Transcriptional activation of auxin biosynthesis drives developmental reprogramming of differentiated cells

Reprogramming of mature plant cells requires histone acetylation-mediated activation of auxin biosynthesis to reinitiate the mitotic cell cycle. Plant cells exhibit remarkable plasticity of their differentiation states, enabling regeneration of whole plants from differentiated somatic cells. How they revert cell fate and express pluripotency, however, remains unclear. In this study, we demonstrate that transcriptional activation of auxin biosynthesis is crucial for reprogramming differentiated Arabidopsis (Arabidopsis thaliana) leaf cells. Our data show that interfering with the activity of histone acetyltransferases dramatically reduces callus formation from leaf mesophyll protoplasts. Histone acetylation permits transcriptional activation of PLETHORAs, leading to the induction of their downstream YUCCA1 gene encoding an enzyme for auxin biosynthesis. Auxin biosynthesis is in turn required to accomplish initial cell division through the activation of G2/M phase genes mediated by MYB DOMAIN PROTEIN 3-RELATED (MYB3Rs). We further show that the AUXIN RESPONSE FACTOR 7 (ARF7)/ARF19 and INDOLE-3-ACETIC ACID INDUCIBLE 3 (IAA3)/IAA18-mediated auxin signaling pathway is responsible for cell cycle reactivation by transcriptionally upregulating MYB3R4. These findings provide a mechanistic model of how differentiated plant cells revert their fate and reinitiate the cell cycle to become pluripotent.

Automated summary

This study demonstrates the importance of transcriptional activation of auxin biosynthesis in reprogramming differentiated plant cells. Histone acetylation facilitates the activation of PLETHORAs, leading to the induction of downstream YUCCA1 gene. Auxin biosynthesis is required for initial cell division and the expression of MYB3R4 gene.