Computational modeling of cambium activity provides a regulatory framework for simulating radial plant growth

Abstract

Precise organization of growing structures is a fundamental process in developmental biology. In plants, radial growth is mediated by the cambium, a stem cell niche continuously producing wood (xylem) and bast (phloem) in a strictly bidirectional manner. While this process contributes large parts to terrestrial biomass, cambium dynamics eludes direct experimental access due to obstacles in live cell imaging. Here, we present a cell-based computational model visualizing cambium activity and integrating the function of central cambium regulators. Performing iterative comparisons of plant and model anatomies, we conclude that the receptor-like kinase PXY and its ligand CLE41 are part of a minimal framework sufficient for instructing tissue organization. By integrating tissue-specific cell wall stiffness values, we moreover probe the influence of physical constraints on tissue geometry. Our model highlights the role of intercellular communication within the cambium and shows that a limited number of factors is sufficient to create radial growth by bidirectional tissue production.

Endogenous and environmental signals in regulating vascular development and secondary growth

“…Tools that combine the quantitative 3D image analysis and clonal analysis may be essential to understand cambium development ( Bencivenga et al., 2016 ). In addition, integrating cell-based computational model and the function of central cambium regulators help to determine the framework for instructing tissue organization ( Lebovka et al., 2023 ). Lastly, pulse labeling, lineage tracing, and molecular genetic techniques have advanced our understanding on the bifacial nature of vascular stem cells in both hypocotyl and root tissues in model plants Arabidopsis ( Shi et al., 2019 ; Smetana et al., 2019 ).…”

Gene Regulatory Network topology mediates the role of diffusible components in cellular patterns: the root epidermis of Arabidopsis thaliana as a study system

“…Of interest for this model is the Epilog platform that allows the logical simulation of genetic and signaling processes and the coupling of these in a cellular domain using hexagonal grids [119]; this approach has been applied to explain the emergence of dorsal-ventral patterns of organization in sea urchin embryo [39], which shows that approaches such as the one proposed in this work can be easily extended to reduce their limitations. On the other hand, specific platforms have been applied or developed to explore the coupling of intracellular processes with cellular dynamics to understand tissue and organ formation in plants, for example, VirtualLeaf [2,68,81], Virtual Plant Tissue [25], CellModeller [36], CellZilla [102] and CompuCell3D [44]. These platforms allow the incorporation of intracellular dynamics such as GRNs based on different formalisms (from Boolean networks to nonlinear differential equations) with cell-cell signaling dynamics through diffusion or active transport processes in cellular domains of very different geometries, which could allow us to solve the limitations previously discussed in our model.…”

Transcriptome Analyses in Adult Olive Trees Indicate Acetaldehyde Release and Cyanide-Mediated Respiration Traits as Critical for Tolerance against Xylella fastidiosa and Suggest AOX Gene Family as Marker for Multiple-Resilience

“…To our knowledge, the role of cambial vascular tissues and the possibility of de novo xylem formation were not, or not sufficiently, explored in host responses to Xf -infection. This is in contrast to the important functional role of stem cells, such as xylem cambium, for adaptive robustness of organisms through cell renewal and de novo structuring [ 23 , 28 ]. Also, cambial vascular cells are important for stress perception and its transformation into energy-dependent cell fate decisions through cell cycle activity regulation [ 29 , 30 ].…”