Abstract
The transition to flowering in many plant species, including Arabidopsis (Arabidopsis thaliana), is marked by the elongation of internodes to make an inflorescence upon which lateral branches and flowers are arranged in a characteristic pattern. Inflorescence patterning relies in part on the activities of two three-amino-acid loop-extension homeodomain transcription factors: BREVIPEDICELLUS (BP) and PENNYWISE (PNY) whose interacting products also promote meristem function. We examine here the genetic interactions between BP-PNY whose expression is up-regulated in stems at the floral transition, and the lateral organ boundary genes BLADE-ON-PETIOLE1 (BOP1) and BOP2, whose expression is restricted to pedicel axils. Our data show that bp and pny inflorescence defects are caused by BOP1/2 gain of function in stems and pedicels. Compatible with this, inactivation of BOP1/2 rescues these defects. BOP expression domains are differentially enlarged in bp and pny mutants, corresponding to the distinctive patterns of growth restriction in these mutants leading to compacted internodes and clustered or downward-oriented fruits. Our data indicate that BOP1/2 are positive regulators of KNOTTED1-LIKE FROM ARABIDOPSIS THALIANA6 expression and that growth restriction in BOP1/2 gain-of-function plants requires KNOTTED1-LIKE FROM ARABIDOPSIS THALIANA6. Antagonism between BOP1/2 and BP is explained in part by their reciprocal regulation of gene expression, as evidenced by the identification of lignin biosynthetic genes that are repressed by BP and activated by BOP1/2 in stems. These data reveal BOP1/2 gain of function as the basis of bp and pny inflorescence defects and reveal how antagonism between BOP1/2 and BP-PNY contributes to inflorescence patterning in a model plant species.
Highlights
Flowering plants display a remarkable variety of inflorescence architectures selected to optimally display flowers for pollination and seed dispersal
While analysis of loss-of-function bop1 bop2 mutants has revealed that BOP1/2 transcriptionally repress meristematic genes in leaves (Ha et al, 2007) and floral primordia (Xu et al, 2010) relatively little is known about how BOP1/2 gain-of-function perturbs plant architecture
The meristem expression of BP diminishes with the floral transition and becomes restricted to the cortex of the inflorescence stem and pedicel, where its activity together with PNY promotes internode elongation and vascular patterning (Lincoln et al, 1994; Douglas et al, 2002; Venglat et al, 2002; Smith and Hake, 2003)
Summary
Flowering plants display a remarkable variety of inflorescence architectures selected to optimally display flowers for pollination and seed dispersal. The SAM produces a series of reiterative modules known as phytomers to generate the aerial parts of the plant. Elaboration of the different parts of a module (leaves, internodes, and axillary meristems) varies according to the phase of development and between species to generate architectural diversity (Sussex and Kerk, 2001). The SAM generates leaf primordia on its flanks; both internode and axillary meristem formation are inhibited resulting in a compact rosette of leaves. Internodes elongate and axillary meristems proliferate at the expense of leaves to generate lateral branches and flowers in a regular spiral pattern on the inflorescence (Bowman and Eshed, 2000; Fletcher, 2002; Barton, 2010). Whilst the pathways that promote floral fate of axillary meristems and repress leaf development are well-studied, less is known about the formation and patterning of internodes
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