Plant chromatin feels the heat.

Temperature is a key environmental signal regulating plant development, but the mechanisms by which plants sense small changes in ambient temperature have remained elusive. Kumar and Wigge (2010) now reveal that eviction of the histone variant H2A.Z from nucleosomes performs a central role in plant thermosensory perception.

ELONGATED HYPOCOTYL5 (HY5) and HY5 HOMOLOGUE (HYH) maintain shade avoidance suppression in UV-B.

Reductions in red to far-red ratio (R:FR) provide plants with an unambiguous signal of vegetational shade and are monitored by phytochrome photoreceptors. Plants integrate this information with other environmental cues to determine the proximity and density of encroaching vegetation. Shade-sensitive species respond to reductions in R:FR by initiating a suite of developmental adaptations termed shade avoidance. These include the elongation of stems to facilitate light foraging. Hypocotyl elongation is driven by increased auxin biosynthesis promoted by PHYTOCHROME INTERACTING FACTORs (PIF) 4, 5 and 7. UV-B perceived by the UV RESISTANCE LOCUS 8 (UVR8) photoreceptor rapidly inhibits shade avoidance, in part by suppressing PIF4/5 transcript accumulation and destabilising PIF4/5 protein. Here, we show that longer-term inhibition of shade avoidance is sustained by ELONGATED HYPOCOTYL 5 (HY5) and HY5 HOMOLOGUE (HYH), which regulate transcriptional reprogramming of genes involved in hormone signalling and cell wall modification. HY5 and HYH are elevated in UV-B and suppress the expression of XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASE (XTH) genes involved in cell wall loosening. They additionally increase expression GA2-OXIDASE1 (GA2ox1) and GA2ox2, encoding gibberellin catabolism enzymes that act redundantly to stabilise the PIF-inhibiting DELLA proteins. UVR8 therefore regulates temporally distinct signalling pathways to first rapidly inhibit and subsequently maintain suppression of shade avoidance following UV-B exposure.

Phytochrome A elevates plant circadian-clock components to suppress shade avoidance in deep-canopy shade.

Shade-avoiding plants can detect the presence of neighboring vegetation and evoke escape responses before canopy cover limits photosynthesis. Rapid stem elongation facilitates light foraging and enables plants to overtop competitors. A major regulator of this response is the phytochrome B photoreceptor, which becomes inactivated in light environments with a low ratio of red to far-red light (low R:FR), characteristic of vegetational shade. Although shade avoidance can provide plants with a competitive advantage in fast-growing stands, excessive stem elongation can be detrimental to plant survival. As such, plants have evolved multiple feedback mechanisms to attenuate shade-avoidance signaling. The very low R:FR and reduced levels of photosynthetically active radiation (PAR) present in deep canopy shade can, together, trigger phytochrome A (phyA) signaling, inhibiting shade avoidance and promoting plant survival when resources are severely limited. The molecular mechanisms underlying this response have not been fully elucidated. Here, we show that Arabidopsis thaliana phyA elevates early-evening expression of the central circadian-clock components TIMING OF CAB EXPRESSION 1 (TOC1), PSEUDO RESPONSE REGULATOR 7 (PRR7), EARLY FLOWERING 3 (ELF3), and ELF4 in photocycles of low R:FR and low PAR. These collectively suppress stem elongation, antagonizing shade avoidance in deep canopy shade.

Guard Cells Integrate Light and Temperature Signals to Control Stomatal Aperture.

High temperature promotes guard cell expansion, which opens stomatal pores to facilitate leaf cooling. How the high-temperature signal is perceived and transmitted to regulate stomatal aperture is, however, unknown. Here, we used a reverse-genetics approach to understand high temperature-mediated stomatal opening in Arabidopsis (Arabidopsis thaliana). Our findings reveal that high temperature-induced guard cell movement requires components involved in blue light-mediated stomatal opening, suggesting cross talk between light and temperature signaling pathways. The molecular players involved include phototropin photoreceptors, plasma membrane H+-ATPases, and multiple members of the 14-3-3 protein family. We further show that phototropin-deficient mutants display impaired rosette evapotranspiration and leaf cooling at high temperatures. Blocking the interaction of 14-3-3 proteins with their client proteins severely impairs high temperature-induced stomatal opening but has no effect on the induction of heat-sensitive guard cell transcripts, supporting the existence of an additional intracellular high-temperature response pathway in plants.

Integration of light and circadian signals that regulate chloroplast transcription by a nuclear-encoded sigma factor.

