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MicroRNAs (miRNAs) are ∼21 nt small RNAs that regulate gene expression in animals and plants. They can be grouped into families comprising different genes encoding similar or identical mature miRNAs. Several miRNA families are deeply conserved in plant lineages and regulate key aspects of plant development, hormone signaling, and stress response. The ancient miRNA miR396 regulates conserved targets belonging to the  GROWTH-REGULATING FACTOR  ( GRF ) family of transcription factors, which are known to control cell proliferation in  Arabidopsis  leaves. In this work, we characterized the regulation of an additional target for miR396, the transcription factor  bHLH74 , that is necessary for  Arabidopsis  normal development.  bHLH74  homologs with a miR396 target site could only be detected in the sister families  Brassicaceae  and  Cleomaceae.  Still,  bHLH74  repression by miR396 is required for margin and vein pattern formation of  Arabidopsis  leaves. MiR396 contributes to the spatio-temporal regulation of  GRF  and  bHLH74  expression during leaf development. Furthermore, a survey of miR396 sequences in different species showed variations in the 5′ portion of the miRNA, a region known to be important for miRNA activity. Analysis of different miR396 variants in  Arabidopsis thaliana  revealed that they have an enhanced activity toward  GRF  transcription factors. The interaction between the  GRF  target site and miR396 has a bulge between positions 7 and 8 of the miRNA. Our data indicate that such bulge modulates the strength of the miR396-mediated repression and that this modulation is essential to shape the precise spatio-temporal pattern of  GRF2  expression. The results show that ancient miRNAs can regulate conserved targets with varied efficiency in different species, and we further propose that they could acquire new targets whose control might also be biologically relevant.

Functional Specialization of the Plant miR396 Regulatory Network through Distinct MicroRNA–Target Interactions