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Article

Responses to Solar UV-B Exclusion and Drought Stress in Two Cultivars of Chestnut Rose with Different Leaf Thickness

by
Dapeng Luo
1,
Jielin Li
2,
Jianxun Luo
3,
Yan Ma
4,
Yongzhi Wang
5,
Wei Liu
2,
Lucas Gutierrez Rodriguez
2 and
Yinan Yao
2,*
1
Sichuan Academy of Environmental Sciences, Chengdu 610041, China
2
College of Life Science and Engineering, Southwest University of Science and Technology, Mianyang 621010, China
3
Institute of Forestry, Sichuan Academy of Forestry, Chengdu 610081, China
4
College of Horticulture and Landscape Architecture, Jinling Institute of Technology, Nanjing 211100, China
5
College of Life Sciences, Guizhou University, Guiyang 550025, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(1), 50; https://doi.org/10.3390/f14010050
Submission received: 6 October 2022 / Revised: 8 December 2022 / Accepted: 16 December 2022 / Published: 27 December 2022
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

:
Plants adopt a series of strategies to tolerate solar UV-B radiation (with the side effects of growth reduction), but the positive effects of solar UV-B radiation have not been yet clarified. In this study, two cultivars with different leaf thickness for Chestnut rose (Rosa roxburghii Tratt), a pioneering species for ecological restoration in Karst region of Southwest China, were employed to investigate its responses to ultraviolet-B (UV-B) exclusion, moderate drought, and their combination in an outdoor experiment. Thin-leaf cultivars (Gui 2) adopt an opportunistic growth strategy, growing better than Gui 7 under UV-B exclusion combined with well-watered conditions. To avoid the penetration of solar UV-B wavelengths into the underlying leaf tissues, Gui 2 exhibited higher enhancements in leaf thickness, palisade/spongy tissue ratio, antioxidant responses such as the leaf concentration of flavonols compounds catalyse activity under solar UV-B exposure. Moreover, ambient solar UV-B radiation alleviated the adverse impact caused by drought in both cultivars, improving total biomass and reducing membrane penetration. This alleviation may be related with two potential explanations. First, solar UV-B radiation primes chestnut rose plants with increased antioxidative capacity against drought stress, shown in both antioxidative enzyme activity and non-enzyme antioxidants (in particular, with total flavonols and flavonol ratio [(quercetin+myricetin)/kaempferol]). Second, to avoid nutrition insufficiency, solar UV-B radiation and drought endows chestnut rose plants with complementary effects on nutrition balance. Overall, solar UV-B radiation helps the chestnut tolerate drought stress that occurs frequently in the Karst region by modulating its antioxidative capacity and nutrition balance.

