Dupouy et al. - Nuclear envelope dynamics in connection to chromat

The Plant Journal (2023) doi: 10.1111/tpj.
16246
SPECIAL ISSUE REVIEW
Nuclear envelope dynamics in connection to chromatin

remodeling
Gilles Dupouy , Yihan Dong, Etienne Herzog, Marie-Edith Chaboute* and Alexandre Berr*
Institut de Biologie Mole culaire des Plantes du CNRS- Universite de Strasbourg, 12 rue du Ge ne ral Zimmer, F-67084, Stras-
bourg, France
Received 30 December 2022; revised 29 March 2023; accepted 12 April 2023.

*For correspondence (e-mail marie-edith.chaboute@ibmp-cnrs.unistra.fr; alexandre.berr@ibmp-cnrs.unistra.fr).
SUMMARY
The nucleus is a central organelle of eukaryotic cells undergoing dynamic structural changes during cellular
fundamental processes such as proliferation and differentiation. These changes rely on the integration of
developmental and stress signals at the nuclear envelope (NE), orchestrating responses at the nucleo-
cytoplasmic interface for efficient genomic functions such as DNA transcription, replication and repair. While
in animals, correlation has already been established between NE dynamics and chromatin remodeling using
last-generation tools and cutting-edge technologies, this topic is just emerging in plants, especially in
response to mechanical cues. This review summarizes recent data obtained in this field with more emphasis
on the mechanical stress response. It also highlights similarities/differences between animal and plant cells
at multiples scales, from the structural organization of the nucleo-cytoplasmic continuum to the functional
impacts of NE dynamics.
Keywords: nuclear envelope, cytoskeleton, nucleoskeleton, mechanical cues, chromatin, epigenetics.
INTRODUCTION
networks extend toward the cell periphery with the assem-
The nucleus is a central organelle in eukaryotic cells, bly of actin microfilaments (MFs) at the cellular cortex
where the nuclear envelope (NE) compartmentalizes chro- (Chugh & Paluch, 2018). Conversely, in walled plant cells,
matin by means of two phospholipid bilayer membranes. microtubules (MTs) are mainly present at the cortex to
The outer nuclear membrane (ONM) is derived from the control cell shape through cellulose deposition while MFs
endoplasmic reticulum (ER) and is separated from the are mostly involved in vesicle trafficking and organelle
inner nuclear membrane (INM) by a perinuclear space of movements (Smith, 2003). Another specific feature of acen-
about 30–50 nm (Stewart et al., 2007). The INM is con- trosomal plant cells is that the NE acts as a Microtubule-
nected to the nucleoskeleton, a filamentous meshwork of Organizing Center (MTOC) forming radial MT arrays
10–30 nm, composed primarily of lamins in animals, with extending through the cytoplasm which reorganize during
functional analogs in plants and fungi (Ciska & Moreno pre-spindle assembly upon mitosis entry (Ambrose & Was-
Diaz de la Espina, 2014). The NE is perforated by nuclear teneys, 2014; Masoud et al., 2013). Finally, intermediate fil-
pore complexes (NPCs) allowing molecular exchanges aments (IFs) form an intricate network of complex
between nucleus and cytoplasm. The peripheral nucleoske- filamentous structures, exclusively found in animals, that
leton and NPCs allow chromatin tethering at the nuclear extends from the cell membrane to the nucleus. IFs are
periphery and are required for proper genome organization master integrators of cell and tissue mechanics (van Bode-
and activity (Bi et al., 2017; Boruc et al., 2012; Hu graven & Etienne-Manneville, 2021) and rearrange them-
et al., 2019; Tang, Dong, et al., 2022; Tang, Ho, et al., 2022). selves to serve as stress buffers (Sanghvi-Shah &
The nucleoskeleton is also connected to the cytosol and Weber, 2017).
the cytoskeleton through NPCs and Linker of Nucleoskele- All living organisms perceive mechanical cues from
ton and Cytoskeleton (LINC) complexes (Kirby & Lammerd- their environment and integrate them at the cellular level to
ing, 2018; Zhou et al., 2015). In animals, cytoskeleton respond and to adjust their behavior for proper development
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2 Gilles Dupouy et al.
and survival (Tsata & Beis, 2020). Both external and internal organization and epigenetic landscape ultimately resulting
mechanical stimuli induce cellular deformation and/or con- in transcriptional reprogramming.
straints which are sensed at the cell periphery and trans-
INTEGRATION OF MECHANICAL CUES FROM THE CELL
duced in biochemical and mechanical responses.
PERIPHERY TO THE NUCLEUS
Cytoskeleton reorganization and chromatin structural
changes participate in such mechano-transduction and influ- Cells interact physically with their environment and can
ence all genomic functions including transcriptional gene perceive mechanical constraints. These mechanical cues
expression programs (Fal et al., 2017; Graham & Bur- are sensed at the cell periphery and transmitted to the
ridge, 2016) which are important drivers for cell differentia- nucleus to be converted into coordinated cellular
tion and development in both animals and plants (De Belly responses. This relies on specific subcellular structures in
et al., 2022; Trinh et al., 2021). The NE itself constitutes a site animal cells and walled plant cells, especially at the
for nuclear mechano-transduction, where biochemical and nucleo-cytoplasmic interface (Figure 1).
mechanical stimuli are transferred to the nucleus. In animals,
Mechanosensing at the cell periphery
this occurs either through direct physical interactions at the
NE between the cytoskeleton and the nucleoskeleton or via In animals, cells can be constrained not only during migra-
translocation of macromolecular factors from the cytoplasm tion and/or tissue morphogenesis, but also in response to
to the nucleus through NPCs (Cho et al., 2017; Fal et al., 2017; external mechanical forces. Such forces are driven by the
Uhler & Shivashankar, 2017). Such mechanical perturbation stiffness of the surrounding extracellular matrix inducing
influences nuclear migration and morpho-dynamic changes deformations of the plasma membrane (Shin, 2018) which
affecting key genomic functions (Dos Santos & Tose- may regulate gene expression through direct force trans-
land, 2021; Dupont & Wickstro€ m, 2022; Long & Lammerd- mission and chromatin stretching (Joshi et al., 2022). Cell
ing, 2021). As plants are sessile organisms, they are geometric constraints can also be obtained using micropat-
constantly subjected to external mechanical stresses such as terned substrates, inducing cellular shape changes which
wind, rain or wounding for aerial parts and osmotic pressure are transmitted to the nucleus through cytoskeletal physical
and soil rigidity for roots. While relevant cortical mechano- links (Alisafaei et al., 2019). Resulting mechanical signals
sensing pathways start to be deciphered in plants (Colin & are sensed by focal adhesion complexes, mainly formed by
Hamant, 2021), the nuclear mechano-transduction linking transmembrane proteins of the integrin family that connect
nuclear mechanics to specific gene expression patterns and the plasma membrane to the extracellular matrix and trans-
cell fate decisions remains elusive (Fal et al., 2017). mit mechanical tension to the actin–myosin cytoskeleton.
Recently, we have established that nuclear morpho- Cell–cell junctions with cadherins are also key mechanosen-
dynamics are functionally connected to chromatin remo- sitive modules (Mathieu & Manneville, 2019). In parallel,
deling and gene expression as well as changes in nuclear mechanosensitive (MS) ion channels embedded in the
mechanical properties (Fal, Korsbo, et al., 2021; Goswami, plasma membrane, such as Piezo1/2, integrate various
Asnacios, Milani, et al., 2020). In this context, beyond a mechanical cues typically by increasing the cytoplasmic
simple physical barrier, the NE appears as a highly Ca2+ concentration. Their activation mainly triggers cyto-
dynamic platform controlling communication at the skeleton modulation (Qin et al., 2021). Interestingly, Piezo1
nucleo-cytoplasmic interface, which changes shape and/or is also present at the endoplasmic reticulum (ER) and there,
organization allowing developmental responses and stress upon cell stretching, it can mediate heterochromatin reduc-
adaptation. This process partly relies on epigenetic modifi- tion via Ca2+ release from the ER, thus promoting chroma-
cations impacting specific transcriptional programs for cell tin mobility and decreasing NE tension (Nava et al., 2020).
differentiation and identity (Song et al., 2020). Epigenetic In plants, the high turgor pressure (around the MPa
adjustments can be induced by simple cell deformations, range) is the primary cause of mechanical stress during
for example in response to the surrounding matrix in ani- plant development as it exerts important mechanical con-
mals (Alisafaei et al., 2019) or to prolonged mechanical straints on cell walls (Trinh et al., 2021). Cell wall deforma-
stimulation in plants (Brenya et al., 2022). Together, these tion and remodeling can also transduce external
gave rise to the model of the mechanical priming of cell mechanical signals for changes in gene expression as
identity and stress resistance via epigenetic processes observed at the boundary region of the shoot apical meri-
(Brenya et al., 2022; Li et al., 2022). stem (Landrein et al., 2015). Similarly, touching seedlings
Here, we reviewed the state-of-the-art knowledge lead to an increase of cell wall stiffness and a decrease of
about the impact of cellular deformation on nuclear shape, cell elongation, together resulting in the modulation of the
structure and mechanics through nucleo-cytoskeleton cou- expression of touch-responsive genes (Wu et al., 2020). In
pling in both animals and plants. As a follow-up, we dis- this context, plant mechanosensing and transduction at
cuss the subsequent mechanically induced chromatin the cell periphery begin to be elucidated (Trinh et al.,
changes and their consequences on the spatial genome 2021), with Ca2+ signaling also playing a central role
Ó 2023 Society for Experimental Biology and John Wiley & Sons Ltd.,
The Plant Journal, (2023), doi: 10.1111/tpj.16246
Insight into mechanosensing at the nuclear envelope 3
Figure 1. Mechanical connection from the plasma membrane to the NE in animal mesenchymal cells and differentiated plant cells.
In both cell types, MFs (in red) are connected to protein complexes at the plasma membrane complexes: to focal adhesions allowing cell–matrix connection in
animals and to plasmodesmata allowing cell–cell communication in plants. The other extremities of MFs are connected to the NE via LINC complexes. A particu-
larity of the animal cell in comparison to plants is the presence of elongated membrane structures called lamellipodia which allow cell movement along the sur-
rounding matrix and are formed by the polymerization of MFs pushing against the plasma membrane (black double arrrow). Another feature specific to animal
