Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts.

Liverworts, which are amongst the earliest divergent plant lineages and important ecosystem pioneers, often form nutritional mutualisms with arbuscular mycorrhiza-forming Glomeromycotina and fine-root endophytic Mucoromycotina fungi, both of which coevolved with early land plants. Some liverworts, in common with many later divergent plants, harbour both fungal groups, suggesting these fungi may complementarily improve plant access to different soil nutrients. We tested this hypothesis by growing liverworts in single and dual fungal partnerships under a modern atmosphere and under 1500 ppm [CO ₂ ], as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with ¹⁵ N-labelled algal necromass and ³³ P orthophosphate. Photosynthate allocation to fungi was traced using ¹⁴ CO ₂ . Only Mucoromycotina fungal partners provided liverworts with substantial access to algal ¹⁵ N, irrespective of atmospheric CO ₂ concentration. Both symbionts increased ³³ P uptake, but Glomeromycotina were often more effective. Dual partnerships showed complementarity of nutrient pool use and greatest photosynthate allocation to symbiotic fungi. We show there are important functional differences between the plant-fungal symbioses tested, providing new insights into the functional biology of Glomeromycotina and Mucoromycotina fungal groups that form symbioses with plants. This may explain the persistence of the two fungal lineages in symbioses across the evolution of land plants.
(© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.)