Plant Responses to UV Blocking Greenhouse Covering Materials: A Review

: Pure polyethylene (PE) is enriched with several additives to make it a smart application material in protected cultivation, as a cover material for either greenhouses or screenhouses. When this material completely or partially absorbs ultraviolet (UV) solar radiation, then it is called UV blocking material. The current work presents a review on the e ﬀ ects of the UV blocking covering materials on crop growth and development. Despite the passage of several years and the evolution of the design technology of plastic greenhouse covers, UV blocking materials have not ceased to be a rather interesting technique for the protection of several vegetable and ornamental species. Much of the research on UV blocking materials focuses on their indisputable e ﬀ ect on reducing the activity of pests and viral-related diseases, rather than on the e ﬀ ects on the crop physiology itself. In the present paper, representative studies dealing with the e ﬀ ect of the UV blocking materials on the agronomic factors of di ﬀ erent crops are presented and discussed. The results reveal that UV blocking materials have mainly positive e ﬀ ects on the di ﬀ erent plant physiological functions, such as photosynthesis and transpiration rate, and on growth characteristics, while they might have a negative e ﬀ ect on the production and content of secondary compounds, as anthocyanins and total phenolics.


Introduction
The concern for safer food and environmental protection is increasing among consumers. Regulations on maximum residue limits in crop products are becoming stricter. Growers'/retailers' commercial contracts often demand minor pesticide use within cultivation procedure. In addition, the production cost of vegetables could be reduced by adopting techniques with limited chemical use and alternative methods for sufficient pests and diseases control. In this direction, the use of UV blocking greenhouse covering materials is aligned with the creation of an unfavorable environment for greenhouse crops' enemies. Many authors [1][2][3][4] pointed out that the use of UV blocking films as greenhouse cover leads to decreased insect population and fungal diseases. Thus, a significant number of greenhouse growers indeed uses such type of films. However, these materials also have several effects on crop growth and development. Plant responses to UVB can be photomorphogenetic and protective [5].
The country of study, the year of the study and the UV radiation region that is blocked by the different UV blocking materials referred in the current review, are presented in Table 1.

Necessary Equipment and Instruments on Testing a UV Blocking Material
To measure the UV radiation levels, specific sensors are needed, for the different wavebands. The light sensors under different UV blocking materials could be like the following:
Once the UV blocking material effect is to be investigated, it is useful to test sensors' UV light absorbance every three to six months because it is well known that this ability fades with time (authors' personal experience and unpublished data).

Effects on Photosynthesis and Respiration
In Japan, in 1993, the effect of PVC covering materials with different UV radiation transmissivities on the photosynthetic activity of tomato (Solanum lycopersicum L.) and radish (Raphanus raphanistrum L.) plants was studied [39]. They found that the carbon metabolism was always greater under the UV blocking cover, while dark respiration was found not to be promoted by the UV blocking material.
An increase in photosynthetic activity was also found in mung beans (Vigna radiata L.) [50]. Moreover, in Germany, the effect of three different UV blocking films on a broccoli (Brassica oleracea L.) crop was investigated, where higher C/N ratio values were detected under UV exclusion conditions [42]. Moreover, an increase in gas exchanges, carbonic anhydrase, Rubisco, nitrate reductase activities and total soluble protein content was found in wheat (Triticum aestivum L.) plants [34].
A decrease in the photosynthetic rate of soybean (Glycine max L.) plants was observed under UV blocking covering materials [49]. Also, decreased carbon metabolism (as photosynthetic rate), nitrogen metabolism and protein levels were observed in eggplant (Solanum melongena L.) [51].
Most of the above reports declared that UV blocking covering materials enhanced photosynthetic rate in plant species like tomato, radish, mung bean, broccoli and wheat, and had no effect in eggplant and soybean plants; while in strawberry, green and red lettuce (Lactuca sativa L.) plants, photosynthesis was suppressed. The different results may have occurred due to the fact that Photosystem II (PS II) of some plant species is more sensitive to UVB radiation [7].

