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

Abstract

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.

Hybridization disrupts growth-defense strategies and reveals trade-offs masked in unadmixed populations of a perennial plant

“…Stomatal size ( S ), stomatal cover ( f S ), defined as the covering fraction of the leaf surface by stomatal aperture pores, and theoretical maximum gas exchange ( g s,max ), were respectively calculated as where b is the diffusion of coefficient of water vapor in air ( b = 0.001111607) and m is a morphological constraint of stomatal guard cell length and width, aperture pore length and depth ( m = 0.4320532; see Sack and Buckley, 2016 for details). Interstomatal distances ( U ) were calculated separately for upper and lower leaf surfaces as following Muir (2020). Ratios of stomatal density (SR), stomatal area (AR, calculated from size), and the stomatal cover ratio ( f S R), are calculated as a ratio of the upper leaf surface trait to the total.…”

“…following Muir (2020). Ratios of stomatal density (SR), stomatal area (AR, calculated from size), and the stomatal cover ratio (f S R), are calculated as a ratio of the upper leaf surface trait to the total.…”

Growth‐defense trade‐offs masked in unadmixed populations are revealed by hybridization

“…We observed stomata on the upper leaf surfaces of P. angustifolia hybrids, possibly indicating selection for locally adapted stomatal phenotypes in the parental species' populations. Further simulation work by Muir concludes that greater stomatal size or density increases the probability of pathogen colonization, and the effect is most pronounced when the fraction of leaf surface covered by stomata is low (Muir 2020). Our results are consistent with a decrease in resistance when stomatal densities are low and stomatal size is shifted to the upper leaf surface (Fig.…”

“…Stomatal size ( S ), stomatal cover (), defined as the covering fraction of the leaf surface by stomatal aperture pores, and theoretical maximum gas exchange (), were, respectively, calculated as where b is the diffusion of coefficient of water vapor in air ( b = 0.001111607) and m is a morphological constraint of stomatal guard cell length and width, aperture pore length and depth ( m = 0.4320532; see Sack and Buckley 2016, for details). Interstomatal distances ( U ) were calculated separately for upper and lower leaf surfaces as following Muir (2020). Ratios of stomatal density (SR), stomatal area (AR, calculated from size), and the stomatal cover ratio (R), are calculated as a ratio of the upper leaf surface trait to the total.…”

Stomata Detector: High-throughput automation of stomata counting in a population of African rice (Oryza glaberrima) using transfer learning

“…The speed of stomatal dynamics of opening and closing places a limitation on photosynthetic efficiency under fluctuating light conditions, with consequences for both WUE and productivity and speed may be in part determined by stomata size (Drake et al, 2013;. Stomata are also known to be key players in mediating pathogen resistance, where density and anatomy effect the likelihood of colonisation (Melotto et al, 2008;McKown et al, 2014;Muir, 2020). Consequently, stomatal density and morphology are an important research focus in the search for improved crop productivity and resilience in future climates.…”