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Mechanotransduction in the plant nucleus

Plants have developed many strategies to adapt to their environment. We show that the cell nucleus becomes denser and more rigid in response to drought. This response involves a nuclear envelope regulator and promotes the expression of mechanosensitive genes conferring plants a resistance to stress.

The plant cell, like any eukaryotic cell, is able to perceive environmental signals and transduce them to the nucleus, which in turn modify the cell response (1). Until now, the nuclear response was mostly analyzed from the biochemical and transcriptional points of view. But nuclei are also physical objects and their mechanics likely play an important role in signal transduction.

To modify the mechanical status of the nucleus, we used salt and sugar to mimic drought conditions, a physiological stress, in the model plant A. thaliana. Visualizing a marker of the nuclear envelope by live cell imaging, we found that the nucleus changes its shape in the root tip cells. Using micro-rheometry, this was correlated with increased nucleus stiffness and compactness under such hyperosmotic stress.

Figure 1: Plant isolated nucleus before and after compression (left) (chromatin is labelled) and nuclei in the root tip (nuclear envelope is labelled) before and after hyperosmotic stress. Note the altered nuclear shape in stress conditions.


This response was associated with the induction of mechanosensitive genes that allow the plant to resist stress. All these responses being reversible, we show that the nucleus behaves like a mechanical rheostat in plants. The small multifunctional proteins GIPs/MZT1 (2), located in particular on both sides of the nuclear envelope, and interacting with the microtubule cytoskeleton in the cytoplasm (3) and with the centromeres in the nucleus (4), negatively regulates these responses. Mutants deficient in GIPs exhibit a constitutive response to hyperosmotic stress. In other words, in normal osmotic conditions, the nuclei of the mutant's cells are already deformed and prepared to resist stress. They give plants greater resistance to hyperosmotic stress, in particular by limiting the effects of senescence on their leaf system. These results open a new avenue of research on the role of the nuclear envelope in the perception of environmental and mechanical stresses, and allow a better understanding of how plants resist water stress.

The support of HFSP in this work has been instrumental to set the basis of nuclear mechanics investigation and to further explore the link between nuclear shape and chromatin remodeling through mechano-transduction at the single cell level.

Figure 2: Phenotype of WT (wild type) and gip1gip2 mutant plant after a severe hyperosmotic stress: note the absence of leave senescence in the mutant.



Mechanical Shielding in Plant Nuclei. Goswami R, Asnacios A, Milani P, Graindorge S, Houlné G, Mutterer J, Hamant O, Chabouté ME., Curr. Biol. 2020;30(11):2013-2025.e3. doi:10.1016/j.cub.2020.03.059

Other references

1. Nuclear envelope: a new frontier in plant mechanosensing? Fal K, Asnacios A, Chabouté ME, Hamant O. Biophys Rev. 2017 Aug;9(4):389-403. doi: 10.1007/s12551-017-0302-6.

2. The GCP3-interacting proteins GIP1 and GIP2 are required for γ-tubulin complex protein localization, spindle integrity, and chromosomal stability. Janski N, Masoud K, Batzenschlager M, Herzog E, Evrard JL, Houlné G, Bourge M, Chabouté ME, Schmit AC. Plant Cell. 2012 Mar;24(3):1171-87. doi: 10.1105/tpc.111.094904.

3. The GIP gamma-tubulin complex-associated proteins are involved in nuclear architecture in Arabidopsis thaliana. Batzenschlager M, Masoud K, Janski N, Houlné G, Herzog E, Evrard JL, Baumberger N, Erhardt M, Nominé Y, Kieffer B, Schmit AC, Chabouté ME. Front Plant Sci. 2013 Nov 27;4:480. doi: 10.3389/fpls.2013.00480.

4. Arabidopsis MZT1 homologs GIP1 and GIP2 are essential for centromere architecture. Batzenschlager M, Lermontova I, Schubert V, Fuchs J, Berr A, Koini MA, Houlné G, Herzog E, Rutten T, Alioua A, Fransz P, Schmit AC, Chabouté ME. Proc Natl Acad Sci U S A. 2015 Jul 14;112(28):8656-60. doi: 10.1073/pnas.1506351112

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Mechanical Shielding in Plant Nuclei. Goswami R, Asnacios A, Milani P, Graindorge S, Houlné G, Mutterer J, Hamant O, Chabouté ME., Curr. Biol. 2020;30(11):2013-2025.e3. doi:10.1016/j.cub.2020.03.059