Effects on Transpiration
In a study carried out in Greece, it was stated that the plant height, total leaf area and leaf number were positively affected by the lack of UV radiation [26]. They added that a plant's transpiration rate was thoroughly increased as part of their response to UV exclusion conditions.
As far as the stomatal conductance is concerned, it was found that cut roses (Rosa × hybrida) stomatal conductance was unaffected under reduced UV light conditions [54], while in wheat plants was higher under the UV blocking covers [35]. The differences noticed in stomatal conductance may be attributed to variations in UVB impact rates of diverse UV sensitivities of various species, but also signify the complexity of UV effects on stomata [5].

Effects on Germination and on Seedlings
In a study carried out in Germany, a UV open and a UV blocking plexiglass cover were compared in order to investigate their effect on sunflower (Helianthus annuus L.) growth, and it was found that the hypocotyl length was reduced by 50% under the UV blocking material [41]. Hypocotyl elongation growth is an essential step in the seed germination and a key characteristic for plant emergence, influenced by environmental conditions, phytohormones, and is varying among genotypes [64].
Moreover, the total cotyledons area and fresh weight were reduced by 70%, as well as dry weight being reduced by 8%, while seedlings cumulative stem elongation was reduced by 22% under the UV blocking covering material. Moreover, there was a 27% decrease in sunflower germination. In Japan, it was found that radish and welsh onion (Allium fistulosum L.) germination failure was higher under UV low conditions. It was also found that there was a negative effect on the germination and hypocotyl length of sunflower and blue star (Isotoma axillaris L.) under the UV blocking film [44].
Thus, according to the above, UV blocking covering materials would have a suppressive effect on the growth and development of the germination process, due to the fact that UVB radiation photons are more energetic than visible light photons and, hence, have a stronger effect on the surface of plant cells, causing the ultimate breakdown of seed coating allowing germination to occur [64].