cells is the presence of IFs (in blue) establishing connections with hemidesmosomes and LINC complexes. MTs (in green) are nucleated from c-TuRCs at the
centrosome in animal cells, and plus-ends connect either to the plasma membrane through crosslinks with actin and IFs or to the NE with LINC complexes. In
acentrosomal plant cells, endoplasmic MTs nucleate from both the plasma membrane and the NE. Cortical MTs (here indicated in pale green in the cell back-
ground) guide the movement of cellulose synthase complexes (not shown) and align perpendicularly to the direction of cell elongation. Cortical MTs reorient
during mechanical stress to follow the direction of the strain. Characterized mechanosensory receptors are indicated in both models (FER, Piezo). Mitochondria
(red), chloroplasts (green) and the vacuole (orange) are also represented. Nuclear structures are detailed in Figure 2.
(Hamilton et al., 2015). At the plasma membrane, MS ion cells, locating certain mechanosensory proteins to the
channels named Mid1-complementing activity 1/2 (MCA1/ tonoplast might be more effective for mechanosensing
2) correlate with Ca2+ influx and mechanosensing in Arabi- (Radin et al., 2021).
dopsis roots (Nakagawa et al., 2007). Also at the plasma
Importance of MF and MT dynamics in mechano-
membrane, the receptor-like kinase FERONIA (FER) acts as
transduction
a mechanosensor regulating Ca2+ signaling and the expres-
sion of touch-responsive genes (Feng et al., 2018; Shih In vitro, both MFs and MTs polymerize faster under tensile
et al., 2014). Contrary to animals, Piezo1/2 locate exclu- stress (Trinh et al., 2021) and MFs branch upon
sively to the vacuole tonoplast in Arabidopsis (Radin et al., compression-induced bending (Risca et al., 2012). In ani-
2021). Because the tonoplast may have more freedom of mals, the influence of cytoskeleton organization on nuclear
movement than the plasma membrane in walled plant morphology and chromatin dynamics in driving cell
differentiation is nowadays well documented. For example, dynamics may serve as a strategy to adjust NPC transport
during early differentiation of human hematopoietic stem capacity under different cellular and physiological condi-
cells, MT constraints induce nuclear invaginations associ- tions (Hakhverdyan et al., 2021). In animals and yeast, NPC
ated with heterochromatin reorganization and modification density is constant over a range of nuclear sizes. Neverthe-
in expression of specific hematopoietic genes (Biedzinski less, altered NPC composition can affect nuclear size and
et al., 2020). Similarly, cytoskeleton components were morphology (Jevtic et al., 2014). Among other functions,
found to shape the nucleus of mouse embryonic stem cells NPCs, especially via their nuclear basket, are involved in
and to influence interactions of the pluripotency transcrip- regulating genomic functions by controlling chromatin
tion factor OCT4 with chromatin, thus potentially affecting organization and spatial arrangement (Kadota et al., 2020;
pluripotency (Romero et al., 2022). Krull et al., 2010). Interestingly, many NUPs also have
At the plant cellular cortex, cytoskeleton reorganiza- DNA-related functions inside the nucleoplasm, irrespective
tion is also driven by mechanical stress, with a major of their structural role within NPCs, enabling them to
role for cortical MTs as tension sensors, able to align dynamically, rather than permanently, associate to the
along the maximal tensile stress directions in tissues NPCs (Richards et al., 2022).
(Hamant et al., 2008; Hamant et al., 2019). Organogenesis The molecular functions of NPCs and NUPs in plants
of plant cells within their tissue context, along with the are far less described than in animals. In Arabidopsis, the
regulation of cell wall plasticity, can also generate com- plant-specific nuclear basket NUP1/NUP136 can interact
pression forces. At the boundary between the central with heterochromatic domains such as pericentromeric
shoot apical meristematic zone and the developing organ regions enriched in repressed transposable elements (TEs)
primordia region, nuclear compression was observed or silenced protein-coding genes (Bi et al., 2017). NUP136
with changes in heterochromatin organization and gene and the other plant-specific nuclear basket component
expression (Fal, Korsbo, et al., 2021; Landrein et al., NUP82 were found to interact with the euchromatin bind-
2015). Together with the key role played by MTs in inte- ing factor guanylate-binding protein (GBP)-like GTPase 3
grating mechanical stress to coordinate patterns of apical (GBPL3). GBPL3 acts as a central connector between NPCs,
morphogenesis at the Arabidopsis shoot apex (Hamant the nucleoskeleton, chromatin remodelers, transcription
et al., 2008), this highlights the importance of MT reorga- regulators and components of RNA splicing and proces-
nization for cellular shaping upon mechanical stress in sing machinery to coordinate gene expression during plant
plants. development and stress responses (Tang, Ho, et al., 2022).
Together with a physical link with the plant nucleoskeleton
THE NE AS A CONTINUUM BETWEEN NUCLEOPLASM
proteins CRWN1/2 (functional analogs of animal lamins),
AND CYTOPLASM
GBPL3 acts as a chromatin remodeler and transcriptional
The NE contains many protein complexes linking the cyto- regulator to coordinate stress-responsive gene expression
skeleton and nucleoskeleton. We describe hereafter key NE (Tang, Ho, et al., 2022). Interestingly, NUP136 and CRWN1
components and their respective functional implications are separately involved in nuclear shaping (Tamura et al.,
by emphasizing differences and peculiarities between ani- 2015; Tamura & Hara-Nishimura, 2011). A mutation of the
mals and plants, notably in terms of mechanical stress plant-specific NUP CONSTITUTIVE EXPRESSION OF PR
response (see Figure 2 and Table 1). GENES 5 (CPR5), present at the NPC transmembrane ring,
also leads to defects in nuclear shape and changes in gene
NPCs, responsive gateways at the nucleo-cytoplasmic
expression (Gu et al., 2016). Interestingly, the mis-
interface
regulated genes in cpr5 mutants show significant overlap
NPCs are huge protein conglomerates (40–120 MDa) with genes mis-regulated in the transcriptome of gip1gip2
tunneling the NE at regular intervals where the ONM and mutant also showing altered nuclear shape (Goswami,
INM are fused. NPCs are composed of hundreds of nucleo- Asnacios, Milani, et al., 2020). This highlights an intricate
porin proteins (NUPs) assembled in a cylinder subdivided functional network at the NE for gene and nuclear shape
in four main substructures, namely the cytoplasmic fila- regulation whose dynamic spatial orchestration still needs
ments, the outer and inner rings forming the core compo- clarification.
nent and the nuclear basket (Lin & Hoelz, 2019) (see There is also evidence for a major role of NPCs in
Figure 2). NPCs selectively control the nucleo-cytoplasmic mechano-transduction in animals (Matsuda & Mofrad, 2022).
movement of macromolecules such as proteins and mes- In response to mechanical forces, two related mechanisms
senger ribonucleoproteins across the NE, thereby playing are proposed to affect nuclear import and accumulation of
a key role in regulating gene expression and protein syn- some specific transcription factors. Either the NPC diameter
thesis (Walde & Kehlenbach, 2010). While mechanisms increases inducing structural changes of the nuclear basket
underlying NPC transport selectivity remain elusive, recent or transcription factors change their conformation to
evidence suggests that their structural and constituent increase their affinity with the nuclear transport receptor
(Matsuda & Mofrad, 2022). In fission yeast, NPC diameter (Zhou et al., 2014). While LINC may associate to MTs
was shown to vary according to NE tension (Zimmerli et al., through motor proteins such as kinesin, dynein or fascin
2021), and in mammalian cells, NPC stretching allows the (known to promote cell migration) in animals (Burke &
shuttling of epigenetic and transcription factors, such as the Roux, 2009), there is no such evidence in plants.
mechanosensor and transducer YAP/TAZ (Elosegui-Artola Adding another layer of complexity, direct functional
et al., 2017). In plants, NPCs are important regulators of gene associations between LINC complexes and NPCs were
expression in response to stress (Tamura, 2020) but their reported in animal cells for the control of NPC assembly/
links to mechano-transduction have not yet been distribution and the transport of LINC complex compo-
investigated. nents (Jahed et al., 2016). Reinforcing such association,
SUN2, but not SUN1, was found to directly bind NUP210,
The LINC complexes, physical links between the
forming a complex able to tether the replicative histone H3
cytoskeleton and nucleoskeleton
variants H3.1/H3.2 and the chromatin reader BRD4 at the
LINC complexes are the other main protein complexes pre- nuclear periphery to regulate gene expression during
sent at the NE linking the nucleoskeleton to the cytoskele- metastasis in mouse (Amin et al., 2021).
ton. The primary function of this link is to control nuclear As for NPCs, LINC complexes have been identified as
positioning and movement (Burke, 2019; Tatout et al., nuclear mechano-transduction actors, but so far only in
2014) (see Figure 2). LINC complexes are composed of two animals (Fal et al., 2017). For example, forces transmitted
transmembrane protein families, namely the Sad-1/UNC-84 via the KASH protein Nesprin-1 in isolated nuclei led to
(SUN) domain proteins, which span the INM and interact increased nuclear stiffness (Guilluy et al., 2014). Accord-
with nuclear components, and the C-terminal Klarsicht/ ingly, Nesprins were shown to transfer mechanical forces
ANC-1/Syne-1 Homology (KASH) domain proteins, which from actomyosin to the nucleus through LINC complexes
span the ONM and interact with cytoplasmic components (Arsenovic et al., 2016) and to contribute to the induction
(Burke, 2019; Tatout et al., 2014). SUN proteins contain a of a mechanically responsive gene program (Banerjee
SUN domain located at the perinuclear space that is over- et al., 2014). Local stresses applied to integrins can propa-
all well conserved across eukaryotes and a nucleoplasmic gate to LINC complexes through the actin cytoskeleton
domain that is much less conserved. Compared to SUN and lead to chromatin unpacking as well as epigenetic
proteins, KASH proteins are far less conserved, with the changes promoting transcription (Tajik et al., 2016).
KASH domain being highly variable in sequence and size Finally, in fibroblasts, both SUN1 alteration and changes
(Meier, 2016). The tryptophan–proline–proline (WPP)- in substrate rigidity affect transcription (Alam et al.,
interacting proteins (WIPs) were the first animal KASH ana- 2016).
logs identified as being able to bind SUN proteins at the
The tight connections between the NE, the nucleoskeleton
NE in Arabidopsis (Zhou et al., 2012). Other KASH analogs
and chromatin
were identified in Arabidopsis, including Toll-Interleukin-
