From rhizoids to roots? Experimental evidence of mutualism between liverworts and ascomycete fungi

Abstract

<div class="section"> <a class="named-anchor" id="s1"> <!-- named anchor --> </a> <h5 class="section-title" id="d1226944e170">Background and Aims</h5> <p id="d1226944e172">The rhizoids of leafy liverworts (Jungermanniales, Marchantiophyta) are commonly colonized by the ascomycete fungus <i>Pezoloma ericae</i>. These associations are hypothesized to be functionally analogous to the ericoid mycorrhizas (ErMs) formed by <i>P. ericae</i> with the roots of Ericaceae plants in terms of bi-directional phosphorus for carbon exchange; however, this remains unproven. Here, we test whether associations between the leafy liverwort <i>Cephalozia bicuspidata</i> and <i>P. ericae</i> are mutualistic. </p> </div><div class="section"> <a class="named-anchor" id="s2"> <!-- named anchor --> </a> <h5 class="section-title" id="d1226944e187">Methods</h5> <p id="d1226944e189">We measured movement of phosphorus and carbon between <i>C. bicuspidata</i> and <i>P. ericae</i> using [ ³³P]orthophosphate and ¹⁴CO ₂ isotope tracers in monoxenic cultures. We also measured leafy liverwort growth, with and without <i>P. ericae</i>. </p> </div><div class="section"> <a class="named-anchor" id="s3"> <!-- named anchor --> </a> <h5 class="section-title" id="d1226944e211">Key Results</h5> <p id="d1226944e213">We present the first demonstration of nutritionally mutualistic symbiosis between a non-vascular plant and an ErM-forming fungus, showing transfer of fungal-acquired P to the liverwort and of liverwort-fixed C to the fungus alongside increased growth in fungus-colonized liverworts. </p> </div><div class="section"> <a class="named-anchor" id="s4"> <!-- named anchor --> </a> <h5 class="section-title" id="d1226944e216">Conclusions</h5> <p id="d1226944e218">Thus, this ascomycete–liverwort symbiosis can now be described as mycorrhiza-like, providing further insights into ericoid mycorrhizal evolution and adding Ascomycota fungi to mycorrhizal fungal groups engaging in mutualisms with plants across the land plant phylogeny. As <i>P. ericae</i> also colonizes the rhizoids of Schistochilaceae liverworts, which originated in the Triassic and are sister to all other jungermannialean liverworts associated with fungi, our findings point toward an early origin of ascomycete–liverwort symbioses, possibly pre-dating their evolution in the Ericales by some 150 million years. </p> </div>