Control of plant architecture by the TALE homeobox genes ATH1 and PENNYWISE

Abstract

In plants, pattern formation is an ongoing process that starts during embryogenesis and lasts the entire life span. Most of the plant adult body is formed post-embryonically by continuous organogenic potential of the root and shoot meristems. Proper shoot apical meristem (SAM) function requires maintenance of a delicate balance between the depletion of stem cell daughters into developing primordia and proliferation of the central stem cell population. Mutations in the KNOX-class TALE HD protein SHOOTMERISTEMLESS (STM) cause defective initiation and maintenance of the SAM andresults in early developmental arrests.STM is able to physically interact with members of a distantly related second class of TALE HD transcription factors, the BELL class. Here we show that the BELL-class proteins ARABIDOPSIS THALIANA HOMEOBOX1 (ATH1) and PENNYWISE (PNY)interact with STM and fulfill functional redundant roles with STM during initiation and maintenance of the vegetative SAM. Loss of ATH1 and PNYresults in a stm mutant phenocopies during the embryonic and vegetativephases, whereas generative development appears unaffected. Finally, we present data implying that both KNOX and BELL proteinfunction are regulated through their subcellular distribution by amechanism highly conserved in animals and plants. Floral induction is controlled by a plethora of genes acting in different pathways that either repress or promote floral transition at the shoot apical meristem (SAM). During vegetative development high levels of floral repressors maintain the Arabidopsis SAM incompetent to respond to promoting factors. Among these repressors, FLOWERING LOCUS C (FLC) is the most prominent. The processes underlying down-regulation of FLC in response to environmental and developmental signals have been elucidated in considerable detail. However, the basal induction of FLC and its up-regulation by FRIGIDA (FRI) are less understood. Here we demonstrate that the BELL-class genes ATH1 and PNY act redundantly as positive regulators of FLC expression. Plants that constitutively express ATH1 display a vernalization-sensitive late flowering habit. Analysis of lines that differ in FRI and/or FLC allele strength show that this late flowering is caused by up-regulation of FLC as a result of synergism between ATH1 and FRI. Consistently, ath1 and pny mutants flower early in short days (SD) and display attenuated FLC levels. Moreover, ath1 and pny mutations partially suppress FLC-mediated late flowering of both a FRI-expressing line and that of autonomous pathway mutants. In contrast to the relatively weak effects of either single mutant, absence of both ATH1 and PNY almost fully impairs FRI-mediated late flowering. Intriguingly, no role for the BELL gene POUND-FOOLISH (PNF), an established redundant partner of PNY required for the competence of the SAM to respond properly to floral inductive signals, was found in FLC-mediated flowering time control. Taken together, this suggests that throughout plant development different BELL combinations control meristem maintenance and dictate developmental phase identity by controlling key components of phase identity.