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

Abstract

Summary 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 [CO2], as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with 15N‐labelled algal necromass and 33P orthophosphate. Photosynthate allocation to fungi was traced using 14CO2. Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15N, irrespective of atmospheric CO2 concentration. Both symbionts increased 33P 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.

Mucoromycotina Fine Root Endophyte Fungi Form Nutritional Mutualisms with Vascular Plants

“…Our results contrast with the view that Mucoromycotina FREs enhance plant P uptake, at least in soils with very low P (Ryan and Kirkegaard, 2012;Orchard et al, 2017b). Previous experiments with Mucoromycotina fungi-associated liverworts suggest that in addition to supplying host plants with P, Mucoromycotina fungal associates also play a role in plant N nutrition (Field et al, 2015b(Field et al, , 2016(Field et al, , 2019.…”

“…Exclusive plant-Mucoromycotina FRE symbioses seem to be rare, having been reported before only in the earliest-diverging Haplomitriopsida liverworts (Field et al, 2015a(Field et al, , 2015b, while all other plants including other lycophytes (Rimington et al, 2015) that form associations with these fungi, appear able to do so also with Glomeromycotina, often simultaneously (Rimington et al, 2015). It is possible that the large input to Lycopodiella N-nutrition and minor contribution to P-nutrition by Mucoromycotina FREs reflect a specialized relationship, particularly pertinent when considering heathland habitats have very low plant-available N. Nevertheless, our present data combined with previous demonstrations of N transfer in liverwort-Mucoromycotina symbioses (Field et al, 2015b(Field et al, , 2016 and emerging evidence that Mucoromycotina FREs, but not Glomeromycotina AM fungi, are able to transfer N to host liverworts from organic sources (Field et al, 2019), all point to a critical role of Mucoromycotina FREs in host plant N nutrition. Indeed, our cytological analyses show that, differently from Lycopodiella roots where only fine endophytes were observed (Figs.…”

“…In return, L. inundata hosts receive a relatively large amount of N from their Mucoromycotina FRE partners-;145 times more than nonvascular plants receive from their Mucoromycotina fungal symbionts (Field et al, 2016). Together with our discovery that the same Mucoromycotina fungal symbionts are shared with neighboring grasses, rushes and liverworts, and recent findings of functional complementarity between Mucoromycotina FREs and Glomeromycotina AM (Field et al, 2019), our findings point toward a unique physiological niche for the persistence of Mucoromycotina fungi, both in single and dual colonizations with Glomeromycotina AM.…”

“…We can now begin to address this with the demonstration that a vascular plant assimilates relatively large amounts of 15 N tracer via its Mucoromycotina fungal symbiont when compared to the Mucoromycotina fungal-acquired 33 P tracer ( Fig. 2C), suggesting a potential role for Mucoromycotina FREs in vascular plant nitrogen uptake, complementary to the role of Glomeromycotina AM fungi (Field et al, 2019). This nutritional role could help to explain the persistence of Mucoromycotina FREs across nearly all modern land plant lineages.…”

Evidence for Co-evolutionary History of Early Diverging Lycopodiaceae Plants With Fungi

“…We found it particularly interesting that lycopods are co-colonized by dark septate endophytic fungi, AMF and Endogonales (along with other fungi). This raises questions regarding each taxon's respective function and reinforces the biocomplexity of mutualisms in belowground systems, which includes functional complementarity between Glomeromycotina and Mucoromycotina in ancient plant-fungal mutualisms (Field et al, 2019).…”