Resistance KASH protein (TIK) and SUN-interacting NE Inside the nucleus, both NPCs and LINC complexes interact
proteins 1–4 (SINE1–4) (Groves et al., 2020). Apart from the with a thin fibrous protein meshwork closely juxtaposed
non-conserved KASH domain, the N-terminal cytoplasmic between the nucleoplasmic face of the INM and the chro-
part of the KASH proteins is also highly diverse, as are the matin (Figueiras et al., 2019) (see Figure 2). In metazoans,
functions of KASH proteins. In animals and plants, interac- this meshwork is named the nuclear lamina and is mainly
tions between various KASH proteins and SUN1/2 proteins composed of type V IF lamin proteins (i.e., A- and C-type
in the lumen of the NE constitute physical bridges at the lamins plus several minor tissue-specific isoforms in most
nucleo-cytoplasmic interface and allow the formation of differentiated cells and B-type lamins expressed ubiqui-
various LINC complexes mediating different associations tously). Lamins play major roles in controlling nuclear rigid-
between the cytoskeleton and nucleoskeleton. In animals, ity and chromatin organization and are key elements for
the LINC complexes interact directly with the MFs through mechanosensing and nuclear mechano-transduction (Swift
the N-terminal actin-binding domain of KASH proteins et al., 2013; Vahabikashi et al., 2022). In mammalian cells, A/
such as the two vertebrate paralogs Nesprin-1/2 (Burke & C and B lamins interact with heterochromatin to form
Roux, 2009). Similarly, WIPs and WPP-interacting tail- lamina-associated domains (LADs) enriched in heterochro-
anchored proteins (WITs) oligomerize in Arabidopsis to matin at the nuclear periphery and interact with euchroma-
form a LINC complex where Myosin XI-i attaches and inter- tin domains as well to promote gene expression
acts with long cables of cytoplasmic actin (Groves et al., (Vahabikashi et al., 2022). For example, in progeria (also
2020). Beside this, a more direct and tissue-specific interac- known as Hutchinson–Gilford syndrome) the accumulation
tion was described for stomatal guard cells in which the of progerin, a dominant-negative A-type lamin protein, dis-
KASH protein SINE1 directly attaches to MFs through a rupts heterochromatin–lamina interactions and results in
LINC complex involving SUN1/2 for nuclear positioning disturbed nuclear shape and spatial chromatin organization
FIE
leading to gene expression alterations (McCord et al., modulate chromatin organization at the nuclear periphery
2013). through their direct binding with chromatin regions named
In plants, no IFs or nuclear lamins have been identified, plant LADs (PLADs) (Hu et al., 2019). This link with chromatin
but functional homologs have been regrouped as nuclear was further reinforced by the discovery that CRWN1 interacts
matrix constituent proteins (NMCPs) (Masuda et al., 1997). with chromatin and the polycomb-associated component
NMCP assembly produces an intricate filamentous network PROLINE-TRYPTOPHAN-TRYPTOPHAN--PROLINE INTERAC-
called plamina, including filament bundles across the nuclear TOR OF POLYCOMBS1 (PWO1), possibly linking repressive
periphery (Masuda et al., 2021). They are widely conserved in histone H3 lysine 27 trimethylation (H3K27me3)-marked
land plants; CROWDED NUCLEI 1–4 (CRWN1–4), identified in chromatin and the nuclear periphery in Arabidopsis
Arabidopsis, belong to this family (Ciska & Moreno Diaz de la (Mikulski et al., 2019). In addition, CRWN1 directly associ-
Espina, 2014). CRWN1 and 4 interact and redundantly ates with SUN1 (Graumann, 2014), while the NMCP-binding
Figure 2. Protein complexes and functional modules involved in the organization and dynamics of the NE in animal (left) and plant cells (right). Cytoskeleton
attachment to the NE differs significantly between animals and plants. While MTs can bind to Nesprin-4-specific LINC complexes via kinesin in animal cells (A),
the only way reported so far in plants for their interaction with the NE is through c-TuRC and associated GIP1/2 proteins present at the ONM (H). Positioning of
c-TuRC may involve a TSA1/trans-NE complex which is yet to be fully described. GIP1/2 are also found at the INM associated with the centromere (CENH3). MFs
bind through the LINC complexes in both models but the attachment differs significantly at the ONM: while Nesprin-1/2 are used in animal cells (D), different
KASH proteins are used in plants (F), namely WIP1/2/3 and WIT1/2. It is interesting to highlight that WIP1/2/3 interact with SUN1/2, while WIT1/2 do not. The sta-
bilization of the interaction with MFs via Myosin XI-i also involves two additional proteins, namely WPP and RanGAP. Other KASH proteins such as SINE1/2 can
bind to MFs and were shown to also be necessary for MT patterning, but in a way not yet determined (G). Additional KASH proteins in animals such as
Nesprin-3 can bind Vimentin-based IFs (C), while IFs are absent in plants. Other KASH proteins (TIK, SUN3/4) have been identified as interacting with SUN com-
plexes in plants, but their function still remains unclear. The cytoskeleton network allows the mechanical propagation of tensile and shearing forces from the
cellular periphery to the NE, resulting in its mechanical deformation, but this deformation can also result from the induced condensation/decondensation of the
chromatin from the inside of the nucleus.
Chromatin (pale blue) tethering to the nuclear periphery has been observed in both models and requires the presence of lamins (A/C- and B-type lamins) in ani-
mal cells and lamin-like proteins (CRWN1/4, KAKU4) in plants. Both lamins and lamin-like proteins bind to the SUN complexes (highly conserved between both
kingdoms) with the addition of lamin-associated proteins which are specific to animals (Emerin, Man1, Nur1, Lem2) and plants (PNET2) (B, H). At the INM,
NEAP1/2/3 interact with the transcription factor bZIP18 (E). Some lamin and lamin-like proteins can also be found attached to the chromatin in the nucleoplasm,
especially A/C and B lamins in animals and CRWN2/3 in plants. The chromatin tethered to the nuclear periphery is highly enriched in heterochromatin and
repressing complexes, such as PRC2, which maintain transcriptional repression through the deposition of H3K27me3 epigenetic marks. The nucleoplasm apart
from the nucleolus is on the contrary mostly composed of euchromatin.
Compared to the rest of the nuclear periphery, euchromatin is highly enriched at the NPCs to promote gene expression, involving the nuclear pore basket com-
ponents NUP2 and NUP160 in animals (A) and the basket proteins NUP82 and NUP1/NUP136 and the ring protein CPR5 in plants (G). Other proteins of the bas-
ket were shown to be necessary for heterochromatin organization (i.e., TPR, NUP153 and NUP210 in animals, NUP1/NUP136 in plants) or for the regulation of
chromatin attachment to the NPC (NUP155, NUP93 and NUP62 in animals). Other proteins such as NUP107 were shown to be more specifically involved in the
activation of DNA replication.
NPCs are also important for the shuttling of mechanoresponsive factors through the NE. In animals, TOR is mechanically activated through Piezo1-related Ca2+
signaling from the ER and actively regulates gene expression (B). In plants, it is activated by FER and phosphorylates the PRC2 component FIE, resulting in FIE
shuttling through the NPC for the regulation of gene expression (E). Interestingly, TOR seems to regulate cytoskeleton dynamics in a kingdom-specific way:
while it was shown to regulate MT formation in animals, it appears to regulate the formation of MFs in plants. Finally, other proteins have been shown in ani-
mals to shuttle through the NPC as a response to tensile stress on the NE: G-actin for instance, which can be used as a transcription factor, is exported outside
of the nucleus to help the polymerization of a perinuclear ring of F-actin preventing NE rupture (D). YAP/TAZ is another mechanoresponsive transcription factor
which necessitates F-actin connection at LINC complexes to be transferred through the NPC for the regulation of stress-responsive genes. The question marks
indicate the absence of knowledge about the interactors.
protein KAKU4 indirectly associates with SUN1 via interac- NPCs to regulate gene expression in plants, but the impor-
tion with CRWN1 (Goto et al., 2014). CRWN1 and 4 are key tance of the plamina in the mechanical response remains
factors maintaining nuclear morphology. In contrast to to be investigated.
crwn2 or crwn3 mutants (Wang et al., 2013), kaku4 and
CHROMATIN REMODELING UPON NE DYNAMICS AND
crwn1 mutants exhibit drastic abnormalities in nuclear
MECHANICAL STRESS
shape in differentiated tissues and their combination had
neither synergistic nor additive effects (Goto et al., 2014). The nucleosome is the main structural unit of eukaryotic
The plant-specific NE-associated proteins (NEAPs) are chromatin and consists of DNA wrapped around a core his-
anchored at the INM and directly interact with SUN pro- tone octamer (two each of H2A, H2B, H3 and H4). Chromatin
teins. Further connecting NEAPs with chromatin organiza- is dynamically organized and can promote DNA compaction
tion and gene regulation, a putative transcription factor in heterochromatin or relaxation in euchromatin at different
called AtbZIP18 was identified among the NEAP interactors scales to affect genomic functions (Dogan & Liu, 2018).
(Pawar et al., 2016). More recently, plant NE transmem- Among the mechanisms directly or indirectly affecting chro-
brane protein 2 (PNET2) was identified as a bona fide INM matin compaction, epigenetic processes, including DNA
protein interacting with CRWN1 in Arabidopsis (Tang, methylation, histone variant incorporation and histone post-
Dong, et al., 2022). PNET2 together with KAKU4 contributes translational modifications (PTMs), are involved in the regu-
to the proper maintenance of genome architecture and lation of all DNA-related processes (Lloyd & Lister, 2022;
transcriptome programming during plant development and Mansisidor & Risca, 2022). On a larger scale, during the inter-
stress responses. Interestingly, the simultaneous overex- phase chromatin forms functional loop domains allowing
pression of PNET2 and KAKU4 induces more severe each chromosome to occupy an individual territory. Physi-
nuclear deformations than when they were overexpressed cally, chromatin is considered as a viscoelastic gel display-
separately (Tang, Dong, et al., 2022). Finally, suggesting a ing changes in macromolecular crowding (Mitchison, 2019).
physical link between the nucleoskeleton and NPCs, NUP82 In recent years, chromatin organization and dynamics has
and 136 were revealed to bind CRWN proteins (Mermet emerged as an instrument of the mechanical stress response
et al., 2021). Together, tight functional connections exist in both animals and plants (Goswami, Asnacios, Hamant, &
between the cytoskeleton, the NE, the nucleoskeleton and Chaboute, 2020; Uhler & Shivashankar, 2017).
Impact on constitutive heterochromatin Regulation of facultative heterochromatin

