Early developmental responses to seedling environment modulate later plasticity to light spectral quality

Correlations between developmentally plastic traits may constrain the joint evolution of traits. In plants, both seedling de-etiolation and shade avoidance elongation responses to crowding and foliage shade are mediated by partially overlapping developmental pathways, suggesting the possibility of pleiotropic constraints. To test for such constraints, we exposed inbred lines of Impatiens capensis to factorial combinations of leaf litter (which affects de-etiolation) and simulated foliage shade (which affects phytochrome-mediated shade avoidance). Increased elongation of hypocotyls caused by leaf litter phenotypically enhanced subsequent elongation of the first internode in response to low red:far red (R:FR). Trait expression was correlated across litter and shade conditions, suggesting that phenotypic effects of early plasticity on later plasticity may affect variation in elongation traits available to selection in different light environments.     

Plasticity and environment-specific covariances: an investigation of floral-vegetative and within flower correlations

Floral traits are commonly thought to be more canalized than vegetative ones. In addition, floral and vegetative traits are hypothesized to be genetically decoupled, enabling vegetative structures to respond plastically to environmental heterogeneity, and to evolve in response to selection without disrupting the reproductive function of flowers. To test these hypotheses, we evaluate the genetic architecture of floral and vegetative traits in natural populations of Arabidopsis thaliana raised under variable light-quality environments. Plants were grown either under high or low ratios of red to far-red (R:FR) light, an aspect of light quality that varies with neighbor proximity and regulates competitive shade-avoidance responses. Across environments, we detected significant genetic variation for the average expression of all measured floral traits (petal length and width, stamen length, pistil length, stigma-anther separation, and exsertion of both the stamen and pistil beyond the corolla). Light quality significantly influenced the absolute size of several floral traits as well as the allometry (i.e., relative scaling) of all floral traits, and genotypes differed in the plasticity of floral traits to the light treatments. Exposure to low relative to high R:FR resulted in significantly greater elongation in the vegetative trait, petiole length, and genotypes again differed in the plasticity of this trait to R:FR. Consistent with prior studies, most floral traits were less plastic than the vegetative trait; herkogamy (i.e., stigma-anther separation) was the exception and expressed more variable trait values across environments than petiole length, apparently as a consequence of the independent responses of stamens and pistils. Flowers also showed strong phenotypic integration; genotypic correlations were significantly positive among floral traits within each light treatment. Although floral-vegetative correlations were not significant in the high R:FR light treatment, significant correlations were detected between petal traits, pistil length, and petiole length under low R:FR, in contrast to the widely held hypothesis that floral and vegetative traits are genetically independent. Finally, we detected selection for reduced herkogamy in the low R:FR light treatment. The observed correlation between functional trait groups suggest that vegetative plasticity may affect the expression of floral traits in some environments, and that environment-specific constraints may exist on the evolution of floral and vegetative traits.     

THE GENETIC ARCHITECTURE OF PLASTICITY TO DENSITY IN IMPATIENS CAPENSIS

Plant responses to crowding may be mediated by resource availability and/or by a specific environmental cue, the ratio of red:far red wavelengths (R:FR) perceived by phytochrome. This study examined the contribution of phytochrome-mediated photomorphogenesis to genetic variation in plastic responses to density in the annual plant Impatiens capensis. Inbred lines derived from open and woodland populations were grown under low density high density, and high density with selective removal of FR wavelengths to block phytochrome-mediated perception of neighbor proximity. Genetic variation in plasticity to density and to the R:FR cue was detected for several traits Plants grown at high density displayed increased internode elongation; decreased branch, flower, and node production; increased menstem dormancy; and decreased leaf area and specific leaf weight compared to plants grown at low density. Stem elongation responses to density were suppressed when phytochrome perception was blocked at high density. For these phytochrome-mediated traits, a genotype's plasticity to density was strongly correlated with its response to R:FR. Phytochrome-mediated traits were tightly correlated with one another, regardless of the density environment. However, the responses to density of meristem allocation to branching and leaf traits were less strongly phytochrome-mediated. These traits differed in patterns of plasticity, and their genetic correlations often differed across environments. In particular, genetic trade-offs involving meristem allocation to branching were expressed only at low density. The observed density dependence of phenotypic and genetic correlations implies that indirect selection and the potential for correlated response to selection will depend upon the competitive environment. Thus the differential sensitivity of characters to the R:FR cue can influence the evolution of integrated plastic responses to density.     

