Transcriptomics and resequencing reveal dual evolutionary strategies for salt tolerance in foxtail millet (Setaria italica (L.))

Abstract

Soil salinity poses a major constraint to cereal production, yet the genetic basis underlying salt tolerance in foxtail millet ( Setaria italica (L.)) remains largely elusive. To dissect these tolerance mechanisms, we integrated phenotyping, physiological assays, transcriptomics, and population genomics across 18 extreme salt-tolerant panel (STP) and 18 salt-sensitive panel (SSP) accessions selected from over 500 germplasm resources, with evaluations conducted under NaCl treatment. Under salt stress, STP accessions exhibited better growth and higher chlorophyll content (RCC: 5.9 vs. 3.0 on day 2) alongside lower membrane damage (REC: 14% vs. 24%) and ROS accumulation compared to SSP accessions. Transcriptome profiling identified a tolerance-associated module, STP007, which was enriched for AP2/ERF and IDD motifs and contained candidate transcription factors including YABBY and WRKY. Population genomics revealed that despite a relatively homogeneous genetic background, localized selective sweeps on chromosomes 3 and 6 were associated with salt tolerance. By integrating transcriptomic interaction networks with population evolutionary signatures, five core candidate genes involved in abscisic acid biosynthesis and redox homeostasis were identified, highlighting a probable genetic basis for salt tolerance. In summary, these findings suggest a dual-layered mechanism for foxtail millet salt tolerance, likely coordinated by localized adaptive selection at core genomic nodes and dynamic plasticity within transcriptional networks. This model offers insights into mitigating the growth-stress trade-off, presenting potential candidate targets for breeding resilient cereal crops.