Making the most of canopy light: Shade avoidance under a fluctuating spectrum and irradiance.

In the field, plants face constantly changing light conditions caused by both atmospheric effects and neighbouring vegetation. This interplay creates a complex, fluctuating light environment within plant canopies. Shade-intolerant species rely on light cues from competitors to trigger shade avoidance responses, ensuring access to light for photosynthesis. While research often uses controlled growth chambers with steady light to study shade avoidance responses, the influence of light fluctuations in real-world settings remains unclear. This review examines the dynamic light environments found in woodlands, grasslands, and crops. We explore how plants respond to some fluctuations but not others, analyse the potential reasons for these differences, and discuss the possible molecular mechanisms regulating this sensitivity. We propose that studying shade avoidance responses under fluctuating light conditions offers a valuable tool to explore the intricate regulatory network behind them.

Hysteresis in PHYTOCHROME-INTERACTING FACTOR 4 and EARLY-FLOWERING 3 dynamics dominates warm daytime memory in Arabidopsis.

Despite the identification of temperature sensors and downstream components involved in promoting stem growth by warm temperatures, when and how previous temperatures affect current plant growth remain unclear. Here we show that hypocotyl growth in Arabidopsis thaliana during the night responds not only to the current temperature but also to preceding daytime temperatures, revealing a short-term memory of previous conditions. Daytime temperature affected the levels of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) and LONG HYPOCOTYL 5 (HY5) in the nucleus during the next night. These factors jointly accounted for the observed growth kinetics, whereas nighttime memory of prior daytime temperature was impaired in pif4 and hy5 mutants. PIF4 promoter activity largely accounted for the temperature-dependent changes in PIF4 protein levels. Notably, the decrease in PIF4 promoter activity triggered by cooling required a stronger temperature shift than the increase caused by warming, representing a typical hysteretic effect; this hysteretic pattern required EARLY-FLOWERING 3 (ELF3). Warm temperatures promoted the formation of nuclear condensates of ELF3 in hypocotyl cells during the afternoon but not in the morning. These nuclear speckles showed poor sensitivity to subsequent cooling. We conclude that ELF3 achieves hysteresis and drives the PIF4 promoter into the same behavior, enabling a short-term memory of daytime temperature conditions.

Functional convergence of growth responses to shade and warmth in Arabidopsis.

Shade and warmth promote the growth of the stem, but the degree of mechanistic convergence and functional association between these responses is not clear. We analysed the quantitative impact of mutations and natural genetic variation on the hypocotyl growth responses of Arabidopsis thaliana to shade and warmth, the relationship between the abundance of PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and growth stimulation by shade or warmth, the effects of both cues on the transcriptome and the consequences of warm temperature on carbon balance. Growth responses to shade and warmth showed strong genetic linkage and similar dependence on PIF4 levels. Temperature increased growth and phototropism even within a range where damage by extreme high temperatures is unlikely to occur in nature. Both cues enhanced the expression of growth-related genes and reduced the expression of photosynthetic genes. However, only warmth enhanced the expression of genes involved in responses to heat. Warm temperatures substantially increased the amount of light required to compensate for the daily carbon dioxide balance. We propose that the main ecological function of hypocotyl growth responses to warmth is to increase the access of shaded photosynthetic organs to light, which implies functional convergence with shade avoidance.

Phytochrome B links the environment to transcription.

Phytochrome B (phyB) senses the difference between darkness and light, the level of irradiance, the red/far-red ratio, and temperature. Thanks to these sensory capacities, phyB perceives whether plant organs are buried in the soil, exposed to full sunlight, in the presence of nearby vegetation, and/or under risk of heat stress. In some species, phyB perceives seasonal daylength cues. phyB affects the activity of several transcriptional regulators either by direct physical interaction or indirectly by physical interaction with proteins involved in the turnover of transcriptional regulators. Typically, interaction of a protein with phyB has either negative or positive effects on the interaction of the latter with a third party, this being another protein or DNA. Thus, phyB mediates the context-dependent modulation of the transcriptome underlying changes in plant morphology, physiology, and susceptibility to biotic and abiotic stress. phyB operates as a dynamic switch that improves carbon balance, prioritizing light interception and photosynthetic capacity in open places and the projection of the shoot towards light in the soil, under shade and in warm conditions.

Shade avoidance responses become more aggressive in warm environments.