Is photomorphogenic shade avoidance adaptive? Perspectives from population biology

Photomorphogenic shade avoidance responses provide an ideal model system for integrating genetic, physiological and population biology approaches to the study of adaptive plasticity. The adaptive plasticity hypothesis predicts that shade avoidance phenotypes induced by low ratios of red to far-red light (R:FR) will have high relative fitness in dense stands, but will suffer a fitness disadvantage at low density. Experiments with transgenic and mutant plants in which photomorphogenic genes are disabled, as well as phenotype manipulation by means of altered R:FR, strongly support the shade avoidance hypothesis. The observation of photomorphogenic ecotypes in different selective environments also suggests that the shade avoidance response has undergone adaptive evolution. Quantitative genetic variation in R:FR sensitivity has been detected in wild populations, indicating that the evolutionary potential exists for response to natural selection. However, evolutionary response may be constrained by genetic correlations among developmentally linked traits. Therefore it cannot be assumed that an observed suite of photomorphogenic responses represents an adaptive optimum for every trait.     

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.     

Population differentiation for plasticity to light in an annual herb: Adaptation and cost

Phenotypic plasticity allows plants to cope with environmental heterogeneity. Environmental variation among populations may select for differentiation in plasticity. To test this idea, we used the annual plant Geranium carolinianum, which inhabits old fields that are densely vegetated and lack canopy cover and wood margins with tree shade but less neighbor shade. Individuals from three populations of each habitat were planted in natural low and high light environments, and morphological traits important for light acquisition were measured. Old-field plants were more plastic, with greater elongation of petioles and internodes in low light than those from wood margins. This larger shade avoidance response suggests evolution of greater plasticity to neighbor shade than to the tree canopy. Fitness of old-field plants was high across both light environments, whereas fitness of wood-margin plants was reduced in low light. Selection favored longer internodes in low than high light. Finally, plasticity for internode length was negatively associated with fitness in high light, suggesting a cost of plasticity for this trait. Together these results indicate that shade-avoidance plasticity of petiole and internode length is adaptive. However, greater elongation of internode length may be constrained by the cost of plasticity expressed in high light. The evolution of plasticity appears to reflect a balance between its adaptive nature and its cost to fitness.     

Testing adaptive plasticity to UV: costs and benefits of stem elongation and light-induced phenolics

On exposure to ultraviolet radiation (UV), many plant species both reduce stem elongation and increase production of phenolic compounds that absorb in the UV region of the spectrum. To demonstrate that such developmental plasticity to UV is adaptive, it is necessary to show that the induced phenotype is both beneficial in inductive environments and maladaptive in non-inductive environments. We measured selection on stem elongation and phenolic content of seedlings of Impatiens capensis transplanted into ambient-UV and UV-removal treatments. We extended the range of phenotypes expressed, and thus the opportunity for selection in each UV treatment, by pretreating seedlings with either a low ratio of red:far-red wavelengths (R:FR), which induced stem elongation and reduced phenolic concentrations, or high R:FR, which had the opposite effect on these two phenotypic traits. Reduced stem length relative to biomass was advantageous for elongated plants under ambient UV, whereas increased elongation was favored in the UV-removal treatment. Selection favored an increase in the level of phenolics induced by UV in the ambient-UV treatment, but a decrease in phenolics in the absence of UV. These results are consistent with the hypotheses that reduced elongation and increased phenolic concentrations serve a UV-protective function and provide the first explicit demonstration in a wild species that plasticity of these traits to UV is adaptive. The observed cost to phenolics in the absence of UV may explain why many species plastically upregulate phenolic production when exposed to UV, rather than evolve constitutively high levels of these compounds. Finally, pretreatment with low R:FR simulating foliar shade did not exacerbate the fitness impact of UV exposure when plants had several weeks to acclimate to UV. This observation suggests that the evolution of adaptive shade avoidance responses to low R:FR in crowded stands will not be constrained by increased sensitivity to UV in elongated plants when they overtop their neighbors.     

Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs

Plants shaded by neighbors or overhead foliage experience both a reduction in the ratio of red to far red light (R:FR), a specific cue perceived by phytochrome, and reduced photosynthetically active radiation (PAR), an essential resource. We tested the adaptive value of plasticity to crowding and to the cue and resource components of foliage shade in the annual plant Arabidopsis thaliana by exposing 36 inbred families from four natural populations to four experimental treatments: (1) high density, full sun; (2) low density, full sun; (3) low density, neutral shade; and (4) low density, low R:FR-simulated foliage shade. Genotypic selection analysis within each treatment revealed strong environmental differences in selection on plastic life-history traits. We used specific contrasts to measure plasticity to density and foliage shade, to partition responses to foliage shade into phytochrome-mediated responses to the R:FR cue and responses to PAR, and to test whether plasticity was adaptive (i.e., in the same direction as selection in each environment). Contrary to expectation, we found no evidence for adaptive plasticity to density. However, we observed both adaptive and maladaptive responses to foliage shade. In general, phytochrome-mediated plasticity to the R:FR cue of foliage shade was adaptive and counteracted maladaptive growth responses to reduced PAR. These results support the prediction that active developmental responses to environmental cues are more likely to be adaptive than are passive resource-mediated responses. Multiple regression analysis detected a few costs of adaptive plasticity and adaptive homeostasis, but such costs were infrequent and their expression depended on the environment. Thus, costs of plasticity may occasionally constrain the evolution of adaptive responses to foliage shade in Arabidopsis, but this constraint may differ among environments and is far from ubiquitous.     

THE DEVELOPMENTAL RESPONSES OF PAPAYA LEAVES TO SIMULATED CANOPY SHADE

The developmental responses of plants to shade underneath foliage are influenced by reductions in irradiance and shifts in spectral quality (characterized by reductions in the quantum ratio of red to far-red wavelengths, R:FR). Previous research on the influence of shadelight on leaf development has neglected the reductions in R:FR characteristic of foliage shade, and these studies have almost certainly underestimated the extent and array of developmental responses to foliage shade. We have studied the effects of reduced irradiance and R:FR on the leaf development of papaya (Carica papaya L., Caricaceae). Using experimental shadehouses, replicates of plants grown in high light conditions (0.20 of sunlight and R:FR = 0.90) were compared to low light conditions (0.02 of sunlight) with either the spectral quality of sunlight (R:FR = 0.99) or of foliage shade (F:FR = 0.26). Although many characteristics, such as leaf thickness, specific leaf weight, stomatal density, palisade parenchyma cell shape, and the ratio of mesophyll air surface/leaf surface were affected by reductions in irradiance, reduced R:FR contributed to further changes. Some characters, such as reduced chlorophyll a/b ratios, reduced lobing, and greater internode length, were affected primarily by low R:FR. The reduced R:FR of foliage shade, presumably affecting phytochrome equilibrium, strongly influences the morphology and anatomy of papaya leaves.     

