Individual leaf microbiota tunes a genetic regulatory network to promote leaf growth

In natural ecosystems, microbes have the ability to stably colonize plant leaves, overcoming the fluctuating environmental conditions that the leaves represent. How the phyllosphere microbiota influences the growth of individual leaves remains poorly understood. Here, we investigate the growth of Zea mays (maize/corn) leaves in plants grown in three soils with differing amounts of nutrients and water and identify a leaf-growth-promoting effect driven by the leaf microbiota, which we also validate in field studies. We built and used a bacterial strain collection for recolonization experiments to study the microbiota-mediated mechanisms involved in leaf growth promotion. We demonstrate that prevalent bacteria inhabiting young leaves promote individual leaf growth. Using transcriptomic analyses, we reveal a defense-related genetic network that integrates the beneficial effect of the phyllosphere microbiota into the leaf development program. We demonstrate that the individual leaf microbiota differentially represses this genetic network to modulate the growth-defense trade-off at single-leaf resolution.