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Tissue folding at the organ–meristem boundary results in nuclear compression and chromatin compaction

Fal, Kateryna LU ; Korsbo, Niklas ; Alonso-Serra, Juan ; Teles, Jose LU ; Liu, Mengying ; Refahi, Yassin ; Chabouté, Marie Edith ; Jönsson, Henrik LU and Hamant, Olivier (2021) In Proceedings of the National Academy of Sciences of the United States of America 118(8).
Abstract

Artificial mechanical perturbations affect chromatin in animal cells in culture. Whether this is also relevant to growing tissues in living organisms remains debated. In plants, aerial organ emergence occurs through localized outgrowth at the periphery of the shoot apical meristem, which also contains a stem cell niche. Interestingly, organ outgrowth has been proposed to generate compression in the saddle-shaped organ–meristem boundary domain. Yet whether such growth-induced mechanical stress affects chromatin in plant tissues is unknown. Here, by imaging the nuclear envelope in vivo over time and quantifying nucleus deformation, we demonstrate the presence of active nuclear compression in that domain. We developed a quantitative... (More)

Artificial mechanical perturbations affect chromatin in animal cells in culture. Whether this is also relevant to growing tissues in living organisms remains debated. In plants, aerial organ emergence occurs through localized outgrowth at the periphery of the shoot apical meristem, which also contains a stem cell niche. Interestingly, organ outgrowth has been proposed to generate compression in the saddle-shaped organ–meristem boundary domain. Yet whether such growth-induced mechanical stress affects chromatin in plant tissues is unknown. Here, by imaging the nuclear envelope in vivo over time and quantifying nucleus deformation, we demonstrate the presence of active nuclear compression in that domain. We developed a quantitative pipeline amenable to identifying a subset of very deformed nuclei deep in the boundary and in which nuclei become gradually narrower and more elongated as the cell contracts transversely. In this domain, we find that the number of chromocenters is reduced, as shown by chromatin staining and labeling, and that the expression of linker histone H1.3 is induced. As further evidence of the role of forces on chromatin changes, artificial compression with a MicroVice could induce the ectopic expression of H1.3 in the rest of the meristem. Furthermore, while the methylation status of chromatin was correlated with nucleus deformation at the meristem boundary, such correlation was lost in the h1.3 mutant. Altogether, we reveal that organogenesis in plants generates compression that is able to have global effects on chromatin in individual cells.

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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Chromatin, Mechanical forces, Nucleus, Organogenesis, Plant
in
Proceedings of the National Academy of Sciences of the United States of America
volume
118
issue
8
article number
e2017859118
publisher
National Acad Sciences
external identifiers
  • pmid:33608459
  • scopus:85101285372
ISSN
0027-8424
DOI
10.1073/pnas.2017859118
language
English
LU publication?
yes
id
fb6ddcdf-72cd-4cf3-ad63-17887fedd78a
date added to LUP
2021-03-09 10:59:36
date last changed
2021-06-16 05:05:15
@article{fb6ddcdf-72cd-4cf3-ad63-17887fedd78a,
  abstract     = {<p>Artificial mechanical perturbations affect chromatin in animal cells in culture. Whether this is also relevant to growing tissues in living organisms remains debated. In plants, aerial organ emergence occurs through localized outgrowth at the periphery of the shoot apical meristem, which also contains a stem cell niche. Interestingly, organ outgrowth has been proposed to generate compression in the saddle-shaped organ–meristem boundary domain. Yet whether such growth-induced mechanical stress affects chromatin in plant tissues is unknown. Here, by imaging the nuclear envelope in vivo over time and quantifying nucleus deformation, we demonstrate the presence of active nuclear compression in that domain. We developed a quantitative pipeline amenable to identifying a subset of very deformed nuclei deep in the boundary and in which nuclei become gradually narrower and more elongated as the cell contracts transversely. In this domain, we find that the number of chromocenters is reduced, as shown by chromatin staining and labeling, and that the expression of linker histone H1.3 is induced. As further evidence of the role of forces on chromatin changes, artificial compression with a MicroVice could induce the ectopic expression of H1.3 in the rest of the meristem. Furthermore, while the methylation status of chromatin was correlated with nucleus deformation at the meristem boundary, such correlation was lost in the h1.3 mutant. Altogether, we reveal that organogenesis in plants generates compression that is able to have global effects on chromatin in individual cells.</p>},
  author       = {Fal, Kateryna and Korsbo, Niklas and Alonso-Serra, Juan and Teles, Jose and Liu, Mengying and Refahi, Yassin and Chabouté, Marie Edith and Jönsson, Henrik and Hamant, Olivier},
  issn         = {0027-8424},
  language     = {eng},
  number       = {8},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {Tissue folding at the organ–meristem boundary results in nuclear compression and chromatin compaction},
  url          = {http://dx.doi.org/10.1073/pnas.2017859118},
  doi          = {10.1073/pnas.2017859118},
  volume       = {118},
  year         = {2021},
}