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.     

Higher amounts of anthocyanins and UV-absorbing compounds effectively lowered CPD photorepair in purple rice (Oryza sativa L.)

Growth of a near‐isogenic line (NIL) for the purple leaf gene Pl of rice with a genetic background of Taichung 65 (T‐65) rice was significantly retarded by supplementary ultraviolet‐B radiation (UV‐B), despite the fact that the amounts of UV‐absorbing compounds and anthocyanins in NIL were significantly higher than those in T‐65. In order to understand the role of flavonoids in UV‐B induced damage protection in T‐65 and the NIL, both the (1) relationships between changes in the steady state of cyclobutane pyrimidine dimer (CPD) levels and changes in accumulation of anthocyanins and UV‐absorbing compounds in leaves with leaf age, and (2) the susceptibility to CPD induction by UV‐B radiation and the ability to photorepair CPD were examined. Although supplementary UV‐B elevated the steady state of CPD levels in leaves in both strains, the level in the leaf of the NIL was higher than that in T‐65 at any time. The susceptibility to CPD induction by short‐term (challenge) UV‐B exposure was lower in the NIL than in T‐65. On the other hand, the CPD photorepair was also lower in the leaves of the NIL than in those of T‐65. The decrease in CPD‐photorepair in the NIL was due to a lowering of the leaf‐penetrating blue/UV‐A radiation, which is effective for photoreactivation by photolyase, by anthocyanins. Thus, accumulation of anthocyanins and UV‐absorbing compounds did not effectively function as screening against damage caused by elevated UV‐B radiation in the NIL, and the retardation of growth in the NIL resulted from its lower ability to photorepair CPD by higher amounts of anthocyanins.     

The ecophysiology of foliar anthocyanin

The accumulation of foliar anthocyanins can be consistently attributed to a small range of contexts. Foliar anthocyanin accumulates in young, expanding foliage, in autumnal foliage of deciduous species, in response to nutrient deficiency or ultraviolet (UV) radiation exposure, and in association with damage or defense against browsing herbivores or pathogenic fungal infection. A common thread through these causative factors is low photosynthetic capacity of foliage with accumulated anthocyanin relative to leaves at different ontogenetic stages or unaffected by the environmental factor in question. The ecophysiological function of anthocyanin has been hypothesized as: 1) a compatible solute contributing to osmotic adjustment to drought and frost stress; 2) an antioxidant; 3) a UV protectant; and 4) protection from visible light. Review of the internal leaf distribution of anthocyanin, of experimental evidence using seedlings, and of studies that directly investigated light absorption by anthocyanin and its development relative to recognized processes of photoprotection support the hypothesis that anthocyanins provide protection from visible light.     

Ultraviolet-B Radiation-induced Inhibition of Leaf Expansion and Promotion of Anthocyanin Production: Lack of Involvement of the Low Irradiance Phytochrome System

Leaf discs from expanding leaves of Rumex patientia L. were exposed to 7 hours of visible plus different levels of ultraviolet radiation in the 290 to 315 nm waveband (UV-B) and then placed in darkness. Leaf disc expansion was reduced and anthocyanin production was increased in discs exposed to moderate or high levels of UV-B radiation when compared to control discs. The possibility that the inhibition of leaf expansion by UV-B radiation might be at least partially phytochrome-mediated was examined by giving discs brief red or far red irradiation following exposure to UV-B radiation. Brief red radiation (R) following treatment with moderate or high UV-B radiation did not alter the pattern of growth or anthocyanin production compared to discs placed in darkness following UV-B treatment. However, a posttreatment with far red radiation (FR) reduced the growth of discs subjected previously to either moderate UV-B or no UV-B irradiation to the level of growth of discs given high UV-B. FR posttreatment also decreased anthocyanin production in discs in moderate and high UV-B treatments. Effects of FR and UV-B radiation apparently do not involve the same mechanism. This was demonstrated by experiments in which FR following the UV-B treatments was in turn followed by R, which reversed the effects of the FR but did not alter the growth inhibition or increased anthocyanin production induced by moderate or high levels of UV-B radiation.     

