Phytochrome A Mediates Rapid Red Light–Induced Phosphorylation of<i>Arabidopsis</i>FAR-RED ELONGATED HYPOCOTYL1 in a Low Fluence Response

Shen, Yulong; Zhang, Zhou; Feng, Suhua; Li, Jigang; Tan-Wilson, Anna L.; Liu, Qu; Wang, Haiyang; Deng, Xing Wang

doi:10.1105/tpc.108.061259

Cited by 69 publications

(83 citation statements)

References 68 publications

(123 reference statements)

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“…By contrast, for the group v, vi, and vii ciselements, transcription factors physically interact with phyA or FHY1 for their unique associations, as well as the coordinate association if the subsequent recruitment of the other protein occurs favorably (Fig. 6, TF 6 , TF 7 , and TF 9 cases). FHY1 and phyA coassociations on RHA1B and SEX4 corroborate the group iii and vii models, respectively.…”

Section: Discussionmentioning

confidence: 99%

“…Two essential partners for phyA nuclear translocation, FAR-RED ELONGATED HYPOCOTYL1 (FHY1) and its less abundant homolog FHY1-LIKE (FHL), influence this process at two levels; first, after the initial burst of phyA nuclear importation under R, FHY1 is gradually phosphorylated by action of the Pfr form of phyA (7). This event inhibits the nuclear translocation of FHY1 and consequently prevents further nuclear accumulation of phyA.…”

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confidence: 99%

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Photoreceptor partner FHY1 has an independent role in gene modulation and plant development under far-red light

Chen

Demone

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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To incorporate the far-red light (FR) signal into a strategy for optimizing plant growth, FAR-RED ELONGATED HYPOCOTYL1 (FHY1) mediates the nuclear translocation of the FR photoreceptor phytochrome A (phyA) and facilitates the association of phyA with the promoters of numerous associated genes crucial for the response to environmental stimuli. However, whether FHY1 plays additional roles after FR irradiation remains elusive. Here, through the global identification of FHY1 chromatin association sites through ChIP-seq analysis and by the comparison of FHY1-associated sites with phyA-associated sites, we demonstrated that nuclear FHY1 can either act independently of phyA or act in association with phyA to activate the expression of distinct target genes. We also determined that phyA can act independently of FHY1 in regulating phyA-specific target genes. Furthermore, we determined that the independent FHY1 nuclear pathway is involved in crucial aspects of plant development, as in the case of inhibited seed germination under FR during salt stress. Notably, the differential presence of cis-elements and transcription factors in common and unique FHY1-and/or phyA-associated genes are indicative of the complexity of the independent and coordinated FHY1 and phyA pathways. Our study uncovers previously unidentified aspects of FHY1 function beyond its currently recognized role in phyA-dependent photomorphogenesis.L ight is one of the most important environmental cues in plant growth and development. Arabidopsis has thus evolved several photoreceptors to perceive different wavelengths in the visible light spectrum (1). Among them, phytochrome A (phyA) is the primary photoreceptor to mediate the far-red light (FR) and early red light (R) responses (2, 3). PhyA therefore plays a predominant role in plant adaptation to a shade environment where the R/FR ratio decreases. Upon FR and R irradiation phyA will shuttle between the inactive R-absorbing Pr form and the active FR-absorbing Pfr form. These two forms display distinct biological activities, nuclear translocation rates, degradation rates, and affinities for various signaling intermediates (2, 4, 5).Both FR and R trigger the localization of cytosolic phyA to the nucleus (6), albeit through different mechanisms. Two essential partners for phyA nuclear translocation, FAR-RED ELONGATED HYPOCOTYL1 (FHY1) and its less abundant homolog FHY1-LIKE (FHL), influence this process at two levels; first, after the initial burst of phyA nuclear importation under R, FHY1 is gradually phosphorylated by action of the Pfr form of phyA (7). This event inhibits the nuclear translocation of FHY1 and consequently prevents further nuclear accumulation of phyA. Under FR, however, persistent phyA nuclear translocation is observed with nonphosphorylated FHY1 (8); second, the nucleo-cytoplasmic shuttling of FHY1/FHL is also reduced under R owing to the low dissociation rate of the Pfr-FHY1/ FHL complex. The FR-driven phyA conversion to its Pr form benefits the recycling of FHY1/FHL for continuous phyA n...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Photoreceptor partner FHY1 has an independent role in gene modulation and plant development under far-red light

