An intron-split microRNA mediates cleavage of the mRNA encoded by low phosphate root in Solanaceae

A microRNA with a non-canonical precursor structure harbours an intron in between its miRNA-5p and miRNA-3p relevant for its biogenesis, is conserved across Solanaceae, and targets the mRNA of low phosphate root. Hundreds of miRNAs have been identified in plants and great advances have been accomplished in the understanding of plant miRNA biogenesis, mechanisms and functions. Still, many miRNAs, particularly those with less conventional features, remain to be discovered. Likewise, additional layers of regulation from miRNA generation to action and turnover are still being revealed. The current study describes a microRNA not previously identified given its unusual intron-split stem-loop structure, that has been previously observed only within the monocot-specific miRNA444 family. It shows its conservation across a branch of Solanales including agriculturally relevant Solanaceae family, where its transcripts had already been predicted in several species within sequence databases. The miRNA is absent in Arabidopsis thaliana but present in Solanum lycopersicum, Nicotiana benthamiana, Petunia axillaris, and Ipomoea nil. It proves that at least two different pri-miRNA variants are produced from this miRNA gene, one spliced and the other one retaining the intron. It demonstrates the dual function of its intron in the miRNA biogenesis. On the one hand, its presence in the pri-miRNA positively influences mature miRNA accumulation, but on the other hand, it needs to be removed from the pri-miRNA for efficient mature miRNA production. Finally, it sets low phosphate root as one of its targets, a protein known to be involved in root growth regulation under phosphate starvation in other plant species.