We investigated the signalling pathways that regulate chloroplast transcription in response to environmental signals. One mechanism controlling plastid transcription involves nuclear-encoded sigma subunits of plastid-encoded plastid RNA polymerase. Transcripts encoding the sigma factor SIG5 are regulated by light and the circadian clock. However, the extent to which a chloroplast target of SIG5 is regulated by light-induced changes in SIG5 expression is unknown. Moreover, the photoreceptor signalling pathways underlying the circadian regulation of chloroplast transcription by SIG5 are unidentified. We monitored the regulation of chloroplast transcription in photoreceptor and sigma factor mutants under controlled light regimes in Arabidopsis thaliana. We established that a chloroplast transcriptional response to light intensity was mediated by SIG5; a chloroplast transcriptional response to the relative proportions of red and far red light was regulated by SIG5 through phytochrome and photosynthetic signals; and the circadian regulation of chloroplast transcription by SIG5 was predominantly dependent on blue light and cryptochrome. Our experiments reveal the extensive integration of signals concerning the light environment by a single sigma factor to regulate chloroplast transcription. This may originate from an evolutionarily ancient mechanism that protects photosynthetic bacteria from high light stress, which subsequently became integrated with higher plant phototransduction networks.

UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance.

Plants detect different facets of their radiation environment via specific photoreceptors to modulate growth and development. UV-B is perceived by the photoreceptor UV RESISTANCE LOCUS 8 (UVR8). The molecular mechanisms linking UVR8 activation to plant growth are not fully understood, however. When grown in close proximity to neighboring vegetation, shade-intolerant plants initiate dramatic stem elongation to overtop competitors. Here we show that UV-B, detected by UVR8, provides an unambiguous sunlight signal that inhibits shade avoidance responses in Arabidopsis thaliana by antagonizing the phytohormones auxin and gibberellin. UV-B triggers degradation of the transcription factors PHYTOCHROME INTERACTING FACTOR 4 and PHYTOCHROME INTERACTING FACTOR 5 and stabilizes growth-repressing DELLA proteins, inhibiting auxin biosynthesis via a dual mechanism. Our findings show that UVR8 signaling is closely integrated with other photoreceptor pathways to regulate auxin signaling and plant growth in sunlight.

Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis.

In view of the extensive literature on phytochrome mutants in the Ler accession of Arabidopsis, we sought to secure a phytochrome-null line in the same genetic background for comparative studies. Here we report the isolation and phenotypic characterization of phyABCDE quintuple and phyABDE quadruple mutants in the Ler background. Unlike earlier studies, these lines possess a functional allele of FT permitting measurements of photoperiod-dependent flowering behavior. Comparative studies of both classes of mutants establish that phytochromes are dispensable for completion of the Arabidopsis life cycle under red light, despite the lack of a transcriptomic response, and also indicate that phyC is nonfunctional in the absence of other phytochromes. Phytochrome-less plants can produce chlorophyll for photosynthesis under continuous red light, yet require elevated fluence rates for survival. Unexpectedly, our analyses reveal both light-dependent and -independent roles for phytochromes to regulate the Arabidopsis circadian clock. The rapid transition of these mutants from vegetative to reproductive growth, as well as their insensitivity to photoperiod, establish a dual role for phytochromes to arrest and to promote progression of plant development in response to the prevailing light environment.

Temperature-dependent shade avoidance involves the receptor-like kinase ERECTA.

Plants detect the presence of neighbouring vegetation by monitoring changes in the ratio of red (R) to far-red (FR) wavelengths (R:FR) in ambient light. Reductions in R:FR are perceived by the phytochrome family of plant photoreceptors and initiate a suite of developmental responses termed the shade avoidance syndrome. These include increased elongation growth of stems and petioles, enabling plants to overtop competing vegetation. The majority of shade avoidance experiments are performed at standard laboratory growing temperatures (>20°C). In these conditions, elongation responses to low R:FR are often accompanied by reductions in leaf development and accumulation of plant biomass. Here we investigated shade avoidance responses at a cooler temperature (16°C). In these conditions, Arabidopsis thaliana displays considerable low R:FR-mediated increases in leaf area, with reduced low R:FR-mediated petiole elongation and leaf hyponasty responses. In Landsberg erecta, these strikingly different shade avoidance phenotypes are accompanied by increased leaf thickness, increased biomass and an altered metabolite profile. At 16°C, low R:FR treatment results in the accumulation of soluble sugars and metabolites associated with cold acclimation. Analyses of natural genetic variation in shade avoidance responses at 16°C have revealed a regulatory role for the receptor-like kinase ERECTA.

Interaction of light and temperature signalling.

