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Abstract Within the North American boreal forest, a widespread outbreak of the epidermal leaf miner Phyllocnistis populiella has damaged quaking aspen (Populus tremuloides) for nearly 20 years. In a series of experiments, we tested the effects of feeding damage by P. populiella on leaf water relations and gas exchange. Relative to insecticide-treated trees, the leaves of naturally-mined trees had lower photosynthesis, stomatal conductance to water vapor, transpiration, water use efficiency, predawn water potential, and water content, as well as more enriched foliar δ13C. The magnitude of the difference between naturally-mined and insecticide-treated trees did not change significantly throughout the growing season, suggesting the effect is not caused by accumulation of incidental damage to mined portions of the epidermis over time. The contributions of mining-related stomatal malfunction and cuticular transpiration to these overall effects were investigated by restricting mining damage to stomatous abaxial and astomatous adaxial leaf surfaces. Mining of the abaxial epidermis decreased photosynthesis and enriched leaf δ13C, while increasing leaf water potential and water content relative to unmined leaves; effects consistent with stomatal closure due to disfunction of mined guard cells. Mining of the adaxial epidermis also reduced photosynthesis but had different effects on water relations, reducing midday leaf water potential and water content relative to unmined leaves, and did not affect δ13C. In the laboratory, extent of mining damage to the adaxial surface was positively related to the rate of water loss by leaves treated to prevent water loss through stomata. We conclude that overall, despite water savings due to closure of mined stomata, natural levels of damage by P. populiella negatively impact water relations due to increased cuticular permeability to water vapor across the mined portions of the epidermis. Leaf mining by P. populiella could exacerbate the negative effects of climate warming and water deficit in interior Alaska.
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Does stomatal patterning in amphistomatous leaves minimize the CO2 diffusion path length within leaves?
Abstract Photosynthesis is co-limited by multiple factors depending on the plant and its environment. These include biochemical rate limitations, internal and external water potentials, temperature, irradiance and carbon dioxide ( CO2). Amphistomatous leaves have stomata on both abaxial and adaxial leaf surfaces. This feature is considered an adaptation to alleviate CO2 diffusion limitations in productive environments as the diffusion path length from stomate to chloroplast is effectively halved in amphistomatous leaves. Plants may also reduce CO2 limitations through other aspects of optimal stomatal anatomy: stomatal density, distribution, patterning and size. Some studies have demonstrated that stomata are overdispersed compared to a random distribution on a single leaf surface; however, despite their prevalence in nature and near ubiquity among crop species, much less is known about stomatal anatomy in amphistomatous leaves, especially the coordination between leaf surfaces. Here, we use novel spatial statistics based on simulations and photosynthesis modelling to test hypotheses about how amphistomatous plants may optimize CO2 diffusion in the model angiosperm Arabidopsis thaliana grown in different light environments. We find that (i) stomata are overdispersed, but not ideally dispersed, on both leaf surfaces across all light treatments; (ii) the patterning of stomata on abaxial and adaxial leaf surfaces is independent and (iii) the theoretical improvements to photosynthesis from abaxial–adaxial stomatal coordination are miniscule (≪1%) across the range of feasible parameter space. However, we also find that (iv) stomatal size is correlated with the mesophyll volume that it supplies with CO2, suggesting that plants may optimize CO2 diffusion limitations through alternative pathways other than ideal, uniform stomatal spacing. We discuss the developmental, physical and evolutionary constraints that may prohibit plants from reaching this theoretical adaptive peak of uniform stomatal spacing and inter-surface stomatal coordination. These findings contribute to our understanding of variation in the anatomy of amphistomatous leaves.
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- Award ID(s):
- 2307341
- PAR ID:
- 10617636
- Editor(s):
- Salter, William
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- AoB PLANTS
- Volume:
- 16
- Issue:
- 2
- ISSN:
- 2041-2851
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/aobpla/plae015
