Competition for epidermal space in the evolution of leaves with high physiological rates

Baresch, Andres; Crifò, Camilla; Boyce, C. Kevin

doi:10.1111/nph.15476

Cited by 24 publications

(20 citation statements)

References 71 publications

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“…Recently, the competition hypothesis for epidermal space between veins (mainly the vascular bundle sheath extensions) and stomata has been highlighted by Baresch et al . (2019). Allocating the stomatal pores to both surfaces in amphistomatous species potentially helps to lift the constraint of competition with veins for epidermal space.…”

Section: Discussionmentioning

confidence: 99%

From one side to two sides: the effects of stomatal distribution on photosynthesis

Xiong

Flexas

2020

New Phytologist

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The functions of stomata have been studied for a long time; however, a clear understanding of the influences of stomatal distribution on photosynthesis, especially the CO 2 diffusion, is still unclear. Here, we investigated the stomatal morphology, distribution on leaf surfaces, vein traits and gas exchange parameters of 61 species, of which 29 were amphistomatous, spanning 32 families. Photosynthesis (A) was tightly coupled with operational stomatal conductance (g s) and mesophyll conductance (g m) regardless of whether phylogenetic relationships were accounted for. Although the enhancement of g s from ferns and gymnosperms to angiosperms could largely be explained by the increase in leaf vein density (VLA) and stomatal density (SD), the g s was decoupled from VLA and SD across angiosperm species. Instead, A in angiosperms was further influenced by the allocation of stomatal pores on leaf surfaces, which dramatically increased g s and g m. Moreover, the ratio of g s to anatomically based maximum g s was, on average, 0.12 across species. Our results show that the shift of stomatal pores from one leaf side to both sides played an important role in regulating CO 2 diffusion via both stomata and mesophyll tissues. Modifications of stomata distribution have potential as a functional trait for photosynthesis improvement.

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Section: Discussionmentioning

confidence: 99%

From one side to two sides: the effects of stomatal distribution on photosynthesis

Xiong

Flexas

2020

New Phytologist

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“…For a given leaf volume, the number of cells that can be packed into a space and the distance between different cell types is fundamentally limited by the size of these cells 15,16 . Because increasing investment in any one cell type will displace other cell types 17,18 , reducing cell size is a primary way of allowing more cell surface area of a given type to be packed into a given leaf volume. How small a cell can be is limited by the volume of its nucleus, which is commonly measured as genome size 19,20 .…”

Section: Main Textmentioning

confidence: 99%

Maximum CO₂diffusion inside leaves is limited by the scaling of cell size and genome size

Théroux‐Rancourt

Roddy

Gilbert

et al. 2020

Preprint

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SummaryMaintaining high rates of photosynthesis in leaves requires efficient movement of CO2 from the atmosphere to the chloroplasts inside the leaf where it is converted into sugar. Throughout the evolution of vascular plants, CO2 diffusion across the leaf surface was maximized by reducing the sizes of the guard cells that form stomatal pores in the leaf epidermis1,2. Once inside the leaf, CO2 must diffuse through the intercellular airspace and into the mesophyll cells where photosynthesis occurs3,4. However, the diffusive interface defined by the mesophyll cells and the airspace and its coordinated evolution with other leaf traits are not well described5. Here we show that among vascular plants variation in the total amount of mesophyll surface area per unit mesophyll volume is driven primarily by cell size, the lower limit of which is defined by genome size. The higher surface area enabled by smaller cells allows for more efficient CO2 diffusion into photosynthetic mesophyll cells. Our results demonstrate that genome downsizing among the flowering plants6 was critical to restructuring the entire pathway of CO2 diffusion, facilitating high rates of CO2 supply to the leaf mesophyll cells despite declining atmospheric CO2 levels during the Cretaceous.

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“…An effect of stomatal size and density on foliar pathogen colonization could change our understanding of stomatal sizedensity scaling. Since allocating leaf epidermis to stomata may be costly (Assmann and Zeiger, 1987;Franks and Farquhar, 2007;Dow et al, 2014b;Lehmann and Or, 2015;Baresch et al, 2019), selection should favor leaves that achieve a desired g s,max while minimizing f S (Boer et al, 2016). Because of their different scaling exponents (Equation 1, 2), smaller, densely packed stomata can achieve the same g s,max at minimum f S .…”

Section: Model Prediction How To Test Itmentioning

confidence: 99%

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

Muir

2020

Front. Plant Sci.

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Stomatal pores control leaf gas exchange and are one route for infection of internal plant tissues by many foliar pathogens, setting up the potential for tradeoffs between photosynthesis and pathogen colonization. Anatomical shifts to lower stomatal density and/or size may also limit pathogen colonization, but such developmental changes could permanently reduce the gas exchange capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen colonization on the leaf as a function of stomatal size and density, anatomical traits which partially determine maximum rates of gas exchange. The model predicts greater stomatal size or density increases the probability of colonization, but the effect is most pronounced when the fraction of leaf surface covered by stomata is low. I also derived scaling relationships between stomatal size and density that preserves a given probability of colonization. These scaling relationships set up a potential anatomical conflict between limiting pathogen colonization and minimizing the fraction of leaf surface covered by stomata. Although a connection between gas exchange and pathogen defense has been suggested empirically, this is the first mathematical model connecting gas exchange and pathogen defense via stomatal anatomy. A limitation of the model is that it does not include variation in innate immunity and stomatal closure in response to pathogens. Nevertheless, the model makes predictions that can be tested with experiments and may explain variation in stomatal size and density among plants. The model is generalizable to many types of pathogens, but lacks significant biological realism that may be needed for precise predictions.

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Competition for epidermal space in the evolution of leaves with high physiological rates

Cited by 24 publications

References 71 publications

From one side to two sides: the effects of stomatal distribution on photosynthesis

From one side to two sides: the effects of stomatal distribution on photosynthesis

Maximum CO₂diffusion inside leaves is limited by the scaling of cell size and genome size

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

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Competition for epidermal space in the evolution of leaves with high physiological rates

Cited by 24 publications

References 71 publications

From one side to two sides: the effects of stomatal distribution on photosynthesis

From one side to two sides: the effects of stomatal distribution on photosynthesis

Maximum CO2diffusion inside leaves is limited by the scaling of cell size and genome size

A Stomatal Model of Anatomical Tradeoffs Between Gas Exchange and Pathogen Colonization

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Maximum CO₂diffusion inside leaves is limited by the scaling of cell size and genome size