Mycorrhizal symbiosis and the nitrogen nutrition of forest trees

Abstract

Terrestrial plants form primarily mutualistic symbiosis with mycorrhizal fungi based on a compatible exchange of solutes between plant and fungal partners. A key attribute of this symbiosis is the acquisition of soil nutrients by the fungus for the benefit of the plant in exchange for a carbon supply to the fungus. The interaction can range from mutualistic to parasitic depending on environmental and physiological contexts. This review considers current knowledge of the functionality of ectomycorrhizal (EM) symbiosis in the mobilisation and acquisition of soil nitrogen (N) in northern hemisphere forest ecosystems, highlighting the functional diversity of the fungi and the variation of symbiotic benefits, including the dynamics of N transfer to the plant. It provides an overview of recent advances in understanding 'mycorrhizal decomposition' for N release from organic or mineral-organic forms. Additionally, it emphasises the taxon-specific traits of EM fungi in soil N uptake. While the effects of EM communities on tree N are likely consistent across different communities regardless of species composition, the sink activities of various fungal taxa for tree carbon and N resources drive the dynamic continuum of mutualistic interactions. We posit that ectomycorrhizas contribute in a species-specific but complementary manner to benefit tree N nutrition. Therefore, alterations in diversity may impact fungal-plant resource exchange and, ultimately, the role of ectomycorrhizas in tree N nutrition. Understanding the dynamics of EM functions along the mutualism-parasitism continuum in forest ecosystems is essential for the effective management of ecosystem restoration and resilience amidst climate change. KEY POINTS: • Mycorrhizal symbiosis spans a continuum from invested to appropriated benefits. • Ectomycorrhizal fungal communities exhibit a high functional diversity. • Tree nitrogen nutrition benefits from the diversity of ectomycorrhizal fungi.

Keywords: Decomposition; Ectomycorrhizal functional traits; Mutualistic spectrum; Nitrogen cycle.

Fig. 1

a Benefits of mutualistic ectomycorrhizal symbiosis: reciprocal invested benefits occur when both partners actively invest in each other; by-product benefits arise when one organism (the tree) incidentally benefits the other (the fungus); and appropriated benefits happen when one partner (the fungus) exploits the resources of the other (the plant). b The contribution of ectomycorrhizal (EM) fungi to tree nitrogen (N) nutrition in forest ecosystems: ectomycorrhizas formed with different fungal taxa vary in their abilities to retrieve N from diverse substrates, their mechanisms of organic matter decomposition and their preferences for specific N sources. The allocation of plant carbon (C) to different ectomycorrhizas is influenced by their C/N ratio. When soil N availability decreases, EM fungi may enhance decomposition activities to access N that requires higher C needs. Under severe N limitation, the mutualistic symbiosis may shift towards appropriated N benefits. The fungus optimises its N use efficiency to lower the C/N ratio, thereby securing more C from the plant without transferring the N to the plant. Created with BioRender.com