FAR-RED ELONGATED HYPOCOTYL3 promotes floral meristem determinacy in Arabidopsis

Abstract

The transposase-derived transcription factor genes FAR-RED ELONGATED HYPOCOTYL3 (FHY3) and FAR-RED IMPAIRED RESPONSE1 (FAR1) have redundant and multifaceted roles in plant growth and development during the vegetative stage, including phytochrome A-mediated far-red light (FR) signaling and circadian clock entrainment. Little is known about their functions in the reproductive stage. We recently demonstrated that FHY3 plays important roles in shoot apical meristem (SAM) maintenance and floral meristem (FM) determinacy through its target genes CLAVATA3 (CLV3), SEPALLATA1 (SEP1) and SEP2. Here we present data that FHY3 but not its homolog, FAR1, has a distinct role in FM determinacy in a manner independent of its light signaling and circadian pathway functions. Moreover, genome-wide gene expression profiling showed that the homeostasis of the FM is critical for the regulation of FM activity. Light is one of the most important environmental signals for plant growth and development. In Arabidopsis, 5 distinct photoreceptors perceive and respond to different wavelengths of light. While phytochrome B (phyB) is the primary photoreceptor of the red-light (R) signal, phytochrome A (phyA) is responsible for the transduction of the far-red light (FR) signal and the early R response.1,2 Upon FR and R irradiation, phyA is light activated and translocates to the nucleus to regulate the FR/R response. These events are mediated by FAR-RED ELON-GATED HYPOCOTYL1 (FHY1) and its homolog FHY1-LIKE (FHL), as evidenced by the cytosolic localization of phyA in the fhy1 fhl double mutant. 3,4FAR-RED ELONGATED HYPOCOTYL3 (FHY3) and its homolog FAR-RED IMPAIRED RESPONSE1 (FAR1) were isolated as positive regulators of the phyA signaling pathway in Arabidopsis and were found to encode Mutator-like transposase-derived transcription factors. [5][6][7][8] In this response, FHY3 functions redundantly with but dominantly over FAR1.9 Further molecular analysis revealed that FHY3/FAR1 induce FHY1/FHL expression by directly binding to FHY3/FAR1-binding sites (FBS, CACGCGC) in their promoters and facilitating the nuclear accumulation of light-activated phyA. 8,10 FHY3 is also involved in the gating of light signals to the circadian clock.11 The complex network of interconnected feedback loops and endogenous key oscillators, including CIRCADIAN CLOCK ASSOCIATED1 (CCA1), EARLY FLOWERING4 (ELF4) and TIMING OF CAB1 (TOC1), ensures that daily processes occur at the optimum time of day and that metabolism proceeds in an efficient sequence. 12,13 In fhy3 mutants, CCA1 and ELF4 are dramatically reduced, and the expression of TOC1 becomes arrhythmic.14 Besides phytochrome and circadian signaling, FHY3/FAR1 have been found to function in diverse plant developmental and physiological processes such as UV-B signaling, programmed cell death, chloroplast biogenesis, chlorophyll biosynthesis, ABA signaling, branching and plant architecture. 15 However, these findings focus on FHY3/ FAR1 functions at the plant vegetative stage. The roles of FHY3/FAR1 in flower...

An Acyl-CoA N-Acyltransferase Regulates Meristem Phase Change and Plant Architecture in Barley

“…Moreover, transcripts with roles in light signal transduction were also primarily upregulated in the mnd1.a mutant and included, for example, two FAR-RED IM-PAIRED1 (FAR1) genes (HORVU0Hr1G038960.25 and HORVU4Hr1G014170.1; Fig. 6E), which have multiple roles in plant development, including meristem as well as floral development (Wang and Wang, 2015;Liu et al, 2016). Interestingly, transcripts of Lys-specific demethylase 5D (HORVU2Hr1G045000.1) were detected only in Bowman, and not in apices of the mnd1.a mutant (Fig.…”

AUXIN RESPONSE FACTOR3 Regulates Floral Meristem Determinacy by Repressing Cytokinin Biosynthesis and Signaling

“…Nevertheless, we previously isolated and functionally characterized several FM determinacy regulators via EMS mutagenesis of ag-10 (Cao et al, 2015;Li et al, 2016a). We therefore reasoned that the FM homeostasis that is perturbed in ag-10 is critical for FM maintenance and termination (Liu et al, 2016). Analysis of longitudinal sections revealed that the siliques of cytokinin-treated ag-10 had more bulges compared with untreated plants and produced additional tissues within the primary carpel, indicating a severe FM determinacy defect due to exogenous cytokinin treatment (Figures 1C and 1D).…”

“…Besides regulating WUS expression directly and indirectly (Sun et al, 2009;Liu et al, 2011), AG helps maintain FM homeostasis. In terms of genome-wide gene expression, the impact of the ag-10 point mutation is minimal, but FM homeostasis is effectively destroyed: in the ag-10 genetic background, even small perturbations in the FM determinacy regulatory network are amplified and result in severe FM determinacy defects (Liu et al, 2016). For example, the expression of major cytokinin biosynthesis and signaling genes, such as IPTs, AHK4, ARRs, and LOGs, was significantly derepressed in ag-10 arf3-29 relative to the single ag-10 and arf3-29 mutants (Figures 2F and 4B), indicating that ARF3 and AG function synergistically to regulate cytokinin activity.…”

THERMOSENSITIVE BARREN PANICLE (TAP) is required for rice panicle and spikelet development at high ambient temperature

“…The Arabidopsis FHY3 protein directly activates the E‐class MADS‐box gene SEPALLATA2 ( SEP2 ) (Liu et al ., 2016). We have demonstrated that the tap mutation causes the downregulation of 10 OsMADS genes and three YAB genes (Fig.…”

“…One such protein family is the FAR‐RED IMPAIRED RESPONSE1 (FAR1)‐related sequences (FRS) family of transcription factors in Arabidopsis (Hudson et al ., 2003). Arabidopsis FAR1 and FAR‐RED ELONGATED HYPOCOTYLS3 (FHY3) are homologous FRS proteins that participate in a wide range of cellular processes, including signal transduction in photomorphogenesis (Hudson et al ., 1999, 2003), circadian clock regulation (Allen et al ., 2006; Li et al ., 2011), chloroplast division (Chang et al ., 2015), abscisic acid signaling (Tang et al ., 2013), and shoot meristem and floral development (Stirnberg et al ., 2012; Li et al ., 2016; Liu et al ., 2016). Despite the higher number of FRS genes in monocot genomes, their functions are poorly understood.…”