Integration Of Light Signals Research Articles

HY5-HDA9 orchestrates the transcription of HsfA2 to modulate salt stress response in Arabidopsis.

Integration of light signaling and diverse abiotic stress responses contribute to plant survival in a changing environment. Some reports have indicated that light signals contribute a plant's ability to deal with heat, cold, and stress. However, the molecular link between light signaling and the salt-response pathways remains unclear. We demonstrate here that increasing light intensity elevates the salt stress tolerance of plants. Depletion of HY5, a key component of light signaling, causes Arabidopsis thaliana to become salinity sensitive. Interestingly, the small heat shock protein (sHsp) family genes are upregulated in hy5-215 mutant plants, and HsfA2 is commonly involved in the regulation of these sHsps. We found that HY5 directly binds to the G-box motifs in the HsfA2 promoter, with the cooperation of HISTONE DEACETYLASE 9 (HDA9), to repress its expression. Furthermore, the accumulation of HDA9 and the interaction between HY5 and HDA9 are significantly enhanced by salt stress. On the contrary, high temperature triggers HY5 and HDA9 degradation, which leads to dissociation of HY5-HDA9 from the HsfA2 promoter, thereby reducing salt tolerance. Under salt and heat stress conditions, fine tuning of protein accumulation and an interaction between HY5 and HDA9 regulate HsfA2 expression. This implies that HY5, HDA9, and HsfA2 play important roles in the integration of light signaling with salt stress and heat shock response.

The PHY Domain Dimer Interface of Bacteriophytochromes Mediates Cross-talk between Photosensory Modules and Output Domains

Protein dynamics play a major role for the catalytic function of enzymes, the interaction of protein complexes or signal integration in regulatory proteins. In the context of multi-domain proteins involved in light-regulation of enzymatic effectors, the central role of conformational dynamics is well established. Light activation of sensory modules is followed by long-range signal transduction to different effectors; rather than domino-style structural rearrangements, a complex interplay of functional elements is required to maintain functionality. One family of such sensor-effector systems are red-light-regulated phytochromes that control diguanylate cyclases involved in cyclic-dimeric-GMP formation. Based on structural and functional studies of one prototypic family member, the central role of the coiled-coil sensor-effector linker was established. Interestingly, subfamilies with different linker lengths feature strongly varying biochemical characteristics. The dynamic interplay of the domains involved, however, is presently not understood. Here we show that the PHY domain dimer interface plays an essential role in signal integration, and that a functional coupling with the coiled-coil linker element is crucial. Chimaeras of two biochemically different family members highlight the phytochrome-spanning helical spine as an essential structural element involved in light-dependent upregulation of enzymatic turnover. However, isolated structural elements can frequently not be assigned to individual characteristics, which further emphasises the importance of global conformational dynamics. Our results provide insights into the intricate processes at play during light signal integration and transduction in these photosensory systems and thus provide additional guidelines for a more directed design of novel sensor-effector combinations with potential applications as optogenetic tools.

Influence of the N-terminal segment and the PHY-tongue element on light-regulation in bacteriophytochromes

Photoreceptors enable the integration of ambient light stimuli to trigger lifestyle adaptations via modulation of central metabolite levels involved in diverse regulatory processes. Red light–sensing bacteriophytochromes are attractive targets for the development of innovative optogenetic tools because of their natural modularity of coupling with diverse functionalities and the natural availability of the light-absorbing biliverdin chromophore in animal tissues. However, a rational design of such tools is complicated by the poor understanding of molecular mechanisms of light signal transduction over long distances—from the site of photon absorption to the active site of downstream enzymatic effectors. Here we show how swapping structural elements between two bacteriophytochrome homologs provides additional insight into light signal integration and effector regulation, involving a fine-tuned interplay of important structural elements of the sensor, as well as the sensor–effector linker. Facilitated by the availability of structural information of inhibited and activated full-length structures of one of the two homologs (Idiomarina species A28L phytochrome-activated diguanylyl cyclase (IsPadC)) and characteristic differences in photoresponses of the two homologs, we identify an important cross-talk between the N-terminal segment, containing the covalent attachment site of the chromophore, and the PHY-tongue region. Moreover, we highlight how these elements influence the dynamic range of photoactivation and how activation can be improved to light/dark ratios of ∼800-fold by reducing basal dark-state activities at the same time as increasing conversion in the light state. This will enable future optimization of optogenetic tools aiming at a direct allosteric regulation of enzymatic effectors.

