To What Extent Are the Effects of UV Radiation on Grapes Conserved in the Resulting Wines?

Ultraviolet (UV) radiation strongly influences grape composition, but only a few studies have focused on how this influence is conserved in the resulting wines. Here we analyzed to what extent the changes induced by exposing Tempranillo grapes to UV radiation from budbreak to harvest were conserved in wine. By using different cut-off filters and lamps, we differentiated the effects of ambient levels of UV-A and UV-B wavelengths, as well as the effects of a realistic UV-B enhancement associated with climate change. Among phenolic compounds, the most consistent responses to UV were those of flavonols (particularly quercetin-, kaempferol-, isorhamnetin- and myricetin-glycosides), which significantly increased in wines whose grapes had been exposed to a synergic combination of UV-A and UV-B radiation. This confirms that flavonols are the phenolic compounds most reliably conserved from UV-exposed grapes to wine, despite the possible influence of the winemaking process. Flavonols are important compounds because they contribute to wine co-pigmentation by stabilizing anthocyanins, and they are interesting antioxidants and nutraceuticals. Hydroxycinnamic acids also increased under the same UV combination or under UV-A alone. Wine VOCs were much less reactive to the UV received by grapes than phenolic compounds, and only esters showed significantly higher values under (mainly) UV-A alone. This was surprising because (1) UV-A has been considered to be less important than UV-B to induce metabolic changes in plants, and (2) esters are produced during winemaking. Esters are relevant due to their contribution to the fruity aroma in wines. In general, the remaining phenolic compounds (stilbenes, flavanols, hydroxybenzoic acids, and anthocyanins) and VOCs (alcohols, hydrocarbons, and fatty acids), together with wine color and antioxidant capacity, showed inconsistent or non-significant responses to UV radiation. These results were summarized by a multivariate analysis. Our study opens up new possibilities to artificially manipulate UV radiation in grapevine cultivation to improve both grape and wine quality.

Secondary metabolites and related genes in Vitis vinifera L. cv. Tempranillo grapes as influenced by ultraviolet radiation and berry development.

The effects of UV radiation on Vitis vinifera cv Tempranillo grapes were studied under field conditions as influenced by ultraviolet (UV) band (UV-A and UV-B), UV-B level (ambient vs enhanced), grape phenological stage (pea-size, veraison, and harvest), grape component (skin, flesh, and seeds), and fraction from which phenolic UV-absorbing compounds (UVACs) were extracted (soluble vs insoluble). Ambient UV-B levels caused stronger effects than ambient UV-A. These effects included increases in flavonol contents (particularly quercetins and kaempferols), the expression of flavonol synthase and chalcone synthase genes (VvFLS4 and VvCHS1), and grape weight and size. In addition, the contents of flavanols and hydroxycinnamic acids increased under UV-B radiation at pea-size stage. All these compounds play physiological roles as antioxidants and UV screens. Synergic effects between UV-B and UV-A were observed. The responses of anthocyanins, stilbenes, and volatile compounds to UV were diffuse or nonexistent. Enhanced UV-B led to rather subtle changes in comparison with ambient UV-B, but differences between both treatments could be demonstrated by multivariate analysis. Pea-size and harvest were the phenological stages where the most significant responses to UV were found, while the skin was the most UV-responsive grape component. Soluble phenolic compounds were much more UV-responsive than insoluble compounds. In conclusion, UV radiation was essential for the induction of specific grape phenolic and volatile compounds. Given the physiological roles of these compounds, as well as their contribution to grape and wine quality, and their potential use as nutraceuticals, our results may have implications on the artificial manipulation of UV radiation.

Developmental Stage Determines the Accumulation Pattern of UV-Absorbing Compounds in the Model Liverwort Marchantia polymorpha subsp. ruderalis under Controlled Conditions.

The liverwort Marchantia polymorpha subsp. ruderalis is an emerging model plant, and some data are available on its responses to ultraviolet (UV) radiation. However, it is unknown if the developmental stage of the thalli modulates the effects of UV radiation on the contents of potentially protecting phenolic compounds. To fill this gap, liverwort samples were exposed or non-exposed to UV radiation for 38 days under controlled conditions, using three developmental stages: gemmae (G), one-month thalli (T1), and two-month thalli (T2). Then, the bulk level of methanol-soluble UV-absorbing compounds and the contents of six flavones (apigenin and luteolin derivatives) were measured. The UV responsiveness decreased with thallus age: G and T1 plants were the most UV-responsive and showed a strong increase in all the variables, with G plants more responsive than T1 plants. In UV-exposed T2 plants, only apigenin derivatives increased and more modestly, probably due to a lower acclimation capacity. Nevertheless, the thalli became progressively tougher due to a decreasing water content, representing a possible structural protection against UV. In UV-exposed plants, the temporal patterns of the accumulation of phenolic compounds were compound-specific. Most compounds decreased with thallus age, but di-glucuronide derivatives showed a bell-shaped pattern, with T1 plants showing the highest contents. A Principal Components Analysis (PCA) ordination of the different samples summarized the results found. The patterns described above should be taken into account to select thalli of an adequate developmental stage for experiments investigating the induction of phenolic compounds by UV radiation.

