Metabolomics-driven gene mining and genetic improvement of tolerance to salt-induced osmotic stress in maize

The farmland of the world's main corn-producing area is increasingly affected by salt stress. Therefore, the breeding of salt-tolerant cultivars is necessary for the long-term sustainability of global corn production. Previous studies have shown that natural maize varieties display a large diversity of salt tolerance, yet the genetic variants underlying such diversity remain poorly discovered and applied, especially those mediating the tolerance to salt-induced osmotic stress (SIOS). Here we report a metabolomics-driven understanding and genetic improvement of maize SIOS tolerance. Using a LC-MS-based untargeted metabolomics approach, we profiled the metabolomes of 266 maize inbred lines under control and salt conditions, and then identified 37 metabolite biomarkers of SIOS tolerance (METO1-37). Follow-up metabolic GWAS (mGWAS) and genotype-to-phenotype modeling identified 10 candidate genes significantly associating with the SIOS tolerance and METO abundances. Furthermore, we validated that a citrate synthase, a glucosyltransferase and a cytochrome P450 underlie the genotype-METO-SIOS tolerance associations, and showed that their favorable alleles additively improve the SIOS tolerance of elite maize inbred lines. Our study provides a novel insight into the natural variation of maize SIOS tolerance, which boosts the genetic improvement of maize salt tolerance, and demonstrates a metabolomics-based approach for mining crop genes associated with this complex agronomic trait.

Automated summary

Research has shown that natural maize varieties display a large diversity of salt tolerance, yet the genetic variants underlying such diversity remain poorly discovered and applied. An LC-MS-based untargeted metabolomics approach identified 37 metabolite biomarkers related to SIOS tolerance, and 10 candidate genes significantly associated with SIOS tolerance and METO abundances. A citrate synthase, a glucosyltransferase, and a cytochrome P450 were validated to underlie genotype-METO-SIOS tolerance associations and improve the SIOS tolerance of elite maize inbred lines through additive effects.