Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer

Environmental light information such as quality, intensity, and duration in red (approximately 660 nm) and far-red (approximately 730 nm) wavelengths is perceived by phytochrome photoreceptors in plants, critically influencing almost all developmental strategies from germination to flowering. Phytochromes interconvert between red light-absorbing Pr and biologically functional far-red light-absorbing Pfr forms. To ensure optimal photoresponses in plants, the flux of light signal from Pfr-phytochromes should be tightly controlled. Phytochromes are phosphorylated at specific serine residues. We found that a type 5 protein phosphatase (PAPP5) specifically dephosphorylates biologically active Pfr-phytochromes and enhances phytochrome-mediated photoresponses. Depending on the specific serine residues dephosphorylated by PAPP5, phytochrome stability and affinity for a downstream signal transducer, NDPK2, were enhanced. Thus, phytochrome photoreceptors have developed an elaborate biochemical tuning mechanism for modulating the flux of light signal, employing variable phosphorylation states controlled by phosphorylation and PAPP5-mediated dephosphorylation as a mean to control phytochrome stability and affinity for downstream transducers.     

Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development.

Phytochromes are a family of plant photoreceptors that mediate physiological and developmental responses to changes in red and far-red light conditions. In Arabidopsis, there are genes for at least five phytochrome proteins. These photoreceptors control such responses as germination, stem elongation, flowering, gene expression, and chloroplast and leaf development. However, it is not known which red light responses are controlled by which phytochrome species, or whether the different phytochromes have overlapping functions. We report here that previously described hy3 mutants have mutations in the gene coding for phytochrome B (PhyB). These are the first mutations shown to lie in a plant photoreceptor gene. A number of tissues are abnormally elongated in the hy3(phyB) mutants, including hypocotyls, stems, petioles, and root hairs. In addition, the mutants flower earlier than the wild type, and they accumulate less chlorophyll. PhyB thus controls Arabidopsis development at numerous stages and in multiple tissues.     

Arabidopsis thaliana TERMINAL FLOWER2 is involved in light-controlled signalling during seedling photomorphogenesis

Plants respond to changes in the environment by altering their growth pattern. Light is one of the most important environmental cues and affects plants throughout the life cycle. It is perceived by photoreceptors such as phytochromes that absorb light of red and far-red wavelengths and control, for example, seedling de-etiolation, chlorophyll biosynthesis and shade avoidance response. We report that the terminal flower2 (tfl2) mutant, carrying a mutation in the Arabidopsis thaliana HETEROCHROMATIN PROTEIN1 homolog, functions in negative regulation of phytochrome dependent light signalling. tfl2 shows defects in both hypocotyl elongation and shade avoidance response. Double mutant analysis indicates that mutants of the red/far-red light absorbing phytochrome family of plant photoreceptors, phyA and phyB, are epistatic to tfl2 in far-red and red light, respectively. An overlap between genes regulated by light and by auxin has earlier been reported and, in tfl2 plants light-dependent auxin-regulated genes are misexpressed. Further, we show that TFL2 binds to IAA5 and IAA19 suggesting that TFL2 might be involved in regulation of phytochrome-mediated light responses through auxin action.     

Phytochrome photoreceptors mediate plasticity to light quality in flowers of the Brassicaceae

The family of phytochrome photoreceptors mediates stem-elongation responses to ambient ratios of red?:?far-red light (R?:?FR). Although phytochrome genes are expressed in flowers in addition to vegetative parts, nothing is known about floral plasticity to R?:?FR or the pleiotropic effects of phytochrome genes on flowers. Here, the following floral morphologies were compared: (1) wild-type Arabidopsis thaliana and Brassica rapa plants experiencing high R?:?FR characteristic of sunlight vs. low R?:?FR typical of foliar shade and (2) wild-type and phytochrome-deficient A. thaliana plants. Wild-type A. thaliana exposed to low R?:?FR had diminished petal and pistil lengths but longer filaments for a given petal size than plants experiencing high R?:?FR. Brassica rapa plants had qualitatively similar responses. In comparison to wild-type A. thaliana, mutants lacking phytochrome A had smaller flowers (smaller petals, pistils, and filaments), whereas phytochrome B-deficient mutants exhibited longer filament lengths. These results provide the first evidence that R?:?FR and phytochromes affect floral phenotypes in addition to vegetative ones. Although the ecological relevance remains to be established, the observed plasticity of flowers to R?:?FR may be relevant to individual fitness in some species because stigma and filament positions can affect pollen removal and levels of self-pollination.     

