Many plant leaves have two layers of photosynthetic tissue: the palisade and spongy mesophyll. Whereas palisade mesophyll consists of tightly packed columnar cells, the structure of spongy mesophyll is not well characterized and often treated as a random assemblage of irregularly shaped cells. Using micro‐computed tomography imaging, topological analysis, and a comparative physiological framework, we examined the structure of the spongy mesophyll in 40 species from 30 genera with laminar leaves and reticulate venation. A spectrum of spongy mesophyll diversity encompassed two dominant phenotypes: first, an ordered, honeycomblike tissue structure that emerged from the spatial coordination of multilobed cells, conforming to the physical principles of Euler’s law; and second, a less‐ordered, isotropic network of cells. Phenotypic variation was associated with transitions in cell size, cell packing density, mesophyll surface‐area‐to‐volume ratio, vein density, and maximum photosynthetic rate. These results show that simple principles may govern the organization and scaling of the spongy mesophyll in many plants and demonstrate the presence of structural patterns associated with leaf function. This improved understanding of mesophyll anatomy provides new opportunities for spatially explicit analyses of leaf development, physiology, and biomechanics.
The spongy mesophyll is a complex, porous tissue found in plant leaves that enables carbon capture and provides mechanical stability. Unlike many other biological tissues, which remain confluent throughout development, the spongy mesophyll must develop from an initially confluent tissue into a tortuous network of cells with a large proportion of intercellular airspace. How the airspace in the spongy mesophyll develops while the tissue remains mechanically stable is unknown. Here, we use computer simulations of deformable polygons to develop a purely mechanical model for the development of the spongy mesophyll tissue. By stipulating that cell wall growth and remodelling occurs only near void space, our computational model is able to recapitulate spongy mesophyll development observed in
- Award ID(s):
- 2029756
- NSF-PAR ID:
- 10480720
- Publisher / Repository:
- Royal Society
- Date Published:
- Journal Name:
- Journal of The Royal Society Interface
- Volume:
- 19
- Issue:
- 197
- ISSN:
- 1742-5662
- Page Range / eLocation ID:
- 20220602
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Mechanical forces generated by dynamic cellular activities play a crucial role in the morphogenesis and growth of biological tissues. While the influence of mechanics is clear, many questions arise regarding the way by which mechanical forces communicate with biological processes at the level of a confluent cell population. Some answers may be found in the development of mathematical models that are capable of describing the emerging behavior of a large population of active agents based on individualistic rules (single-cell response). In this perspective, the present work presents a continuum-scale model that can capture, in an average sense, the active mechanics and evolution of a confluent tissue with or without external mechanical constraints. For this, we conceptualize a confluent cell population (in a monolayer) as a deformable dynamic network, where a single cell can modify the topology of its neighborhood by swapping neighbors or dividing. With this description, we use concepts from statistical mechanics and the transient network theory to derive an equivalent active visco-elastic continuum model, which can recapitulate some of the salient features of the underlying network at the macroscale. Without loss of generality, the cell network is here assumed to follow well-known rules used in vertex model simulations, which are: (a) cell elasticity based on its bulk and cortical elasticity, (b) cell intercalation (or T1 transition), and (c) cell proliferation (expansion and division). We show, through examples and illustrations, that the model is able to characterize complex cross-talk between mechanical forces and biological processes, which are likely to drive the emergent growth and deformation of cell aggregates.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rsif.2022.0602