1. Introduction

The effects of enhanced UV-B radiation due to the depletion of the stratospheric ozone have been extensively studied on a range of terrestrial plants [1,2]. However, only a few studies have used the method of UV-B exclusion to determine the effects of prevailing solar UV-B radiation on plants [3,4]. Solar UV-B radiation is an important environmental factor that influences growth, competition, and physiology of plants [5]. Searles et al. observed that ambient levels of UV-B reduced biomass and seedling height of shade-tolerant trees [6]. Hunt and McNeil found that present-day levels of solar UV-B radiation increased leaf number and mid-day photoinhibition in beech seedlings [7]. Rozema et al. also found that UV-B radiation would change the status of the arbuscular mycorrhiza plant and affect nutrient availability, in particular, phosphorus and nitrogen [8]. Moreover, plant responses to UV-B radiation depend upon concomitant stresses. Previous studies showed that water deficit might exacerbate or decrease UV-B effects [9]. Meanwhile, earlier studies reported that UV-B alleviated drought stress due to changes in epidermal anatomy [10] and an increase in carbon assimilation [11]. However, the knowledge of such interactions is still elusive, and their underlying mechanism is not yet understood. Under the protective conditions of garden plants, solar UV-B radiation is generally excluded and thus the plant characteristics are changed in growth, pigment, and photosynthetic as well as photochemical parameters, and plants are more sensitive to other stresses such as drought and pest infection [11,12]. Here we hypothesize that ambient UV-B radiation endows plants with priming effects against environmental challenges.
The sensitivity of plants to UV-B radiation largely depends on their ability to evolve protecting mechanisms, involving alterations both in leaf morphology/anatomy and leaf biochemical traits [12,13]. One important protective mechanism is attenuating harmful UV-B radiation by changes in leaf anatomy. Increase in leaf thickness due to expansion in the number of cells is common under UV-B stress [9,14,15], which enlarges the cell wall surface area and prevents UV-B radiation from reaching the abaxial photosynthetically active mesophyll. A second layer and even third additional palisade layer formed due to supplemental UV-B in coffee plants [16] and in mutant of Arabidopsis thaliana [17]. Another important mechanism is screening out UV-B radiation by accumulation of flavonoids or other UV-absorbing compounds in the leaf epidermis [18]. When the unscreened UV-B radiation enters the photosynthetically active mesophyll, high levels of oxidative pressure will occur. An additional third important mechanism unfolds, i.e., the initiation of enzymatic and nonenzymatic antioxidative defense systems, resulting in mitigating UV-B induced damages. In addition, Xu et al. observed that the soybean genotype with lower levels of flavonoid compounds exhibited higher activity of the antioxidative enzymes than the other genotype [19]. However, the extent of these mechanisms, or whether there is a trade-off among them, is still poorly understood.
Chestnut rose (Rosa roxburghii Tratt) is a species belonging to the Rosaceae family, which has been recently labeled as a new promising crop in East Asia, its fruits presenting high levels of vitamin C and superoxide dismutase [20]. The species has been introduced to America and Europe. In addition, the majority of this species is distributed across the Karst region and has been widely used as a pioneering species in forest ecological restoration in such regions, where different cultivars have evolved long-term adaptation leaf traits, showing variation in leaf thickness and palisade tissue thickness. During its growth period, Chestnut rose suffers a long-term water deficit typical of the Karst region and high level of sunshine UV-B radiation. We hypothesize that plant cultivars with higher leaf thickness would be more tolerant to environmental stress, such as drought and UV-B radiation. On the other hand, the Chestnut rose is a calciphile species, and how it retains ion homeostasis under UV-B and drought is an important research question. In this study, two cultivars of Chestnut rose with different leaf traits were employed to compare their responses to drought and UV-B exclusion, as measured in biomass accumulation, nutrition uptake, and physiological properties. The objectives of our study are: (1) To evaluate inter-cultivar differences in the responses to drought and UV-B exclusion in two genotypes of Chestnut rose with different leaf thickness; (2) To evaluate the potential interaction effects between drought and UV-B exclusion; (3) To clarify how the different protective mechanisms cooperate to mitigate the induced damage caused by UV-B and drought.

2. Materials and Methods

2.1. Plant Materials and Experimental Design

Cuttings of two cultivars of R. roxburghii, Gui 2, and Gui 7 were screened from similar environmental conditions in Guizhou province in Southwest China (26°57′ N, 106°71′ E, 1200 m.a.s.l, average 8.20 kJ m−2 day−1 UV-B dose in summer, annual rainfall, 1450 mm). Gui 7 has a higher thickness in terms of both leaf cross section and leaf palisade tissue as compared with Gui 2. On February 2nd, cuttings of a uniform size (24–28 cm in height, 0.5–0.6 cm in basal stem diameter) were selected and transferred into 5 L plastic pots filled with homogeneous natural soil, locating two plants in each pot. The soil had 4.21% organic matter, 132.0 mg kg−1 available N, 107.3 mg kg−1 available P and 123.0 mg kg−1 available K, with pH 7.23.
Forty-eight pots of each cultivar were randomly divided into four groups, which were exposed to four different treatments, 3 replicates for each treatment. Each treatment included twelve pots, one replicate containing 4 pots of plants. Additionally, pots were rotated in order to minimize differences in microenvironment.
The four treatments in our study were: (1) Ambient UV-B radiation and well-watered condition (control); (2) UV-B exclusion and well-watered condition (-UV-B); (3) Ambient UV-B radiation and drought condition (D); (4) UV-B exclusion and drought condition (-UV-B+D). In the well-watered treatment, all pots were watered to 80% of field capacity, equally with 38.0% of soil water content, by supplying an amount of water equal to transpiration losses. In the drought treatment, all pots were maintained at 45% of field capacity, and with 25.0% of soil water content. Evaporation from the soil surface was prevented by enclosing the pots in plastic bags tied to the stems of the plants. Transpiration water loss was measured gravimetrically by weighing all pots every three days.
UV-B radiation exclusion (-UVB, 0.03 kJ m−2 day−1 UV-B) and ambient UV-B radiation (average 7.50 kJ m−2 day−1 during growth duration) were created by the frames covered by different plastic films in the top to exclude or transmit solar UV-B radiation, totally 12 frames (blocks) including six blocks for UV-B exclusion and the other six blocks for ambient UV-B radiation. Four pots for each replicate in each treatment were assigned to two blocks with similar UV-B treatment (because the blocks for solar UV-B transmission or exclusion were small and not containing one replicates in one block). Each frame (3.5 × 3.0 × 1.5 m) was made of light alloyed metal and erected with four sticks (stuck deep into the soil) and a roof with parallel rails spaced at 0.75 m intervals as described by Yao et al. [21]. The frame roof was covered with 0.038 mm Teflon plastic film (Chengguang Chem, Zigong, China) or 0.08 mm polyester film in order to provide differing UV-B radiation environments. Teflon film was used to provide ambient solar UV-B radiation (ca. 84%–88% transmittance of solar UV-B radiation), and polyester film was used to absorb all UV-B radiation (below 315 nm). PAR under the plastic filters was ca. 87%–93% of ambient with Teflon and ca. 80%–90% of ambient with the polyester film [21]. Solar UV and visible irradiance were measured at plant level by HR2000CG-UV-NIR high-resolution composite-grating spectrometer (Ocean Optics Inc., Dunedin, FL, USA), and the transmittance of UV-B and PAR for polyester and Teflon plastic film were determined according to standard test method for haze and luminous transmittance of transparent plastics [22]. The roofs were designed in such a way that they were easy to disassemble for weekly cleaning of the Teflon and polyester film and then to reassemble, and the films were replaced every 4 weeks throughout the growing seasons from March 1st to August 30th. The solar UV-B intensity in our study was determined at plant level by USB2000 Fibre Optic spectrometer (Ocean Optics Inc., Dunedin, FL, USA) with CC-3-UV Cosine Corrector.
All treatments started on March 1st and ended on August 30th. Fully expanded leaves (2nd–3rd leaves in the main vein) were randomly sampled for anatomical and physiological measurements at harvest time. Leaf samples for each cultivar/treatment combination in each block were pooled before measurements. Therefore, each tested index had three replicates.