Light and temperature are arguably two of the most important signals regulating the growth and development of plants. In addition to their direct energetic effects on plant growth, light and temperature provide vital immediate and predictive cues for plants to ensure optimal development both spatially and temporally. While the majority of research to date has focused on the contribution of either light or temperature signals in isolation, it is becoming apparent that an understanding of how the two interact is essential to appreciate fully the complex and elegant ways in which plants utilize these environmental cues. This review will outline the diverse mechanisms by which light and temperature signals are integrated and will consider why such interconnected systems (as opposed to entirely separate light and temperature pathways) may be evolutionarily favourable.

Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature.

At high ambient temperature, plants display dramatic stem elongation in an adaptive response to heat. This response is mediated by elevated levels of the phytohormone auxin and requires auxin biosynthesis, signaling, and transport pathways. The mechanisms by which higher temperature results in greater auxin accumulation are unknown, however. A basic helix-loop-helix transcription factor, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), is also required for hypocotyl elongation in response to high temperature. PIF4 also acts redundantly with its homolog, PIF5, to regulate diurnal growth rhythms and elongation responses to the threat of vegetative shade. PIF4 activity is reportedly limited in part by binding to both the basic helix-loop-helix protein LONG HYPOCOTYL IN FAR RED 1 and the DELLA family of growth-repressing proteins. Despite the importance of PIF4 in integrating multiple environmental signals, the mechanisms by which PIF4 controls growth are unknown. Here we demonstrate that PIF4 regulates levels of auxin and the expression of key auxin biosynthesis genes at high temperature. We also identify a family of SMALL AUXIN UP RNA (SAUR) genes that are expressed at high temperature in a PIF4-dependent manner and promote elongation growth. Taken together, our results demonstrate direct molecular links among PIF4, auxin, and elongation growth at high temperature.

Low-temperature and circadian signals are integrated by the sigma factor SIG5.

Chloroplasts are a common feature of plant cells and aspects of their metabolism, including photosynthesis, are influenced by low-temperature conditions. Chloroplasts contain a small circular genome that encodes essential components of the photosynthetic apparatus and chloroplast transcription/translation machinery. Here, we show that in Arabidopsis, a nuclear-encoded sigma factor that controls chloroplast transcription (SIGMA FACTOR5) contributes to adaptation to low-temperature conditions. This process involves the regulation of SIGMA FACTOR5 expression in response to cold by the bZIP transcription factors ELONGATED HYPOCOTYL5 and ELONGATED HYPOCOTYL5 HOMOLOG. The response of this pathway to cold is gated by the circadian clock, and it enhances photosynthetic efficiency during long-term cold and freezing exposure. We identify a process that integrates low-temperature and circadian signals, and modulates the response of chloroplasts to low-temperature conditions.

25 Years of thermomorphogenesis research: milestones and perspectives.

In 1998, Bill Gray and colleagues showed that warm temperatures trigger arabidopsis hypocotyl elongation in an auxin-dependent manner. This laid the foundation for a vibrant research discipline. With several active members of the 'thermomorphogenesis' community, we here reflect on 25 years of elevated ambient temperature research and look to the future.

Chromatin remodelling in plant light signalling.

The structure and compaction of chromatin exerts a major regulatory influence on eukaryotic transcription. Changes in both histone composition and post-translational modifications of individual histone proteins can lead to remodelling of higher order chromatin structure. Chromatin remodelling regulates transcriptional activity through modifying gene accessibility, via DNA/histone interactions and the recruitment of non-histone proteins to DNA. Plant growth and development is regulated by the integration of multiple environmental signals. Of these, light is one of the most important. Chromatin remodelling processes have been identified in plants following a variety of different light treatments. These include the initiation of seedling de-etiolation, changes in photon irradiance and ultraviolet-B radiation exposure. In this review, we will summarize the roles of chromatin remodelling in plant photomorphogenesis and discuss these in the wider context of plant environmental adaptation.

Phytochrome functions in Arabidopsis development.

Light signals are fundamental to the growth and development of plants. Red and far-red light are sensed using the phytochrome family of plant photoreceptors. Individual phytochromes display both unique and overlapping roles throughout the life cycle of plants, regulating a range of developmental processes from seed germination to the timing of reproductive development. The evolution of multiple phytochrome photoreceptors has enhanced plant sensitivity to fluctuating light environments, diversifying phytochrome function, and facilitating conditional cross-talk with other signalling systems. The isolation of null mutants, deficient in all individual phytochromes, has greatly advanced understanding of phytochrome functions in the model species, Arabidopsis thaliana. The creation of mutants null for multiple phytochrome combinations has enabled the dissection of redundant interactions between family members, revealing novel regulatory roles for this important photoreceptor family. In this review, current knowledge of phytochrome functions in the light-regulated development of Arabidopsis is summarised.

