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Liao, Zhen
Publications (2 of 2) Show all publications
Kjellin, J., Avesson, L., Reimegård, J., Liao, Z., Eichinger, L., Noegel, A., . . . Söderbom, F. (2021). Abundantly expressed class of noncoding RNAs conserved through the multicellular evolution of dictyostelid social amoebas. Genome Research, 31(3), 436-447
Open this publication in new window or tab >>Abundantly expressed class of noncoding RNAs conserved through the multicellular evolution of dictyostelid social amoebas
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2021 (English)In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 31, no 3, p. 436-447Article in journal (Refereed) Published
Abstract [en]

Aggregative multicellularity has evolved multiple times in diverse groups of eukaryotes, exemplified by the well-studied development of dictyostelid social amoebas, for example, Dictyostelium discoideum. However, it is still poorly understood why multicellularity emerged in these amoebas while the majority of other members of Amoebozoa are unicellular. Previously, a novel type of noncoding RNA, Class I RNAs, was identified in D. discoideum and shown to be important for normal multicellular development. Here, we investigated Class I RNA evolution and its connection to multicellular development. We identified a large number of new Class I RNA genes by constructing a covariance model combined with a scoring system based on conserved upstream sequences. Multiple genes were predicted in representatives of each major group of Dictyostelia and expression analysis confirmed that our search approach identifies expressed Class I RNA genes with high accuracy and sensitivity and that the RNAs are developmentally regulated. Further studies showed that Class I RNAs are ubiquitous in Dictyostelia and share highly conserved structure and sequence motifs. In addition, Class I RNA genes appear to be unique to dictyostelid social amoebas because they could not be identified in outgroup genomes, including their closest known relatives. Our results show that Class I RNA is an ancient class of ncRNAs, likely to have been present in the last common ancestor of Dictyostelia dating back at least 600 million years. Based on previous functional analyses and the presented evolutionary investigation, we hypothesize that Class I RNAs were involved in evolution of multicellularity in Dictyostelia.

Place, publisher, year, edition, pages
Cold Spring Harbor Laboratory Press (CSHL)COLD SPRING HARBOR LAB PRESS, PUBLICATIONS DEPT, 2021
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-441378 (URN)10.1101/gr.272856.120 (DOI)000625081500001 ()33479022 (PubMedID)
Funder
Swedish Research CouncilSwedish Research CouncilKnut and Alice Wallenberg FoundationCarl Tryggers foundation , CST 18:381
Available from: 2021-05-05 Created: 2021-05-05 Last updated: 2024-01-15Bibliographically approved
Liao, Z., Kjellin, J., Höppner, M. P., Grabherr, M. & Söderbom, F. (2018). Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum. RNA Biology, 15(7), 937-954
Open this publication in new window or tab >>Global characterization of the Dicer-like protein DrnB roles in miRNA biogenesis in the social amoeba Dictyostelium discoideum
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2018 (English)In: RNA Biology, ISSN 1547-6286, E-ISSN 1555-8584, Vol. 15, no 7, p. 937-954Article in journal (Refereed) Published
Abstract [en]

Micro (mi)RNAs regulate gene expression in many eukaryotic organisms where they control diverse biological processes. Their biogenesis, from primary transcripts to mature miRNAs, have been extensively characterized in animals and plants, showing distinct differences between these phylogenetically distant groups of organisms. However, comparably little is known about miRNA biogenesis in organisms whose evolutionary position is placed in between plants and animals and/or in unicellular organisms. Here, we investigate miRNA maturation in the unicellular amoeba Dictyostelium discoideum, belonging to Amoebozoa, which branched out after plants but before animals. High-throughput sequencing of small RNAs and poly(A)-selected RNAs demonstrated that the Dicer-like protein DrnB is required, and essentially specific, for global miRNA maturation in D. discoideum. Our RNA-seq data also showed that longer miRNA transcripts, generally preceded by a T-rich putative promoter motif, accumulate in a drnB knock-out strain. For two model miRNAs we defined the transcriptional start sites (TSSs) of primary (pri)-miRNAs and showed that they carry the RNA polymerase II specific m7G-cap. The generation of the 3’-ends of these pri-miRNAs differs, with pri-mir-1177 reading into the downstream gene, and pri-mir-1176 displaying a distinct end. This 3´-end is processed to shorter intermediates, stabilized in DrnB-depleted cells, of which some carry a short oligo(A)-tail. Furthermore, we identified 10 new miRNAs, all DrnB dependent and developmentally regulated. Thus, the miRNA machinery in D. discoideum shares features with both plants and animals, which is in agreement with its evolutionary position and perhaps also an adaptation to its complex lifestyle: unicellular growth and multicellular development.

Place, publisher, year, edition, pages
UK: Taylor & Francis Group, 2018
Keywords
Dicer, microRNA, amoeba, biogenesis, evolution, transcriptional start site, intron, development, Dictyostelium discoideum
National Category
Microbiology
Research subject
Biology
Identifiers
urn:nbn:se:uu:diva-354016 (URN)10.1080/15476286.2018.1481697 (DOI)000445654400013 ()
Funder
Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning, 621-2013-4665Carl Tryggers foundation , CST12:485
Available from: 2018-06-19 Created: 2018-06-19 Last updated: 2020-04-15Bibliographically approved
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