Phenolic characteristics acquired by berry skins of Vitis vinifera cv. Tempranillo in response to close-to-ambient solar ultraviolet radiation are mostly reflected in the resulting wines.

BACKGROUND: It is widely recognized that ambient levels of solar ultraviolet (UV) radiation strongly influence the phenolic composition of grape skins. However, it is unknown to what extent this influence is reflected in the resulting wines. RESULTS: Tempranillo grapevines were exposed or non-exposed to close-to-ambient solar UV levels using appropriate filters, and the phenolic profiles and antioxidant capacity of both grape skins and the resulting wines were analyzed. In total, 47 phenolic compounds were identified in skins and wines, including flavonols, anthocyanins, flavanols, stilbenes, and hydroxycinnamic and hydroxybenzoic acids. In UV-exposed grape skins, flavonols and anthocyanins increased, whereas flavanols and hydroxybenzoic acids showed no significant change. These characteristics were conserved in the resulting wines. However, for stilbenes, hydroxycinnamic acids and antioxidant capacity, the effect of UV on grape skins was not conserved in wines, probably as a result of changes during winemaking. In addition, color intensity, total phenols and total polyphenol index of wines elaborated from UV-exposed grapes increased (although non-significantly) compared to those made from non-UV-exposed grapes. CONCLUSION: The phenolic composition of grape skins exposed to close-to-ambient solar UV could predict, to some extent, the phenolic composition of the resulting wines, particularly regarding higher contents of flavonols and anthocyanins. Thus, manipulating the UV radiation received by grape skins could improve wine quality by positively influencing color stability and healthy properties. To our knowledge, this is the first study in which the effects of solar UV radiation on phenolic composition have been assessed from grape skins to wine. © 2019 Society of Chemical Industry.

Acclimation of Bryophytes to Sun Conditions, in Comparison to Shade Conditions, Is Influenced by Both Photosynthetic and Ultraviolet Radiations.

We studied the acclimation modalities of bryophytes to sun and shade under ambient or close-to-ambient conditions, measuring variables usually influenced by photosynthetically active (PAR) and ultraviolet (UV) radiations. Our aim was to elucidate to what extent the responses to changing radiations were influenced by PAR and UV wavelengths. For this aim, we used three taxonomically and structurally different species: the thalloid liverwort Marchantia polymorpha subsp. polymorpha, the leafy liverwort Jungermannia exsertifolia subsp. cordifolia, and the moss Fontinalis antipyretica. In the field, liverworts were more radiation-responsive than the moss, and the thalloid liverwort was more responsive than the leafy liverwort. Sun plants of M. polymorpha showed, in comparison to shade plants, higher sclerophylly, lower Chl a + b contents, higher Chl a/b ratios, higher (antheraxanthin + zeaxanthin)/(violaxanthin + antheraxanthin + zeaxanthin) ratios (xanthophyll index), lower F v/F m values, higher contents of methanol-soluble vacuolar UV-absorbing compounds (soluble UVACs), higher values of the ratio between the contents of methanol-insoluble cell wall-bound UVACs (insoluble UVACs) and soluble UVACs, higher contents of soluble luteolin and apigenin derivatives and riccionidin A, and higher contents of insoluble p-coumaric and ferulic acids. Overall, these responses reduced light absorption, alleviated overexcitation, increased photoprotection through non-photochemical energy dissipation, increased UV protection through UV screening and antioxidant capacity, and denoted photoinhibition. J. exsertifolia showed moderate differences between sun and shade plants, while responses of F. antipyretica were rather diffuse. The increase in the xanthophyll index was the most consistent response to sun conditions, occurring in the three species studied. The responses of soluble UVACs were generally clearer than those of insoluble UVACs, probably because insoluble UVACs are relatively immobilized in the cell wall. These modalities of radiation acclimation were reliably summarized by principal components analysis. Using the most radiation-responsive species in the field (M. polymorpha), we found, under close-to-ambient greenhouse conditions, that sclerophylly and Chl a + b content were only influenced by PAR, F v/F m, and luteolin and apigenin derivatives were only determined by UV, and xanthophyll index was influenced by both radiation types. Thus, responses of bryophytes to radiation can be better interpreted considering the influence of both PAR and UV radiation.

