Split-root transcriptomics reveals the molecular basis of genotype-dependent root boron retention in rice

Abstract

Soil boron pollution poses an increasing threat to crop productivity and agricultural sustainability, yet the early mechanisms underlying plant adaptation to boron toxicity remain poorly understood. Using a split-root system combined with transcriptome profiling, we dissected genotype-dependent responses to boron stress in two rice varieties with contrasting boron accumulation and allocation characteristics. Under localized boron exposure, BJ retained more boron in roots, whereas YR translocated more boron to shoots, indicating distinct genotype-dependent strategies of boron allocation. Early responses to boron toxicity were characterized by suppression of cell wall biosynthesis and assembly, cell cycle progression, and gibberellin signaling, together with induction of DNA repair, antioxidant defense (mediated by glutathione and catalase), and abscisic acid- and jasmonic acid-related hormone pathways. Boron transport was also rapidly reprogrammed, as reflected by the down-regulation of boron transporter 1 (BOR1) and the up-regulation of polyol transporter 5 (PLT5) and detoxification transporter 16 (DTX16). Spatial transcriptomic analyses further distinguished External-Boron-Responsive and Internal-Boron-Responsive modules, supporting a framework of local perception and systemic integration. Notably, weighted gene co-expression network analysis (WGCNA) showed broader repression of MAPK signaling, plant hormone signal transduction, amino acid and lipid metabolism, and phenylpropanoid biosynthesis in BJ, suggesting reduced root physiological activity. In contrast, YR maintained these functions more effectively, consistent with its lower root boron retention. These findings advance our understanding of rice adaptation to boron toxicity and highlight candidate pathways associated with improved boron tolerance.