Atmospheric drought and low light impede mycorrhizal effects on leaf photosynthesis—a glasshouse study on tomato under naturally fluctuating environmental conditions

Arbuscular mycorrhiza fungi (AMF) consume plant carbon and impact photosynthesis, but effects of AMF on plant gas exchange are transient and hardly predictable. This is at least partially because plant-internal nutrient-, water-, and sink-related effects, which can be influenced AMF, and atmospheric conditions integrate at the photosynthesis level. In nature and in plant production, plants face periodical and random short-term switches of environmental conditions that limit photosynthesis, which may impede stimulatory effects of AMF on leaf photosynthetic capacities. We hypothesized that mycorrhizal effects on plant internal-photosynthetic potentials will only translate to actual photosynthetic rates, if atmospheric conditions do not superimpose limitations to the photosynthetic process. We aimed to cover wide ranges of within and between-day variations in light intensities and vapor pressure deficits with an untargeted approach. We grew tomato plants hydroponically for 8 weeks in open pots and irrigated beyond pot water capacity every morning. Plants were inoculated or not with Funneliformis mosseae and were fertilized with a low-strength nutrient solution, which guaranteed good AMF colonization and comparable sets of mycorrhizal and non-mycorrhizal plants regarding developmental stage and leaf age. Instantaneous leaf photosynthesis was monitored continuously with transparent chambers during 3 days under naturally fluctuating greenhouse conditions on the two uppermost fully expanded leaves. We fitted mechanistic gas exchange models and modeled continuous daytime dynamics of net photosynthetic rates and stomatal conductance for representative sunlit canopies of random populations of mycorrhizal and non-mycorrhizal plants. Depending on time, mycorrhizal plants showed enhanced or decreased stomatal conductance over wide ranges of light intensities. Higher or lower stomatal opening in mycorrhizal plants became ineffective for photosynthetic rates under low light. In contrast and in accordance with the effects on stomatal conductance, photosynthetic rates were comparatively increased or decreased in mycorrhizal plants under high light conditions. This required at least moderate vapor pressure deficits. Under high atmospheric drought, stomatal conductance strongly declined in all plants, which also capped maximum photosynthetic rates under high light. Leaf photosynthetic capacities were higher in mycorrhizal plants when leaves contained more proteins and/or the plant-internal moisture stress was lower than in non-mycorrhizal plants. However, this only resulted in enhanced photosynthetic rates as long as leaves were not exposed to low radiation or high atmospheric drought. We conclude that light and atmospheric moisture are decisive factors for potential carbon cost and gain scenarios of plants associated with AMF.