Tolerance mechanism of rice (Oryza sativa L.) seedings towards polycyclic aromatic hydrocarbons toxicity: The activation of SPX-mediated signal transduction to maintain P homeostasis

Abstract

Plant tolerance to abiotic stress depends on fast molecular cascades involving stress perception, signal transduction, gene expression alterations, and metabolic rearrangement. This study sheds light on the tolerance mechanism of rice (Oryza sativa L.) towards the toxicity of the polycyclic aromatic hydrocarbons (PAHs), including phenanthrene (Phe), pyrene (Pyr), and benzo[a]pyrene (BaP). Results showed that three PAHs significantly activated the phosphoinositide signaling system involving the phosphorus (P) metabolism and homeostasis in rice roots. This activation increased phytic acid (IP6) levels to over 54.12% of the control (p < 0.05). Molecular docking verified that three PAHs occupied the IP6 binding site in SPX3, a negative regulatory factor of P homeostasis, where ARG229 interacted with PAHs via the van der Waals force. Moreover, the expression of gene encoding SPX3 was significantly downregulated 2.81-, 2.83-, and 2.18-fold under Phe, Pyr, and BaP stress, respectively, relative to the control. Conversely, the expression levels of the gene coding SDEL2 was significantly increased, promoting the degradation of SPX3. Ultimately, P absorption and nucleic acid synthesis were enhanced, alleviating the inhibition effect of PAHs on rice growth. Notably, Pyr demonstrated the strongest binding affinity for SPX3, confirming its critical interference with P homeostasis. These findings provide insight into the molecular mechanisms regulating plant responses to PAHs, and offer guidance for improving crop resistance against organic pollutants and protecting food security.