Rhizosphere-to-intracellular adaptation in Ricinus communis roots under alkali stress: Pentose phosphate and pyruvate pathways mediate cross-dimensional regulation

Alkaline stress severely impairs root development and function in crops by inducing osmotic imbalance, oxidative stress, and elevated rhizosphere pH. Ricinus communis, a promising stress-resilient oil crop, exhibits notable alkali tolerance; however, the underlying root response mechanisms remain largely unexplored. In this study, we performed an integrated multi-omics analysis, encompassing root transcriptomics, metabolomics, and root exudate metabolomics, on alkali-tolerant (ST) and alkali-sensitive (SS) Ricinus communis genotypes to elucidate the cross-dimensional regulatory network governing root responses to alkaline stress. Our results revealed that the ST genotype mitigates alkali-induced damage via a dual adaptive strategy that encompasses both intracellular and rhizospheric responses. Specifically, ST roots upregulated PPP-associated gene expression and enzymatic activity to maintain intracellular redox homeostasis, while simultaneously enhancing pyruvate biosynthesis and exudation pathways to secrete organic acids that acidify the rhizosphere. In the ST genotype, genes encoding key metabolic enzymes—including fructose-bisphosphate aldolase (FBA), 6-phosphogluconate dehydrogenase (PGD), and fructose-1,6-bisphosphatase (FBP)—were significantly upregulated, thereby synergistically enhancing the efficient operation of stress-resistant key pathways, namely PPP and gluconeogenesis. Furthermore, pyruvate and methylglyoxal accumulated markedly in ST root exudates, serving as putative signaling molecules that modulate rhizosphere pH and activate stress responses. This study presents the first integrated transcription-metabolism-exudation model for the alkali stress response in Ricinus communis, underscoring the central roles of PPP and pyruvate metabolism in coordinating rhizosphere and intracellular adaptations. These findings offer valuable insights and molecular targets for breeding alkali-tolerant oilseed crops.