Plant carbohydrate depletion impairs water relations and spreads via ectomycorrhizal networks

Abstract Carbon and water relations are fundamental to plant life and strongly interact. Under drought, the ability of plants to assimilate carbon is reduced, which increases their consumption of stored labile carbon in the form of non-structural carbohydrates (NSC). Stored NSC depletion may impair plant water relations, but mechanisms are not clear, and we do not know if its effects are independent of water deficit. If so, carbon costs of fungal symbionts could also indirectly influence plant drought tolerance through stored NSC depletion. We connected well-watered Pinus ponderosa seedling pairs via ectomycorrhizal (EM) networks where one seedling was shaded and the other experienced full light and compared responses to seedling pairs in the light. We measured plant water relations and traced carbon movements using 13CO2 to explore the mechanisms linking stored NSC to water relations, and to identify potential tradeoffs between the ability to endure low water potentials and maintaining EM fungi under carbon-limiting conditions. Even in the absence of drought, mild NSC depletion impaired osmoregulation capacity and turgor maintenance, a critical strategy to tolerate drought. This demonstrates that NSC storage influences plant water relations independently of plant water status. We also found that EM networks propagated NSC depletion and its negative effects on water relations from carbon stressed hosts to non-stressed hosts. These results highlight carbon allocation tradeoffs between supporting fungal symbionts and retaining water via stored NSC and have implications for biotic interactions and forest drought responses. Significance Statement The potential effects of future drought on global carbon cycles, vegetation-climate feedbacks, species distributions and their ecological impacts, urgently call for a clear understanding of factors influencing vegetation tolerance to drought. Key to this is the understanding of mechanisms and processes by which plants tolerate drought and how prevalent plant-fungal interactions may influence these processes. We demonstrate that even mild depletion of plant non-structural carbohydrate (NSC) storage readily decreases plant water retention capacity, therefore decreasing tolerance to drought. Because plant-fungal interactions depend on NSC exchange, plants face carbon-allocation tradeoffs between maintaining drought tolerance and feeding fungal symbionts. The impacts of these tradeoffs extend across plants connected via ectomycorrhizal networks as fungi propagate NSC depletion from NSC-limited plants to non-stressed individuals.