Effects on Pigment Synthesis
During the ripening process, fruit chlorophyll content decreases while other pigments are synthesized. UV ambient light is a crucial factor for the development of many pigments such as carotenoids (i.e., xanthophyll), flavonoids (i.e., anthocyanin), and phenolics. In ripe fruits, chlorophyll still exists but in a small proportion [65]. It has been reported that a lack of UV radiation has a negative effect on pigment synthesis [66,67].
Chlorophyll in tomato and radish leaves was found decreased [39], and also it was observed that the total content of anthocyanins was reduced in eggplant plants [51]. Moreover, flavonoids (kaempferol 3-glucoside) in scots pine (Pinus sylvestris) seedlings in the subarctic region [17], and in arabidopsis (Arabidopsis thaliana L.) plants were also found reduced under UV exclusion conditions [33]. Furthermore, it was observed that total phenolics and phenolic acids content in tomato fruit were affected by cultivar and UV solar radiation [31]. The total amount of phenolic compounds in tomato fruit, as caffeic acid, as well as the content of total phenolics, were reduced by 16% for both cultivars tested, under the UV blocking cover. Lastly, a decreased concentration of total polyphenols including luteolin, quercetin galactoside and quercetin glucoside was detected in rocket salad (Eruca vesicaria L.) plants grown under a UV blocking cover [55].
In a study in the UK, the effect of two polyethylene films with various transmissivities in the UV radiation, on the phenol content and flavonoid concentration in a red lettuce crop was tested [24]. Moreover, a study carried in UK stated that total content of flavonoids (anthocyanin) and phenolic compounds were decreased under UV blocking film (red and green lettuce) [10]. The same results were also found for strawberry crops under UV blocking films [19]. In Germany, a comparative study was made regarding the total amount of bioactive compounds in greenhouse grown and open field strawberries. The total content of flavonoids, anthocyanins, and kaempferol derivatives, under the UV blocking cover was decreased by approximately 15-35% [43]. Moreover, strawberry cultivars grown under UV blocking films showed a reduction in total phenolics (ellagic acid) and flavonoid content (anthocyanin). It was also found that the main flavonoid compounds (quercetin and cyanidin) detected in Red Oak lettuce leaf were increasing with the increase in UVB radiation [56]. In China, it was reported that ambient UVB radiation results in delayed growth and development in rapeseed plants (Brassica napus L.). UV radiation seemed to inhibit photo-morphogenesis and chlorophyll production while there was an increase on carotenoid content. Moreover there was a reduction in the accumulation of UVB absorbing compounds in the leaves under the UV blocking film [38].
In India, a positive plant response in pigment synthesis of guar beans (Cyamopsis tetragonoloba L.), urad beans (Vigna mungo L.) and mung beans was detected under films with different transmissivities in UVA radiation [36]. In Argentina, the accumulation of phenolic compounds in arabidopsis was greater in plants grown under UV blocking conditions [57].
The red color parameters detected in eggplants grown under UV blocking films were positively affected, while lightness (L*) was unaffected [27]. In UK, strawberry responses under different UV blocking covering films were investigated, and found that the fruit produced under UV blocking films had higher chroma values (by 10-23%) than under UV open films [25]. In Greece, it was studied the effect of reduced UV radiation on tomato color [28]. When the color measurements took place on harvested fruits, no significant differences were found, while when the color measurements were held in vivo, they observed differences in color parameters at the later stages of maturity (light red and red stages). These ripening stages in red colored tomatoes are characterized by the synthesis of red pigmentation (lycopene and β-carotene), which is affected by the presence of UV radiation. As the authors found no differences in lycopene content, they assumed possible differences in other pigments (β-carotene, etc.) content. On the contrary, other authors showed that in tomatoes grown under pearl shade UV blocking films, the lycopene content was found to be decreased [29].
Furthermore, strawberry fruit color is correlated with UV radiation levels [53]. The values of strawberry fruit color were all reported to be significantly higher under a UV blocking cover, followed by the low UV blocking and the UV open film. Moreover, it was found that when peppers (Capsicum annuum L.) were grown under UV blocking nets they had higher concentration of phenolic compounds during storage. Moreover, higher amounts of ascorbic acid were detected under UV blocking conditions [58]. Lack of UV radiation also resulted in increase in total chlorophyll content in three tropical plants, under the UV blocking films [36]. Moreover, L*, a* and b* parameters values (in upper leaves) of red amaranth were found to be significantly higher under UV exclusion conditions [48], where L* parameters values vary between light (L* = 100) and dark (L* = 0), a* values may vary from green (a* = −50) to red (a* = 50) and b* values from blue (b* = −50) to yellow (b* = 50) [28]. Rose petal blackening and appearance of brown spots on white petal cultivars are correlated with the increase in UV radiation levels [54].
White clover showed a neutral response in chlorophyll content (Trifolium repens L.) [40], while the same was stated for cocoplum (Chrysobalanus icaco L.) leaves [18]. While in Spain, a comparative study on two strawberry cultivars (Camarosa and Ventana) under a cellulose acetate and a PE UV blocking film showed no significant differences on the antioxidant activity, the content of carbohydrates and anthocyanin [19]. Moreover, green lettuce plants, cv. Lollo Biondo, showed no phytochemical responses to different UV radiation levels and total phenolics in raspberries (Rubus idaeus L.), and blueberries (Vaccinium Cyanococcus R.) were not affected by the covering material [56].
Strawberry tree (Arbutus unedo L.) and grape vine (Vitis vinifera L.) leaves showed different responses when cultivated under different UV blocking films. On day 191, the plants that grown inside the greenhouses transferred outdoors, and at that day, the total content of flavonols was lower. Later flavonol index in grape vine plants that grow under the UV blocking film was increased significantly when these plants were moved in UV open conditions [37]. In Australia, two plastic films, a UV open and a UV blocking were tested and found a free fraction of phenols (caffeic acid), and flavonoids (cyanidin) under the UV blocking film. Moreover, in all tested sorghum (Sorghum bicolor L.) genotypes, they found higher concentrations of the bound forms of these compounds under the UV blocking film. Moreover, the antioxidant activity was lower under UV blocking treatment for all genotypes [32].
Based on the above studies, as also presented in Table 3, it can be summarized that: (a) chlorophyll content is positively (in 56% of the studies) or negatively (in 11% of the studies) affected or is unaffected (in 33% of the studies) by UV blocking covering materials, (b) flavonoid concentration and phenolic compounds were positively, negatively or not affected by UV blocking covering materials. The discrepancies that have been noticed among the results in the same pigment categories concern different plant species. However, when differences are noticed in the same species, these can be attributed to the different environmental conditions and, more specifically, to the different ambient UV radiation levels.