When exposed to neighbour cues, competitive plants increase stem growth to reduce the degree of current or future shade. The aim of this work is to investigate the impact of weather conditions on the magnitude of shade avoidance responses in Arabidopsis thaliana. We first generated a growth rate database under controlled conditions and elaborated a model that predicts daytime hypocotyl growth as a function of the activity of the main photosensory receptors (phytochromes A and B, cryptochromes 1 and 2) in combination with light and temperature inputs. We then incorporated the action of thermal amplitude to account for its effect on selected genotypes, which correlates with the dynamics of the growth-promoting transcription factor PHYTOCHROME-INTERACTING FACTOR 4. The model predicted growth rate in the field with reasonable accuracy. Thus, we used the model in combination with a worldwide data set of current and future whether conditions. The analysis predicted enhanced shade avoidance responses as a result of higher temperatures due to the geographical location or global warming. Irradiance and thermal amplitude had no effects. These trends were also observed for our local growth rate measurements. We conclude that, if water and nutrients do not become limiting, warm environments enhance the shade avoidance response.

Phytochrome B dynamics departs from photoequilibrium in the field.

Vegetation shade is characterized by marked decreases in the red/far-red ratio and photosynthetic irradiance. The activity of phytochrome in the field has typically been described by its photoequilibrium, defined by the photochemical properties of the pigment in combination with the spectral distribution of the light. This approach represents an oversimplification because phytochrome B (phyB) activity depends not only on its photochemical reactions but also on its rates of synthesis, degradation, translocation to the nucleus, and thermal reversion. To account for these complex cellular reactions, we used a model to simulate phyB activity under a range of field conditions. The model provided values of phyB activity that in turn predicted hypocotyl growth in the field with reasonable accuracy. On the basis of these observations, we define two scenarios, one is under shade, in cloudy weather, at the extremes of the photoperiod or in the presence of rapid fluctuations of the light environment caused by wind-induced movements of the foliage, where phyB activity departs from photoequilibrium and becomes affected by irradiance and temperature in addition to the spectral distribution. The other scenario is under full sunlight, where phyB activity responds mainly to the spectral distribution of the light.

Perception of Sunflecks by the UV-B Photoreceptor UV RESISTANCE LOCUS8.

Sunflecks, transient patches of light that penetrate through gaps in the canopy and transiently interrupt shade, are eco-physiologically and agriculturally important sources of energy for carbon gain, but our molecular understanding of how plant organs perceive and respond to sunflecks through photoreceptors remains limited. The UV-B photoreceptor UV RESISTANCE LOCUS8 (UVR8) is a recent addition to the list of plant photosensory receptors, and we have made considerable advances in our understanding of the physiology and molecular mechanisms of action of UVR8 and its signaling pathway. However, the function of UVR8 in the natural environment is poorly understood. Here, we show that the UVR8 dimer/monomer ratio responds quantitatively and reversibly to the intensity of sunflecks that interrupt shade in the field. Sunflecks reduced hypocotyl growth and increased CHALCONE SYNTHASE (CHS) and ELONGATED HYPOCOTYL5 gene expression and CHS protein abundance in wild-type Arabidopsis (Arabidopsis thaliana) seedlings, but the uvr8 mutant was impaired in these responses. UVR8 was also required for normal nuclear dynamics of CONSTITUTIVELY PHOTOMORPHOGENIC1. We propose that UVR8 plays an important role in the plant perception of and response to sunflecks.

Multiple links between shade avoidance and auxin networks.

Auxin has emerged as a key player in the adjustment of plant morphology to the challenge imposed by variable environmental conditions. Shade-avoidance responses, including the promotion of stem and petiole growth, leaf hyponasty, and the inhibition of branching, involve an intimate connection between light and auxin signalling. Low activity of photo-sensory receptors caused by the presence of neighbouring vegetation enhances the activity of PHYTOCHROME INTERACTING FACTORs (PIFs), which directly promote the expression of genes involved in auxin biosynthesis, conjugation, transport, perception, and signalling. In seedlings, neighbour signals increase auxin levels in the foliage, which then moves to the stem, where it reaches epidermal tissues to promote growth. However, this model only partially accounts for shade-avoidance responses (which may also occur in the absence of increased auxin levels), and understanding the whole picture will require further insight into the functional significance of the multiple links between shade and auxin networks.

Meta-Analysis of the Transcriptome Reveals a Core Set of Shade-Avoidance Genes in Arabidopsis.

