A single transcription factor SlYABBY5b synchronizes gibberellin-mediated stature and basal immunity in tomato

Abstract

Optimizing plant architecture without compromising disease resistance is a fundamental challenge in crop breeding, particularly for space-efficient systems such as vertical farming (VF). Here, we identify the YABBY-family transcription factor SlYABBY5b as a pivotal regulator that synchronizes these traits in tomato. Through a genome-wide association study (GWAS), we establish SlYABBY5b as a major locus governing natural variation in plant height. Functional analyses reveal that SlYABBY5b directly orchestrates gibberellin (GA) metabolism by activating the inactivation gene SlGA2ox2 and repressing the biosynthetic gene SlGA3ox1, thereby reducing bioactive GA pools and causing GA-reversible dwarfism. In parallel, SlYABBY5b enhances resistance to the major greenhouse pathogen Botrytis cinerea by directly targeting the promoters of the immune genes SlNLR and SlPR1a. Evolutionary analyses reveal functional divergence: while SlYABBY5b acts redundantly with its paralog SlYABBY5a in growth regulation, it has acquired a specialized, non-redundant role in enhancing basal immunity. Furthermore, natural promoter haplotypes of SlYABBY5b associate with stature and show signs of selection during domestication, positioning SlYABBY5b as a key target for breeding compact crops. Our findings illustrate how a single transcription factor can coordinate compact architecture with enhanced immunity, offering a promising target for developing resilient, high-density crops for controlled-environment agriculture.