An ectomycorrhizal fungus alters developmental progression during endogenous rhythmic growth in pedunculate oak

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Pedunculate oak (Quercus robur L.), a long-lived forest tree species, forms symbiotic relationships with ectomycorrhizal (ECM) fungi, which can promote nutrient uptake, stress resilience, and growth. Like other tropical and temperate tree species, pedunculate oak exhibits endogenous rhythmic growth (ERG), a trait conferring the ability to repeatedly alternate root and shoot flushes as well as growth cessation as response to changing environmental conditions. However, the effects of different ECM fungal species on the ERG dynamics remain largely unknown. Here, we investigated the impact of two ECM fungi-Piloderma croceum, a basidiomycete previously shown to promote growth while not found in natural oak stands, and Cenococcum geophilum, an oak-native ascomycete with broad ecological range-on growth performance, biomass partitioning, and ERG patterns in a clonal oak system (clone DF159). By combining in vitro experiments with Bayesian modelling, we show that P. croceum promotes tree growth among treatments, without disrupting the endogenous growth rhythm. In contrast, C. geophilum, while showing high mycorrhization rates, led to reduced biomass accumulation and altered developmental progression through the ERG stages, especially by prolonging the steady state development stage-part of the root flush and characterized by peak net carbon assimilation. Co-inoculation revealed a competitive advantage of C. geophilum in root colonization, yet growth responses resembled those of the control. Our findings demonstrate that ECM species exert species-specific effects on biomass production and temporal development of plants, underscoring the functional importance of ECM fungi in shaping host development. Assessing these interactions provides new insights into the functional diversity of ectomycorrhizal symbiosis and can inform forest management strategies aimed at enhanced resilience in oak-dominated ecosystems under rapidly changing climatic conditions.

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