The Oryza sativa transcriptome responds spatiotemporally to polystyrene nanoplastic stress

Nanoplastic represents an emerging abiotic stress facing modern agriculture, impacting global crop production. However, the molecular response of crop plants to this stress remains poorly understood at a spatiotemporal resolution. We therefore used RNA sequencing to profile the transcriptome expressed in rice (Oryza sativa) root and leaf organs at 1, 2, 4, and 8 d post exposure with nanoplastic. We revealed a striking similarity between the rice biomass dynamics in aboveground parts to that in belowground parts during nanoplastic stress, but transcriptome did not. At the global transcriptomic level, a total of 2332 differentially expressed genes were identified, with the majority being spatiotemporal specific, reflecting that nanoplastics predominantly regulate three processes in rice seedlings: (1) down-regulation of chlorophyll biosynthesis, photosynthesis, and starch, sucrose and nitrogen metabolism, (2) activation of defense responses such as brassinosteroid biosynthesis and phenylpropanoid biosynthesis, and (3) modulation of jasmonic acid and cytokinin signaling pathways by transcription factors. Notably, the genes involved in plant-pathogen interaction were shown to be successively modulated by both root and leaf organs, particularly plant disease defense genes (OsWRKY24, OsWRKY53, Os4CL3, OsPAL4, and MPK5), possibly indicating that nanoplastics affect rice growth indirectly through other biota. Finally, we associated biomass phenotypes with the temporal reprogramming of rice transcriptome by weighted gene co-expression network analysis, noting a significantly correlation with photosynthesis, carbon metabolism, and phenylpropanoid biosynthesis that may reflect the mechanisms of biomass reduction. Functional analysis further identified PsbY, MYB, cytochrome P450, and AP2/ERF as hub genes governing these pathways. Overall, our work provides the understanding of molecular mechanisms of rice in response to nanoplastics, which in turn suggests how rice might behave in a nanoplastic pollution scenario.