Poor plant performance under simulated climate change is linked to mycorrhizal responses in a semi-arid shrubland

Warmer and drier conditions associated with ongoing climate change will increase abiotic stress for plants and mycorrhizal fungi in drylands world-wide, thereby potentially reducing vegetation cover and productivity and increasing the risk of land degradation and desertification. Rhizosphere-microbial interactions and feedbacks are critical processes that could either mitigate or aggravate the vulnerability of dryland vegetation to forecasted climate change. We conducted a 4-year manipulative study in a semi-arid shrubland in the Iberian Peninsula to assess the effects of warming (c. 2.5 degrees C; W), rainfall reduction (c. 30%; RR) and their combination (W+RR) on the performance of native shrubs (Helianthemum squamatum) and their associated mycorrhizal fungi. Warming (W and W+RR) decreased the net photosynthetic rates of H.squamatum shrubs by c. 31% despite concurrent increases in stomatal conductance (c. 33%), leading to sharp decreases (c. 50%) in water use efficiency. Warming also advanced growth phenology, decreased leaf nitrogen and phosphorus contents per unit area, reduced shoot biomass production by c. 36% and decreased survival during a dry year in both W and W+RR plants. Plants under RR showed more moderate decreases (c. 10%-20%) in photosynthesis, stomatal conductance and shoot growth. Warming, RR and W+RR altered ectomycorrhizal fungal (EMF) community structure and drastically reduced the relative abundance of EMF sequences obtained by high-throughput sequencing, a response associated with decreases in the leaf nitrogen, phosphorus and dry matter contents of their host plants. In contrast to EMF, the community structure and relative sequence abundances of other non-mycorrhizal fungal guilds were not significantly affected by the climate manipulation treatments.Synthesis. Our findings highlight the vulnerability of both native plants and their symbiotic mycorrhizal fungi to climate warming and drying in semi-arid shrublands, and point to the importance of a deeper understanding of plant-soil feedbacks to predict dryland vegetation responses to forecasted aridification. The interdependent responses of plants and ectomycorrhizal fungi to warming and rainfall reduction may lead to a detrimental feedback loop on vegetation productivity and nutrient pool size, which could amplify the adverse impacts of forecasted climate change on ecosystem functioning in EMF-dominated drylands.