Natural variation in the transcription factor REPLUMLESS contributes to both disease resistance and plant growth in Arabidopsis

When attacked by pathogens, plants need to reallocate energy from growth to defense to fend off the invaders, frequently incurring growth penalties. This phenomenon is known as the growth-defense tradeoff and is orchestrated by a hardwired transcriptional network. Altering key factors involved in this network has the potential to increase disease resistance without growth or yield loss, but the mechanisms underlying such changes require further investigation. By conducting a genome-wide association study (GWAS) of leaves infected by the hemi-biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000, we discovered that the Arabidopsis transcription factor REPLUMLESS (RPL) is necessary for bacterial resistance. More importantly, RPL functions in promoting both disease resistance and growth. Transcriptome analysis revealed a cluster of genes in the GRETCHEN HAGEN 3 (GH3) family that were significantly upregulated in rpl mutants, leading to the accumulation of indole-3-acetic acid-aspartic acid (IAA-Asp). Consistent with this observation, transcripts of virulence effector genes were activated by IAA-Asp accumulated in the rpl mutants. We found that RPL protein could directly bind to GH3 promoters and repress their expression. RPL also repressed flavonol synthesis by directly repressing CHI expression and thus activated the auxin transport pathway, which promotes plant growth. Therefore, RPL plays an important role in plant immunity and functions in the auxin pathway to optimize Arabidopsis growth and defense.