Arabidopsis ANGUSTIFOLIA3 (AN3) is associated with the promoter of CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) to regulate light-mediated stomatal development.

Light signals are perceived by multiple photoreceptors that converge to suppress the RING E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) for the regulation of stomatal development. Thus, COP1 is a point of integration between light signaling and stomatal patterning. However, how light signaling is collected into COP1 for the production and spacing of stomata is still unknown. Here, we report that the loss-of-function mutant of ANGUSTIFOLIA3 (AN3) delays asymmetric cell division, which leads to decreased stomatal index. Furthermore, overexpression of AN3 accelerates asymmetric cell division, which results in clusters of stomata. In addition, the stomatal development through AN3 regulation is mediated by light signaling. Finally, we find that an3 is a light-signaling mutant, and that AN3 protein is light regulated. Self-activation by AN3 contributes to the control of AN3 expression. Thus, AN3 is a point of collection between light signaling and stomatal patterning. Target-gene analysis indicates that AN3 is associated with COP1 promoter for the regulation of light-controlling stomatal development. Together, these components for regulating stomatal development form an AN3-COP1-E3 ubiquitin ligase complex, allowing the integration of light signaling into the production and spacing of stomata.

Integration of light signals in Arabidopsis thaliana

Integration of light signals in Arabidopsis thaliana

The expression of melanopsin and clock genes in Xenopus laevis melanophores and their modulation by melatonin

Vertebrates have a central clock and also several peripheral clocks. Light responses might result from the integration of light signals by these clocks. The dermal melanophores of Xenopus laevis have a photoreceptor molecule denominated melanopsin (OPN4x). The mechanisms of the circadian clock involve positive and negative feedback. We hypothesize that these dermal melanophores also present peripheral clock characteristics. Using quantitative PCR, we analyzed the pattern of temporal expression of Opn4x and the clock genes Per1, Per2, Bmal1, and Clock in these cells subjected to a 14-h light:10-h dark (14L:10D) regime or constant darkness (DD). Also, in view of the physiological role of melatonin in the dermal melanophores of X. laevis, we determined whether melatonin modulates the expression of these clock genes. These genes show a time-dependent expression pattern when these cells are exposed to 14L:10D, which differs from the pattern observed under DD. Cells kept in DD for 5 days exhibited overall increased mRNA expression for Opn4x and Clock, and a lower expression for Per1, Per2, and Bmal1. When the cells were kept in DD for 5 days and treated with melatonin for 1 h, 24 h before extraction, the mRNA levels tended to decrease for Opn4x and Clock, did not change for Bmal1, and increased for Per1 and Per2 at different Zeitgeber times (ZT). Although these data are limited to one-day data collection, and therefore preliminary, we suggest that the dermal melanophores of X. laevis might have some characteristics of a peripheral clock, and that melatonin modulates, to a certain extent, melanopsin and clock gene expression.

Integration of Light Signals by the Retinoblastoma Pathway in the Control of S Phase Entry in the Picophytoplanktonic Cell Ostreococcus

