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.

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.

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.

Evolutionary conservation of structure and function of the UVR8 photoreceptor from the liverwort Marchantia polymorpha and the moss Physcomitrella patens.

The ultraviolet-B (UV-B) photoreceptor UV RESISTANCE LOCUS 8 (UVR8) mediates photomorphogenic responses to UV-B in Arabidopsis through differential gene expression, but little is known about UVR8 in other species. Bryophyte lineages were the earliest diverging embryophytes, thus being the first plants facing the UV-B regime typical of land. We therefore examined whether liverwort and moss species have functional UVR8 proteins and whether they are regulated similarly to Arabidopsis UVR8. We examined the expression, dimer/monomer status, cellular localisation and function of Marchantia polymorpha and Physcomitrella patens UVR8 in experiments with bryophyte tissue and expression of green fluorescent protein (GFP)-UVR8 fusions in Nicotiana leaves and transgenic Arabidopsis. P. patens expresses two UVR8 genes that encode functional proteins, whereas the single M. polymorpha UVR8 gene expresses two transcripts by alternative splicing that encode functional UVR8 variants. P. patens UVR8 proteins form dimers that monomerise and accumulate in the nucleus following UV-B exposure, similar to Arabidopsis UVR8, but M. polymorpha UVR8 has weaker dimers and the proteins appear more constitutively nuclear. We conclude that liverwort and moss species produce functional UVR8 proteins. Although there are differences in expression and regulation of P. patens and M. polymorpha UVR8, the mechanism of UVR8 action is strongly conserved in evolution.

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.

Solar ultraviolet radiation is necessary to enhance grapevine fruit ripening transcriptional and phenolic responses.

BACKGROUND: Ultraviolet (UV) radiation modulates secondary metabolism in the skin of Vitis vinifera L. berries, which affects the final composition of both grapes and wines. The expression of several phenylpropanoid biosynthesis-related genes is regulated by UV radiation in grape berries. However, the complete portion of transcriptome and ripening processes influenced by solar UV radiation in grapes remains unknown. RESULTS: Whole genome arrays were used to identify the berry skin transcriptome modulated by the UV radiation received naturally in a mid-altitude Tempranillo vineyard. UV radiation-blocking and transmitting filters were used to generate the experimental conditions. The expression of 121 genes was significantly altered by solar UV radiation. Functional enrichment analysis of altered transcripts mainly pointed out that secondary metabolism-related transcripts were induced by UV radiation including VvFLS1, VvGT5 and VvGT6 flavonol biosynthetic genes and monoterpenoid biosynthetic genes. Berry skin phenolic composition was also analysed to search for correlation with gene expression changes and UV-increased flavonols accumulation was the most evident impact. Among regulatory genes, novel UV radiation-responsive transcription factors including VvMYB24 and three bHLH, together with known grapevine UV-responsive genes such as VvMYBF1, were identified. A transcriptomic meta-analysis revealed that genes up-regulated by UV radiation in the berry skin were also enriched in homologs of Arabidopsis UVR8 UV-B photoreceptor-dependent UV-B -responsive genes. Indeed, a search of the grapevine reference genomic sequence identified UV-B signalling pathway homologs and among them, VvHY5-1, VvHY5-2 and VvRUP were up-regulated by UV radiation in the berry skin. CONCLUSIONS: Results suggest that the UV-B radiation-specific signalling pathway is activated in the skin of grapes grown at mid-altitudes. The biosynthesis and accumulation of secondary metabolites, which are appreciated in winemaking and potentially confer cross-tolerance, were almost specifically triggered. This draws attention to viticultural practices that increase solar UV radiation on vineyards as they may improve grape features.

Effects of enhanced UV-B radiation on hydroxycinnamic acid derivatives extracted from different cell compartments in the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia.

