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Evolutionarily conserved protein motifs drive interactions between the plant nucleoskeleton and nuclear pores


Mermet, Sarah; Voisin, Maxime; Mordier, Joris; Dubos, Tristan; Tutois, Sylvie; Tuffery, Pierre; Baroux, Célia; Tamura, Kentaro; Probst, Aline V; Vanrobays, Emmanuel; Tatout, Christophe (2023). Evolutionarily conserved protein motifs drive interactions between the plant nucleoskeleton and nuclear pores. Plant Cell, 35(12):4284-4303.

Abstract

The nucleoskeleton forms a filamentous meshwork under the nuclear envelope and contributes to the regulation of nuclear shape and gene expression. To understand how the Arabidopsis (Arabidopsis thaliana) nucleoskeleton physically connects to the nuclear periphery in plants, we investigated the Arabidopsis nucleoskeleton protein KAKU4 and sought for functional regions responsible for its localisation at the nuclear periphery. We identified three conserved peptide motifs within the N-terminal region of KAKU4 that are required for intermolecular interactions of KAKU4 with itself, interaction with the nucleoskeleton protein CROWDED NUCLEI (CRWN), localisation at the nuclear periphery and nuclear elongation in differentiated tissues. Unexpectedly, we find these motifs to be present also in NUP82 and NUP136, two plant specific nucleoporins from the nuclear pore basket. We further show that NUP82, NUP136 and KAKU4 have a common evolutionary history predating non-vascular land plants with KAKU4 mainly localising outside the nuclear pore suggesting its divergence from an ancient nucleoporin into a new nucleoskeleton component. Finally, we demonstrate that both NUP82 and NUP136, through their shared N-terminal motifs, interact with CRWN and KAKU4 proteins revealing the existence of a physical continuum between the nuclear pore and the nucleoskeleton in plants.

Abstract

The nucleoskeleton forms a filamentous meshwork under the nuclear envelope and contributes to the regulation of nuclear shape and gene expression. To understand how the Arabidopsis (Arabidopsis thaliana) nucleoskeleton physically connects to the nuclear periphery in plants, we investigated the Arabidopsis nucleoskeleton protein KAKU4 and sought for functional regions responsible for its localisation at the nuclear periphery. We identified three conserved peptide motifs within the N-terminal region of KAKU4 that are required for intermolecular interactions of KAKU4 with itself, interaction with the nucleoskeleton protein CROWDED NUCLEI (CRWN), localisation at the nuclear periphery and nuclear elongation in differentiated tissues. Unexpectedly, we find these motifs to be present also in NUP82 and NUP136, two plant specific nucleoporins from the nuclear pore basket. We further show that NUP82, NUP136 and KAKU4 have a common evolutionary history predating non-vascular land plants with KAKU4 mainly localising outside the nuclear pore suggesting its divergence from an ancient nucleoporin into a new nucleoskeleton component. Finally, we demonstrate that both NUP82 and NUP136, through their shared N-terminal motifs, interact with CRWN and KAKU4 proteins revealing the existence of a physical continuum between the nuclear pore and the nucleoskeleton in plants.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Plant and Microbial Biology
07 Faculty of Science > Zurich-Basel Plant Science Center
Dewey Decimal Classification:580 Plants (Botany)
Language:English
Date:30 November 2023
Deposited On:27 Oct 2023 10:20
Last Modified:31 Jan 2024 02:43
Publisher:American Society of Plant Biologists
ISSN:1040-4651
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1093/plcell/koad236
PubMed ID:37738557