Physiological responses of spring rapeseed (Brassica napus) to red/far‐red ratios and irradiance during pre‐ and post‐flowering stages

Early shade signals promote the shade avoidance syndrome (SAS) which causes, among others, petiole and shoot elongation and upward leaf position. In spite of its relevance, these photomorphogenic responses have not been deeply studied in rapeseed (Brassica napus). In contrast to other crops like maize and wheat, rapeseed has a complex developmental phenotypic pattern as it evolves from an initial rosette to the main stem elongation and an indeterminate growth of floral raceme. In this work, we analyzed (1) morphological and physiological responses at individual level due to low red/far‐red (R/FR) ratio during plant development, and (2) changes in biomass allocation, grain yield and composition at crop level in response to high R/FR ratio and low irradiance in two modern spring rapeseed genotypes. We carried out pot and field experiments modifying R/FR ratios and irradiance at vegetative or reproductive stages. In pot experiments, low R/FR ratio increased the petiole and lamina length, upward leaf position and also accelerated leaf senescence. Furthermore, low R/FR ratio reduced main floral raceme and increased floral branching with higher remobilization of soluble carbohydrates from the stems. In field experiments, low irradiance during post‐flowering reduced grain yield, harvest index and grain oil content, and high R/FR ratio reaching the crop partially alleviated such effects. We conclude that photomorphogenic signals are integrated early during the vegetative growth, and irradiance has stronger effects than R/FR signals at rapeseed crop level.     

Growth and ethylene evolution by shade and sun ecotypes of Stellaria longipes in response to varied light quality and irradiance

Plants growing in the shade receive both low light irradiance and light enriched in far red (FR) (i.e., light with a low red (R) to FR ratio). In an attempt to uncouple the R/FR ratio effects from light irradiance effects, we utilized Stellaria longipes because this species has two distinct natural population ecotypes, alpine (dwarf) and prairie (tall). The alpine population occupies the open, sun habitat. By contrast, the prairie population grows in the shade of other plants. Both 'sun' and 'shade' ecotypes responded with increased stem elongation responses under low irradiance, relative to growth under 'normal' irradiance, and this increased growth was proportionally similar. However, only the shade ecotype had increased shoot elongation in response to a low R/FR ratio. By contrast, the sun ecotype showed increased stem elongation in response to increasing R/FR ratio. Varying the R/FR ratios had no significant effect on ethylene evolution in either sun or shade ecotype. Under low irradiance, only the sun ecotype showed a significantly changed (decreased) ethylene evolution. We conclude that R/FR ratio and irradiance both regulate growth, and that irradiance can also influence ethylene evolution of the sun ecotype. By contrast, R/FR ratio and irradiance, while having profound influences on growth of the shade ecotype, do not appear to regulate these growth changes via effects on ethylene production.     

Shade tolerance plasticity in response to neutral vs green shade cues in Polygonum species of contrasting ecological breadth

Here we examined species differences in perception and response to two distinct types of shade cue, reduced photosynthetically active radiation (PAR) with and without reduced red : far red ratio (R : FR), in Polygonum persicaria and Polygonum hydropiper, two closely related annuals of contrasting ecological breadth. We compared plasticity data for light-gathering traits from glasshouse experiments at equivalently reduced PAR under neutral shade (R : FR 1.03) and green shade (R : FR 0.702). Species shared the ability to distinguish between the two types of shade, as shown by the ability of each to respond differently to neutral vs green shade for one or more traits. However, the species' responses to these cues differed significantly. Polygonum persicaria expressed stronger shade-tolerance responses (increased leaf allocation and leaf area ratio) to reduced PAR alone than to green shade. By contrast, P. hydropiper expressed slightly less plasticity for these traits in neutral than in green shade. The pronounced plastic response of P. persicaria to neutral shade may contribute to the range of habitats this widespread species can occupy, which includes neutral-shade environments such as urban settings.     