Phylogenetic relationships of B-related phytochromes in the Brassicaceae: Redundancy and the persistence of phytochrome D

Plants use phytochrome (phy) photoreceptors to detect and respond to changes in the quantities and proportions of red (R) and far-red (FR) light in their environments. The principal mediators of responses to R and FR in Arabidopsis thaliana are phyA and phyB, which are found in all angiosperms surveyed. The present study is concerned with a phytochrome gene pair in Arabidopsis, PHYB and PHYD, which are of relatively recent origin, share high sequence identity, and are partially redundant. Our data suggest that the duplication occurred after the mustard family (Brassicaceae) diverged from its closest relatives but before the radiation of extant Brassicaceae, and that both copies have persisted for up to 40myr. We detected no evidence of positive selection in the divergence of PHYD from PHYB; the evolution of both sequences is constrained by purifying selection. Levels of diversity at both loci are among the lowest observed at nuclear genes in A. thaliana. In common with other loci in A. thaliana, PHYB and PHYD showed elevated levels of intraspecific replacement variation, and each showed an excess of rare nucleotide polymorphisms, consistent with a recent, rapid population expansion. Our results are consistent with the functional importance of amino acid divergence in the central regions of phyB and phyD and suggest specific sites for mutagenesis that may yield insights into the functional differences of phyB and phyD.     

Phytochrome and photoperiodic induction

The photoreceptor phytochrome has been extensively characterized at the chromophore, protein and gene level. It consists of a family of red/far-red reversible molecules and the genes for three members have been sequenced. Phytochromes are chromoproteins, which probably exist as dimers in vivo. Photoperiodism in higher plants involves the interaction of phytochrome with an endogenous timekeeping system. The interaction is complex, and several distinct actions of light can be distinguished. The possible involvement of different phytochromes in different actions of light in both long-day plants and short-day plants is discussed. Potential roles for different members of the phytochrome family and homo-and hetero-dimers of phytochrome are proposed.     

Phytochrome A regulates red-light induction of phototropic enhancement in Arabidopsis.

Phytochrome A (phyA) and phytochrome B photoreceptors have distinct roles in the regulation of plant growth and development. Studies using specific photomorphogenic mutants and transgenic plants overexpressing phytochrome have supported an evolving picture in which phyA and phytochrome B are responsive to continuous far-red and red light, respectively. Photomorphogenic mutants of Arabidopsis thaliana that had been selected for their inability to respond to continuous irradiance conditions were tested for their ability to carry out red-light-induced enhancement of phototropism, which is an inductive phytochrome response. We conclude that phyA is the primary photoreceptor regulating this response and provide evidence suggesting that a common regulatory domain in the phyA polypeptide functions for both high-irradiance and inductive phytochrome responses.     

Phytochrome control of the growth and development of Rumex obtusifolius under simulated canopy light environments*

Abstract Studies on the growth and development of Rumex obtusifolius seedlings under simulated shade conditions show that both light quantity and quality contribute to the observed responses. In the shade situation the plants have lower dry matter, lower leaf area and lower net assimilation rates. Petiole elongation occurs under shade conditions only after transfer of the plants from non-shade environments. The effects of light quality are related to phytochrome photoequilibria set up by the increased relative photon flux in the far-red found under vegetation canopies.     

Photochemical characterization of phytochrome missense mutants

Phytochromes are photoreceptors that regulate many aspects of plant growth and development in response to red/far-red light signals from the environment. In this study, we analyzed chromophore ligation and photochromism of missense phytochrome mutants in the Per-Arnt-Sim (PAS)-related domain (PRD). Among the 14 mutants analyzed, the Gly768Asp mutant of Avena phytochrome A showed aberrant photochromism and dark reversion, suggesting that amino acid residues in the C-terminal domain affect the photochemical properties of the photosensory N-terminal domain.     

Phytochrome evolution in green and nongreen plants

Photoreceptors are critical molecules that function at the interface between organism and environment. Plants use specific light signals to determine their place in time and space, allowing them to synchronize their growth, metabolism, and development to the environments in which they occur. Thus, innovation in light sensing mechanisms is expected to coincide with adaptation and diversification. Three studies involving the well-characterized phytochrome photoreceptor system in plants indicate that much work is yet needed to test this expectation. In early diverging flowering plants, episodic positive selection influenced the evolution of phytochrome A, but little of the functional data needed to link molecular adaptation with a change in gene function are available. In the model plant Arabidopsis thaliana, known functional differences between a recently duplicated gene pair remain difficult to characterize at the sequence level. In parasitic plants, patterns of development that in autotrophs are under the control of light signals are highly modified, suggesting that phytochromes and other photoreceptors function differently in nonphotosynthetic plants. Analyses of phytochrome A coding sequences indicate that they are evolving under relaxed constraints in nonphotosynthetic Orobanchaceae, consistent with the expectation of functional change. Further work is needed to determine which of the processes mediated by phyA may have been altered, a line of investigation that may improve our understanding of divergence points in downstream signaling pathways.     

