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Abstract The leaf economics spectrum (LES) characterizes a tradeoff between building a leaf for durability versus for energy capture and gas exchange, with allocation to leaf dry mass per projected surface area (LMA) being a key trait underlying this tradeoff. However, regardless of the biomass supporting the leaf, high rates of gas exchange are typically accomplished by small, densely packed stomata on the leaf surface, which is enabled by smaller genome sizes. Here, we investigate how variation in genome size‐cell size allometry interacts with variation in biomass allocation (i.e. LMA) to influence the maximum surface conductance to CO₂and the rate of resource turnover as measured by leaf water residence time. We sampled both evergreen and deciduousRhododendron(Ericaceae) taxa from wild populations and botanical gardens, including naturally occurring putative hybrids and artificially generated hybrids. We measured genome size, anatomical traits related to cell sizes, and morphological traits related to water content and dry mass allocation. Consistent with the LES, higher LMA was associated with slower water residence times, and LMA was strongly associated with leaf thickness. Although anatomical and morphological traits varied orthogonally to each other, cell size had a pervasive impact on leaf functional anatomy: for a given leaf thickness, reducing cell size elevated the leaf surface conductance and shortened the mean water residence time. These analyses clarify how anatomical traits related to genome size‐cell size allometry can influence leaf function independently of morphological traits related to leaf longevity and durability. 

Summary 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. 

Mangroves have evolved at least 27 times across ~20 plant families to survive coastal. To environments characterized by high salinity, inundation, intense light, and strong winds survive these extreme conditions, mangroves exhibit a variety of physiological strategies to tolerate the low osmotic potentials associated with saltwater inundation. Because low osmotic potentials are counterbalanced by high turgor pressure, saltwater exposure exerts mechanical demands on cells. Analyzing 34 mangrove species and 33 closely related inland taxa from 17 plant families, we show that compared to their inland relatives, mangroves have unusually small leaf epidermal pavement cells and thicker cell walls, which together confer greater mechanical strength and tolerance to low osmotic potentials. However, mangroves do not exhibit smaller, more numerous stomata that enable higher photosynthetic rates , suggesting selection on biomechanical integrity rather than on gas exchange capacity. Notably, mangroves break the allometric scaling between the sizes of epidermal pavement cells and stomata typically seen in land plants, highlighting that strong selection in saline habitats can override genome size–mediated scaling rules. Phylogenetic comparative analyses revealed repeated convergent evolution of cell traits across independent transitions from inland to coastal habitats. These anatomical changes constitute a simple but effective adaptation to salt stress. Our findings underscore the role of biomechanics in driving convergent evolution of cell traits and suggest that manipulating cell size and wall properties could be a promising strategy to engineering salt-tolerant plants. 

Throughout leaf development, cell expansion is dynamic and driven by the balance between local cell wall mechanical properties and the intracellular turgor pressure that overcomes the stiffness of the cell wall leading to plastic deformation. The epidermal pavement cells in most leaves begin development as small, polygonally shaped cells, but in mature leaves epidermal pavement cells are often shaped as highly lobed puzzle pieces. However, the developmental and biomechanical trajectories between these two end points have not before been fully characterized. Here we characterized how epidermal pavement cell size and shape, cell wall thickness, and hydraulic traits change during leaf expansion in the tropical understory fern Microsorum grossum (Polypodiaceae). As fronds expanded by approximately two orders of magnitude in size, epidermal pavement cells became increasingly lobed as cell walls thickened. Furthermore, the timing of these developmental changes varied across the lamina, start first near the frond base and midrib, followed by more apical and lateral regions. During expansion, fronds also underwent substantial physiological changes: as cells expanded and cell walls thickened, intracellular turgor pressure and the bulk cell wall modulus of elasticity both increased while the water potential at turgor loss and the minimum epidermal conductance to water vapor both decreased. These results highlight the dynamic coordination between anatomical and physiological traits throughout leaf development, provide valuable data for biophysical modeling of leaf development, and highlight the vulnerability of developing leaves to drought conditions. 