Photosynthetically-active radiation, UV-A and UV-B, causes both common and specific damage and photoprotective responses in the model liverwort Marchantia polymorpha subsp. ruderalis.

We studied the effects of different radiation treatments on the physiology and UV-absorbing compounds of the model liverwort Marchantia polymorpha subsp. ruderalis. Starting from gemmae, samples were exposed to five radiation treatments: low photosynthetically active radiation (PAR), low PAR+ UV-A, low PAR + UV-B, low PAR + UV-A + UV-B, and high PAR. After 35 days, the maximum quantum yield of photosystem II was similar between treatments, which suggested comparable photoinhibition and physiological vitality, also supported by results showing an unchanged chlorophyll a/b ratio and only slight changes in growth. However, the total contents of both chlorophylls and carotenoids decreased in the UV radiation treatments and, more strongly, in the high-PAR samples, suggesting mainly PAR-dependent damage to the photosynthetic pigments. The xanthophyll index (antheraxanthin + zeaxanthin)/(violaxanthin + antheraxanthin + zeaxanthin) was only increased in the high-PAR samples, indicating an increase in photoprotection through nonphotochemical dissipation of the excess energy. The sclerophylly index (the ratio between the thallus dry mass and surface area) was increased in the UV-B-exposed samples, suggesting a UV-induced structural protection. Only the UV-B-exposed samples showed DNA damage. Several apigenin and luteolin derivatives were found in the methanol-soluble vacuolar fraction of the liverwort and p-coumaric and ferulic acids in the methanol-insoluble cell wall-bound fraction. Most individual soluble compounds, the bulk level of soluble compounds, and chalcone synthase expression increased in UV-B-exposed samples, whereas individual insoluble compounds increased in the samples exposed to only PAR. Principal components analysis summarized these responses, showing the strong influence of both UV-B and PAR levels on the physiology and UV protection of the samples.

Phenolic compounds from different bryophyte species and cell compartments respond specifically to ultraviolet radiation, but not particularly quickly.

To study the potential quick responses to ultraviolet (UV) radiation of bryophyte phenolic compounds, we cultivated two thalloid liverworts, two leafy liverworts, and two mosses under three moderate realistic UV levels in the laboratory for 22 days. At the end of the daylight period on the first and last culture days, we measured the bulk levels and individual contents of phenolic UV-absorbing compounds (UVACs) of each species, differentiating in both cases the UVACs located in the methanol-soluble (mainly vacuolar) and -insoluble (cell wall-bound) fractions (SUVACs and IUVACs, respectively). The bulk levels of SUVACs and IUVACs mostly showed linear or hyperbolic relationships with the UV dose applied. Thirteen flavones (apigenin and luteolin derivatives) and two hydroxycinnamic acids (p-coumaric and ferulic acids) were identified in the soluble and insoluble fractions, respectively. Only two compounds (p-coumaric and ferulic acids) from the insoluble fraction of the leafy liverwort Plagiochila asplenioides showed a significant quick accumulation in response to UV radiation in the first day of culture, whereas six UVACs (mainly soluble apigenin and luteolin derivatives) from different species (mainly liverworts) were significantly accumulated at the end of the culture. In conclusion, the responses of bryophyte UVACs to UV radiation were influenced by the specific compound considered, the fraction in which each UVAC was located, the global or individual way of UVACs quantification, the bryophyte species and evolutionary lineage, and the experimental conditions used. Particularly, SUVACs were more UV-responsive than IUVACs and liverworts than mosses, and responses were not especially quick.

Spores potentially dispersed to longer distances are more tolerant to ultraviolet radiation: A case study in the moss genus Orthotrichum.