Chen

Demone

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…The coding sequence of FyPP3, PIN1, and PIN2 were amplified by PCR and cloned into the pSY vectors containing either the N-terminal (1 to 155 amino acids) or C-terminal (156 to 239 amino acid) regions of the YFP fluorescent protein (YFP N and YFP C ). Particle bombardment of possible pairwise combinations of plasmids and culture of the onion (Allium cepa) epidermal cells after bombardment were performed as described previously (Shen et al, 2009). YFP fluorescence was observed with a Carl Zeiss LSM510 confocal microscope.…”

Section: Bifc Assaymentioning

confidence: 99%

“…The vectors for BiFC assays were derived from pSY728, pSY735, pSY736, and pSY738 vectors, as described previously (Bracha-Drori et al, 2004;Shen et al, 2009). The coding sequence of FyPP3, PIN1, and PIN2 were amplified by PCR and cloned into the pSY vectors containing either the N-terminal (1 to 155 amino acids) or C-terminal (156 to 239 amino acid) regions of the YFP fluorescent protein (YFP N and YFP C ).…”

Section: Bifc Assaymentioning

confidence: 99%

A PP6-Type Phosphatase Holoenzyme Directly Regulates PIN Phosphorylation and Auxin Efflux in Arabidopsis

et al. 2012

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The directional transport of the phytohormone auxin depends on the phosphorylation status and polar localization of PIN-FORMED (PIN) auxin efflux proteins. While PINIOD (PID) kinase is directly involved in the phosphorylation of PIN proteins, the phosphatase holoenzyme complexes that dephosphorylate PIN proteins remain elusive. Here, we demonstrate that mutations simultaneously disrupting the function of Arabidopsis thaliana FyPP1 (for Phytochrome-associated serine/threonine protein phosphatase1) and FyPP3, two homologous genes encoding the catalytic subunits of protein phosphatase6 (PP6), cause elevated accumulation of phosphorylated PIN proteins, correlating with a basal-to-apical shift in subcellular PIN localization. The changes in PIN polarity result in increased root basipetal auxin transport and severe defects, including shorter roots, fewer lateral roots, defective columella cells, root meristem collapse, abnormal cotyledons (small, cup-shaped, or fused cotyledons), and altered leaf venation. Our molecular, biochemical, and genetic data support the notion that FyPP1/3, SAL (for SAPS DOMAIN-LIKE), and PP2AA proteins (RCN1 [for ROOTS CURL IN NAPHTHYLPHTHALAMIC ACID1] or PP2AA1, PP2AA2, and PP2AA3) physically interact to form a novel PP6-type heterotrimeric holoenzyme complex. We also show that FyPP1/3, SAL, and PP2AA interact with a subset of PIN proteins and that for SAL the strength of the interaction depends on the PIN phosphorylation status. Thus, an Arabidopsis PP6-type phosphatase holoenzyme acts antagonistically with PID to direct auxin transport polarity and plant development by directly regulating PIN phosphorylation. INTRODUCTIONAuxin is a fundamental plant hormone that regulates almost every aspect of plant growth and development, including embryogenesis, organogenesis, apical dominance, tissue regeneration, and tropisms (reviewed in Bennett and Scheres, 2010;Grunewald and Friml, 2010;Peris et al., 2010). Auxin is transported from its sites of biosynthesis to its sites of action by a polarized auxin transport system. Molecular genetic studies in Arabidopsis thaliana have lead to the identification and functional characterization of several key players of the polarized auxin transport system, such as the auxin uptake carriers AUXIN RESISTANT1/LIKE AUX1 (AUX1/ LAX) (Swarup et al., 2008), the auxin efflux carriers, including PIN-FORMED (PIN) family proteins Chen et al., 1998;Müller et al., 1998;Friml et al., 2002;Petrásek et al., 2006), and P-glycoprotein auxin transporters ABCB1 (for ATP BINDING CASSETTE PROTEIN SUBFAMILY B1), ABCB4, and ABCB19 (Terasaka et al., 2005;Bouchard et al., 2006;Blakeslee et al., 2007;Lin and Wang, 2005). PIN proteins are asymmetrically targeted to the plant cell plasma membranes, resulting in distinct polar subcellular localization in a given tissue. For example, PIN1 is localized in the basal (rootward, lower) plasma membrane of stele cells and xylem cells in the vascular system, which is required for long-distance auxin flow from the shoot apex to the root tip Friml e...

