Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms

Plants ‘forage’ for light in plant canopies using a variety of photosensory systems. Far-red radiation (FR) reflected by neighbours is an early signal of competition that elicits anticipatory shade-avoidance responses. In Arabidopsis and cucumber, perception of reflected FR requires phytochrome B. Horizontal blue (B) light gradients also guide plant shoots to canopy gaps in patchy vegetation, and these B light signals are perceived by specific photoreceptors. When plants are shaded by neighbours they undergo extensive reprogramming of their morphological development. Although phytochromes and B light receptors are certainly involved in these responses to shading, other sensory systems probably play important roles in the field. Recent studies of plant–plant signalling are unveiling a paradigm of sensory diversity and sophistication, which has important implications for understanding the functioning of plant populations and communities.     

Light from below matters: Quantifying the consequences of responses to far‐red light reflected upwards for plant performance in heterogeneous canopies

In vegetation stands, plants receive red to far‐red ratio (R:FR) signals of varying strength from all directions. However, plant responses to variations in R:FR reflected from below have been largely ignored despite their potential consequences for plant performance. Using a heterogeneous rose canopy, which consists of bent shoots down in the canopy and vertically growing upright shoots, we quantified upward far‐red reflection by bent shoots and its consequences for upright shoot architecture. With a three‐dimensional plant model, we assessed consequences of responses to R:FR from below for plant photosynthesis. Bent shoots reflected substantially more far‐red than red light, causing reduced R:FR in light reflected upwards. Leaf inclination angles increased in upright shoots which received low R:FR reflected from below. The increased leaf angle led to an increase in simulated plant photosynthesis only when this low R:FR was reflected off their own bent shoots and not when it reflected off neighbour bent shoots. We conclude that plant response to R:FR from below is an under‐explored phenomenon which may have contrasting consequences for plant performance depending on the type of vegetation or crop system. The responses are beneficial for performance only when R:FR is reflected by lower foliage of the same plants.     

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.     

Variation in growth form in relation to spectral light quality (red/far-red ratio) in Plantago lanceolata L. in sun and shade populations

Plants from a sun and shade population were grown in two environments differing in the ratio of red to far-red light (R/FR ratio). A low R/FR ratio, simulating vegetation shade, promoted the formation of long, upright-growing leaves and allocation towards shoot growth, whereas a high R/FR ratio had the opposite effects. The increase in plant height under the low R/FR ratio was accompanied by a reduction in the number of leaves. Population differences in growth form resembled the differences between plants grown in different light environments: plants from the shade population had rosettes with long erect leaves, whereas plants from the sun population formed prostrate rosettes with short leaves. Plants from the shade population were more responsive to the R/FR ratio than plants from the sun population: the increases in leaf length, plant height, and leaf area ratio under a low R/FR ratio were larger in the shade population. However, differences in plasticity were small compared to the population difference in growth form itself. We argue that plants do not respond optimally to shading and that developmental constraints might have limited the evolution of an optimal response. Received: 8 December 1996 / Accepted: 31 March 1997     

Light signals generated by vegetation shade facilitate acclimation to low light in shade-avoider plants

When growing in search for light, plants can experience continuous or occasional shading by other plants. Plant proximity causes a decrease in the ratio of R to far-red light (low R:FR) due to the preferential absorbance of R light and reflection of FR light by photosynthetic tissues of neighboring plants. This signal is often perceived before actual shading causes a reduction in photosynthetically active radiation (low PAR). Here, we investigated how several Brassicaceae species from different habitats respond to low R:FR and low PAR in terms of elongation, photosynthesis, and photoacclimation. Shade-tolerant plants such as hairy bittercress (Cardamine hirsuta) displayed a good adaptation to low PAR but a poor or null response to low R:FR exposure. In contrast, shade-avoider species, such as Arabidopsis (Arabidopsis thaliana), showed a weak photosynthetic performance under low PAR but they strongly elongated when exposed to low R:FR. These responses could be genetically uncoupled. Most interestingly, exposure to low R:FR of shade-avoider (but not shade-tolerant) plants improved their photoacclimation to low PAR by triggering changes in photosynthesis-related gene expression, pigment accumulation, and chloroplast ultrastructure. These results indicate that low R:FR signaling unleashes molecular, metabolic, and developmental responses that allow shade-avoider plants (including most crops) to adjust their photosynthetic capacity in anticipation of eventual shading by nearby plants.

Vegetation proximity light signals inform shade-avoider plants to adjust their photosynthetic capacity in anticipation of eventual shading by nearby plants.     

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.     

