Ethylene signal-driven plant-multitrophic synergy boosts crop performance

Efficient nutrient use in agriculture depends on the dynamic interplay between plant roots, soil, and microbial communities. The root-rhizosphere interface is central to nutrient uptake and serves as a key hub for interactions with beneficial microbes. Arbuscular mycorrhizal (AM) fungi, positioned at the nexus between plant roots and soil microbiota, play a critical role in enhancing crop performance under nutrient-limited conditions. In this study, we dissected the genetic and molecular basis of AM fungi-induced lateral root development in maize (Zea mays), focusing on the role of ethylene-responsive transcription factors (ERFs). We identified ERF genes as essential regulators of pericycle cell division, acting downstream of ethylene biosynthesis genes (ACS6 and ACS7) and AM fungal signaling. Our findings reveal that AM fungi promote lateral root initiation by activating ERF expression and reprogramming flavonoid metabolism, particularly reducing the accumulation of flavonols such as kaempferol and quercetin, which otherwise inhibit root development when over-accumulated. Furthermore, we demonstrated that Massilia, a beneficial rhizobacterium, synergizes with AM fungi to enhance lateral root formation by colonizing fungal hyphae, degrading flavonoids, and contributing to auxin production. Together, our results uncover a tripartite signaling network linking ethylene signaling, flavonoid-mediated microbial recruitment, and AM symbiosis. This study highlights ERFs as central integrators of plant-microbe interactions and provides a molecular framework for engineering root architecture and microbiome assembly to improve nutrient acquisition and support sustainable crop productivity.