Dissecting the genetic regulation of lateral root development in tomato under salt stress

Abstract

Roots are the primary site for sensing salt, making them critical to understanding how plants adapt to salinity. Unraveling the genetic and molecular mechanisms that maintain root growth under salt stress is essential for developing resilient crops. Tomatoes are vulnerable to salinity, as over 50% of arable land is projected to become saline by 2050. While salt stress effects on tomato seed germination, shoot growth, and fruit yield are well-documented, the genetic basis of root development under salinity remains underexplored. Previous studies focused on physiological responses of roots in a narrow range of cultivated-tomatoes, overlooking the genetic diversity for salt resilience in wild-relatives like Solanum pimpinellifolium. Here, we investigated salt-induced changes in root system architecture (RSA) across a natural diversity panel of 220 wild- and 25 cultivated-tomato varieties. We identified tolerant accessions with different RSA strategies; prioritizing lateral root elongation versus emergence. To identify genes involved in specific aspects of lateral root development, an F1 hybrid was generated that exhibited both parents combined characteristics. An F2-segregating population was then used to identify four distinct subpopulations for Bulk Segregant Analysis (BSA). Simultaneously, we conducted Genome-Wide-Association Studies (GWAS) on root architecture of wild-tomato accessions under salt stress. By integrating the results of BSA and GWAS, we identified 22 candidates involved in the maintenance of root architecture. We utilized RNA-Seq to examine transcriptome reprogramming of the 22 genes in tomato accessions with contrasting lateral root responses. This approach resulted in the identification of 2 genes, AP2-like-ethylene-responsive transcription factor TOE3 and L-ascorbate peroxidase. Using exogenous ethylene, we demonstrated that root architecture exhibits plasticity, which benefits the plant by reducing Na+ accumulation. We profiled H2O2 waves across root systems of tomatoes, emphasizing the role of ROS in maintaining root system architecture under salt stress. These findings provide novel genetic targets for enhancing salt resilience in tomatoes, opening avenues for future research and breeding programs.