Maize leaves turn away from neighbors

In commercial crops, maize (Zea mays) plants are typically grown at a larger distance between rows (70 cm) than within the same row (16-23 cm). This rectangular arrangement creates a heterogeneous environment in which the plants receive higher red light (R) to far-red light (FR) ratios from the interrow spaces. In field crops, the hybrid Dekalb 696 (DK696) showed an increased proportion of leaves toward interrow spaces, whereas the experimental hybrid 980 (Exp980) retained random leaf orientation. Mirrors reflecting FR were placed close to isolated plants to simulate the presence of neighbors in the field. In addition, localized FR was applied to target leaves in a growth chamber. During their expansion, the leaves of DK696 turned away from the low R to FR ratio signals, whereas Exp980 leaves remained unaffected. On the contrary, tillering was reduced and plant height was increased by low R to FR ratios in Exp980 but not in DK696. Isolated plants preconditioned with low R/FR-simulating neighbors in a North-South row showed reduced mutual shading among leaves when the plants were actually grouped in North-South rows. These observations contradict the current view that phytochrome-mediated responses to low R/FR are a relic from wild conditions, detrimental for crop yield.     

Auxin and Ethylene Regulate Elongation Responses to Neighbor Proximity Signals Independent of Gibberellin and DELLA Proteins in Arabidopsis

Plants modify growth in response to the proximity of neighbors. Among these growth adjustments are shade avoidance responses, such as enhanced elongation of stems and petioles, that help plants to reach the light and outgrow their competitors. Neighbor detection occurs through photoreceptor-mediated detection of light spectral changes (i.e. reduced red:far-red ratio [R:FR] and reduced blue light intensity). We recently showed that physiological regulation of these responses occurs through light-mediated degradation of nuclear, growth-inhibiting DELLA proteins, but this appeared to be only part of the full mechanism. Here, we present how two hormones, auxin and ethylene, coregulate DELLAs but regulate shade avoidance responses through DELLA-independent mechanisms in Arabidopsis (Arabidopsis thaliana). Auxin appears to be required for both seedling and mature plant shoot elongation responses to low blue light and low R:FR, respectively. Auxin action is increased upon exposure to low R:FR and low blue light, and auxin inhibition abolishes the elongation responses to these light cues. Ethylene action is increased during the mature plant response to low R:FR, and this growth response is abolished by ethylene insensitivity. However, ethylene is also a direct volatile neighbor detection signal that induces strong elongation in seedlings, possibly in an auxin-dependent manner. We propose that this novel ethylene and auxin control of shade avoidance interacts with DELLA abundance but also controls independent targets to regulate adaptive growth responses to surrounding vegetation.     

Physiological regulation and functional significance of shade avoidance responses to neighbors

Plants growing in dense vegetations compete with their neighbors for resources such as water, nutrients and light. The competition for light has been particularly well studied, both for its fitness consequences as well as the adaptive behaviors that plants display to win the battle for light interception. Aboveground, plants detect their competitors through photosensory cues, notably the red:far-red light ratio (R:FR). The R:FR is a very reliable indicator of future competition as it decreases in a plant-specific manner through red light absorption for photosynthesis and is sensed with the phytochrome photoreceptors. In addition, also blue light depletion is perceived for neighbor detection. As a response to these light signals plants display a suite of phenotypic traits defined as the shade avoidance syndrome (SAS). The SAS helps to position the photosynthesizing leaves in the higher zones of a canopy where light conditions are more favorable. In this review we will discuss the physiological control mechanisms through which the photosensory signals are transduced into the adaptive phenotypic responses that make up the SAS. Using this mechanistic knowledge as a starting point, we will discuss how the SAS functions in the context of the complex multi-facetted environments, which plants usually grow in.Key words: competition, shade avoidance, hormones, cell wall, adaptive plasticity, photoreceptor, light     

Far-red light reflected from neighbouring vegetation promotes shoot elongation and accelerates flowering in spring barley plants

Field experiments were conducted in St Paul, MN, USA, to test the hypothesis that early season declines in the red:far-red ratio (R:FR) associated with FR reflection from neighbouring leaves have a role in regulating barley development. Treatment plants were grown adjacent to densely sown border rows of barley. The borders functioned to reflect far-red (FR), which reduced R:FR within the treatment plant light environment without shading treatment plants. Barriers were set in the soil to minimize root interactions between treatment plants and borders. Treatment plants were spaced either 2 or 16 cm apart. The presence of borders significantly increased shoot leaf and internode lengths at both plant spacings. Leaf sheath length data suggest that interactions between 2 cm spaced treatment plants enhanced plant responsiveness to the presence of borders. Border treatments shortened the period of vegetative growth prior to initiation of main shoot floral primordia. Bordered plants formed fewer main shoot leaves, initiated internode elongation at a lower node, and had slightly earlier heading dates than unbordered controls. Leaf appearance rate was not influenced by border treatments. We conclude that barley shoot development is photomorphogenically modulated by R:FR. Early season shifts in R:FR could have a significant influence on shoot development given that barley has the capacity to detect and developmentally respond to declines in R:FR associated with FR reflection from neighbours.     

