Activation dynamics and assembly of root zone soil bacterial communities in response to stress-associated phytohormones.

Abstract

Plants can "cry for help" to recruit supportive microbiome members during stress, but the precise signals a plant uses to activate and assemble these microorganisms remain unclear. We evaluated the activation dynamics of root zone soil bacteria in response to phytohormones produced when plants are stressed, hypothesizing that responsive taxa could support plant resilience. We conducted a mesocosm experiment using root zone soil collected from the planted fields of two crops: the annual legume common bean (Phaseolus vulgaris L.) and the perennial grass switchgrass (Panicum virgatum). In the absence of any plant, we inactivated the root zone microbiome by drying the soil and then added abscisic acid, salicylic acid, a carrier control, or water to test their capacities to reactivate microbiome members and assessed responses for 2 weeks. Using amplicon sequencing of the 16S rRNA and rRNA genes to determine active populations, we found several actinobacteria that became active after exposure to abscisic acid and salicylic acid, with Microbispora lineages being especially responsive. While some taxa activated only in one crop's root soil, others were activated in both crops' soils in response to the same phytohormone. By comparing microbes that immediately activated 24 h after phytohormone addition with those that activated and also persisted over several days, we distinguished taxa that responded to phytohormones as signals from those that potentially also used them as resources. This work suggests that different root zone bacteria exhibit distinct specificities to phytohormones, providing insights into the signals by which plants may "cry for help" to recruit bacteria.

Importance: Global food security is a pressing societal challenge that has been exacerbated by climate change and other anthropogenic stressors on the environment. Microbial bioinoculants are a promising solution for improving crop health and resilience, but ensuring their persistence and activation in the field remains a significant challenge. This study examined how dormant root-zone-associated bacteria reactivate after exposure to the plant stress hormones abscisic acid and salicylic acid. The experiment revealed that certain bacterial taxa could reactivate in response to these plant stress signals and persist for at least 2 weeks. This work advances our understanding of the potential cues for reactivating beneficial plant-associated microbes and supports the goal of developing microbial solutions for sustainable agriculture.