In both animals and plants, chromocenters are predomi- Facultative LADs harbor developmentally regulated genes
nantly composed of silent, condensed and gene-poor peri- controlled by Polycomb complexes involved in H3K27me3
centromeric heterochromatin, and are attached in a non- modification at the nuclear periphery. Their interaction with
random way to the nuclear periphery via lamins or func- lamins is reported in numerous tissues to allow the regula-
tional analogs (Fransz et al., 2002; Rullens & Kind, 2021). A tion of gene expression via chromatin distortion resulting
recent report on epidermis stem cells highlights the fact from NE deformation by mechanical stress conditions and/
that heterochromatin decondensation induced under short- or during cellular differentiation (Bianchi & Lanzuolo, 2015).
time stretching tension happens mostly in non-coding In human epidermal stem cells, application of long-term bi-
regions, resulting in no major transcriptional changes axial stretches prevents cells from realigning to minimize
(Nava et al., 2020). More recently, a decrease of H3K9me3 strain on the nucleus and provokes the accumulation of the
constitutive heterochromatin mark levels accompanied by silencing H3K27me3 mark at epidermal differentiation
a decrease of DNA methylation and of A/C type lamin genes, thus preventing epidermal stem cell differentiation
levels at the nuclear periphery was reported after squeez- (Le et al., 2016). Thus, beyond rapid chromatin remodeling
ing isolated mouse nuclei through a microfluidic device coping mechanisms dedicated to releasing tension on the
(Song et al., 2022). Based on these results, the mechani- nucleus, long-term mechanical deformations can actually
cally induced chromatin softening resulting from the con- modify cell fate (Dupont & Wickstro € m, 2022).
stitutive heterochromatin decompaction was proposed to Similar mechanisms exist in plants. In the shoot apical
decrease nuclear stiffness to protect the genome against meristem, transcriptional repression and activation dynam-
mechanical stress-induced DNA damage. ically occur to specify cell fate and to promote organized
In plants, few examples illustrate the effects of cell growth and differentiation (Nguyen & Gutzat, 2022).
mechanical forces or NE destabilization on constitutive het- For example, expression of the shoot meristem mainte-
erochromatin, but correlations with stress and chromatin/ nance homeobox gene SHOOT MERISTEMLESS (STM) is
nuclear softening are far from being clear. In the Arabidop- quantitatively correlated to curvature in the saddle-shaped
sis shoot apical meristem, tissue curvature generates boundary domain of the shoot apical meristem, where tis-
nuclear compression at the boundary between organs and sue curvature generates nuclear compression (Landrein
meristem. This nuclear compression correlates with et al., 2015). Because STM repression during organogene-
decreases in DNA methylation level and chromocenter sis relies on the deposition of H3K27me3 by Polycomb
numbers and an increase in the expression of the abiotic Repressive Complex 2 (PRC2) (Kim et al., 2012), it would
stress-related linker histone H1.3 (Fal, Korsbo, et al., 2021). be interesting to determine whether mechanical stress at
Upon hyperosmotic stress in root meristematic cells, while the boundary helps to keep low levels of H3K27me3 at the
nuclei become smaller, less spherical and stiffer, the num- STM loci. In any case, this example suggests a striking dif-
ber of chromocenters was found to be decreased, suggest- ference as to the functional link between mechanical stress
ing heterochromatin reorganization (Goswami, Asnacios, and H3K27me3 in animals and plants. One possible expla-
Milani, et al., 2020). On the contrary, under hypoosmotic nation could originate from the limited cell fate plasticity
conditions nuclear rigidity was found to be decreased, with of the unipotent epidermal stem cells compared to the plu-
more diffuse heterochromatic signals (Goswami, Asnacios, ripotent character of plant stem cells. Another interesting
Milani, et al., 2020). Further supporting the links between finding was that defects at the nuclear periphery in Arabi-
the NE and constitutive heterochromatin compaction, chro- dopsis can lead to premature aging effects such as the
mocenters were also found to be affected in differentiated presence of cell death lesions through aberrant H3K27me3
tissues when plamina and LINC complex components were deposition. Thus, stress-related genes were found constitu-
mutated. Indeed, despite similar changes in nuclear mor- tively upregulated in crwn mutants due to a decrease in
phology (i.e., smaller but more spherical), an increased H3K27me3 levels at their loci (Choi et al., 2019).
compaction of chromocenters in crwn1crwn2 mutants cor- In animals, mechanistic/mammalian target of rapamy-
relates with maintenance of their transcriptional silencing, cin (mTOR) regulates PRC2-mediated gene silencing (Hara-
while altering LINC complexes causes chromocenter chi et al., 2020) and nuclear architecture in response to
decondensation and defects in their silencing (Poulet et al., stress (Lamm et al., 2020). Additionally, mTOR is also able
2017). Together, these works illustrate the complexity of to sense interruptions between chromatin and the NE,
the functional links between the NE, the plamina and con- since lamin deficiency leads to mTOR hyperactivation
stitutive heterochromatin, which may vary depending on (Chiarini et al., 2019; Ramos et al., 2012). In plants, TOR
examined tissues, e.g., cell wall stiffness differs between has recently been found to be involved in H3K27me3 depo-
meristematic and differentiated root tissues (Somssich sition and PRC2-mediated silencing of genes involved in
et al., 2016). development and stress responses (Dong et al., 2023; Ye
Table 1 NE components and their involvement in mechanosensing
Functional
Animal homologs
proteins Role References in plants Role References
Linker of Nucleoskeleton and Cytoskeleton (LINC) complex