Effects on Plant Roots, Leaves and Stems
In Belgium, it was reported that white clover grown under a UV blocking plexiglass cover that blocked 88% of the solar UV radiation produced significantly higher root biomass (compared with a UV blocking cover that blocked the 82% of UV ambient radiation [40]), and that soybean plants grown under open field had significantly higher root weight, compared to those grown under a UV deficient environment [49].
Stem elongation in eggplant at the early stages of development was enhanced under UVB exclusion conditions [51]. In USA, it was observed that chrysanthemum (Chrysanthemum indicum L.) and goldenrod (Solidago sp. L.) plant height was slightly increased under UV blocking covers, due to an increased number of internodes, without any effect on internode length, number of branches and number of buds per branch [4], as was also the case for tomato plants under UV blocking materials [20,28]. In addition, eggplant [27] and pepper crops were taller, and had longer stems when grown under UV blocking films or nets [59]. Furthermore, the shoot length of pot rose cultivars was found to be increased by 25-35% [54]. The only exception where a neutral response of plants to UV blocking material was mentioned for cucumber (Cucumis sativus L.) and tomato plants [46].
Cucumber leaf area and dry matter were affected by UV blocking material, showing an increase when they were grown under UV exclusion conditions [52,60]. The same positive reaction was also evident in tomato [25], guar, urad and mung beans [36], eggplant [27], radish and welsh onion [44], broccoli and turnip (Brassica rapa L.) seedlings [47], soybean [49] and roses [54]. Lastly, a neutral reaction of plant leaf growth under UV blocking materials was only found in some wheat varieties [34], rapeseed [38], and pea (Pisum sativum) [45], while a negative response was stated for strawberry plants; but this parameter was not affected by the different UV blocking materials [43]. Moreover, red amaranth (Amaranthus tricolor L.) showed a decrease in the total number of leaves, total leaf area and leaf brix when grown under UV exclusion conditions [48].
The above studies regarding the effect of UV blocking material on plant height, leaf number and leaf area presented a positive or neutral response in most of the plant species tested, because of the fact that plants exposed to UV radiation show typically less elongated leaves, stems, and hypocotyls, increased branching of stems and roots, and thicker leaves [7].
A summary of the effects of UV blocking greenhouse covering materials on plant growth are presented in Table 4.

Effects on Flowering
The effect of UV blocking covering materials on flowering has not been studied extensively. In the case of white clover, it was found that there was an increase in number and biomass allocation in flowers [40]. The same results were also found in tomato plants [20].

Effects on Fruit Setting
The positive effect of UV blocking materials on fruit setting has been stated in many studies (Table 5). In Spain, it was found that the number of set fruits in tomato plants was greater under the UV blocking covering material [20]. In Greece, a higher number of marketable fruits and mean fruit weight were observed under UV blocking covering materials, while total fruit number and shape, total soluble solids, ascorbic acid, lycopene content, pH and titratable acidity were found to be unaffected, and finally injuries caused by insects were suppressed [28]. In Spain, a lower number of fruits per m 2 were found in tomato plants grown under UV exclusion conditions [21].
Crops such as eggplant [27], strawberries [25] and peppers [58] grown under UV blocking covering materials showed higher marketable yield and significantly lower weight and firmness loss in postharvest storage. In the case of strawberry plants, positive effects are present in most cases [19,25,43,53], while neutral reactions were found only in very few studies [43,53].
Evaluating the results of different reports relevant to the effect of a UV blocking material on fruit setting, the 78% of reports reported positive effect, the 11% of them negative and the remain 11% neutral response, respectively. Most of the discrepancies found on the above results are due to the different environmental conditions during the conduct of the experiments.

