Auxin signalling of Arachis hypogaea activated by colonization of mutualistic fungus Phomopsis liquidambari enhances nodulation and N2-fixation

Abstract

Beneficial fungal and rhizobial symbioses share commonalities in phytohormones responses, especially in auxin signalling. Mutualistic fungus Phomopsis liquidambari effectively increases symbiotic efficiency of legume peanut (Arachis hypogaea L.) with another microsymbiont, bradyrhizobium, but the underlying mechanisms are not well understood. We quantified and manipulated the IAA accumulation in ternary P. liquidambari–peanut–bradyrhizobial interactions to uncover its role between distinct symbioses. We found that auxin signalling is both locally and systemically induced by the colonization of P. liquidambari with peanut and further confirmed by Arabidopsis harbouring auxin-responsive reporter, DR5:GUS, and that auxin action, including auxin transport, is required to maintain fungal symbiotic behaviours and beneficial traits of plant during the symbiosis. Complementation and action inhibition experiments reveal that auxin signalling is involved in P. liquidambari-mediated nodule development and N2-fixation enhancement and symbiotic gene activation. Further analyses showed that blocking of auxin action compromised the P. liquidambari-induced nodule phenotype and physiology changes, including vascular bundle development, symbiosome and bacteroids density, and malate concentrations, while induced the accumulation of starch granules in P. liquidambari-inoculated nodules. Collectively, our study demonstrated that auxin signalling activated by P. liquidambari symbiosis is recruited by peanut for bradyrhizobial symbiosis via symbiotic signalling pathway activation and nodule carbon metabolism enhancement.