KASH proteins
Nesprin-1 Connection to actomyosin. Involved in nuclear Burke & Roux, 2009; WIP1 Interacts with SUN1/2/3, WITs, RAnGAPs and Tatout et al., 2014
mechano-transduction. Guilluy et al., 2014; WPPs. Controls nuclear shape.
Arsenovic et al., 2016
Nesprin-2 Connection to Actin. Involved in the gravity Burke & Roux, 2009; WIP2 Interacts with SUN1/2, WITs, RAnGAPs and Groves et al., 2020
response. Touchstone et al., 2019 WPPs. Controls nuclear shape.
Nesprin-3 Connection to Vimentin IFs via plectin. Burke & Roux, 2009 WIP3 Interacts with SUN1/2, WITs, RAnGAPs and Groves et al., 2020
WPPs. Controls nuclear shape.
Nesprin-4 Connection to MTs via kinesin. Burke & Roux, 2009 TIK Interacts with all SUNs but SUN5. Controls Groves et al., 2020
nuclear size.
SINE1 Interacts with SUN1/2 and SINE2. Connection to Zhou et al., 2014;

actin. Controls nuclear positioning. Necessary Groves et al., 2020;
for MT and actin patterning. Biel et al., 2020, 2022
SINE2 Interacts with SUN1/2 and SINE1. Necessary for Groves et al., 2020; Biel
MT patterning. Necessary for Piezo-related Ca2+ et al., 2020, 2022
oscillations.
SINE3 Interacts with SUN1/2. Groves et al., 2020
SINE4 Interacts with SUN1/2. Groves et al., 2020
KASH-associated proteins
WIT1 Interaction with WIPs, RanGAPs and WPPs. Tatout et al., 2014;
Connection to actin via myosin XI-i. Groves et al., 2020
Association with NPC. Controls nuclear shape.
WIT2 Interaction with WIPs, RanGAPs and WPPs. Tatout et al., 2014;
Connection to actin via myosin XI-i. Affects Groves et al., 2020
nuclear shape.
SUN proteins
SUN1 Regulates chromatin elasticity and epigenetic Sankaran et al., 2019; SUN1 Connects to KASH proteins to lamina and Alam et al., 2016; Poulet
changes. Promotes b-catenin association with Ghosh et al., 2020; plamina and interacts with LADs. Interacts with et al., 2017; Groves
cytoskeleton upon mechanical stress. Tajik et al., 2016 SUN3/4. Controls chromocenter condensation et al., 2020
and positioning from the nuclear periphery.
Controls nuclear shape.
SUN2 Binds NUP210 to interact with histone H3.1/H3.2 Sankaran et al., 2019; SUN2 Connects to KASH proteins and to lamina and Groves et al., 2020
and BRD4 to regulate gene expression. Touchstone et al., plamina and interacts with LADs. Interacts
Promotes b-catenin association with 2019; Amin et al., 2021 withs SUN3/4. Controls nuclear shape
cytoskeleton upon mechanical stress. Involved
in gravity response.
SUN3 Functions in the NE as well as the ER. Interacts Graumann et al., 2014
with other SUNs, WIP and TIK.
(continued)
Table 1. (continued)
Functional
Animal homologs
SUN4 Functions in the NE as well as the ER. Interacts Graumann et al., 2014;
with SUN1/2/3. Specific to KASH protein TIK. Poulet et al., 2017
Affects nuclear size with SUN5. Implicated in
chromocenter condensation and distance from
the nuclear periphery.

