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Feedback from Tissue Mechanics Self-Organizes Efficient Outgrowth of Plant Organ.

ABSTRACT: Plant organ outgrowth superficially appears like the continuous mechanical deformation of a sheet of cells. Yet, how precisely cells as individual mechanical entities can act to morph a tissue reliably and efficiently into three dimensions during outgrowth is still puzzling, especially when cells are tightly connected as in plant tissue. In plants, the mechanics of cells within a tissue is particularly well-defined because individual cell growth is essentially the mechanical yielding of the cell wall in response to internal turgor pressure. Cell-wall stiffness is controlled by biological signaling, which is impacted by stresses, and hence, cell growth is observed to respond to mechanical stresses building up within a tissue. What is the role of the mechanical feedback during morphing of tissue in three dimensions? Here, we develop a three-dimensional vertex model to investigate tissue mechanics at the onset of organ outgrowth at the tip of a plant shoot. We find that organ height is primarily governed by the ratio of growth rates of faster-growing cells initiating the organ versus slower-growing cells surrounding them. Remarkably, the outgrowth rate is higher when cell growth responds to the tissue-wide mechanical stresses. Our quantitative analysis of simulation data shows that tissue mechanical feedback on cell growth can act via a twofold mechanism. First, the feedback guides patterns of cellular growth. Second, the feedback modifies the stress patterns on the cells, consequently amplifying and propagating growth anisotropies. This mechanism may allow plants to grow organs efficiently out of the meristem by reorganizing the cellular growth rather than inflating growth rates.

SUBMITTER: Khadka J

PROVIDER: S-EPMC7019024 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Feedback from Tissue Mechanics Self-Organizes Efficient Outgrowth of Plant Organ.

Khadka Jason J Julien Jean-Daniel JD Alim Karen K

Biophysical journal 20191024 10

Plant organ outgrowth superficially appears like the continuous mechanical deformation of a sheet of cells. Yet, how precisely cells as individual mechanical entities can act to morph a tissue reliably and efficiently into three dimensions during outgrowth is still puzzling, especially when cells are tightly connected as in plant tissue. In plants, the mechanics of cells within a tissue is particularly well-defined because individual cell growth is essentially the mechanical yielding of the cell ...[more]

PMID: 31727319

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Project description:BackgroundEndoderm organ primordia become specified between gastrulation and gut tube folding in Amniotes. Although the requirement for RA signaling for the development of a few individual endoderm organs has been established a systematic assessment of its activity along the entire antero-posterior axis has not been performed in this germ layer.Methodology/principal findingsRA is synthesized from gastrulation to somitogenesis in the mesoderm that is close to the developing gut tube. In the branchial arch region specific levels of RA signaling control organ boundaries. The most anterior endoderm forming the thyroid gland is specified in the absence of RA signaling. Increasing RA in anterior branchial arches results in thyroid primordium repression and the induction of more posterior markers such as branchial arch Hox genes. Conversely reducing RA signaling shifts Hox genes posteriorly in endoderm. These results imply that RA acts as a caudalizing factor in a graded manner in pharyngeal endoderm. Posterior foregut and midgut organ primordia also require RA, but exposing endoderm to additional RA is not sufficient to expand these primordia anteriorly. We show that in chick, in contrast to non-Amniotes, RA signaling is not only necessary during gastrulation, but also throughout gut tube folding during somitogenesis. Our results show that the induction of CdxA, a midgut marker, and pancreas induction require direct RA signaling in endoderm. Moreover, communication between CdxA(+) cells is necessary to maintain CdxA expression, therefore synchronizing the cells of the midgut primordium. We further show that the RA pathway acts synergistically with FGF4 in endoderm patterning rather than mediating FGF4 activity.Conclusions/significanceOur work establishes that retinoic acid (RA) signaling coordinates the position of different endoderm organs along the antero-posterior axis in chick embryos and could serve as a basis for the differentiation of specific endodermal organs from ES cells.

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Feedback from Tissue Mechanics Self-Organizes Efficient Outgrowth of Plant Organ.

Publications

Feedback from Tissue Mechanics Self-Organizes Efficient Outgrowth of Plant Organ.

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