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DICER-LIKE1a autoregulation based on intronic microRNA processing is required for stress adaptation in Physcomitrium patens.

The Physcomitrium patens DICER-LIKE1a (PpDCL1a) mRNA encoding the essential Dicer protein for microRNA (miRNA) biogenesis harbors an intronic miRNA (miR1047). An autoregulatory mechanism to control PpDCL1a abundance that is based on competitive processing of the intronic miRNA and proper PpDCL1a mRNA splicing was previously proposed. If intron splicing occurs first the mRNA can be translated into functional PpDCL1a protein whereas processing of the intronic miRNA catalyzed by PpDCL1a itself prior to pre-mRNA splicing generates a truncated transcript unable to produce a functional protein. This proposed autoregulation of DCL1 has not been functionally analyzed in any plant species and the existence of this autoregulatory control is expected to have a general impact on the overall miRNA biogenesis pathway and the transcriptome that is under miRNA control. We abolished the PpDCL1a autoregulatory feedback control by the precise deletion of the MIR1047 containing intron. The generated line displayed salt stress hypersensitivity and hyposensitivity to the plant hormone ABA that are accompanied by disturbed expression of miRNAs and mRNAs revealed by transcriptome analyses. The feedback control together with the phenotypic abnormalities and molecular changes in the intronless line can be rescued by the re-insertion of a modified intron harboring a sequence unrelated artificial miRNA. Our findings indicate a physiological importance of the miR1047 based feedback control of the PpDCL1a transcript abundance that controls the expression of miRNAs and their cognate target RNAs during salt stress adaptation and suggests a key role to this autoregulation in the molecular adaptation of land plants to terrestrial habitats.