Red : far-red light ratio and UV-B radiation: their effects on leaf phenolics and growth of silver birch seedlings

The natural variation in quantity and quality of light modifies plant morphology, growth rate and concentration of biochemicals. The aim of two growth‐room experiments was to study the combined effects of red (R) and far‐red (FR) light and ultraviolet‐B (UV‐B) radiation on the concentrations of leaf phenolics and growth and morphology of silver birch (Betula pendula Roth) seedlings. Analysis by high‐performance liquid chromatography showed that the leaves exposed to supplemental FR relative to R contained higher concentrations of total chlorogenic acids and a cinnamic acid derivative than the leaves treated with supplemental R relative to FR. In contrast, concentration of a flavonoid, quercetin 3‐galactoside, was higher in the R + UV‐B leaves than in the FR + UV‐B leaves. The UV‐B induced production of kaempferols, chlorogenic acids and most quercetins were not modified by the R : FR ratio. Growth measurements showed that the leaf petioles and stems of FR seedlings were clearly longer than those of R seedlings, but leaf area was reduced by UV‐B radiation. Results of these experiments show that exposure of silver birch seedlings to supplemental FR compared to R leads to fast elongation growth and accumulation of phenolic acids in the leaves.     

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.     

Short communication. Do anthocyanins play a role in UV protection of the red juvenile leaves of Syzygium?

The biological function of juvenile leaves pigmented with anthocyanin is poorly understood. The role anthocyanins play in UV protection was assessed in juvenile leaves of two Syzygium species (S. luehmannii and S. wilsonii) which contain high anthocyanin concentrations. HPLC was used to separate UV-absorbing anthocyanins from other soluble UV-absorbing phenolic compounds. The isolated anthocyanins (predominantly malvidin-3,5-diglucoside) contributed little to the total absorbance of UV-A and UV-8 radiation. This was because the non-acylated anthocyanins only effectively absorbed shortwave UV-B radiation and the strong absorbance by other compounds. These results suggest that the UV protection hypothesis is not valid for anthocyanins in juvenile Syzygium leaves.     

Seasonal dynamics of foliar antioxidative enzymes and total anthocyanins in natural populations of Iris pumila L.

Aims Plants in their natural habitats frequently cope with a multitude of abiotic stresses, such as high light intensity, extreme temperatures and water deficit, which often co-occur during periods of drought, especially in semi-arid and arid regions. Exposure of plants to stressful environmental conditions usually induce overproduction of reactive oxygen species (ROS) that, as highly toxic derivatives of O 2, can assault all cell macromolecules, leading to the disruption of cellular homeostasis and, consequently, the uncoupling of major metabolic processes, the photosynthesis and photorespiration. In order to minimize ROS-mediated cellular damage, plants have evolved highly efficient antioxidative defense systems that include both enzymatic and non-enzymatic components. Since abiotic stress can also operate as a strong evolutionary force that shapes adaptations in natural plant populations, the aim of this study was to examine the seasonal variation patterns of two distinct antioxidative systems, ROS-scavenging enzymes and anthocyanin pigments, in the leaf tissue of a steppe plant, Iris pumila, as expressed under contrasting light conditions that the species regularly experiences in the wild.Methods We selected two natural populations of I.pumila inhabiting the alternative radiation environments in the Deliblato Sands, a sun-exposed dune site and a woodland understory. The specific activity of three antioxidative enzymes, superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD) and the content of total anthocyanins were examined in leaves of I.pumila plants collected from each of the 31 Iris clones (17 in the exposed population and 14 in the shaded population) once during each of the three seasons, spring, summer and autumn in 2004. Specifically, a fully expanded leaf was cut from each clonal plant between 15:00 and 16:00 h, immediately frozen in liquid nitrogen and stored at ?70°C until preparation.Important findings Generally, all three antioxidative enzymes were up-regulated in summer-harvested leaves compared to their spring or autumn counterparts, as was observed for the concentration of foliar anthocyanins, indicating that strengthening of antioxidant systems was the key mechanism for long-term acclimatization of I.pumila plants to stressful environmental conditions within their natural ecological niches. When plants from contrasting radiation environments were compared, SOD and CAT activities appeared to be greater in shade-exposed than in sun-exposed leaves. Conversely, POD activity and the content of foliar anthocyanins were notably higher in foliage experiencing full sunlight relative to those developed under vegetation canopy, suggesting the synergistic function of these two molecules in protecting leaf cells against photoinhibitory and photooxidative effects of strong light.     

Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage.

Diverse flavonoid compounds are widely distributed in angiosperm families. Flavonoids absorb radiation in the ultraviolet (UV) region of the spectrum, and it has been proposed that these compounds function as UV filters. We demonstrate that the DNA in Zea mays plants that contain flavonoids (primarily anthocyanins) is protected from the induction of damage caused by UV radiation relative to the DNA in plants that are genetically deficient in these compounds. DNA damage was measured with a sensitive and simple assay using individual monoclonal antibodies, one specific for cyclobutane pyrimidine dimer damage and the other specific for pyrimidine(6,4)pyrimidone damage.     

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     

UV irradiance as a major influence on growth, development and secondary products of commercial importance in Lollo Rosso lettuce ‘Revolution’ grown under polyethylene films

The growth and production of anthocyanin, flavonoid and phenolic compounds were evaluated in Lollo Rosso lettuce ‘Revolution’ grown continuously under films varying in their ability to transmit UV radiation (completely transparent to UV, transparent above 320, 350, 370 and 380 nm and completely opaque to UV radiation). Plants were grown from seed under UV transparent and UV blocking films and destructively harvested 3–4 weeks after transplanting. Plants under a complete UV blocking film (UV400) produced up to 2.2 times more total above ground dry weight than plants under the UV transparent film. In contrast, anthocyanin content in plants under the UV blocking film was approximately eight times lower than in plants under a UV transparent film. Furthermore, there was a curvilinear relationship between the anthocyanin content and UV wavelength cutoff such that above 370 nm there was no further reduction in anthocyanin content. Fluorescence measurements indicated that photosynthetic performance index was 15% higher under the presence of UVB and UVA (UV280) than under the presence of UVA (UV320) and 53% higher than in the absence of UV radiation suggesting protection of the photosynthetic apparatus possibly by phenolic compounds. These findings are of particular importance as the potential of UV transmitting films to increase secondary compounds may offer the opportunity to produce plants commercially with increased health benefits compared to those grown under conventional films.     

Screening of visible and UV radiation as a photoprotective mechanism in plants

Prolonged exposure of plants to high fluxes of solar radiation as well as to other environmental stressors disturbs the balance between absorbed light energy and capacity of its photochemical utilization resulting in photoinhibition of and eventually in damage to plants. Under such circumstances, the limiting of the light absorption by the photosynthetic apparatus efficiently augments the general photoprotective mechanisms of the plant cell, such as reparation of macromolecules, elimination of reactive oxygen species, and thermal dissipation of the excessive light energy absorbed. Under stressful conditions, plants accumulate, in different cell compartments and tissue structures, pigments capable of attenuation of the radiation in the UV and visible parts of the spectrum. To the date, four principle key groups of photoprotective pigments are known: mycosporine-like amino acids, phenolic compounds (including phenolic acids, flavonols, and anthocyanins), alkaloids (betalains), and carotenoids. The accumulation of UV-absorbing compounds (mycosporine-like amino acids and phenolics in lower and higher plants, respectively) is a ubiquitous mechanism of adaptation to and protection from the damage by high fluxes of solar radiation developed by photoautotrophic organisms at the early stages of their evolution. Extrathylakoid carotenoids, betalains, and anthocyanins play an important role in long-term adaptation to the illumination conditions and in protection of plants against photodamage. A prominent feature of certain plant taxa lacking some classes of photoprotective pigments (such as anthocyanins) is their substitution by other compounds (e.g. keto-carotenoids or betalains) disparate in terms of chemical structure and subcellular localization but possessing close spectral properties.     

