Microbial Modulation of Host Plant Proteasome Activity Improves Heat Stress Tolerance

AbstractGlobal climate change marked by rising temperatures and increasingly frequent, severe heat waves, threatens plant health, productivity, and ecosystem function. Beneficial plant-microbe associations are increasingly recognized for their role in mitigating abiotic stress, yet the molecular mechanisms underlying microbially-conferred thermotolerance remain poorly understood. Here, we developed a population-based assay usingSphagnumpeat mosses, a key species in peatland ecosystems that sequester 33–50% of the world’s soil carbon as recalcitrant peat, to perform microbiome transfers and assess microbial contributions to heat resilience. Strain-based assays inSphagnumandArabidopsisidentifiedVariovoraxas a key thermotolerance-enhancing microbe and identified ECM29, a proteasome-associated protein, as critical for this interaction. InArabidopsis, Variovoraxsp. CF313 association led to ECM29 preferentially binding the RPT1 subunit of the 19S regulatory particle, inhibiting 20S proteasome gate opening and slightly reducing proteasomal activity. This results in the accumulation of ubiquitinated proteins and inducesHSP70transcription, priming the host for heat shock stress even in the absence of prior heat exposure. These findings establish ECM29 as a key regulator of proteasome activity in response to microbial interactions, highlighting a previously unknown mechanism by which microbes enhance plant thermotolerance. More broadly, this work highlights the importance of leveraging natural systems and ecologically relevant models to identify strategies for enhancing plant and ecosystem resilience to a changing climate.Significance StatementGlobal climate change poses severe threats to plant health and productivity, with cascading impacts on ecosystems. Beneficial plant-microbe interactions offer promising strategies to mitigate abiotic stress, yet the molecular mechanisms often remain unclear. This study uncovers a novel thermotolerance mechanism mediated byVariovoraxmodulating the plant host proteasome. Using a QTL derived fromSphagnumpeat mosses, and tested within a genetically tractableArabidopsismodel, we identified ECM29, a highly conserved protein across diverse plant species, as a key regulator of proteasome activity. ECM29 primes plants for heat stress by inducing HSP70 transcription through proteasome modulation. Additionally, we demonstrated that ECM29 is required for the host to receive microbially conferred thermotolerance, but is not necessary for innate priming to heat stress. These findings highlight the potential of leveraging natural systems and ecologically relevant species to develop innovative genetic models, advancing plant resilience and productivity in a warming world.