SUN5 Functions in the NE as well as the ER. Interacts Graumann et al., 2014;
with SUN3. Affects nuclear size with SUN4. Poulet et al., 2017
Implicated in chromocenter condensation and
distance from the nuclear periphery.
Nucleopore complex (NPC)
NUP1 Necessary for the nuclear peripheral positioning Tan-Wong et al., 2009 NUP1/ Plant-specific. Interaction with heterochromatin Tamura & Hara-
of active genes via TREX2. NUP136 (TE, PcG-repressed genes). Interaction with the Nishimura, 2011;
euchromatin binding factor GBPL3. Involved in Barneche &
nuclear shaping and mRNA export. Regulates Baroux, 2017; Bi
the expression of immune-related genes. et al., 2017; Gozalo
Recruits repressed chromatin to the NPC. et al., 2020; Goto
et al., 2021; Wu et al.,
2022; Tang, Dong,
et al., 2022; Tang, Ho,
et al., 2022
NUP2 Interacts with the promoter of active genes. Tan-Wong et al., 2009 NUP82 Plant-specific. Interaction with the euchromatin Tang, Dong, et al., 2022;
binding factor GBPL3. Regulates the expression Tang, Ho, et al., 2022;
of immune-related genes. Wu et al., 2022
NUP62 Suppresses chromatin attachment on NUP155. Breuer & Ohkura, 2015 NUP98 Regulates shade-induced gene expression. Wu et al., 2022
NUP93 Controls transcriptional activation. Associates Breuer & Ohkura, 2015; NUP CPR5 Plant-specific. Regulates nuclear shape and gene Gu et al., 2016
with regions silenced via PcG-mediated Gozalo et al., 2020; expression.
repression. Regulates chromatin attachment to Zhu et al., 2022
the NPC by recruiting NUP62.
NUP107 Associates with actively transcribed genes. Gozalo et al., 2020;
Facilitates loading of ORC on specific Richards et al., 2022
chromatin regions for replication with NUP160.
NUP153 Interacts with chromatin architectural proteins Boumendil et al., 2019;
allowing rapid gene response to developmental Kadota et al., 2020
cues.
NUP155 Regulates chromatin attachment to the NPC by Breuer & Ohkura, 2015
recruiting NUP62.
NUP160 Facilitates the loading of ORC on specific Richards et al., 2022
chromatin regions for replication with NUP107.
NUP210 Regulates chromatin accessibility at the nuclear Amin et al., gulates
periphery. chromatin accessibility
at the nuclear pe
(continued)
Functional
Animal homologs
TPR Contributes to heterochromatin exclusion zones. Krull et al., 2010;

Interacts with NUP153. Boumendil et al., 2019
Lamina/plamina
A-type Modulate cortical and cytoplasmic stiffness. Bianchi & CRWN1 Necessary for chromatin binding at the nuclear Goto et al., 2014; Poulet
lamins Maintain NE rigidity. Bind to heterochromatin Lanzuolo, 2015; Cho periphery and implicated in chromocenter et al., 2017; Hirakawa
and to Nesprin-2/3 and regulate et al., 2017; formation. Interacts with GBPL3 to coordinate & Matsunaga, 2019; Hu
heterochromatin marks. Prevent NE rupture Vahabikashi stress-responsive gene expression. Involved in et al., 2019; Pontvianne
during cellular stretching. et al., 2022; Song nuclear shaping. Interacts with SUN1/2, & Liu, 2020; Tang,
et al., 2022 KAKU4, NTL9 and PWO1. Necessary for RAD54 Dong, et al., 2022;
recruitment at the nuclear periphery. Tang, Ho, et al., 2022
B-type Modulate cortical and cytoplasmic stiffness. Bianchi & CRWN2 Controls nuclear shape. Interacts with chromatin Poulet et al., 2017;
lamins Maintain NE rigidity. Bind to heterochromatin Lanzuolo, 2015; from the nucleoplasm. Implicated in Groves et al., 2020

and to Nesprin-2/3 and regulate Pascual-Reguant et al., chromocenter formation.
heterochromatin marks. Prevent NE rupture 2018
during cellular stretching. Interact with
chromatin via euchromatin lamin-associated
domains (eLADs).
C-type Prevent NE rupture during cellular stretching. Cho et al., 2017; Song CRWN3 Interacts with chromatin from the nucleoplasm. Groves et al., 2020
lamins Bind to heterochromatin and regulate et al., 2022;
heterochromatin marks. Vahabikashi
et al., 2022
CRWN4 Necessary for chromatin binding at the nuclear Hirakawa &
periphery. Controls nuclear shape and size. Matsunaga, 2019
Interacts with KAKU4, PWO1 and PUX3/4/5.
Necessary for RAD54 recruitment at the nuclear
periphery.
KAKU4 Interacts with CRWN1, CRWN4, PUX3/4/5 and Tang, Dong, et al., 2022;
GBPL3. Tang, Ho, et al., 2022
Lamina- and plamina/INM-associated proteins
Emerin Transferred from the INM to the ONM after Brachner & Foisner, PNET2 Interacts with GBPL3, KAKU4 and CRWN1. Tang, Dong, et al., 2022;
chromatin detachment from the lamina to help 2011; Cho et al., 2017 Associates with nucleosome-enriched Tang, Ho, et al., 2022
actin polymerization around the NE in response chromatin and maintains chromatin
to shearing forces. organization. Necessary for growth and stress
responses.
Man1 Binds heterochromatin at the nuclear periphery. Brachner & Foisner, NEAP1 Interacts with SUN1/2 and bZIP18. Controls Pawar et al., 2016
2011; Tang, Dong, nuclear size and maintains heterochromatin.
et al., 2022; Tang, Ho,
et al., 2022
Lem2 Binds heterochromatin at the nuclear periphery. Pieper et al., 2020 NEAP2 Interacts with SUN1/2 and bZIP18. Pawar et al., 2016
Nur1 Binds heterochromatin at the nuclear periphery. Pieper et al., 2020 NEAP3 Interacts with SUN1/2 and bZIP18. Controls Pawar et al., 2016
nuclear size and maintains heterochromatin.
(continued)
et al., 2022). Together with the growing body of evidence
Nakamura et al., 2012;
Nakamura et al., 2012;

Goswami, Asnacios,
Goswami, Asnacios,
that TOR also controls cytoskeleton organization and
Mikulski et al., 2019
Milani, et al., 2020
Milani, et al., 2020

et al., 2013, 2015;
et al., 2013, 2015;

Janski et al., 2012;
Janski et al., 2012;

dynamics (Cao et al., 2019; Dai et al., 2022), the position of
Batzenschlager
Batzenschlager
TOR at the nexus between cytoskeleton and nuclear
References
dynamics (Dong et al., 2023) in plant cells becomes

increasingly clear.
Regulation of euchromatin
Histone acetylation and trimethylation of H3K4 are typical
euchromatic marks that positively correlate with gene tran-
Association with CRWN1 necessary for the
Regulates NPC distribution around the NE.
Regulates NPC distribution around the NE.

