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The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants

By Rui Xia, Jing Xu, Blake C. Meyers

Posted 06 Dec 2016
bioRxiv DOI: 10.1101/090647 (published DOI: 10.1105/tpc.17.00185)

In plants, miR390 directs the production of tasiRNAs from TRANS-ACTING SIRNA 3 (TAS3) transcripts to regulate AUXIN RESPONSIVE FACTOR (ARF) genes, transcription factors critical for auxin signaling; these tasiRNAs are known as tasiARFs. This pathway is highly conserved, with the TAS3 as the only one noncoding gene present almost ubiquitously in land plants. To understand the evolution of this miR390-TAS3-ARF pathway, we characterized homologs of these three genes from thousands of plant species, from bryophytes to angiosperms. Both miR390 and TAS3 are present and functional in liverworts, confirming their ancestral role to regulate ARFs in land plants. We found the lower-stem region of MIR390 genes, critical for accurate DCL1 (DICER-LIKE 1) processing, is conserved in sequence in seed plants. We propose a model for the transition of functional tasiRNA sequences in TAS3 genes occurred at the emergence of vascular plants, in which the two miR390 target sites of TAS3 genes showed distinct pairing patterns in different plant lineages. Based on the cleavability of miR390 target sites and the distance between target site and tasiARF, we inferred a potential bidirectional processing mechanism exists for some TAS3 genes. We also demonstrated a tight mutual selection between tasiARF and its target genes, and characterized unusual aspects and diversity of regulatory components of this pathway. Taken together, these data illuminate the evolutionary path of the miR390-TAS3-ARF pathway in land plants, and demonstrate the significant variation that occurs in the production of phasiRNAs in plants, even in the functionally important and archetypal miR390-TAS3-ARF regulatory circuit.

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