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

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 (H₂ O₂ )-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.