mRNA decapping machinery targets transcripts of the LBD3/ASL9 transcription factor to authorize formation of apical hook and lateral roots in Arabidopsis

Multicellular organisms perceive and transduce multiple cues to optimize developmental reprogramming and cell state switching. Core transcription factors drive developmental changes, but transitions also require the attenuation of previous states. Here, we demonstrate that the levels of mRNAs of the LATERAL ORGAN BOUNDARIES DOMAIN (LBD)/ASYMMETRIC LEAVES9-LIKE (ASL9) transcription factor are directly regulated by mRNA decapping. Capped ASL9 transcripts accumulate in decapping deficient plants and ASL9 mRNAs are found together with decapping components. Accumulation of ASL9 inhibits apical hook and lateral roots formation and interestingly, exogenous auxin application restores apical and lateral roots in both ASL9 and mRNA decay deficient mutants. Moreover, mutations in the cytokinin transcription factors type-B ARABIDOPSIS RESPONSE REGULATORS (B-ARRs) ARR10 and ARR12 restore these developmental defects of ASL9 overexpression. Thus, the mRNA decay machinery directly targets ASL9 transcripts for decay to balance cytokinin/auxin responses during developmental reprogramming. Significance StatementPlants build new structures to shape their growth in response to environmental and developmental cues. Most developmental studies focus on the transcription rates of key regulators but largely neglect the contribution of mRNA stability or decay. Our work describes an essential function of mRNA decay in cellular reprogramming and developmental programs through functional analysis of the PAT (Proteins associated with Topoisomerase II) mRNA decapping components, and of DCP2 (Decapping 2) and DCP5. Developmental defects caused by accumulation of the mRNA decapping target ASL9 could be restored by interference with a cytokinin pathway and/or exogenous auxin application. Thus, mRNA decapping machinery targets ASL9 transcripts for decay to keep cytokinin/auxin response in balance and to promote developmental processes including apical hooking and lateral root formation.