Evolution of small RNA expression following hybridization and allopolyploidization: insights from Spartina species (Poaceae, Chloridoideae).

KEY MESSAGE: Differential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in Spartina. The role of small RNAs on gene expression regulation and genome stability is arousing increased interest and is being explored in various plant systems. In spite of prominence of reticulate evolution and polyploidy that affects the evolutionary history of all plant lineages, very few studies analysed RNAi mechanisms with this respect. Here, we explored small RNAs diversity and expression in the context of recent allopolyploid speciation, using the Spartina system, which offers a unique opportunity to explore the immediate changes following hybridization and genome duplication. Small RNA-Seq analyses were conducted on hexaploid parental species (S. alterniflora and S. maritima), their F1 hybrid S. x townsendii, and the neoallododecaploid S. anglica. We identified 594 miRNAs, 2197 miRNA-target genes, and 3730 repeat-associated siRNAs (mostly targeting Class I/Copia-Ivana- Copia-SIRE and LINEs elements). For both mi- and ra-siRNAs, we detected differential expression patterns following genome merger and genome duplication. These misregulations include non-additive expression of miRNAs in the F1 hybrid and additional changes in the allopolyploid targeting developmental processes. Expression of repeat-associated siRNAs indicates a strengthen of transposable element repression during the allopolyploidization process. Altogether, these results confirm the central role small RNAs play in shaping regulatory changes in naturally formed recent allopolyploids.