Natural variation in phytochrome signaling

The phytochromes, photoreceptors sensitive to red and far-red light, are critical for sensing foliage shade, canopy breaks, and neighbor proximity. A combination of molecular genetic, evolutionary, and ecological techniques are being used to understand how phytochromes function in the natural environment. We discuss studies on the adaptive value of phytochrome mediated plasticity, as well as the role that variation in phytochrome expression and function might play in allowing plants to adapt to unique light environments. Continued study of phytochrome signaling variation may reveal how natural selection acts at the molecular level.     

Influence of the Dietary Protein Deficiency on the Protein Synthetic Activity of Microsome and Soluble Fraction from Muscle and Liver of Rats

Phytochromes are photoreceptors that regulate many aspects of plant growth and development in response to red/far-red light signals from the environment. In this study, we analyzed chromophore ligation and photochromism of missense phytochrome mutants in the Per-Arnt-Sim (PAS)-related domain (PRD). Among the 14 mutants analyzed, the Gly768Asp mutant of Avena phytochrome A showed aberrant photochromism and dark reversion, suggesting that amino acid residues in the C-terminal domain affect the photochemical properties of the photosensory N-terminal domain.     

Duplication,divergence and persistence in the Phytochrome photoreceptor gene family of cottons (<Emphasis Type="Italic">Gossypium</Emphasis> spp.)

Background  

Phytochromes are a family of red/far-red photoreceptors that regulate a number of important developmental traits in cotton (Gossypium spp.), including plant architecture, fiber development, and photoperiodic flowering. Little is known about the composition and evolution of the phytochrome gene family in diploid (G. herbaceum, G. raimondii) or allotetraploid (G. hirsutum, G. barbadense) cotton species. The objective of this study was to obtain a preliminary inventory and molecular-evolutionary characterization of the phytochrome gene family in cotton.     

Missense mutation in the amino terminus of phytochrome A disrupts the nuclear import of the photoreceptor

Phytochromes are the red/far-red photoreceptors in higher plants. Among them, phytochrome A (PHYA) is responsible for the far-red high-irradiance response and for the perception of very low amounts of light, initiating the very-low-fluence response. Here, we report a detailed physiological and molecular characterization of the phyA-5 mutant of Arabidopsis (Arabidopsis thaliana), which displays hyposensitivity to continuous low-intensity far-red light and shows reduced very-low-fluence response and high-irradiance response. Red light-induced degradation of the mutant phyA-5 protein appears to be normal, yet higher residual amounts of phyA-5 are detected in seedlings grown under low-intensity far-red light. We show that (1) the phyA-5 mutant harbors a new missense mutation in the PHYA amino-terminal extension domain and that (2) the complex phenotype of the mutant is caused by reduced nuclear import of phyA-5 under low fluences of far-red light. We also demonstrate that impaired nuclear import of phyA-5 is brought about by weakened binding affinity of the mutant photoreceptor to nuclear import facilitators FHY1 (for FAR-RED ELONGATED HYPOCOTYL1) and FHL (for FHY1-LIKE). Finally, we provide evidence that the signaling and degradation kinetics of constitutively nuclear-localized phyA-5 and phyA are identical. Taken together, our data show that aberrant nucleo/cytoplasmic distribution impairs light-induced degradation of this photoreceptor and that the amino-terminal extension domain mediates the formation of the FHY1/FHL/PHYA far-red-absorbing form complex, whereby it plays a role in regulating the nuclear import of phyA.     

Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant-plant signalling

Plants growing at high densities express shade avoidance traits as a response to the presence of neighbours. Enhanced shoot elongation is one of the best researched shade avoidance components and increases light capture in dense stands. We show here that also leaf movements, leading to a more vertical leaf orientation (hyponasty), may be crucial in the early phase of competition. The initiation of shade avoidance responses is classically attributed to the action of phytochrome photoreceptors that sense red:far-red (R:FR) ratios in light reflected by neighbours, but also other signals may be involved. It was recently shown that ethylene-insensitive, transgenic (Tetr) tobacco plants, which are insensitive to the gaseous plant hormone ethylene, have reduced shade avoidance responses to neighbours. Here, we report that this is not related to a reduced response to low R:FR ratio, but that Tetr tobacco plants are unresponsive to a reduced photon fluence rate of blue light, which normally suppresses growth inhibition in wild-type (WT) plants. In addition to these light signals, ethylene levels in the canopy atmosphere increased to concentrations that could induce shade avoidance responses in WT plants. Together, these data show that neighbour detection signals other than the R:FR ratio are more important than previously anticipated and argue for a particularly important role for ethylene in determining plant responses to neighbours.