A novel CO2-responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

Abstract

Elevated atmospheric carbon dioxide (eCO2) concentrations promote symbiosis between roots and arbuscular mycorrhizal fungi (AMF), modifying plant nutrient acquisition and cycling of carbon, nitrogen and phosphate. However, the biological mechanisms by which plants transmit aerial eCO2 cues to roots, to alter the symbiotic associations remain unknown. We used a range of interdisciplinary approaches, including gene silencing, grafting, transmission electron microscopy, liquid chromatography tandem mass spectrometry (LC–MS/MS), biochemical methodologies and gene transcript analysis to explore the complexities of environmental signal transmission from the point of perception in the leaves at the apex to the roots. Here we show that eCO2 triggers apoplastic hydrogen peroxide (H2O2)-dependent auxin production in tomato shoots followed by systemic signaling that results in strigolactone biosynthesis in the roots. This redox-auxin-strigolactone systemic signaling cascade facilitates eCO2-induced AMF symbiosis and phosphate utilization. Our results challenge the current paradigm of eCO2 effects on AMF and provide new insights into potential targets for manipulation of AMF symbiosis for high nutrient utilization under future climate change scenarios.