Effects on Yield
The positive effect of UV blocking covering materials on plant yield was first reported in tomato plants in Japan, where the fresh and dry weight of tomato fruit was found to be greater under the UV blocking cover [39]. In Spain, a 14-19% increase in tomato total yield and a 37% increase in marketable yield per plant, when tomatoes grown under the UV blocking film [21].
Furthermore, an up to 60% increase in the total yield of guar, urad amd mung beans was reported [36]. The same trend was also observed in the case of an eggplant crop where fruit weight was higher under UV blocking conditions [27]. A similar trend was also noticed in lettuce crop (cv. Constance) where fresh and dry weight increased under the UV blocking film [24]. Red lettuce (cv. Revolution) produced 40% more dry weight under complete UV exclusion conditions [22]. The same results were observed for strawberry [19] and broccoli plants [42]. Strawberries grown under UV blocking covers showed a 20-40% higher yield [19], while the opposite was reported for melon (Cucumis melo L.) and watermelon (Citrullus lanatus L.) plants, a reduction in yield under UV blocking film due to a decrease in insect activity [68].
It was reported that tomato total yield was increased under pearl shade UV blocking nets [29]. On the Qinghai-Tibetan plateau, rapeseed biomass increased about 12-20% under UV blocking films [38]. In India, it was found that wheat plants had a greater grain yield under the UV blocking films [34]. Relative results were also obtained in Ethiopia where in open field conditions pea produced more branches compared to the other UV blocking treatments and for both tested altitudes shoot elongation was affected similarly by UV radiation [45].
In Bangladesh, broccoli and turnip seedlings fresh weight was increased by 50-70%, while dry weight did not follow a similar trend and in broccoli seedlings, the highest amounts of dry matter were recorded inside the tunnels that were covered with the UV blocking film that blocked wavelengths shorter than 340 nm, while turnip seedlings' dry matter was higher in plants that grew outdoors [47].
In the case of red amaranth, fresh and dry weight were greater under UV-blocking films than under UV open films or in open field [48].
In the case of ornamental plants, the shoot length and number of leaves of three pot rose cultivars were increased (25-35% and 15-19%, respectively) under the UV blocking films, and the color of the marketable cut flowers was also optimized [54].
No differences were found on Brussels sprouts' average weight and total yield, but the quality of sprouts was significantly lower under the UV blocking cover [30]. A neutral response to UV radiation levels was also reported for strawberry [43] and tomato plants where only the total yield was unaffected while marketable yield was increased [28]. In Egypt, there are two reports concerning cucumber cultivation under UV blocking materials where a neutral response of the crop was found [52,60].
Welsh onion and radish shoot fresh weight under photoselective red and blue films (low UV levels) was found to be greater than in UV open films. Shoot dry weight was higher under red films followed by blue (UV blocking) and clear film, respectively [44].
In the USA, it was reported that soybean total pod dry weight was lower under UV exclusion conditions, while no differences were observed in total seed weight per plant, individual seed weight, number of nodes, or stem weight [49]. In Spain, it was reported a decrease in lettuce average weight grown under UV blocking nets [22].
The effect of UV blocking covering materials on plant yield was thoroughly investigated (28 relative papers). The 61% of them reported in a positive, 11% negative and 28% neutral reaction, respectively, concerning different plant species. Moreover, it was reported that the 86% of the studies revised showed an increase in shoots' fresh and dry weight-results that can be explained by the fact that higher exposure to UV radiation leads to the increased branching of stems [5] (Table 6).

Effects on Plant Earliness/Senescence
Flowering earliness and rate of fruit and crop development seems to be affected by UV blocking materials. Studies have shown that the use of UV blocking covers can delay tomato and radish leaf senescence [39]. The same was observed for eggplant plants [51].
Relative results in UK and Spain reported quicker establishment and development of strawberry crops [25] as well as a delay in ripening process [19], when the plants were grown under UV blocking covers. In addition fruit color development of the same plant was also delayed [53].
Moreover, UV blocking material had a negative effect on flowering process of pea plant [45]. Regarding the effect of UV blocking material on plant development, varied results have been emerged. As it concerns leaf aging, 33% of the relative reports showed a positive response while a 67% showed a negative. Regarding ripening, 50% of the studies reported positive response while an equal negative response was also published. Color development and flower delay were both depressed (under UV blocking material) in all the examined cases, due to the limited activity of cryptochromes, which are responsible for the plant development process [6], as shown in Table 7. Table 7. Effect of UV blocking covering material on plant Development/Earliness.