Uncoupling light quality from light irradiance effects in Helianthus annuus shoots: putative roles for plant hormones in leaf and internode growth

An attempt has been made to uncouple the effects of the two primary components of shade light, a reduced red to far-red (R/FR) ratio and low photosynthetically active radiation (PAR), on the elongation of the youngest internode of sunflower (Helianthus annuus) seedlings. Maximal internode growth (length and biomass) was induced by a shade light having a reduced R/FR ratio (0.85) under the low PAR of 157 micromol m(-2) s(-1). Reducing the R/FR ratio under normal PAR (421 micromol m(-2) s(-1)) gave similar growth trends, albeit with a reduced magnitude of the response. Leaf area growth showed a rather different pattern, with maximal growth occurring at the higher (normal) PAR of 421 micromol m(-2) s(-1)), but with variable effects being seen with changes in light quality. Reducing the R/FR ratio (by enrichment with FR) gave significant increases in gibberellin A(1) (GA(1)) and indole-3-acetic acid (IAA) contents in both internodes and leaves. By contrast, a lower PAR irradiance had no significant effect on GA(1) and IAA levels in internodes or leaves, but did increase the levels of other GAs, including two precursors of GA(1). Interestingly, both leaf and internode hormone content (GAs, IAA) are positively and significantly correlated with growth of the internode, as are leaf levels of abscisic acid (ABA). However, changes in these three hormones bear little relationship to leaf growth. By implication, then, the leaf may be the major source of GAs and IAA, at least, for the rapidly elongating internode. Several other hormones were also assessed in leaves for plants grown under varying R/FR ratios and PARs. Leaf ethylene production was not influenced by changes in R/FR ratio, but was significantly reduced under the normal (higher) PAR, the irradiance treatment which increased leaf growth. Levels of the growth-active free base and riboside cytokinins were significantly increased in leaves under a reduced R/FR ratio, but only at the higher (normal) PAR irradiance; other light quality treatments evoked no significant changes. Taken in toto, these results indicate that both components of shade light can influence the levels of a wide range of endogenous hormones in internodes and leaves while evoking increased internode elongation and biomass accumulation. However, it is light quality changes (FR enrichment) which are most closely tied to increased hormone content, and especially with increased GA and IAA levels. Finally, the increases seen in internode and leaf GA content with a reduced R/FR ratio are consistent with FR enrichment inducing an overall increase in sunflower seedling GA biosynthesis.     

Interaction of red to far red light ratio and ethylene in regulating stem elongation of <Emphasis Type="Italic">Helianthus annuus</Emphasis>

Sunflower (Helianthus annuus L.) stems showed increased elongation under two types of vegetative shade: canopy shade (low red to far red [R/FR] ratio) and neighbouring proximity shade (FR enrichment). Hypocotyls also elongated more under narrow-band FR light than under narrow-band R light. Ethylene levels were determined in actively elongating 7-day-old hypocotyls and 17-day-old internodes under three R/FR ratios. Ethylene levels were lower in both sunflower hypocotyls and internodes when the R/FR ratio was reduced. Both FR enrichment of normal R/FR ratio and narrow-band FR light with very low light irradiance resulted in reduction in ethylene levels in 7-day-old hypocotyls. Further, in application experiments, sunflower stems grown under low R/FR ratio were more sensitive to ethephon and less sensitive to aminoethoxyvinylglycine (AVG) than stems grown under high R/FR ratio. Low R/FR ratio appears to initiate reduction in ethylene levels in sunflower seedlings, allowing maximum stem elongation. These results, and findings of other authors, suggest that various plant species may have developed different ways of regulating stem elongation and ethylene levels in response to low R/FR ratio.     

