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. Key transcription factors drive developmental changes, but transitions also require the attenuation of previous states. Here, we demonstrate that the mRNA levels of the LATERAL ORGAN BOUNDARIES DOMAIN 3 (LBD3) / ASYMMETRIC LEAVES 2-LIKE 9 (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 lateral roots formation in both ASL9 overexpressor and mRNA decay-deficient mutants. Moreover, mutations in the cytokinin transcription factors type-B ARABIDOPSIS RESPONSE REGULATORS (B-ARRs) ARR10 and ARR12 restore the developmental defects in apical hooking and lateral root formation caused by over-accumulation of capped ASL9 transcript upon ASL9 overexpression. Thus, the mRNA decay machinery directly targets ASL9 transcripts for decay to balance cytokinin/auxin responses during developmental reprogramming.