Necessary for MT nucleation on the NE.
Necessary for MT nucleation on the NE. scription. In mouse melanoma cells, the histone deacety-
centromeric cohesion, nuclear size and
centromeric cohesion, nuclear size and

expression of touch-responsive genes.
Interaction with centromeres. Controls
expression of touch-responsive genes
lase (HDAC) inhibitor trichostatin A (TSA) was used to

Interacts with centromeres. Controls
soften stiff nuclei and alter chromatin structure in order to

inhibit cell migration (Gerlitz & Bustin, 2010). Because TSA
regulation of specific genes.
also leads to increased tubulin acetylation and stability,

resulting in reduced cytoskeletal stiffness (Fischer et al.,
2020), its impact on nuclear rigidity probably reflects a
combined effect on both euchromatin and the cytoskele-
ton. Inversely, forcing animal cells (i.e., mammary epithe-
lial cells, mesenchymal stem cells or fibroblasts) into
micropatterned substrates to alter cellular geometry results
Role
in smaller and stiffer nuclei, global histone deacetylation,

chromatin condensation and an overall reduction in gene
€ m, 2022). Besides this, a
Functional
expression (Dupont & Wickstro

homologs
in plants
strong positive correlation was observed between nuclear

PWO1
GIP1
GIP2
volume and histone acetylation, suggesting that changes

in nuclear morphology might enhance accessibility to tran-
scriptional machinery and hence regulate total transcrip-
tion levels (Jain et al., 2013). The notion that active histone
marks positively respond to changes in mechanical force
was further explored in melanoma aggregates, in which
References
tissue curvature promotes H3K4 methylation and H3 acety-

lation to increase expression of pro-oncogenic genes (Lee
et al., 2020). As a possible mechanism, the cytoplasmic-to-
nuclear redistribution of HDAC3 was reported to depend
on actomyosin contractility (Jain et al., 2013). In plants,
only indirect proof has been reported so far. On one side,
nuclei change their shape during root elongation from
spherical in the meristem to spindle-shaped in the epider-
mis (Meier et al., 2016). On the other side, using TSA to
inhibit HDAC results in hyperacetylation of histones H3
and H4 and alters the expression of specific genes involved
in root cellular patterning (Xu et al., 2005). Together,
nuclear shape and histone acetylation may function in
mediating gene expression for root tissue patterning.
Gene positioning inside the nucleus is critical for
expression (Egecioglu & Brickner, 2011). In yeast, most
transcription factors are capable of tethering target genes
Role
to NPCs, thus promoting their expression (Brickner et al.,

2019). Accordingly, specific NPC components are attached
to chromatin loops harboring actively transcribed genes
Others
(Bianchi & Lanzuolo, 2015). Relocation of chromatin close

