Insights into the conservation and diversification of the molecular functions of YTHDF proteins

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Insights into the conservation and diversification of the molecular functions of YTHDF proteins. / Flores-Téllez, Daniel; Tankmar, Mathias Due; von Bülow, Sören; Chen, Junyu; Lindorff-Larsen, Kresten; Brodersen, Peter; Arribas-Hernández, Laura.

I: PLOS Genetics, Bind 19, Nr. 10, e1010980, 2023.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningfagfællebedømt

Harvard

Flores-Téllez, D, Tankmar, MD, von Bülow, S, Chen, J, Lindorff-Larsen, K, Brodersen, P & Arribas-Hernández, L 2023, 'Insights into the conservation and diversification of the molecular functions of YTHDF proteins', PLOS Genetics, bind 19, nr. 10, e1010980. https://doi.org/10.1371/journal.pgen.1010980

APA

Flores-Téllez, D., Tankmar, M. D., von Bülow, S., Chen, J., Lindorff-Larsen, K., Brodersen, P., & Arribas-Hernández, L. (2023). Insights into the conservation and diversification of the molecular functions of YTHDF proteins. PLOS Genetics, 19(10), [e1010980]. https://doi.org/10.1371/journal.pgen.1010980

Vancouver

Flores-Téllez D, Tankmar MD, von Bülow S, Chen J, Lindorff-Larsen K, Brodersen P o.a. Insights into the conservation and diversification of the molecular functions of YTHDF proteins. PLOS Genetics. 2023;19(10). e1010980. https://doi.org/10.1371/journal.pgen.1010980

Author

Flores-Téllez, Daniel ; Tankmar, Mathias Due ; von Bülow, Sören ; Chen, Junyu ; Lindorff-Larsen, Kresten ; Brodersen, Peter ; Arribas-Hernández, Laura. / Insights into the conservation and diversification of the molecular functions of YTHDF proteins. I: PLOS Genetics. 2023 ; Bind 19, Nr. 10.

Bibtex

@article{f1904a7acd0943e390d6c1faefe6d618,
title = "Insights into the conservation and diversification of the molecular functions of YTHDF proteins",
abstract = "YT521-B homology (YTH) domain proteins act as readers of N6-methyladenosine (m6A) in mRNA. Members of the YTHDF clade determine properties of m6A-containing mRNAs in the cytoplasm. Vertebrates encode three YTHDF proteins whose possible functional specialization is debated. In land plants, the YTHDF clade has expanded from one member in basal lineages to eleven so-called EVOLUTIONARILY CONSERVED C-TERMINAL REGION1-11 (ECT1-11) proteins in Arabidopsis thaliana, named after the conserved YTH domain placed behind a long N-terminal intrinsically disordered region (IDR). ECT2, ECT3 and ECT4 show genetic redundancy in stimulation of primed stem cell division, but the origin and implications of YTHDF expansion in higher plants are unknown, as it is unclear whether it involves acquisition of fundamentally different molecular properties, in particular of their divergent IDRs. Here, we use functional complementation of ect2/ect3/ect4 mutants to test whether different YTHDF proteins can perform the same function when similarly expressed in leaf primordia. We show that stimulation of primordial cell division relies on an ancestral molecular function of the m6A-YTHDF axis in land plants that is present in bryophytes and is conserved over YTHDF diversification, as it appears in all major clades of YTHDF proteins in flowering plants. Importantly, although our results indicate that the YTH domains of all arabidopsis ECT proteins have m6A-binding capacity, lineage-specific neo-functionalization of ECT1, ECT9 and ECT11 happened after late duplication events, and involves altered properties of both the YTH domains, and, especially, of the IDRs. We also identify two biophysical properties recurrent in IDRs of YTHDF proteins able to complement ect2 ect3 ect4 mutants, a clear phase separation propensity and a charge distribution that creates electric dipoles. Human and fly YTHDFs do not have IDRs with this combination of properties and cannot replace ECT2/3/4 function in arabidopsis, perhaps suggesting different molecular activities of YTHDF proteins between major taxa.",
author = "Daniel Flores-T{\'e}llez and Tankmar, {Mathias Due} and {von B{\"u}low}, S{\"o}ren and Junyu Chen and Kresten Lindorff-Larsen and Peter Brodersen and Laura Arribas-Hern{\'a}ndez",
note = "Publisher Copyright: Copyright: {\textcopyright} 2023 Flores-T{\'e}llez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",
year = "2023",
doi = "10.1371/journal.pgen.1010980",
language = "English",
volume = "19",
journal = "P L o S Genetics",
issn = "1553-7390",
publisher = "Public Library of Science",
number = "10",

