A variome-transcriptome-metabolome network links GABA biosynthesis to stress resilience in maize

Abstract Root metabolites are essential for plant development and environmental stress adaptation. However, the genetic basis controlling root metabolome variation in crops and its role in stress resilience remain largely uncharacterized. In this study, we employed a comprehensive multi-omics approach, integrating root metabolome and transcriptome profiles of 273 maize (Zea mays L.) inbred lines at the seedling stage. Our analysis annotated 407 metabolites, of which 155 exhibited significant correlations with root traits. Using a variome-transcriptome-metabolome association (VTM) network, we identified the glutamate decarboxylase (GAD) gene ZmGAD as a crucial regulator that enhances root growth and stress tolerance by modulating gamma-aminobutyric acid (GABA) biosynthesis. ZmGAD-derived GABA confers stress tolerance by regulating stomatal aperture and scavenging reactive oxygen species. A transcription factor, ZmZIM2, acts as a negative regulator of ZmGAD expression and GABA accumulation. Moreover, a 2-bp insertion in ZmGAD causes a premature translation termination, resulting in reduced GABA content, shorter roots, and decreased stress tolerance in maize. The reduced frequency of a 2-bp deletion suggests it may have been inadvertently lost during maize domestication and modern breeding. This study elucidates the genetic and molecular framework underlying root metabolite regulation in maize and provides a valuable resource for enhancing root traits and stress tolerance in maize breeding.