PREMISE OF THE STUDY: Ultraviolet (UV) radiation influences the viability of algal spores and seed-plant pollen depending on the species, the dose, and the wavelength. In bryophytes, one of the dominant groups of plants in many habitats, UV radiation could determine their spore dispersal strategy, and such data are critical for reconstructing the ancestral state in plants and for determining the distribution range and persistence of bryophyte species. METHODS: Spores of four bryophyte species of the moss genus Orthotrichum that were either hygrochastic or xerochastic (spores dispersed under wet or dry conditions, respectively) were exposed to realistic doses of UV radiation under laboratory conditions. Spore viability was evaluated through germination experiments and, for the first time in bryophytes, ultrastructural observations. Given that the UV-B doses used were relatively higher than the UV-A doses, the UV effect was probably due more to UV-B than UV-A wavelengths. KEY RESULTS: All four species reduced their spore germination capacity in a UV dose-dependent manner, concomitantly increasing spore ultrastructural damage (cytoplasmic and plastid alterations). Most spores eventually died when exposed to the highest UV dose. Interestingly, spores of hygrochastic species were much more UV-sensitive than those of xerochastic species. CONCLUSIONS: UV tolerance determines moss spore viability, as indicated by germination capacity and ultrastructural damage, and differs between spores of species with different dispersal strategies. Specifically, the higher UV tolerance of xerochastic spores may enable them to be dispersed to longer distances than hygrochastic spores, thus extending more efficiently the distribution range of the corresponding species.

Environmental Factors Correlated with the Metabolite Profile of Vitis vinifera cv. Pinot Noir Berry Skins along a European Latitudinal Gradient.

Mature berries of Pinot Noir grapevines were sampled across a latitudinal gradient in Europe, from southern Spain to central Germany. Our aim was to study the influence of latitude-dependent environmental factors on the metabolite composition (mainly phenolic compounds) of berry skins. Solar radiation variables were positively correlated with flavonols and flavanonols and, to a lesser extent, with stilbenes and cinnamic acids. The daily means of global and erythematic UV solar radiation over long periods (bud break-veraison, bud break-harvest, and veraison-harvest), and the doses and daily means in shorter development periods (5-10 days before veraison and harvest) were the variables best correlated with the phenolic profile. The ratio between trihydroxylated and monohydroxylated flavonols, which was positively correlated with antioxidant capacity, was the berry skin variable best correlated with those radiation variables. Total flavanols and total anthocyanins did not show any correlation with radiation variables. Air temperature, degree days, rainfall, and aridity indices showed fewer correlations with metabolite contents than radiation. Moreover, the latter correlations were restricted to the period veraison-harvest, where radiation, temperature, and water availability variables were correlated, making it difficult to separate the possible individual effects of each type of variable. The data show that managing environmental factors, in particular global and UV radiation, through cultural practices during specific development periods, can be useful to promote the synthesis of valuable nutraceuticals and metabolites that influence wine quality.

Effects of ambient solar UV radiation on grapevine leaf physiology and berry phenolic composition along one entire season under Mediterranean field conditions.

In the present study we assessed the effects of ambient solar UV exclusion on leaf physiology, and leaf and berry skin phenolic composition, of a major grapevine cultivar (Tempranillo) grown under typically Mediterranean field conditions over an entire season. In general, the effects of time were stronger than those of UV radiation. Ambient UV caused a little stressing effect (eustress) on leaf physiology, with decreasing net photosynthesis rates and stomatal conductances. However, it was not accompanied by alterations in Fv/Fm or photosynthetic pigments, and was partially counterbalanced by the UV-induced accumulation of protective flavonols. Consequently, Tempranillo leaves are notably adapted to current UV levels. The responses of berry skin phenolic compounds were diverse, moderate, and mostly transitory. At harvest, the clearest response in UV-exposed berries was again flavonol accumulation, together with a decrease in the flavonol hydroxylation level. Contrarily, responses of anthocyanins, flavanols, stilbenes and hydroxycinnamic derivatives were much more subtle or nonexistent. Kaempferols were the only compounds whose leaf and berry skin contents were correlated, which suggests a mostly different regulation of phenolic metabolism for each organ. Interestingly, the dose of biologically effective UV radiation (UVBE) was correlated with the leaf and berry skin contents of quercetins and kaempferols; relationships were linear except for the exponential relationship between UVBE dose and berry skin kaempferols. This opens management possibilities to modify kaempferol and quercetin contents in grapevine through UV manipulation.

Spatial variability of ultraviolet-absorbing compounds in an aquatic liverwort and their usefulness as biomarkers of current and past UV radiation: a case study in the Atlantic-Mediterranean transition.