Gating of the rapid shade-avoidance response by the circadian clock in plants.

The phytochromes are a family of plant photoreceptor proteins that control several adaptive developmental strategies. For example, the phytochromes perceive far-red light (wavelengths between 700 and 800 nm) reflected or scattered from the leaves of nearby vegetation. This provides an early warning of potential shading, and triggers a series of 'shade-avoidance' responses, such as a rapid increase in elongation, by which the plant attempts to overgrow its neighbours. Other, less immediate, responses include accelerated flowering and early production of seeds. However, little is known about the molecular events that connect light perception with increased growth in shade avoidance. Here we show that the circadian clock gates this rapid shade-avoidance response. It is most apparent around dusk and is accompanied by altered expression of several genes. One of these rapidly responsive genes encodes a basic helix-loop-helix protein, PIL1, previously shown to interact with the clock protein TOC1 (ref. 4). Furthermore PIL1 and TOC1 are both required for the accelerated growth associated with the shade-avoidance response.

UVR8 disrupts stabilisation of PIF5 by COP1 to inhibit plant stem elongation in sunlight.

Alterations in light quality significantly affect plant growth and development. In canopy shade, phytochrome photoreceptors perceive reduced ratios of red to far-red light (R:FR) and initiate stem elongation to enable plants to overtop competitors. This shade avoidance response is achieved via the stabilisation and activation of PHYTOCHROME INTERACTING FACTORs (PIFs) which elevate auxin biosynthesis. UV-B inhibits shade avoidance by reducing the abundance and activity of PIFs, yet the molecular mechanisms controlling PIF abundance in UV-B are unknown. Here we show that the UV-B photoreceptor UVR8 promotes rapid PIF5 degradation via the ubiquitin-proteasome system in a response requiring the N terminus of PIF5. In planta interactions between UVR8 and PIF5 are not observed. We further demonstrate that PIF5 interacts with the E3 ligase COP1, promoting PIF5 stabilisation in light-grown plants. Binding of UVR8 to COP1 in UV-B disrupts this stabilisation, providing a mechanism to rapidly lower PIF5 abundance in sunlight.

Short- and Long-Term Effects of UVA on Arabidopsis Are Mediated by a Novel cGMP Phosphodiesterase.

Although UVA radiation (315-400 nm) represents 95% of the UV radiation reaching the earth's surface, surprisingly little is known about its effects on plants [1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase (AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans.

Shade avoidance.

The threat to plant survival presented by light limitation has driven the evolution of highly plastic adaptive strategies to either tolerate or avoid shading by neighbouring vegetation. When subject to vegetational shading, plants are exposed to a variety of informational signals, which include altered light quality and a reduction in light quantity. The former includes a decrease in the ratio of red to far-red wavelengths (low R : FR) and is detected by the phytochrome family of plant photoreceptors. Monitoring of R : FR ratio can provide an early and unambiguous warning of the presence of competing vegetation, thereby evoking escape responses before plants are actually shaded. The molecular mechanisms underlying physiological responses to alterations in light quality have now started to emerge, with major roles suggested for the PIF (PHYTOCHROME INTERACTING FACTOR) and DELLA families of transcriptional regulators. Such studies suggest a complex interplay between endogenous and exogenous signals, mediated by multiple photoreceptors. The phenotypic similarities between physiological responses habitually referred to as 'the shade avoidance syndrome' and other abiotic stress responses suggest plants may integrate common signalling mechanisms to respond to multiple perturbations in their natural environment.

UV-B antagonises shade avoidance and increases levels of the flavonoid quercetin in coriander (Coriandrum sativum).

Despite controlling a diverse array of regulatory processes in plants, UV-B wavelengths (280-315 nm) are attenuated by common greenhouse materials such as glass and polycarbonate and are therefore depleted in many commercial growing environments. In this study, we analysed the architecture, pigment accumulation and antioxidant capacity of coriander (Coriandrum sativum, also known as cilantro) plants grown with and without supplementary UV-B (1.5 µmol m-2 s-1). We demonstrate that UV-B limits stem elongation responses to neighbour proximity perception (shade avoidance), promoting a more compact plant architecture. In addition, UV-B increased leaf quercetin content and total antioxidant capacity. Arabidopsis thaliana mutants deficient in flavonoid biosynthesis were not impaired in shade avoidance inhibition, suggesting that UV-B-induced flavonoid synthesis is not a component of this response. Our results indicate that UV-B supplementation may provide a method to manipulate the architecture, flavour and nutritional content of potted herbs whilst reducing the deleterious impacts of dense planting on product quality.