}

RIS

TY - JOUR

T1 - Insights into the conservation and diversification of the molecular functions of YTHDF proteins

AU - Flores-Téllez, Daniel

AU - Tankmar, Mathias Due

AU - von Bülow, Sören

AU - Chen, Junyu

AU - Lindorff-Larsen, Kresten

AU - Brodersen, Peter

AU - Arribas-Hernández, Laura

N1 - Publisher Copyright: Copyright: © 2023 Flores-Téllez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2023

Y1 - 2023

N2 - YT521-B homology (YTH) domain proteins act as readers of N6-methyladenosine (m6A) in mRNA. Members of the YTHDF clade determine properties of m6A-containing mRNAs in the cytoplasm. Vertebrates encode three YTHDF proteins whose possible functional specialization is debated. In land plants, the YTHDF clade has expanded from one member in basal lineages to eleven so-called EVOLUTIONARILY CONSERVED C-TERMINAL REGION1-11 (ECT1-11) proteins in Arabidopsis thaliana, named after the conserved YTH domain placed behind a long N-terminal intrinsically disordered region (IDR). ECT2, ECT3 and ECT4 show genetic redundancy in stimulation of primed stem cell division, but the origin and implications of YTHDF expansion in higher plants are unknown, as it is unclear whether it involves acquisition of fundamentally different molecular properties, in particular of their divergent IDRs. Here, we use functional complementation of ect2/ect3/ect4 mutants to test whether different YTHDF proteins can perform the same function when similarly expressed in leaf primordia. We show that stimulation of primordial cell division relies on an ancestral molecular function of the m6A-YTHDF axis in land plants that is present in bryophytes and is conserved over YTHDF diversification, as it appears in all major clades of YTHDF proteins in flowering plants. Importantly, although our results indicate that the YTH domains of all arabidopsis ECT proteins have m6A-binding capacity, lineage-specific neo-functionalization of ECT1, ECT9 and ECT11 happened after late duplication events, and involves altered properties of both the YTH domains, and, especially, of the IDRs. We also identify two biophysical properties recurrent in IDRs of YTHDF proteins able to complement ect2 ect3 ect4 mutants, a clear phase separation propensity and a charge distribution that creates electric dipoles. Human and fly YTHDFs do not have IDRs with this combination of properties and cannot replace ECT2/3/4 function in arabidopsis, perhaps suggesting different molecular activities of YTHDF proteins between major taxa.

AB - YT521-B homology (YTH) domain proteins act as readers of N6-methyladenosine (m6A) in mRNA. Members of the YTHDF clade determine properties of m6A-containing mRNAs in the cytoplasm. Vertebrates encode three YTHDF proteins whose possible functional specialization is debated. In land plants, the YTHDF clade has expanded from one member in basal lineages to eleven so-called EVOLUTIONARILY CONSERVED C-TERMINAL REGION1-11 (ECT1-11) proteins in Arabidopsis thaliana, named after the conserved YTH domain placed behind a long N-terminal intrinsically disordered region (IDR). ECT2, ECT3 and ECT4 show genetic redundancy in stimulation of primed stem cell division, but the origin and implications of YTHDF expansion in higher plants are unknown, as it is unclear whether it involves acquisition of fundamentally different molecular properties, in particular of their divergent IDRs. Here, we use functional complementation of ect2/ect3/ect4 mutants to test whether different YTHDF proteins can perform the same function when similarly expressed in leaf primordia. We show that stimulation of primordial cell division relies on an ancestral molecular function of the m6A-YTHDF axis in land plants that is present in bryophytes and is conserved over YTHDF diversification, as it appears in all major clades of YTHDF proteins in flowering plants. Importantly, although our results indicate that the YTH domains of all arabidopsis ECT proteins have m6A-binding capacity, lineage-specific neo-functionalization of ECT1, ECT9 and ECT11 happened after late duplication events, and involves altered properties of both the YTH domains, and, especially, of the IDRs. We also identify two biophysical properties recurrent in IDRs of YTHDF proteins able to complement ect2 ect3 ect4 mutants, a clear phase separation propensity and a charge distribution that creates electric dipoles. Human and fly YTHDFs do not have IDRs with this combination of properties and cannot replace ECT2/3/4 function in arabidopsis, perhaps suggesting different molecular activities of YTHDF proteins between major taxa.

U2 - 10.1371/journal.pgen.1010980

DO - 10.1371/journal.pgen.1010980

M3 - Journal article

C2 - 37816028

AN - SCOPUS:85174361857

VL - 19

JO - P L o S Genetics

JF - P L o S Genetics

SN - 1553-7390

IS - 10

M1 - e1010980

ER -

ID: 390578357