Plastic and constant developmental traits contribute to adaptive differences in co-occurring Polygonum species

Adaptive differences among species are often thought to result from developmentally constant trait differences that enhance fitness in alternative environments. Species differences in patterns of individual phenotypic plasticity can also have ecological consequences. Indeed, functionally related constant and plastic traits may interact to determine the phenotype's adaptive value in particular conditions. We compared juvenile shade avoidance traits (height and its components, internode length and node number) across two field density treatments in Polygonumpersicaria and P. hydropiper, annual plant species that co‐occur in pastures comprised of a mosaic of plant densities. We used selection analyses to test trait contributions to fitness in alternative density treatments. Seedlings of both species expressed plasticity for internode elongation in response to density; P. persicaria plants increased internode length and consequently height significantly more in high density than did those of P. hydropiper. As predicted by the shade avoidance hypothesis, increased height was adaptive for both species in high density stands, so P. persicaria plants had higher fitness in this environment. By contrast, node numbers were relatively constant across density treatments in both species: P. hydropiper seedlings consistently produced more nodes than did those of P. persicaria. This constant trait difference contributed to P. hydropiper's greater relative fitness at low density, where more nodes and hence leaves enable plants to better exploit available light. Differences between species in these juvenile shade‐avoidance traits did not result from the evolutionary constraints of lack of heritable variation or costs of plasticity. We discuss how these interspecific trait differences may have been generated by divergent selective histories resulting from differences in herbivore resistance. These results illustrate how adaptive differences in both plastic and constantly expressed traits may jointly contribute to ecological distribution, including coexistence in patchy habitats.     

PHENOTYPIC PLASTICITY EARLY IN LIFE CONSTRAINS DEVELOPMENTAL RESPONSES LATER

Abstract.— Plastic stem‐elongation responses to the ratio of red:far‐red (R:FR) wavelengths enable plants to match their phenotype to local competitive conditions. However, elongation responses early in the life history may occur at the cost of reduced plasticity later in the life history, because elongation influences both allocation patterns and structural integrity. A common‐garden experiment was performed to test whether seedling responses to R:FR affect biomass allocation, biomass accumulation, and subsequent plasticity to the cue. Seedlings of Abutilon theophrasti were stimulated to elongate by low R:FR treatments, and subsequent growth and plasticity was compared with nonelongated individuals. Elongated seedlings were less responsive than nonelongated ones to a second bout of low R:FR. Thus, seedling plasticity to R:FR reduces subsequent responsiveness to this cue. This negative association across life‐history stages suggests an important constraint on the evolution of plastic stem responses, because selection in A. theophrasti has previously been shown to favor increases in early elongation in combination with increased later elongation. The reduced responsiveness of elongated seedlings to R:FR appeared to result from a structural feedback mechanism, indicating that the opportunity cost of early responses may be lower in environments providing structural support.     

Indirect consequences of artificial selection on plasticity to light quality in Arabidopsis thaliana

Covariation between light quality- and photoperiod-mediated phenotypic plasticity was investigated using Arabidopsis thaliana. Three episodes of artificial selection were imposed on an index that quantified the plastic response to reduced red to far-red ratios (R:FR), with higher index values indicating greater plasticity. Relative to control lines, two high plasticity (HP) lines showed 1.6- and 2.4-fold increases in the index; low plasticity (LP) lines showed 1.4- and 1.1-fold decreases. A factorial experiment combining high and low R:FR conditions with long and short photoperiods assessed indirect consequences of selection on plasticity. Despite divergent R:FR-mediated plasticities in HP vs. LP lines, all four lines showed increases in photoperiod-mediated responses and decreases in mean leaf number. Complex relationships among trait means, plasticities and underlying mechanisms caution against generalizing about the genetic architecture of plastic traits. Partially independent developmental and evolutionary responses to R:FR and photoperiod are somewhat unsurprising, given this species' cosmopolitan nature.     