proteins
Animal
to NPCs for high transcriptional activity is also observed in

animals, with several NPC components being responsive
to mechanical signals (Matsuda & Mofrad, 2022). This is diseases in both animals and plants (Goto et al., 2021;
the case for NUP210, which was recently found to promote Skinner & Johnson, 2017). For example, lobulated nuclei
chromatin accessibility at the nuclear periphery in occur in the most mature form of neutrophils, making
response to extracellular mechanical signals during metas- nuclei more deformable and helping neutrophils to easily
tasis (Amin et al., 2021). In Drosophila, NUP107, a core pass through small gaps in the endothelium and the extra-
component of the outer ring subcomplex, and NUP93, a cellular matrix (Hoffmann et al., 2007). Besides altered
core component of the inner ring subcomplex, were found cytoskeleton organization, differentiation of bovine and
to associate with actively transcribed genes and Polycomb- human mesenchymal stem cells implies changes in
silenced regions, respectively, revealing a complex land- nuclear shape, stiffness and organization due to restructur-
scape of NE–genome interactions (Gozalo et al., 2020). This ing of the A/C-type lamin network and an increase in het-
duality has a central role in cellular differentiation and its erochromatin content. Even if these changes can be both
disequilibrium is associated with specific diseases (Bianchi consequences and mediators of differentiation, the nucleus
& Lanzuolo, 2015). seems to act as a mechanosensor during cell differentia-
In plants, NPCs are largely surrounded by repressive tion (Heo et al., 2016). Further supporting this, in human
heterochromatin domains (Barneche & Baroux, 2017; Bi mesenchymal stem cells undergoing adipocyte differentia-
et al., 2017; Gozalo et al., 2020) and some of their compo- tion, the size of nuclei was found to be decreased and their
nents can interact with heterochromatic factors such as aspect ratio was increased, while at the same time, A/C-
LIKE HETEROCHROMATIN PROTEIN1 (LHP1) (Chen et al., type lamins were more highly expressed and redistributed
2020). Reminiscent of bacterial operons, silent biosynthetic toward the nuclear periphery (McColloch et al., 2019). Simi-
gene clusters in Arabidopsis were found at the nuclear larly, during the stepwise differentiation program that gov-
periphery associated with heterochromatic domains, while erns epidermal stratification, epidermal cells decrease their
transcriptionally active ones relocate away from the intrinsic tension and undergo marked nuclear changes,
nuclear periphery (Nutzmann et al., 2020). In contrast, sev- such as a decrease of the nuclear volume and of transcrip-
eral light-inducible loci were reported to relocate from the tional activity, an increase of heterochromatin levels, and a
nuclear interior to the periphery upon their activation in relocation of heterochromatin toward the nuclear interior
response to light stress in Arabidopsis (Feng et al., 2014). (Miroshnikova et al., 2019). Beside this, the nucleus can
Similarly, artificial targeting of a luciferase reporter gene to perceive tension, compression or shear from the extracel-
the NPC using the Lac Operator/Lac Repressor system lular environment through cytoskeleton reorganization
results in its increased expression (Smith et al., 2015). Fur- (Kirby & Lammerding, 2018). Under hypoosmotic stress,
ther supporting that NPCs act as transcriptional hubs to the nucleus expands thanks to lamina stretching, while
promote gene expression, the euchromatin binding factor under hyperosmotic stress, the nucleoplasm contracts and
GBPL3 interacts with the nuclear basket components the nucleus shrinks (Finan & Guilak, 2010). By increasing
NUP82 and NUP136, as well as with CRWN1 (Tang, Ho, surface tension at the NE, mechanical stimuli increase the
et al., 2022), to coordinate expression during plant devel- NPC diameter and consequently affect all NPC-related
opment and stress responses (Bi et al., 2017). Together, functions (Allen & Strader, 2021). Also, since the ONM
NPCs and the nuclear periphery seem to have dichoto- forms a continuum with the ER, which contains MS ion
mous functions in both animal and plant cells, and the channels, tension at the NE activates these channels, lead-
question whether these functions are differently driven by ing to Ca2+ release, impacting cell contractility (Lomakin
mechanical forces remains to be answered. et al., 2020) and chromatin organization (Nava et al., 2020).
During plant root development, besides cell shape
NE DYNAMICS AND ITS FUNCTIONAL RELEVANCE
modifications, nuclei change from rounded in the meri-
Changes in nuclear structure and morphology modulate stem to elongated in the differentiation area (Meier et al.,
key cellular and genomic functions, thus being critical for 2016). Nuclear migration in growing root hairs (Singh, Per-
cell differentiation and organism development (Kalukula eira, et al., 2021) or pollen tubes (Zhou & Meier, 2014) in
et al., 2022). For that reason, particular nuclear shapes Arabidopsis is also accompanied by nuclear shape
were correlated to specific cell identities and/or tissue con- changes. In contrast to animals, in which nuclei are moved
texts in both animals and plants (Deolal & Mishra, 2021; by motor proteins along the MT cytoskeleton, in root hairs
Meier et al., 2016). the actin cytoskeleton and a myosin motor physically inter-
act with the NE through a SUN–WIP–WIT bridge to enable
Nuclear shaping during development and in response to
nuclear movement (Tamura et al., 2013). In addition, hyper-
extracellular constraints
osmotic stress results in marked chromatin condensation
Changes in nuclear shape usually reflect altered nuclear (Martins et al., 2012). In Arabidopsis root meristematic
mechanics and are highly relevant to normal development cells, similar changes were observed, with nuclei and het-
and physiology, as well as for responses to stress and erochromatic chromocenters shrinking upon hyperosmotic
stress and mechanoresponsive genes being induced (Gos- DNA breaks at the nuclear periphery of root meristematic
wami, Asnacios, Milani, et al., 2020). Even if this knowl- nuclei (Singh, Batzenschlager, et al., 2021). Therefore, the
edge is just emerging in plants, the nucleus appears to act NE in eukaryotes contributes to homologous recombina-
as a mechanosensor in response to developmental and tion repair and genome stability at the nuclear periphery.
environmental cues (Fal et al., 2017; Goswami, Asnacios,
OUTLOOK: A NEED TO DEVELOP TOOLS FOR LIVE CELL
Hamant, & Chaboute, 2020).
IMAGING LINKING NUCLEAR MECHANICS AND
Impacts of NE dynamics on chromatin during the cell CHROMATIN REMODELING
cycle and upon DNA damage
Up to now most nuclear and cytoplasmic membrane shape
During the transition from G1 to the S/G2 phase, nuclei changes were evaluated through morphological and physi-
from proliferating human cells change their shape (Chu cal parameters using technical approaches such as micro-
et al., 2017). Interestingly, inhibition of myosin II during the rheometry, atomic force microscopy (AFM) or optical
G1 phase prevents nuclear flattening and impedes progres- tweezers (Goswami, Asnacios, Hamant, & Chaboute, 2020).
sion to the S phase (Aureille et al., 2019). In plants, chro- In order to quantify and visualize intracellular membrane
matin also undergoes drastic changes affecting its degree tensions in cellulo, new tools have to be developed. In ani-
of compaction during the cell cycle (Pecinka et al., 2020). mals, the Fluorescent Lipid Tension Reporter (FliptR) can
During cell division, the NE disassembles upon entry into measure external membrane tension based on lifetime
mitosis and reforms in the telophase around the two sepa- measurements (Colom et al., 2018). More recently, the
rated sets of daughter chromosomes. In animals, MT- development of a HaloTag-Nuclear Localization Signal
induced tearing of the nuclear lamina seems to contribute photocleavable fluorescent probe to evaluate tension in
to NE breakdown (Beaudouin et al., 2002). Then, upon the NE seems very promising (Lopez-Andarias et al., 2022).
mitosis exit, the NE reassembles around decondensed In plants, the recent development of an imaging microvisc-
chromosomes through the binding of INM proteins to osity toolbox for cells and tissues has enabled to specifi-
chromatin (Ulbert et al., 2006). In plants, NE breakdown is cally visualize tension at the plasma membrane and cell
also dictated by MT dynamics with the relocation of the € rster resonance energy trans-
wall (Michels et al., 2020). Fo
nucleoporin RAE1 on spindle MTs (Masoud et al., 2013). In fer protein biosensors of osmotic stress, such as SENSOR
mammalian cells, SUN1 and the membrane-associated his- EXPRESSING DISORDERED PROTEIN 1 (SED1), based on
tone acetyltransferase hALP contribute to chromosome the Arabidopsis intrinsically disordered AtLEA4-5 protein,
decondensation at the end of mitosis during NE reforma- have already been developed and used to track the effects
tion (Chi et al., 2007). Following NE dynamics, Arabidopsis of osmotic stress on living bacterial, plant and human cells
SUN1 orthologs change their localization dynamically dur- (Cuevas-Velazquez et al., 2021). Non-destructive and non-
ing mitosis (Oda & Fukuda, 2011). However, the underlying invasive methods such as the new type of optical elasto-
mechanisms of NE reformation are not yet understood. graphy named Brillouin microscopy, based on photon–
In human cancer cells, mechanical forces can increase phonon interactions, can be used to evaluate cellular and
DNA replication stress and genome instability, thereby tissue mechanical properties in 3D (Prevedel et al., 2019)
contributing to tumorigenesis. Indeed, nuclear deforma- and also intranuclear mechanics (Liu et al., 2022). Live cell
tions resulting from cell migration in tight spaces or exter- imaging of macromolecular crowding will also provide
nal cell compression were found to cause DNA damage new information about changes of cell physical properties
associated with replication stress without NE rupture (Shah in response to mechanical cues. Recently, the development
et al., 2021). One explanation could be that torsional stress of genetically encoded multimeric nanoparticles (GEMs) as
in DNA increases due to physical deformations of the microrheology probes has allowed to evaluate biophysical
nucleus. This explanation is supported by the fact that the properties of the cytoplasm and nucleoplasm of yeast and
ataxia telangiectasia-mutated and Rad3-related (ATR) pro- human cells (Delarue et al., 2018). At the chromatin level,
tein, which is an upstream regulator of replicative stress, live-cell imaging has to be addressed in different genetic
has been reported to be mechanosensitive (Kumar et al., backgrounds by modifying epigenetic status through
2014). ATR-defective cells exhibit altered nuclear morphol- directed global and local histone modifications using for
ogy and mechanical properties, together with aberrant instance chromatybodies and dCas9 approaches (Fal, Tom-
perinuclear chromatin organization and increased hetero- kova, et al., 2021).
chromatinization (Kidiyoor et al., 2020). In Arabidopsis, Altogether, current and future technical improvements
crwn1crwn4 double mutants are hypersensitive to geno- will contribute to further address and unravel mechano-
toxic stress and show reduced anchoring of RAD54 at the biology processes in the very particular context of walled
nuclear periphery (Hirakawa & Matsunaga, 2019). Similarly, plant cells. These recent technological developments will
gip1gip2 mutants present increased genome instability also allow to investigate in more detail reciprocal inter-
due to impaired recruitment of RAD51 at double-stranded plays between chromatin, the nucleoskeleton, the NE and
the cytoskeleton impacting nuclear mechanics in the con- Biedzinski, S., Agsu, G., Vianay, B., Delord, M., Blanchoin, L., Larghero, J.
et al. (2020) Microtubules control nuclear shape and gene expression
text of plant growth and development. Lastly, considering
during early stages of hematopoietic differentiation. The EMBO Journal,
mechanical stress acclimation/adaptation of plants, the 39, e103957.
expected new findings will certainly contribute to our Biel, A., Moser, M. & Meier, I. (2020) Arabidopsis KASH proteins SINE1 and
SINE2 are involved in microtubule reorganization during ABA-induced
understanding of how mechanical stress may confer tran-
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FUNDING INFORMATION
Boumendil, C., Hari, P., Olsen, K.C.F., Acosta, J.C. & Bickmore, W.A. (2019)
Nuclear pore density controls heterochromatin reorganization during
This work was supported by the Centre National de la
senescence. Genes and Development, 33, 144–149.
Recherche Scientifique (CNRS), Human Frontier Science Brachner, A. & Foisner, R. (2011) Evolvement of LEM proteins as chromatin
Program grant RGP 0009/2018, ANR-18-CE20-0011 project tethers at the nuclear periphery. Biochemical Society Transactions, 39,
1735–1741.
REWIRE and ANR-20-CE13-0025 project MechaNUC.
Brenya, E., Pervin, M., Chen, Z.H., Tissue, D.T., Johnson, S., Braam, J. et al.
(2022) Mechanical stress acclimation in plants: linking hormones and
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The Plant Journal (2023) doi: 10.1111/tpj.

SPECIAL ISSUE REVIEW

Nuclear envelope dynamics in connection to chromatin

Received 30 December 2022; revised 29 March 2023; accepted 12 April 2023.

Keywords: nuclear envelope, cytoskeleton, nucleoskeleton, mechanical cues, chromatin, epigenetics.

Impact on constitutive heterochromatin Regulation of facultative heterochromatin

Linker of Nucleoskeleton and Cytoskeleton (LINC) complex

The Plant Journal, (2023), doi: 10.1111/tpj.16246

the nuclear periphery.

TPR Contributes to heterochromatin exclusion zones. Krull et al., 2010;

The Plant Journal, (2023), doi: 10.1111/tpj.16246

et al., 2022). Together with the growing body of evidence

Nakamura et al., 2012;

Nakamura et al., 2012;

Milani, et al., 2020

Milani, et al., 2020

et al., 2013, 2015;

Janski et al., 2012;

dynamics (Dong et al., 2023) in plant cells becomes

Regulates NPC distribution around the NE.

Regulates NPC distribution around the NE.

centromeric cohesion, nuclear size and

lase (HDAC) inhibitor trichostatin A (TSA) was used to

soften stiff nuclei and alter chromatin structure in order to

also leads to increased tubulin acetylation and stability,

in smaller and stiffer nuclei, global histone deacetylation,

expression (Dupont & Wickstro

strong positive correlation was observed between nuclear

volume and histone acetylation, suggesting that changes

tissue curvature promotes H3K4 methylation and H3 acety-

to NPCs, thus promoting their expression (Brickner et al.,

(Bianchi & Lanzuolo, 2015). Relocation of chromatin close

to NPCs for high transcriptional activity is also observed in

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