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.     

Enhanced UV-B radiation under field conditions increases anthocyanin and reduces the risk of photoinhibition but does not affect growth in the carnivorous plant Pinguicula vulgaris

The effects of enhanced UV-B radiation were investigated in the carnivorous plant Pinguicula vulgaris in a field experiment performed in Abisko, North Sweden (68° 21' N, 18° 49' E, 380 m above sea level). Potted plants were exposed to either ambient or ambient plus supplemental UV-B radiation, simulating a 15% ozone depletion. No effect was observed on either the epicuticular (external) or cellular (internal) UV absorbing capacity of the leaves. However, the anthocyanin content was more than doubled by supplemental UV-B radiation. In laboratory experiments, the anthocyanin rich, UV-B treated leaves were less susceptible to a low temperature/high light photoinhibitory treatment, as judged by in vivo chlorophyll fluorescence measurements. Yet, this potential benefit did not considerably affect the growth of the plant in the field (leaf area and dry mass, reproductive dry mass, flowering frequency, senescence rates, dry mass of winter buds). However, there was a marginally significant increase in root dry mass and in the root to shoot ratio, which may underlie the significant increase in the nitrogen content of the leaves. We suggest that P. vulgaris is resistant against UV-B radiation damage and that the possible negative effects of additional UV-B radiation on the growth of these plants may have been effectively counterbalanced by the lower risk of photoinhibition, due to the concomitant increase in anthocyanins.     

Photomorphogenetic responses to UV radiation and short-term red light in lettuce seedlings

Effects of red light (R), far-red light (FR) and UV radiation on growth and greening of lettuce seedlings (Latuca sativa L., cv. Berlinskii) have been investigated. UV-B and UV-C inhibited hypocotyl elongation and stimulated cotyledonary growth. R in combination with UV-B and UV-C partly eliminated these effects, but FR increased those and reversed the R effect. Chlorophyll accumulation was inhibited by UV-B and UV-C. In comparison with cotyledonary growth, R strengthened the UV inhibitory effect, and FR reversed this effect of R. Thus, UV and phytochrome system modify the effects of each other on hypocotyl and leaf growth in lettuce seedlings depending on the level of active phytochrome formed.     

Far-red enrichment and photosynthetically active radiation level influence leaf senescence in field-grown sunflower

Basal leaves frequently senesce before anthesis in high population density crops. This paper evaluates the hypothesis that quantitative and qualitative changes in the light environment associated with a high leaf area index (LAI) trigger leaf senescence in sunflower ( Helianthus annuus L.) canopies. Mean leaf duration (LD, time from achievement of maximum leaf area) of leaf 8 was significantly ( P < 0.05) reduced from 51 to 19 days as crop population density was increased from 0.47 to 4.76 plants m⁻². High compared to low plant population density was associated with earlier reduction in the photosynthetically active radiation (PAR) and red/far-red ratio (R/FR) reaching the target leaf. However the changes in R/FR preceded those in PAR. When the light environment of individual leaves of isolated plants growing under field conditions was manipulated using filters and FR-reflecting mirrors, LD was positively and linearly related with the mean daily PAR (MDR) received in the FR- (no FR enrichment) treatments. FR enrichment of light reaching the abaxial surface of the leaf significantly ( P < 0.05) reduced LD by 9 days at intermediate PAR levels with respect to FR-controls, but did not affect LD at the maximum PAR used in these experiments. However, when light reaching both leaf surfaces was enriched with FR, LD (for leaves receiving maximum PAR) was 13 days shorter than that of the FR- control. These results show that basal leaf senescence in sunflower is enhanced both by a decrease in PAR and by a decrease in R/FR.     