Maternal and ambient environmental effects of light on germination in Plantago lanceolata: correlated responses to selection on leaf length

1. Seeds from artificial selection lines were exposed to different maternal and ambient conditions, simulating sunlight and vegetation shade.
2. Lines selected for longer leaves also produced larger seeds, indicating a positive genetic correlation between leaf length and seed size.
3. Light conditions during maturation had no large effect on seed size.
4. Seed germination was reduced by a low ratio of red to far-red light (R/FR ratio) in the ambient environment.
5. Seeds maturated under simulated vegetation shade germinated less readily and were more inhibited by a low ambient R/FR ratio than seeds maturated under full sunlight or R/FR-neutral shade. Thus, low R/FR-ratios in the maternal and ambient environment operated synergistically.
6. Large genotypic variation in the germination responses to both maternal and ambient light conditions was found among and within selection lines, indicating that such responses might have the potential to evolve in response to natural selection.
7. Artificial selection for leaf length had affected seed germination characteristics but correlated responses and thus genetic correlations largely depended on light conditions in the selective environment. Selection for longer leaves under a low R/FR ratio increased seed dormancy and plasticity of germination in response to the R/FR ratio. However, in the opposite selective environment selection for longer leaves reduced seed dormancy and plasticity to the R/FR ratio. It is argued that leaf length and seed germination characteristics are somehow linked by shared physiological mechanisms, which may facilitate concerted changes in shade avoidance responses.     

Blue light regulated shade avoidance

Most plants grow in dense vegetation with the risk of being out-competed by neighboring plants. These neighbors can be detected not only through the depletion in light quantity that they cause, but also through the change in light quality, which plants perceive using specific photoreceptors. Both the reduction of the red:far-red ratio and the depletion of blue light are signals that induce a set of phenotypic traits, such as shoot elongation and leaf hyponasty, which increase the likelihood of light capture in dense plant stands. This set of phenotypic responses are part of the so called shade avoidance syndrome (SAS). This addendum discusses recent findings on the regulation of the SAS of Arabidopsis thaliana upon blue light depletion. Keller et al. and Keuskamp et al. show that the low blue light attenuation induced shade avoidance response of seedling and rosette-stage A. thaliana plants differ in their hormonal regulation. These studies also show there is a regulatory overlap with the R:FR-regulated SAS.     

Tree seedling canopy responses to conflicting photosensory cues

Light with decreased red:far-red (R:FR) ratios may signal neighbor presence and trigger plant developmental responses. There is some evidence that plant canopies forage towards increased R:FR ratios, but it is unclear to what extent R:FR versus the total amount of photosynthetically active radiation (PAR) influences canopy foraging responses among forest trees. The objective of this study was to examine the relative importance of PAR and R:FR as photosensory cues leading to tree canopy foraging responses. Seedlings of Betula papyrifera Marshall (paper birch) were grown in an experimental garden. Each seedling was germinated and grown in its own shading structure and exposed to two spatially separated light environments, in a factorial design of PAR and R:FR. Plant canopy foraging was evaluated at the end of one growing season in terms of canopy displacement, canopy area, leaf number, direction of stem lean, petiole aspect, and lamina aspect with respect to experimental light treatments. Leaf number and canopy area were greater on the high PAR sides of plants, irrespective of the R:FR treatment. Seedling canopies were displaced towards the direction of high PAR, but this relationship was not significant across all treatments. Petiole aspect was random and showed no significant directedness towards any of the light treatments. Lamina aspect and the direction of stem lean were distributed towards the direction of high PAR, irrespective of the R:FR treatment. Overall, first-year B. papyrifera seedlings used PAR, rather than R:FR ratio, as a photosensory cue for canopy light foraging.     

Differential responses of invasive Celastrus orbiculatus (Celastraceae) and native C. scandens to changes in light quality

When plants are subjected to leaf canopy shade in forest understories or from neighboring plants, they not only experience reduced light quantity, but light quality in lowered red : far red light (R : FR). Growth and other developmental responses of plants in reduced R : FR can vary and are not consistent across species. We compared how an invasive liana, Celastrus orbiculatus, and its closely related native congener, C. scandens, responded to changes in the R : FR under controlled, simulated understory conditions. We measured a suite of morphological and growth attributes under control, neutral shading, and low R : FR light treatments. Celastrus orbiculatus showed an increase in height, aboveground biomass, and total leaf mass in reduced R : FR treatments as compared to the neutral shade, while C. scandens had increased stem diameter, single leaf area, and leaf mass to stem mass ratio. These differences provide a mechanistic understanding of the ability of C. orbiculatus to increase height and actively forage for light resources in forest understories, while C. scandens appears unable to forage for light and instead depends upon a light gap forming. The plastic growth response of C. orbiculatus in shaded conditions points to its success in forested habitats where C. scandens is largely absent.     

