Evolutionary conserved protein motifs drive attachment of the plant nucleoskeleton at nuclear pores

Mermet, Sarah; Voisin, Maxime; Mordier, Joris; Dubos, Tristan; Tutois, Sylvie; Tufféry, Pierre; Baroux, Célia; Tamura, Kentaro; Av, Probst; Vanrobays, Emmanuel; Tatout, Christophe

doi:10.1101/2021.03.20.435662

Cited by 6 publications

(9 citation statements)

References 85 publications

(117 reference statements)

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“…benthamiana . Overexpression of Nup136 or Nup82 alone led to the formation of condensates at the nuclear periphery ( Fig 2D ), consistent with a recent report [ 43 ]. Those condensates overlapped with GBPL3 condensates ( Fig 2D ), suggesting that GBPL3 can form condensates at the NPC basket.…”

Section: Resultssupporting

confidence: 92%

“…To confirm the association between GBPL3 with the NPC basket and the nucleoskeleton, we transiently coexpressed GBPL3 with the NB nucleoporin Nup136 and Nup82 or nucleoskeleton protein CRWN1 and CRWN3 in N. benthamiana. Overexpression of Nup136 or Nup82 alone led to the formation of condensates at the nuclear periphery (Fig 2D ), consistent with a recent report [43]. Those condensates overlapped with GBPL3 condensates (Fig 2D ), suggesting that GBPL3 can form condensates at the NPC basket.…”

Section: Plos Biologysupporting

confidence: 91%

“…Emerging evidence suggests that the plant NB is intimately associated with the nucleoskeleton distributed underneath the nuclear membrane. NB nucleoporins Nup136 and Nup82 share an evolutionary origin with the nucleoskeleton protein KAKU4 and physically interact with CRWN proteins [ 43 , 64 ]. Here, we showed that GBPL3 interacts with both Nup136/82 and CRWNs.…”

Section: Discussionmentioning

confidence: 99%

“…Nup82 and Nup136 interact with each other in the NB and are redundantly required for activation of SA-mediated pathogen resistance in Arabidopsis [ 42 ]. Nup136 and Nup82 are thought to share a common evolutionary history with a plant-specific nucleoskeleton protein KAKU4, and conserved motifs in these 3 proteins mediate physical interaction with CROWDED NUCLEIs (CRWNs), filamentous proteins that compose the nucleoskeleton in Arabidopsis [ 43 ]. This finding provides an intriguing molecular mechanism for the association between the NB and the nucleoskeleton in plants.…”

Section: Introductionmentioning

confidence: 99%

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GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

Tang

Ho²,

Kang³

et al. 2022

PLoS Biol

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The nuclear basket (NB) is an essential structure of the nuclear pore complex (NPC) and serves as a dynamic and multifunctional platform that participates in various critical nuclear processes, including cargo transport, molecular docking, and gene expression regulation. However, the underlying molecular mechanisms are not completely understood, particularly in plants. Here, we identified a guanylate-binding protein (GBP)-like GTPase (GBPL3) as a novel NPC basket component in Arabidopsis. Using fluorescence and immunoelectron microscopy, we found that GBPL3 localizes to the nuclear rim and is enriched in the nuclear pore. Proximity labeling proteomics and protein-protein interaction assays revealed that GBPL3 is predominantly distributed at the NPC basket, where it physically associates with NB nucleoporins and recruits chromatin remodelers, transcription apparatus and regulators, and the RNA splicing and processing machinery, suggesting a conserved function of the NB in transcription regulation as reported in yeasts and animals. Moreover, we found that GBPL3 physically interacts with the nucleoskeleton via disordered coiled-coil regions. Simultaneous loss of GBPL3 and 1 of the 4 Arabidopsis nucleoskeleton genes CRWNs led to distinct development- and stress-related phenotypes, ranging from seedling lethality to lesion development, and aberrant transcription of stress-related genes. Our results indicate that GBPL3 is a bona fide component of the plant NPC and physically and functionally connects the NB with the nucleoskeleton, which is required for the coordination of gene expression during plant development and stress responses.

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Section: Resultssupporting

confidence: 92%

Section: Plos Biologysupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

Tang

Ho²,

Kang³

et al. 2022

PLoS Biol

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“…The nup82 nup136 double mutant plants are impaired in benzothiadiazole (an analog of SA)-induced resistance to P. syringae ( 62 ). It is worth noting that the NPC nuclear basket is intimately associated with the nucleoskeleton ( 63 ) and that mutations in nucleoskeleton genes also cause altered SA responses in Arabidopsis ( 64 ). The influence of nucleoskeleton on plant immune will be further discussed later.…”

Section: Extensive Involvements Of Nucleoporins In Plant Immune Regulationmentioning

confidence: 99%

Regulation of Plant Immunity by Nuclear Membrane-Associated Mechanisms

Fang

2021

Front. Immunol.

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Unlike animals, plants do not have specialized immune cells and lack an adaptive immune system. Instead, plant cells rely on their unique innate immune system to defend against pathogens and coordinate beneficial interactions with commensal and symbiotic microbes. One of the major convergent points for plant immune signaling is the nucleus, where transcriptome reprogramming is initiated to orchestrate defense responses. Mechanisms that regulate selective transport of nuclear signaling cargo and chromatin activity at the nuclear boundary play a pivotal role in immune activation. This review summarizes the current knowledge of how nuclear membrane-associated core protein and protein complexes, including the nuclear pore complex, nuclear transport receptors, and the nucleoskeleton participate in plant innate immune activation and pathogen resistance. We also discuss the role of their functional counterparts in regulating innate immunity in animals and highlight potential common mechanisms that contribute to nuclear membrane-centered immune regulation in higher eukaryotes.

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Two-step regulation of centromere distribution by condensin II and the nuclear envelope proteins

Sakamoto

Grob

et al. 2022

Nat. Plants

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The arrangement of centromeres within the nucleus differs among species and cell types. However, neither the mechanisms determining centromere distribution nor its biological signi cance are currently well understood. In this study, we demonstrate the importance of centromere distribution for the maintenance of genome integrity through the cytogenic and molecular analysis of mutants defective in centromere distribution. We propose a two-step regulatory mechanism that shapes the non-Rabl-like centromere distribution in Arabidopsis thaliana through condensin II and the linker of the nucleoskeleton and cytoskeleton (LINC) complex. Condensin II is enriched at centromeres and, in cooperation with the LINC complex, induces the scattering of centromeres around the nuclear periphery during late anaphase/telophase. Then, after entering interphase, the positions of the scattered centromeres are stabilized by nuclear lamina proteins of the CROWDED NUCLEI (CRWN) family. We also found that, despite their strong impact on centromere distribution, condensin II and CRWNs have little effect on chromatin organization involved in the control of gene expression, indicating the robustness of chromatin organization regardless of the type of centromere distribution.

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Evolutionary conserved protein motifs drive attachment of the plant nucleoskeleton at nuclear pores

Cited by 6 publications

References 85 publications

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

Regulation of Plant Immunity by Nuclear Membrane-Associated Mechanisms

Two-step regulation of centromere distribution by condensin II and the nuclear envelope proteins

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