Variations of UV Ambient Radiation Levels on Evaluating Data Regarding UV Blocking Material
UV radiation levels and spatial distribution of solar UV radiation must be taken into consideration during the evaluation of the results, including the effect of the UV blocking covering material on the crop. Specifically, UV radiation levels exhibit a seasonal variation pattern within the year (Table 8).
For all these reasons, the establishment of a general rule about the response of plants in several levels of UV radiation must be related to the place and the month. It must be mentioned that higher UV radiation levels have been reported in countries near equator where the latitude is near zero, such as Ethiopia (Lat. = 6) ( Table 8). Besides that, UV radiation levels vary with the presence of clouds, haze, snow, sun position and altitude. The highest UV radiation levels on Earth can be found in: Peru, Bolivia, Chile and Argentina, where the UV index exceeds 24 [69] in high altitudes (alpine).
According to some representative studies, different responses were found for the same species when the experiments, held in different world areas. Specifically, differences have been found on the plant height of cucumber crops grown in Egypt [52] and Japan [46], although both countries exhibit equal UV radiation levels (Table 9). In detail, in Egypt, plant height was enhanced by the exclusion of UV radiation, while no differences where noticed in Japan. This can be attributed to different responses of species and cultivars to UV radiation levels, due to differences in the genetic background.
In some plant species, responses could be proportional to UV radiation levels. For example, in Germany [42], where UV radiation levels are low, flavonoid index in broccoli plants was found to be lower, in contrast with broccoli plants grown in Bangladesh [47], where UV radiation is higher. Similar responses were noticed in the case of strawberry plants' fresh weight, in experiments conducted in Spain [19] and Germany [43], and in ripening process delays of the same plant, comparing the findings in Spain and the UK [23].
Accordingly, the countries examined in this paper are gathered in five categories regarding UV radiation levels (Table 9).

Concluding Remarks
Summarizing the results concerning plant responses on UV blocking material worldwide, it was found that the most examined parameter is the effect of these materials on plant pigments (32 papers), followed by yield (28 papers) and leaf area (25), while the least examined plant organs are roots and flowers (2 papers).
Based on these results, a strong positive or negative effect emerged in chlorophyll or phenolic compounds, respectively, under UV blocking materials, while a more dim response was also reported for flavonoid and carotenoid compounds.
The plant functions that are most affected by UV blocking materials are either enhanced in cases of photosynthesis (found in more than 50% of 9 relevant reports) in plant species such as tomato, radish, mung bean, broccoli and wheat, or in cases of stomatal conductance (wheat), or transpiration. Plant height and leaf area seem to be positively affected by UV blocking cladding materials. The same is evident also for yield and growth characteristics. However, UV blocking materials suppress the total antioxidant content and other health related phytochemicals, and this is considered by many researchers as the basic disadvantage of this material.
Even though there is a decrease in insecticide use, a decreased pest population enters into greenhouses or nethouses [62]. If other chemicals are applied to plants during the growing season, then these residues on fruits that have been produced under UV blocking conditions are characterized by a more consistent retention [63] after harvest. Lastly, the application of UV blocking materials creates a particular light modification in the plant environment which leads to a better canopy light use efficiency [69].
Author Contributions: Conceptualization, N.K. and C.P.; data curation, A.B. and C.P.; writing-original draft preparation, A.B. and C.P.; writing-review and editing, N.K. and C.P.; supervision, N.K.; project administration, N.K.; funding acquisition, N.K. All authors have read and agreed to the published version of the manuscript.
Funding: This research has been co-financed by the European Union and Greek national funds through the Operational Program Competitiveness, Entrepreneurship and Innovation, under the call RESEARCH-CREATE-INNOVATE (project code: T1EDK-01499).

Conflicts of Interest:
The authors declare no conflict of interest.