The Shade Avoidance Syndrome in Arabidopsis: The Antagonistic Role of Phytochrome A and B Differentiates Vegetation Proximity and Canopy Shade

Light limitation caused by dense vegetation is one of the greatest threats to plant survival in natural environments. Plants detect such neighboring vegetation as a reduction in the red to far-red ratio (R:FR) of the incoming light. The low R:FR signal, perceived by phytochromes, initiates a set of responses collectively known as the shade avoidance syndrome, intended to reduce the degree of current or future shade from neighbors by overtopping such competitors or inducing flowering to ensure seed production. At the seedling stage these responses include increased hypocotyl elongation. We have systematically analyzed the Arabidopsis seedling response and the contribution of phyA and phyB to perception of decreased R:FR, at three different levels of photosynthetically active radiation. Our results show that the shade avoidance syndrome, induced by phyB deactivation, is gradually antagonized by phyA, operating through the so-called FR-High Irradiance Response, in response to high FR levels in a range that simulates plant canopy shade. The data indicate that the R:FR signal distinguishes between the presence of proximal, but non-shading, neighbors and direct foliar shade, via a intrafamily photosensory attenuation mechanism that acts to suppress excessive reversion toward skotomorphogenic development under prolonged direct vegetation shade.     

A genome-wide association study identifies variants underlying the Arabidopsis thaliana shade avoidance response

Shade avoidance is an ecologically and molecularly well-understood set of plant developmental responses that occur when the ratio of red to far-red light (R:FR) is reduced as a result of foliar shade. Here, a genome-wide association study (GWAS) in Arabidopsis thaliana was used to identify variants underlying one of these responses: increased hypocotyl elongation. Four hypocotyl phenotypes were included in the study, including height in high R:FR conditions (simulated sun), height in low R:FR conditions (simulated shade), and two different indices of the response of height to low R:FR. GWAS results showed that variation in these traits is controlled by many loci of small to moderate effect. A known PHYC variant contributing to hypocotyl height variation was identified and lists of significantly associated genes were enriched in a priori candidates, suggesting that this GWAS was capable of generating meaningful results. Using metadata such as expression data, GO terms, and other annotation, we were also able to identify variants in candidate de novo genes. Patterns of significance among our four phenotypes allowed us to categorize associations into three groups: those that affected hypocotyl height without influencing shade avoidance, those that affected shade avoidance in a height-dependent fashion, and those that exerted specific control over shade avoidance. This grouping allowed for the development of explicit hypotheses about the genetics underlying shade avoidance variation. Additionally, the response to shade did not exhibit any marked geographic distribution, suggesting that variation in low R:FR-induced hypocotyl elongation may represent a response to local conditions.     

Costs versus risks: Architectural changes with changing light quantity and quality in saplings of temperate rainforest trees of different shade tolerance

Light requirements and functional strategies of plants to cope with light heterogeneity in the field have a strong influence on community structure and dynamics. Shade intolerant plants often show a shade avoidance strategy involving a phytochrome‐mediated stem elongation in response to changes in red : far red ratio, while shade‐tolerant plants typically harvest light very efficiently. We measured plant size, stem diameter, internode and leaf lengths in randomly chosen saplings of 11 woody species differing in their shade tolerance in both a secondary forest and an old‐growth temperate evergreen rainforest in southern Chile. We also recorded the irradiance spectrum and the diffuse and direct light availabilities at each sampling point. Significant differences were found for the mean light environment of the saplings of each species, which also differed in basal stem diameter, internode length and leaf length, but not in plant height. Both plant slenderness (plant height/stem diameter) and mean internode length increased with increasing light availability, but no relationship was found between any of these two traits and red : far red ratio. The change in plant slenderness with light availability was of lesser magnitude with increasing shade tolerance of the species, while internode change with light availability increased with increasing shade tolerance of the species. Shade tolerators afford higher costs (thicker stems and plants), which render more biomechanically robust plants, and respond more to the light environment in a trait strongly influencing light interception (internode length) than shade intolerant species. By contrast, less shade‐tolerant plants afforded higher risks with a plastic response to escape from the understorey by making thinner plants that were biomechanically weaker and poorer light interceptors. Thus, species differing in their shade tolerances do differ in their plastic responses to light. Our results contribute to explain plant coexistence in heterogeneous light environments by improving our mechanistic understanding of species responses to light.