestrial life occurred earlier than previously expected in the evolutionary history of charophyte algae. Both gene duplication and acquisition of new genes was important in the evolution of the plant circadian clock, but gene loss has also contributed to shaping the clock of bryophytes.

Place, publisher, year, edition, pages
2017. Vol. 216, no 2, p. 576-590
Keywords [en]
Marchantia polymorpha, bryophyte, circadian clock, evolution, transcription factor
National Category
Botany Evolutionary Biology Biochemistry and Molecular Biology Developmental Biology
Research subject
Biology with specialization in Evolutionary Functional Genomics
Identifiers
URN: urn:nbn:se:uu:diva-317912DOI: 10.1111/nph.14487ISI: 000427294000024PubMedID: 28244104OAI: oai:DiVA.org:uu-317912DiVA, id: diva2:1083716
Funder
Swedish Research Council, 2011-5609Swedish Research Council, 2014-522Available from: 2017-03-22 Created: 2017-03-22 Last updated: 2019-09-05Bibliographically approved
In thesis
1. Rates and patterns of bryophyte molecular evolution
Open this publication in new window or tab >>Rates and patterns of bryophyte molecular evolution
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

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.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. p. 42
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1850
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Functional Genomics
Identifiers
urn:nbn:se:uu:diva-392462 (URN)978-91-513-0740-4 (ISBN)
Public defence
2019-10-23, Zootissalen, EBC, Villavägen 9, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2019-10-02 Created: 2019-09-05 Last updated: 2019-10-15

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Linde, Anna-MalinEklund, D. MagnusHolm, KarlGyllenstrand, NiclasLagercrantz, Ulf

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