Multiomics unraveled that gibberellin signaling underlies adaptation of rice to ciprofloxacin stress: Calling for concerns on the adverse effects of pharmaceutical residues in water during agricultural irrigations

Abstract

Residual concentrations of antibiotics in water can reach ng mL⁻¹ - µg mL⁻¹ levels, which pose high risks to crops during irrigation; however, the interactions between rice and antibiotics, as well as the defense mechanisms of rice at their early growth phase remain unclear. In this study, we investigated the uptake dynamics of a ubiquitously found antibiotic, ciprofloxacin (CIP) at 0.1, 1, 6.5, and 20 µg mL⁻¹ in rice seedlings. We found gradually bioaccumulated CIP induced significant physiological changes including inhibited growth of roots and leaves of rice seedlings, and decreased pigment contents, which can be caused by disrupted homeostasis of reactive oxygen species. Integrating roots transcriptomics, metabolomics, and validation experiments, we found that rice seedlings synthesized more gibberellins to trigger the expression of transcription factors such as group VII ethylene response factors, which induced metabolic reprogramming to yield more fatty acids derivates. These compounds including eicosanoids, isoprenoids, and fatty acids and conjugates can act as signaling molecules, as well as antioxidants and energy sources to achieve rice recovery. This conclusion is supported by the evidence showing that adding gibberellins in rice seedlings culture decreased the accumulated CIP and improved rice growth; whilst, disrupting gibberellin signaling pathway using paclobutrazol as an inhibitor increased uptaken CIP in both roots and leaves with augmenting the antibiotic stress on rice. This study has demonstrated a gibberellin-based defense mechanism in rice for defense of CIP stress, which might have significant environmental applications since we can add minor gibberellins to reduce bioaccumulated CIP with simultaneously promoting rice growth at their early phases.