Although the decision to proceed through cell division depends largely on the metabolic status or the size of the cell, the timing of cell division is often set by internal clocks such as the circadian clock. Light is a major cue for circadian clock entrainment, and for photosynthetic organisms it is also the main source of energy supporting cell growth prior to cell division. Little is known about how light signals are integrated in the control of S phase entry. Here, we present an integrated study of light-dependent regulation of cell division in the marine green alga Ostreococcus. During early G1, the main genes of cell division were transcribed independently of the amount of light, and the timing of S phase did not occur prior to 6 hours after dawn. In contrast S phase commitment and the translation of a G1 A-type cyclin were dependent on the amount of light in a cAMP–dependent manner. CyclinA was shown to interact with the Retinoblastoma (Rb) protein during S phase. Down-regulating Rb bypassed the requirement for CyclinA and cAMP without altering the timing of S phase. Overexpression of CyclinA overrode the cAMP–dependent control of S phase entry and led to early cell division. Therefore, the Rb pathway appears to integrate light signals in the control of S phase entry in Ostreococcus, though differential transcriptional and posttranscriptional regulations of a G1 A-type cyclin. Furthermore, commitment to S phase depends on a cAMP pathway, which regulates the synthesis of CyclinA. We discuss the relative involvements of the metabolic and time/clock signals in the photoperiodic control of cell division.

Integration of light signaling with photoperiodic flowering and circadian rhythm

Plants become photosynthetic through de-etiolation, a developmental process regulated by red/far-red light-absorbing phytochromes and blue/ultraviolet A light-absorbing cryptochromes. Genetic screens have identified in the last decade many far-red light signaling mutants and several red and blue light signaling mutants, suggesting the existence of distinct red, far-red, or blue light signaling pathways downstream of phytochromes and cryptochromes. However, genetic screens have also identified mutants with defective de-etiolation responses under multiple wavelengths. Thus, the optimal de-etiolation responses of a plant depend on coordination among the different light signaling pathways. This review intends to discuss several recently identified signaling components that have a potential role to integrate red, far-red, and blue light signalings. This review also highlights the recent discoveries on proteolytic degradation in the desensitization of light signal transmission, and the tight connection of light signaling with photoperiodic flowering and circadian rhythm. Studies on the controlling mechanisms of de-etiolation, photoperiodic flowering, and circadian rhythm have been the fascinating topics in Arabidopsis research. The knowledge obtained from Arabidopsis can be readily applied to food crops and ornamental species, and can be contributed to our general understanding of signal perception and transduction in all organisms.

The signal transducing photoreceptors of plants

Light signals are amongst the most important environmental cues regulating plant development. In addition to light quantity, plants measure the quality, direction and periodicity of incident light and use the information to optimise growth and development to the prevailing environmental conditions. Red and far-red wavelengths are perceived by the photoreversible phytochrome family of photoreceptors, whilst the detection of blue and ultraviolet (UV)-A wavelengths is conferred by the cryptochromes and phototropins. Higher plants contain multiple discrete phytochromes, the apoproteins of which are encoded by a small divergent gene family. In Arabidopsis, two cryptochrome and two phototropin family members have been identified and characterized. Photoreceptor action regulates development throughout the lifecycle of plants, from seed germination through to architecture of the mature plant and the onset of reproduction. The roles of individual photoreceptors in mediating plant development have, however, often been confounded by redundant, synergistic and in some cases mutually antagonistic mechanisms of action. The isolation of mutants null for individual photoreceptors and the construction of mutants null for multiple photoreceptors have therefore been paramount in elucidating photoreceptor functions. Photoreceptor action does not, however, operate in isolation from other signalling systems. The integration of light signals with other environmental cues enables plants to adapt their physiology to changing seasonal environments. This paper summarises current understanding of photoreceptor families and their functions throughout the lifecycle of plants. The integration of light signals with other environmental stimuli is also discussed.

Light signals, phytochromes and cross-talk with other environmental cues.

Plants have evolved highly complex sensory mechanisms to monitor their surroundings and adapt their growth and development to the prevailing environmental conditions. The integration of information from multiple environmental cues enables the co-ordination of development with favourable seasonal conditions and, ultimately, determines plant form. Light signals, perceived via the phytochrome, cryptochrome and phototropin photoreceptor families, are especially important environmental signals. Redundancy of function among phytochromes and their interaction with blue light photoreceptors enhance sensitivity to light signals, facilitating the accurate detection of, and response to, environmental fluctuations. In this review, current understanding of Arabidopsis phytochrome functions will be summarized, in particular, the interactions among the phytochromes and the integration of light signals with directional and temperature sensing mechanisms.