Climate change-driven drought events are becoming unescapable in an increasing number of areas worldwide. Understanding how plants are able to adapt to these changing environmental conditions is a non-trivial challenge. Physiologically, improving a plant’s intrinsic water use efficiency (WUEi) will be essential for plant survival in dry conditions. Physically, plant adaptation and acclimatisation are constrained by a plant’s anatomy. In other words, there is a strong link between anatomical structure and physiological function. Former research predominantly focussed on using 2D anatomical measurements to approximate 3D structures based on the assumption of ideal shapes, such as spherical spongy mesophyll cells. As a result of increasing progress in 3D imaging technology, the validity of these assumptions is being assessed, and recent research has indicated that these approximations can contain significant errors. We suggest to invert the workflow and use the less common 3D assessments to provide corrections and functions for the more widely available 2D assessments. By combining these 3D and corrected 2D anatomical assessments with physiological measurements of WUEi, our understanding of how a plant’s physical adaptation affects its function will increase and greatly improve our ability to assess plant survival. 

As the site of almost all terrestrial carbon fixation, the mesophyll tissue is critical to leaf function. However, mesophyll tissue is not restricted only to leaves but also occurs in the laminar, heterotrophic organs of the floral perianth, providing a powerful test of how metabolic differences are linked to differences in tissue structure. Here, we compared mesophyll tissues of leaves and flower perianths of six species using high-resolution X-ray computed microtomography (microCT) imaging. Consistent with previous studies, stomata were nearly absent from flowers, and flowers had a significantly lower vein density compared to leaves. However, mesophyll porosity was significantly higher in flowers than in leaves, and higher mesophyll porosity was associated with more aspherical mesophyll cells. Despite these differences in cell and tissue structure between leaf and flower mesophyll, modeled intercellular airspace conductance did not differ significantly between organs, regardless of differences in stomatal density between organs. These results suggest that in addition to differences between leaves and flowers in vein and stomatal densities, the mesophyll cells and tissues inside these organs also exhibit marked differences that may allow for flowers to be relatively cheaper in terms of biomass investment per unit of flower surface area. 

Flowers are critical for successful reproduction and have been a major axis of diversification among angiosperms. As the frequency and severity of droughts are increasing globally, maintaining water balance of flowers is crucial for food security and other ecosystem services that rely on flowering. Yet remarkably little is known about the hydraulic strategies of flowers. We characterized hydraulic strategies of leaves and flowers of ten species by combining anatomical observations using light and scanning electron microscopy with measurements of hydraulic physiology (minimum diffusive conductance ( g min ) and pressure-volume (PV) curves parameters). We predicted that flowers would exhibit higher g min and higher hydraulic capacitance than leaves, which would be associated with differences in intervessel pit traits because of their different hydraulic strategies. We found that, compared to leaves, flowers exhibited: 1) higher g min , which was associated with higher hydraulic capacitance ( C T ); 2) lower variation in intervessel pit traits and differences in pit membrane area and pit aperture shape; and 3) independent coordination between intervessel pit traits and other anatomical and physiological traits; 4) independent evolution of most traits in flowers and leaves, resulting in 5) large differences in the regions of multivariate trait space occupied by flowers and leaves. Furthermore, across organs intervessel pit trait variation was orthogonal to variation in other anatomical and physiological traits, suggesting that pit traits represent an independent axis of variation that have as yet been unquantified in flowers. These results suggest that flowers, employ a drought-avoidant strategy of maintaining high capacitance that compensates for their higher g min to prevent excessive declines in water potentials. This drought-avoidant strategy may have relaxed selection on intervessel pit traits and allowed them to vary independently from other anatomical and physiological traits. Furthermore, the independent evolution of floral and foliar anatomical and physiological traits highlights their modular development despite being borne from the same apical meristem. 

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 inArabidopsis thalianaleaves. We find that robust generation of pore space in the spongy mesophyll requires a balance of cell growth, adhesion, stiffness and tissue pressure to ensure cell networks become porous yet maintain mechanical stability. The success of this mechanical model of morphogenesis suggests that simple physical principles can coordinate and drive the development of complex plant tissues like the spongy mesophyll.