Overexpression of oat phytochrome A gene differentially affects stem growth responses to red/far-red ratio signals characteristic of sparse or dense canopies

The effects of overexpression of oat phytochrome A on neighbour detection and on stem-growth responses to changes in red light (R), far-red light (FR) and blue light (B) simulating neighbours were investigated in transgenic tobacco seedlings grown under natural radiation. In wild-type (WT) seedlings, stem extension growth was promoted: (1) by lowering the R:FR by means of daytime supplementary FR, end-of-day FR, neighbours reflecting FR, or selective light filters placed around the base of the shoot to reduce R without affecting FR; and (2) by lowering phytochrome-absorbable radiation (R+FR) reaching the stem. Transgenic seedlings only responded to reductions in R:FR involving no significant changes in FR irra-diance, i.e. end-of-day FR and filters placed around the stem to reduce R. Neither daytime supplementary R nor selective filters placed around the stem to reduce B affected stem growth in any genotype. In growing canopies, WT seedlings responded to the reduction of R:FR caused by FR reflected in neighbour plants. Transgenic seedlings responded to plant density about a week later, when mutual plant shading reduced R and (to a lesser extent) FR below sunlight levels. Overexpression of phytochrome A impaired early neighbour detection.     

The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses

Many plants display a characteristic suite of developmental"shade avoidance" responses, such as stem elongation and acceleratedreproduction, to the low ratio of red to far-red wavelengths(R:FR) reflected or transmitted from green vegetation. ThisR:FR cue of crowding and vegetation shade is perceived by thephytochrome family of photoreceptors. Phytochrome-mediated responsesprovide an ideal system for investigating the adaptive evolutionof phenotypic plasticity in natural environments. The molecularand developmental mechanisms underlying shade avoidance responsesare well studied, and testable ecological hypotheses exist fortheir adaptive significance. Experimental manipulation of phenotypesdemonstrates that shade avoidance responses may be adaptive,resulting in phenotypes with high relative fitness in the environmentsthat induce those phenotypes. The adaptive value of shade avoidancedepends upon the competitive environment, resource availability,and the reliability of the R:FR cue for predicting the selectiveenvironment experienced by an induced phenotype. Comparativestudies and a reciprocal transplant experiment with Impatienscapensis provide evidence of adaptive divergence in shade avoidanceresponses between woodland and clearing habitats, which mayresult from population differences in the frequency of selectionon shade avoidance traits, as well as differences in the reliabilityof the R:FR cue. Recent rapid progress in elucidating phytochromesignaling pathways in the genetic model Arabidopsis thalianaand other species now provides the opportunity for studyinghow selection on shade avoidance traits in natural environmentsacts upon the molecular mechanisms underlying natural phenotypicvariation.     

The regulation of cell wall extensibility during shade avoidance: a study using two contrasting ecotypes of Stellaria longipes

Shade avoidance in plants involves rapid shoot elongation to grow toward the light. Cell wall-modifying mechanisms are vital regulatory points for control of these elongation responses. Two protein families involved in cell wall modification are expansins and xyloglucan endotransglucosylase/hydrolases. We used an alpine and a prairie ecotype of Stellaria longipes differing in their response to shade to study the regulation of cell wall extensibility in response to low red to far-red ratio (R/FR), an early neighbor detection signal, and dense canopy shade (green shade: low R/FR, blue, and total light intensity). Alpine plants were nonresponsive to low R/FR, while prairie plants elongated rapidly. These responses reflect adaptation to the dense vegetation of the prairie habitat, unlike the alpine plants, which almost never encounter shade. Under green shade, both ecotypes rapidly elongate, showing that alpine plants can react only to a deep shade treatment. Xyloglucan endotransglucosylase/hydrolase activity was strongly regulated by green shade and low blue light conditions but not by low R/FR. Expansin activity, expressed as acid-induced extension, correlated with growth responses to all light changes. Expansin genes cloned from the internodes of the two ecotypes showed differential regulation in response to the light manipulations. This regulation was ecotype and light signal specific and correlated with the growth responses. Our results imply that elongation responses to shade require the regulation of cell wall extensibility via the control of expansin gene expression. Ecotypic differences demonstrate how responses to environmental stimuli are differently regulated to survive a particular habitat.