We examined the responses of ultraviolet-absorbing compounds (UVAC) to enhanced UV-B radiation in the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia for 31 days under laboratory conditions. Samples were exposed to three radiation regimes: P (only photosynthetic radiation), PA (photosynthetic + UV-A radiation) and PAB (photosynthetic + UV-A + UV-B radiation). We measured both the bulk UV absorbance of the methanolic extracts and the levels of individual UVAC. In both cases, the methanol-soluble and the methanol-insoluble, alkali-extractable cell wall-bound fractions were analyzed. The bulk UV absorbance of the soluble fraction was higher than that of the cell wall-bound fraction. The bulk UV absorbances of both fractions increased under enhanced UV-B (PAB regime). Five different hydroxycinnamic acid (HCA) derivatives were found in the soluble fraction and two additional ones in the cell wall-bound fraction, among which only p-coumaroylmalic acid in the soluble fraction and p-coumaric acid in the cell wall-bound fraction increased under enhanced UV-B. The maximum quantum yield of PSII (F(v) /F(m)) decreased and DNA damage (amount of thymine dimers) strongly increased under enhanced UV-B, showing UV-B-induced damage. We conclude that methanol-soluble and cell wall-bound fractions of the liverwort studied have different UVAC, and each individual compound may respond in a different way to UV-B radiation. Thus, the analysis of individual UVAC in both the methanol-soluble and cell wall-bound fractions is advisable to better evaluate the protection mechanisms of liverworts against UV-B radiation. In particular, p-coumaric acid and p-coumaroylmalic acid seem to be especially UV-B responsive and merit further investigation.

Retrospective bioindication of stratospheric ozone and ultraviolet radiation using hydroxycinnamic acid derivatives of herbarium samples of an aquatic liverwort.

We analyzed bulk UV absorbance of methanolic extracts and levels of five UV-absorbing compounds (hydroxycinnamic acid derivatives) in 135 herbarium samples of the liverwort Jungermannia exsertifolia subsp. cordifolia from northern Europe. Samples had been collected in 1850-2006 (96% in June-August). Both UV absorbance and compound levels were correlated positively with collection year. p-Coumaroylmalic acid (C1) was the only compound showing a significant (and negative) correlation with stratospheric ozone and UV irradiance in the period that real data of these variables existed. Stratospheric ozone reconstruction (1850-2006) based on C1 showed higher values in June than in July and August, which coincides with the normal monthly variation of ozone. Combining all the data, there was no long-term temporal trend from 1850 to 2006. Reconstructed UV showed higher values in June-July than in August, but again no temporal trend was detected in 1918-2006 using the joint data. This agrees with previous UV reconstructions.

Physiological changes and UV protection in the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia along an altitudinal gradient of UV-B radiation.

Here we report the effects of a natural altitudinal gradient of UV-B radiation, from 1140 to 1816 m altitude, on the physiology of the aquatic liverwort Jungermannia exsertifolia Steph. subsp. cordifolia (Dumort.) Váña collected in mountain streams. Photosynthetic pigments, net photosynthesis and dark respiration rates, chlorophyll fluorescence, protein concentration, sclerophylly, and UV-absorbing compounds [both global UV absorbance of methanol-extractable UV-absorbing compounds (MEUVAC) and concentrations of five individual compounds] were measured. Two new caffeic acid derivatives were discovered: 5″-(7″,8″-dihydroxycoumaroyl)-2-caffeoylmalic acid and 5″-(7″,8″-dihydroxy-7-O-ß-glucosyl-coumaroyl)-2-caffeoylmalic acid, whereas three additional compounds were already known in other species: p-coumaroylmalic acid, phaselic acid (both compounds in their cis- and trans- forms) and feruloylmalic acid. Most physiological variables changed considerably along the altitudinal gradient, but only six showed significant linear relationships with altitude: MEUVAC levels, the concentrations of the two new secondary compounds, the maximal apparent electron transport rate through PSII (ETRmax) and the maximal non-photochemical quenching (NPQmax) increased with altitude, whereas photoinhibition percentage decreased. A principal components analysis (PCA) was conducted to rank the values of the physiological and ecological variables obtained along the altitudinal transect, showing that those variables correlated with altitude were responsible for the ordination of the sampling points. The liverwort was not adversely affected by the changing conditions along the altitudinal gradient and, in particular, by the increasing UV-B irradiance, probably because the characteristics shown by high-altitude populations may confer tolerance to high UV-B levels. The response to UV-B of the two new compounds suggests that they could be used as indicators of the spatial changes in UV-B radiation.