Recent allopolyploidy alters Spartina microRNA expression in response to xenobiotic-induced stress

Environmental contamination by xenobiotics represents a major threat for natural ecosystems and public health. In response, xenobiotic detoxification is a fundamental trait of organisms for developmental plasticity and stress tolerance, but the underlying molecular mechanisms remain poorly understood in plants. To decipher this process, we explored the consequences of allopolyploidy on xenobiotic tolerance in the genus Spartina Schreb. Specifically, we focused on microRNAs (miRNAs) owing to their central function in the regulation of gene expression patterns, including responses to stress. Small RNA-Seq was conducted on the parents S. alterniflora and S. maritima, their F1 hybrid S. x townsendii and the allopolyploid S. anglica under phenanthrene-induced stress (phe), a model Polycyclic Aromatic Hydrocarbon (PAH) compound. Differentially expressed miRNAs in response to phe were specifically identified within species. In complement, the respective impacts of hybridization and genome doubling were detected, through changes in miRNA expression patterns between S. x townsendii, S. anglica and the parents. The results support the impact of allopolyploidy in miRNA-guided regulation of plant response to phe. In total, we identified 17 phe-responsive miRNAs in Spartina among up-regulated MIR156 and down-regulated MIR159. We also describe novel phe-responsive miRNAs as putative Spartina-specific gene expression regulators in response to stress. Functional validation using Arabidopsis (L.) Heynh. T-DNA lines inserted in homologous MIR genes was performed, and the divergence of phe-responsive miRNA regulatory networks between Arabidopsis and Spartina was discussed. Key message Phenanthrene-responsive microRNAs were identified in the context of allopolyploid speciation in Spartina. The results support the relative impacts of hybridization and genome doubling in miRNA-guided regulation mechanisms in response to xenobiotics.

Automated summary

Environmental contamination by xenobiotics poses a significant threat to natural ecosystems and public health. The molecular mechanisms underlying xenobiotic detoxification remain poorly understood in plants, particularly in response to allopolyploidy. This study identified phenanthrene-responsive microRNAs in Spartina in the context of allopolyploid speciation, and demonstrated the relative impacts of hybridization and genome doubling in miRNA-guided regulation mechanisms in response to xenobiotics.