The spatial variability of ultraviolet-absorbing compounds (UVACs) in the freshwater liverwort Jungermannia exsertifolia subsp. cordifolia was studied in mid-latitudes (the Atlantic-Mediterranean transition) across a wide lati-altitudinal gradient, with the aim of testing the usefulness of UVACs as biomarkers of current ambient levels of UV radiation. We analysed 17 samples from streams located in the main mountain ranges of the Iberian Peninsula, differentiating methanol-soluble (SUVACs, mainly located in the vacuoles) and methanol-insoluble (IUVACs, bound to cell walls) compounds, since they represent different manners to cope with UV radiation. In both fractions, the bulk level of UVACs and the concentrations of several individual compounds were measured. In addition, we measured Fv/Fm, DNA damage and sclerophylly index (SI) as possible additional UV biomarkers. UVACs showed a high variability, probably due not only to the gradients of macroenvironmental factors (UV radiation, PAR, and water temperature), but also to microenvironmental factors inherent to the dynamic nature of mountain streams. Two soluble coumarins were positively correlated with UV levels and could be used for ambient UV biomonitoring in the spatial scale. In contrast to the variability in UVACs, the relatively homogeneous values of Fv/Fm and the lack of any DNA damage made these variables useless for ambient UV biomonitoring, but suggested a strong acclimation capacity of this liverwort to changing environmental conditions (in particular, to UV levels). Finally, UVACs of fresh samples of the liverwort were compared to those of herbarium samples collected in the same lati-altitudinal gradient. SUVACs were significantly higher in fresh samples, whereas IUVACs generally showed the contrary. Thus, IUVACs were more stable than SUVACs and hence more adequate for retrospective UV biomonitoring. In conclusion, UVAC compartmentation should be taken into account for bryophyte-based UV biomonitoring in future studies.

Effects of UV exclusion on the physiology and phenolic composition of leaves and berries of Vitis vinifera cv. Graciano.

BACKGROUND: Ultraviolet (UV) radiation induces adaptive responses that can be used for plant production improvement. The aim of this study was to assess the effect of solar UV exclusion on the physiology and phenolic compounds of leaves and berry skins of Vitis vinifera L. cv. Graciano under field conditions. Phenolic compounds were analyzed globally and individually in both the vacuolar fraction and, for the first time in grapevine, the cell wall-bound fraction. These different locations may represent diverse modalities of phenolic response to and protection against UV. RESULTS: UV exclusion led to a decrease in Fv /Fm in leaves, revealing that solar UV is needed for adequate photoprotection. Only p-caffeoyl-tartaric acid from the soluble fraction of leaves and myricetin-3-O-glucoside from the soluble fraction of berry skins were significantly higher in the presence of UV radiation, and thus they could play a role in UV protection. Other hydroxycinnamic acids, flavonols, flavanols and stilbenes did not respond to UV exclusion. CONCLUSION: UV exclusion led to subtle changes in leaves and berry skins of Graciano cultivar, which would be well adapted to current UV levels. This may help support decision-making on viticultural practices modifying UV exposure of leaves and berries, which could improve grape and wine quality.

Dynamic response of UV-absorbing compounds, quantum yield and the xanthophyll cycle to diel changes in UV-B and photosynthetic radiations in an aquatic liverwort.

We studied the diel responses of the liverwort Jungermannia exsertifolia subsp. cordifolia to radiation changes under laboratory conditions. The samples were exposed to three radiation regimes: P (only PAR), PA (PAR+UV-A), and PAB (PAR+UV-A+UV-B). The day was divided in four periods: darkness, a first low-PAR period, the high-PAR plus UV period, and a second low-PAR period. After 15 days of culture, we measured photosynthetic pigments, chlorophyll fluorescence and UV-absorbing compounds in the four periods of the day on two consecutive days. With respect to UV-absorbing compounds, we analyzed their global amount (as the bulk UV absorbance of methanolic extracts) and the concentration of seven hydroxycinnamic acid derivatives, both in the soluble (mainly vacuolar) and insoluble (cell wall-bound) fractions of the plant extracts. PAB samples increased the bulk UV absorbance of the soluble and insoluble fractions, and the concentrations of p-coumaroylmalic acid in the soluble fraction and p-coumaric acid in the cell wall. Most of these variables showed significant diel changes and responded within a few hours to radiation changes (more strongly to UV-B), increasing at the end of the period of high-PAR plus UV. F(v)/F(m), Φ(PSII), NPQ and the components of the xanthophyll cycle showed significant and quick diel changes in response to high PAR, UV-A and UV-B radiation, indicating dynamic photoinhibition and protection of PSII from excess radiation through the xanthophyll cycle. Thus, the liverwort showed a dynamic protection and acclimation capacity to the irradiance level and spectral characteristics of the radiation received.