Nuclear envelope: a new frontier in plant mechanosensing?

Abstract

In animals, it is now well established that forces applied at the cell surface are propagated through the cytoskeleton to the nucleus, leading to deformations of the nuclear structure and, potentially, to modification of gene expression. Consistently, altered nuclear mechanics has been related to many genetic disorders, such as muscular dystrophy, cardiomyopathy and progeria. In plants, the integration of mechanical signals in cell and developmental biology has also made great progress. Yet, while the link between cell wall stresses and cytoskeleton is consolidated, such cortical mechanical cues have not been integrated with the nucleoskeleton. Here, we propose to take inspiration from studies on animal nuclei to identify relevant methods amenable to probing nucleus mechanics and deformation in plant cells, with a focus on microrheology. To identify potential molecular targets, we also compare the players at the nuclear envelope, namely lamina and LINC complex, in both plant and animal nuclei. Understanding how mechanical signals are transduced to the nucleus across kingdoms will likely have essential implications in development (e.g. how mechanical cues add robustness to gene expression patterns), in the nucleoskeleton–cytoskeleton nexus (e.g. how stress is propagated in turgid/walled cells), as well as in transcriptional control, chromatin biology and epigenetics.

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

“…The role of mechanical transduction in regulating gene expression is inc reasingly discussed (71, 72). Since CRWN proteins also interact with genomic regions (15), and chromatin modifiers influencing gene expression (73, 74), complexes associating CRWN proteins with the nucleoskeleton and/or the NPC may provide a molecular mechanism to the hypothesized rheostat function of the nuclear envelope (75).…”

Is the plant nucleus a mechanical rheostat?

“…Both NE components, notably LINC complexes (Linker of Nucleoskeleton and Cytoskeleton) and NPC may contribute to changes of mechanical properties of the nucleus in animals [7]. In plants LINC complexes and NPC have been identified [8].…”

Microtubular and Nuclear Functions of γ-Tubulin: Are They LINCed?

“…Mechanical stimuli are transmitted from the extracellular matrix to membranes and through the microtubular and actin cytoskeleton to the nucleus. SUN1 and SUN2 are part of mechanotransduction and nuclear-cytoplasmic communication; for details follow references reviewed in Reference [106]. In animal cells, SUN1 is more tightly bound to the lamina than SUN2 and is required for the positioning of the nucleus based on the microtubular cytoskeleton, while SUN2 is required for actin-mediated nuclear movement [85].…”

“…However, the microtubular and actin cytoskeleton and SUN proteins are conserved. The nuclear envelope is suggested to be important in mechanosensing transduction to the nucleus, with SUN proteins, GIPs, and CRWN proteins being the potential components of the pathway [106].…”

“…The graphical summary of nuclear γ-tubulin interactions and functions in animal and plant cells. Particular sections are based on published data or modified according to the cited references: γ-strings [41], γ-tubulin fibrils [2], LINC complexes [96,106], lamina interactions and INM integral proteins [77], emerin and Samp1 [100,101], SUN protein interactions [82,97], CRWN (former LINC) proteins [97,121,122], GIP [105], Rae1 and MSL6 [123], kinetochore [22,23], E2F regulation [69,77,124], DNA damage response [61,64,125]. ONM: outer nuclear membrane; INM: inner nuclear membrane; NPC: nuclear pore complex; CEN: centromere.…”