The presence of neighboring vegetation modifies the light input perceived by photo-sensory receptors, initiating a signaling cascade that adjusts plant growth and physiology. Thousands of genes can change their expression during this process, but the structure of the transcriptional circuit is poorly understood. Here we present a meta-analysis of transcriptome data from Arabidopsis thaliana exposed to neighbor signals in different contexts, including organs where growth is promoted or inhibited by these signals. We identified a small set of genes that consistently and dynamically respond to neighbor light signals. This group is also affected by light during de-etiolation and day/night cycles. Among these genes, many of those with positive response to neighbor signals are binding targets of PHYTOCHROME-INTERACTING FACTORS (PIFs) and function as transcriptional regulators themselves, but none of these features is observed among those with negative response to neighbor signals. Changes. in neighbor signals can mimic the transcriptional signature of auxin, gibberellins, brassinosteroid, abscisic acid, ethylene, jasmonic acid and cytokinin but in a context-dependent manner. We propose the existence of a small core set of genes involved in downstream communication of PIF signaling status and in the control of light sensitivity and chloroplast metabolism.

Perception and signalling of light and temperature cues in plants.

Light and temperature patterns are often correlated under natural plant growth conditions. In this review, we analyse the perception and signalling mechanisms shared by both these environmental cues and discuss the functional implications of their convergence to control plant growth. The first point of integration is the phytochrome B (phyB) receptor, which senses light and temperature. Downstream of phyB, the signalling core comprises two branches, one involving PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and the other CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) and ELONGATED HYPOCOTYL 5 (HY5). The dynamics of accumulation and/or localization of each of these core signalling components depend on light and temperature conditions. These pathways are connected through COP1, which enhances the activity of PIF4. The circadian clock modulates this circuit, since EARLY FLOWERING 3 (ELF3), an essential component of the evening complex (EC), represses expression of the PIF4 gene and PIF4 transcriptional activity. Phytochromes are probably not the only entry point of temperature into this network, but other sensors remain to be established. The sharing of mechanisms of action for two distinct environmental cues is to some extent unexpected, as it renders these responses mutually dependent. There are nonetheless many ecological contexts in which such a mutual influence could be beneficial.

Heat shock-induced fluctuations in clock and light signaling enhance phytochrome B-mediated Arabidopsis deetiolation.

Moderately warm constant ambient temperatures tend to oppose light signals in the control of plant architecture. By contrast, here we show that brief heat shocks enhance the inhibition of hypocotyl growth induced by light perceived by phytochrome B in deetiolating Arabidopsis thaliana seedlings. In darkness, daily heat shocks transiently increased the expression of pseudo-response regulator7 (PRR7) and PRR9 and markedly enhanced the amplitude of the rhythms of late elongated hypocotyl (LHY) and circadian clock associated1 (CCA1) expression. In turn, these rhythms gated the hypocotyl response to red light, in part by changing the expression of phytochrome interacting FACTOR4 (PIF4) and PIF5. After light exposure, heat shocks also reduced the nuclear abundance of constitutive photomorphogenic1 (COP1) and increased the abundance of its target elongated hypocotyl5 (HY5). The synergism between light and heat shocks was deficient in the prr7 prr9, lhy cca1, pif4 pif5, cop1, and hy5 mutants. The evening element (binding site of LHY and CCA1) and G-box promoter motifs (binding site of PIFs and HY5) were overrepresented among genes with expression controlled by both heat shock and red light. The heat shocks experienced by buried seedlings approaching the surface of the soil prepare the seedlings for the impending exposure to light by rhythmically lowering LHY, CCA1, PIF4, and PIF5 expression and by enhancing HY5 stability.

LOV-domain photoreceptor, encoded in a genomic island, attenuates the virulence of Pseudomonas syringae in light-exposed Arabidopsis leaves.

In Arabidopsis thaliana, light signals modulate the defences against bacteria. Here we show that light perceived by the LOV domain-regulated two-component system (Pst-Lov) of Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) modulates virulence against A. thaliana. Bioinformatic analysis and the existence of an episomal circular intermediate indicate that the locus encoding Pst-Lov is present in an active genomic island acquired by horizontal transfer. Strains mutated at Pst-Lov showed enhanced growth on minimal medium and in leaves of A. thaliana exposed to light, but not in leaves incubated in darkness or buried in the soil. Pst-Lov repressed the expression of principal and alternative sigma factor genes and their downstream targets linked to bacterial growth, virulence and quorum sensing, in a strictly light-dependent manner. We propose that the function of Pst-Lov is to distinguish between soil (dark) and leaf (light) environments, attenuating the damage caused to host tissues while releasing growth out of the host. Therefore, in addition to its direct actions via photosynthesis and plant sensory receptors, light may affect plants indirectly via the sensory receptors of bacterial pathogens.