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“…Both proteins interact in a light-dependent manner with phyA and bear a functional nuclear localization signal (NLS) and nuclear exclusion signal (13,14,(17)(18)(19)(20). In the absence of FHY1 and FHL phyA remains in the cytoplasm and nuclear accumulation of phyA is no longer detected after light irradiation (13).…”

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Interaction with plant transcription factors can mediate nuclear import of phytochrome B

Pfeiffer¹,

Nagel²,

Popp³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Phytochromes (phy) are red/far-red-absorbing photoreceptors that regulate the adaption of plant growth and development to changes in ambient light conditions. The nuclear transport of the phytochromes upon light activation is regarded as a key step in phytochrome signaling. Although nuclear import of phyA is regulated by the transport facilitators far red elongated hypocotyl 1 (FHY1) and fhy1-like, an intrinsic nuclear localization signal was proposed to be involved in the nuclear accumulation of phyB. We recently showed that nuclear import of phytochromes can be analyzed in a cell-free system consisting of isolated nuclei of the unicellular green algae Acetabularia acetabulum. We now show that this system is also versatile to elucidate the mechanism of the nuclear transport of phyB. We tested the nuclear transport characteristics of full-length phyB as well as N-and C-terminal phyB fragments in vitro and showed that the nuclear import of phyB can be facilitated by phytochrome-interacting factor 3 (PIF3). In vivo measurements of phyB nuclear accumulation in the absence of PIF1, -3, -4, and -5 indicate that these PIFs are the major transport facilitators during the first hours of deetiolation. Under prolonged irradiations additional factors might be responsible for phyB nuclear transport in the plant.Arabidopsis | basic helix-loop-helix | signal transduction P lant development is strictly regulated by the environmental light conditions. Even though light is ubiquitously present, spectral composition, intensity, and light direction varies depending on the local environment. To adapt on local light conditions plants are equipped with a highly developed repertory of photoreceptors (1, 2).Plant phytochromes are mainly involved in detection of red and far-red light wavelengths of the spectrum. A family of five members in Arabidopsis thaliana regulates the major developmental steps in the life of the plant: germination, photomorphogenesis, and flowering (3, 4). Despite the sequence similarities and identical spectroscopic features, the two major phytochromes, phyA and phyB, show overlapping as well as unique photosensory and functional characteristics (5-7). The light-stable phyB mediates red/far-red reversible low fluence response, whereas the light-labile phyA, is involved in far-red light sensing (high irradiance response) and in responses to very weak light (very low fluence response, VLFR) (8).Phytochromes are cytosolic proteins of 125 kDa that are translocated into the nucleus upon light activation (6, 9-11). Nuclear transport is an essential step in phytochrome signaling and a prerequisite for the interaction with transcription factors in the nucleus (12, 13). Concerning the kinetics of nuclear import, severe differences can be found between the two major plant phytochromes, phyA and phyB (6). PhyA cannot be detected in nuclei of dark-grown plants but is rapidly transported into the nucleus upon light irradiation. In contrast, low levels of phyB are present in the nucleus even in dark-grown seedlings. The nuclea...

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Phytochrome A Mediates Rapid Red Light–Induced Phosphorylation ofArabidopsisFAR-RED ELONGATED HYPOCOTYL1 in a Low Fluence Response

Cited by 69 publications

References 68 publications

Photoreceptor partner FHY1 has an independent role in gene modulation and plant development under far-red light

Photoreceptor partner FHY1 has an independent role in gene modulation and plant development under far-red light

A PP6-Type Phosphatase Holoenzyme Directly Regulates PIN Phosphorylation and Auxin Efflux in Arabidopsis

Interaction with plant transcription factors can mediate nuclear import of phytochrome B

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