On the interaction of UV-B radiation (280–315 nm) with water stress in crop plants

Cowpea ( Vigna unguiculata L. Walp.) seedlings (3-day-old) were subjected to 4 kinds of experimental treatments: (1) control without exposure to any stress (−D-UV), (2) moderate water stress with no UV-B irradiation (+D-UV), (3) no water stress but to UV-B radiation (−D+UV). and (4)moderate water stress and exposure to UV-B (+D+UV). UV-B and drought stress in the combined form elicited beneficial effects on the morphological and growth characteristics, and a few additive inhibitory effects in some functional processes. An increase in the specific leaf weight (SLW) was observed in the combination of stresses, which could be a defence mechanism against UV-B. The combination of stresses promoted the synthesis of anthocyanins and phenolic compounds. The responses of plants to the combination of stresses indicate that during simultaneous exposure of plants to multiple stresses, one form of stress could minimize the damage by the other. The enhancement of superoxide dismutase (SOD) and catalase activities appear to serve as acclimation mechanisms to scavenge the toxic, free radicals of oxygen produced under stress conditions. However, the inhibition in nitrate metabolism was greater in the combined stresses than in either of the stresses imposed separately. The results of this study illustrate that the interaction of stresses during simultaneous multiple stress conditions brings out certain beneficial effects.     

LIGHT EFFECTS ON LEAF MORPHOLOGY IN WATER HYACINTH (EICHHORNIA CRASSIPES)

Water hyacinth leaves in natural populations vary from being long and thin-petioled to being short with inflated petioles. A variety of factors has been used experimentally to alter water hyacinth leaf shape, but what controls the development of leaf morphology in the field has not been established. We measured photosynthetic photon flux density (PPFD) and spectral distribution of radiation in a natural water hyacinth population. PPFD in the center of the water hyacinth mat was reduced to 2.7% of full sunlight, and the red to far red (R:FR) ratio was reduced to 0.28. When shoot tips of plants were exposed to artificial light environments, only plants in the treatment with a R:FR ratio comparable to that in the natural population produced leaves with long, thin petioles. Shoot tips in full sun or covered with clear plastic bags or bags that reduced light quantity without greatly altering light quality produced shorter leaves with inflated petioles. We hypothesize that the altered light quality inside a mat is a major environmental control of water hyacinth leaf morphology.     

Phytochrome photoreceptors mediate plasticity to light quality in flowers of the Brassicaceae

The family of phytochrome photoreceptors mediates stem-elongation responses to ambient ratios of red?:?far-red light (R?:?FR). Although phytochrome genes are expressed in flowers in addition to vegetative parts, nothing is known about floral plasticity to R?:?FR or the pleiotropic effects of phytochrome genes on flowers. Here, the following floral morphologies were compared: (1) wild-type Arabidopsis thaliana and Brassica rapa plants experiencing high R?:?FR characteristic of sunlight vs. low R?:?FR typical of foliar shade and (2) wild-type and phytochrome-deficient A. thaliana plants. Wild-type A. thaliana exposed to low R?:?FR had diminished petal and pistil lengths but longer filaments for a given petal size than plants experiencing high R?:?FR. Brassica rapa plants had qualitatively similar responses. In comparison to wild-type A. thaliana, mutants lacking phytochrome A had smaller flowers (smaller petals, pistils, and filaments), whereas phytochrome B-deficient mutants exhibited longer filament lengths. These results provide the first evidence that R?:?FR and phytochromes affect floral phenotypes in addition to vegetative ones. Although the ecological relevance remains to be established, the observed plasticity of flowers to R?:?FR may be relevant to individual fitness in some species because stigma and filament positions can affect pollen removal and levels of self-pollination.