Diurnal dependence of growth responses to shade in Arabidopsis: role of hormone, clock, and light signaling.

We investigated the diurnal dependence of the hypocotyl-growth responses to shade under sunlight-night cycles in Arabidopsis thaliana. Afternoon shade events promoted hypocotyl growth, while morning shade was ineffective. The lhy-D, elf3, lux, pif4 pif5, toc1, and quadruple della mutants retained the response to afternoon shade and the lack of response to morning shade while the lhy cca1 mutant responded to both morning and afternoon shade. The phyB mutant, plants overexpressing the multidrug resistance-like membrane protein ABCB19, and the iaa17/axr3 loss-of-function mutant failed to respond to shade. Transient exposure of sunlight-grown seedlings to synthetic auxin in the afternoon caused a stronger promotion of hypocotyl growth than morning treatments. The promotion of hypocotyl growth by afternoon shade or afternoon auxin required light perceived by phytochrome A or cryptochromes during the previous hours of the photoperiod. Although the ELF4-ELF3-LUX complex, PIF4, PIF5, and DELLA are key players in the generation of diurnal hypocotyl-growth patterns, they exert a minor role in the control of the diurnal pattern of growth responses to shade. We conclude that the strong diurnal dependency of hypocotyl-growth responses to shade relates to the balance between the antagonistic actions of LHY-CCA1 and a light-derived signal.

Repression of shade-avoidance reactions by sunfleck induction of HY5 expression in Arabidopsis.

The light environment provides signals that play a critical role in the control of stem growth in plants. The reduced irradiance and altered spectral composition of shade light promote stem growth compared with unfiltered sunlight. However, whereas most studies have used seedlings exposed to contrasting but constant light treatments, the natural light environment may exhibit strong fluctuations. As a result of gaps in the canopy, plants shaded by neighbours may experience sunflecks, i.e., brief periods of exposure to unfiltered sunlight. Here, we show that sunflecks are perceived by phytochromes A and B, and inhibit hypocotyl growth in Arabidopsis thaliana mainly if they occur during the final portion of the photoperiod. By using forward and reverse genetic approaches we found that ELONGATED HYPOCOTYL 5, LATE ELONGATED HYPOCOTYL, PHYTOCHROME KINASE SUBSTRATE 4 and auxin signalling are key players in this response.

Cryptochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis.

Green light added to blue light has been proposed to shift cryptochromes from their semireduced active form to the reduced, inactive state. Whether the increased proportion of green light observed under leaf canopies compared to open places reduces cryptochrome-mediated effects remained to be elucidated. Here we report that the length of the hypocotyl of Arabidopsis (Arabidopsis thaliana) seedlings grown under controlled conditions decreased linearly with increasing blue/green ratios of the light within the range of ratios found in natural environments. This effect was stronger under higher irradiances. We developed a model, parameterized on the basis of field experiments including photoreceptor mutants, where hypocotyl growth of seedlings exposed to different natural radiation environments was related to the action and interaction of phytochromes and cryptochromes. Adding the blue/green ratio of the light in the term involving cryptochrome activity improved the goodness of fit of the model, thus supporting a role of the blue/green ratio under natural radiation. The blue/green ratio decreased sharply with increasing shade by green grass leaves to one-half of the values observed in open places. The impact of blue/green ratio on cryptochrome-mediated inhibition of hypocotyl growth was at least as large as that of irradiance. We conclude that cryptochrome is a sensor of blue irradiance and blue/green ratio.

Synergism of red and blue light in the control of Arabidopsis gene expression and development.

The synergism between red and blue light in the control of plant growth and development requires the coaction of the red light photoreceptor phytochrome B (phyB) and the blue light and UV-A receptor cryptochromes (cry). Here, we describe the mechanism of the coaction of these photoreceptors in controlling both development and physiology. In seedlings grown under red light, a transient supplement with blue light induced persistent changes in the transcriptome and growth patterns. Blue light enhanced the expression of the transcription factors LONG HYPOCOTYL 5 (HY5) and HOMOLOG OF HY5 (HYH) and of SUPPRESSOR OF PHYA 1 (SPA1) and SPA4. HY5 and HYH enhanced phyB signaling output beyond the duration of the blue light signal, and, contrary to their known role as repressors of phyA signaling, SPA1 and SPA4 also enhanced phyB signaling. These observations demonstrate that the mechanism of synergism involves the promotion by cry of positive regulators of phyB signaling. The persistence of the light-derived signal into the night commits the seedling to a morphogenetic and physiological program consistent with a photosynthetic lifestyle.