Repression of lateral organ boundary genes by PENNYWISE and POUND-FOOLISH is essential for meristem maintenance and flowering in Arabidopsis thaliana1

Abstract

ORCID IDs: 0000-0002-0050-4001 (B.C.S.); 0000-0002-3526-7982 (J.L.); 0000-0001-7896-6049 (M.P.); 0000-0001-7144-1274 (D.X.); 0000-0001-5026-095X (S.Ci.); 0000-0002-6496-3792 (S.R.H.); 0000-0003-1808-5172 (V.P.).In the model plant Arabidopsis (Arabidopsis thaliana), endogenous and environmental signals acting on the shoot apical meristem cause acquisition of inflorescence meristem fate. This results in changed patterns of aerial development seen as the transition from making leaves to the production of flowers separated by elongated internodes. Two related BEL1-like homeobox genes, PENNYWISE (PNY) and POUND-FOOLISH (PNF), fulfill this transition. Loss of function of these genes impairs stem cell maintenance and blocks internode elongation and flowering. We show here that pny pnf apices misexpress lateral organ boundary genes BLADE-ON-PETIOLE1/2 (BOP1/2) and KNOTTED-LIKE FROM ARABIDOPSIS THALIANA6 (KNAT6) together with ARABIDOPSIS THALIANA HOMEOBOX GENE1 (ATH1). Inactivation of genes in this module fully rescues pny pnf defects. We further show that BOP1 directly activates ATH1, whereas activation of KNAT6 is indirect. The pny pnf restoration correlates with renewed accumulation of transcripts conferring floral meristem identity, including FD, SQUAMOSA PROMOTER-BINDING PROTEIN LIKE genes, LEAFY, and APETALA1. To gain insight into how this module blocks flowering, we analyzed the transcriptome of BOP1-overexpressing plants. Our data suggest a central role for the microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE-microRNA172 module in integrating stress signals conferred in part by promotion of jasmonic acid biosynthesis. These data reveal a potential mechanism by which repression of lateral organ boundary genes by PNY-PNF is essential for flowering.Plant development relies on the activity of the shoot apical meristem (SAM) as a continuous source of founder cells for production of new leaves, shoots, and internodes throughout the life cycle (for review, see Aichinger et al., 2012). A tight balance between the allocation of cells to developing primordia and the perpetuation of pluripotent stem cells in the central zone maintains the SAM at a constant size. In Arabidopsis (Arabidopsis thaliana), the vegetative SAM produces leaves in a spiral phyllotaxy with dormant axillary meristems. In conjunction, internode elongation is repressed, resulting in a basal rosette. The transition to flowering is governed by internal and external signals that converge at the SAM to promote acquisition of inflorescence meristem (IM) fate (for review, see Amasino and Michaels, 2010;Srikanth and Schmid, 2011;Andrés and Coupland, 2012). This process, known as floral evocation, results in new patterns of growth at the shoot apex, including production of flowers, and an increase in stem elongation, called bolting. Lateral organ boundaries are specialized domains of restricted growth that separate meristem and organ compartments and produce axillary meristems (for review, see Aida and Tasaka, 2006;Tian et al., 2014). Early in the transition t...

Floral induction in Arabidopsis thaliana by FLOWERING LOCUS T requires direct repression of BLADE-ON-PETIOLE genes by homeodomain protein PENNYWISE

“…Indeed, we observed that, in the absence of functional PNY (pny-58), BOP2 expression becomes broader in the meristem. Similarly, Khan et al (2015) found that the BOP1 spatial pattern of expression was enlarged in the inflorescence meristem of pny pnf. This restriction of BOP expression and proper localization of the boundary is required for correct timing of the floral transition, because pny mutants are late flowering, and this is suppressed in the pny bop1 bop2 triple mutant ( Fig.…”

“…During vegetative development, ATH1 is expressed in the SAM and acts as a floral repressor. A recent study reported that BOP1 regulates the expression of ATH1 by directly binding to its promoter (Khan et al, 2015). Therefore, the ectopic expression of BOP1/2 in the meristem of pny mutants might increase ATH1 expression, contributing to the late-flowering phenotype.…”

Ideal crop plant architecture is mediated by tassels replace upper ears1, a BTB/POZ ankyrin repeat gene directly targeted by TEOSINTE BRANCHED1

“…Members of the BTB/POZ clade of ankyrin repeat proteins have a wide range of functions (25) including establishment of floral and inflorescence meristem determinacy (45)(46)(47), but those most similar to tru1 appear to have a clear function in specifying leaf cell identities. The founding members of this clade, BLADE ON PETIOLE 1 and 2, display ectopic distal blade tissue growing down the petiole and lack of stipules (24,48).…”

A homolog of Blade-On-Petiole 1 and 2 (BOP1/2) controls internode length and homeotic changes of the barley inflorescence

“…As members of the NPR1-like gene family, HvLax-a and HvCul4 may play a role in defense responses and jasmonate signaling, as has been shown for the Arabidopsis BOP genes. These putative additional functions may have acted as additional factors influencing the evolutionary history of these genes (Canet et al, 2012;Khan et al, 2015).…”

“…In contrast, the opposite mode of regulation has been reported to control inflorescence stem elongation. The BP and BELL-like homeodomain gene PENNYWISE functions as a repressor of BOP1/2, KNAT6, and the BELL gene ARABIDOPSIS THALIANA HOMEOBOX1 (ATH1), while BOP1/2 activate KNAT6 and ATH1 in a shared pathway (Khan et al, 2012a(Khan et al, , 2012b(Khan et al, , 2015 Recently, it was shown that BOP1/2 function as negative regulators of the bZIP transcription factor (TF) FD, which is a component of the floral transition pathway of FLOWERING TIME LOCUS T (FT) and is required for the activation of the key floral development regulatory genes LEAFY (LYF) and APETALA1 (AP1; Andrés et al, 2015). Opposing roles for BOP1/2 were proposed in later stages of floret development via directly promoting the expression of AP1 and LYF, thus controlling floral organ patterning (Karim et al, 2009;Xu et al, 2010;Andrés et al, 2015).…”