2.2. Determination of Plant Biomass, Leaf Thickness, and Palisade/Spongy Layer Ratio

At the end of the experiment, the above-ground parts were collected and were oven-dried at 105 °C for 15 min, then incubated at 80 °C for 24 h to a constant weight and weighed. Anatomical tissue measurements were performed on six healthy mature leaves obtained from the third and fourth fully expanded leaf from the top branch and collected at the end of the experiment. The thickness of leaf, the palisade, and spongy layer were measured by Image J [23], which was connected to a light microscope. Sections were taken from the middle of the leaves to avoid differences in thickness due to variations along the leaf.

2.3. Determinations of Membrane Permeability (MP), Free Proline, and Ascorbic Acid

Leaf membrane permeability was measured by electrolyte leakage according to Zheng et al. [24]. For each treatment, about 2.0 g youngest (1st and 2nd) fully expanded leaves were transferred to 10 mL distilled water and shaken for 6 h with an interval every 20 min by using an oscillator. After standing for 3 h, the absorbance of the supernatant at 264 nm was measured using a UV spectrophotometer, since non-electrolytes (such as amino acids and polysaccharides) of most plant materials have an absorption peak at 264 nm, and the MP was measured as the increase of absorbance in 264 nm (unit: OD264 nm g−1 h−1). The whole fully expanded leaves were frozen by liquid nitrogen and then ground to powder for the analysis of proline and ascorbic acid. Free proline content was measured according to the method of Bates et al. [25]. An amount of 0.5 g leaf powder was homogenized in 3% aqueous sulphosalicylic acid and the homogenate was then centrifuged. The reaction mixture consisted of 2 mL supernatant, 2 mL acid ninhydrin, and 2 mL of glacial acetic acid, which was boiled at 100 °C for 1 h. After the completion of reaction in ice bath, the reaction mixture was extracted with 4 mL of toluene, and the absorbance was read at 520 nm. Proline contents were derived from a standard curve. The extraction and determination of ascorbic acid (Asa) was followed by DCPIP method as described by Yao et al. [14].

2.4. Measurement of Total Nitrogen, Total Phosphorus and Mineral Concentration in Plants

Leaf samples were dried to constant weight at 70 °C for 24 h, and then ground to fine powder. Nitrogen was measured by the micro-Kjeldahl method and Phosphorus by the Vanadate–molybdate method [26,27]. The leaf K concentration was extracted by NH4OAc solution and determined by flame photometry [26]. For analysis of other mineral elements, the dried leaf tissue was ground, weighed, and then digested using a microwave sample preparation system. An amount of 1g sample powder was digested with a solution containing 4 mL HNO3 (71% w/w) and 1 mL of HCl (32% w/w), and then the digested sample was measured by atomic absorption spectroscopy.

2.5. Antioxidant Enzymes Activity

The youngest (2nd–3rd) healthy fully expanded leaves in each replicate were randomly sampled for antioxidant enzymes activity analysis. The sampled leaves were shock-frozen in liquid nitrogen and stored in −68 °C freezer. The frozen leaves were ground to powder. An amount of 1.0 g leaf powder was extracted by 3 mL of 50 mmol/l sodium phosphate buffer (pH 7.8) including 1.0 mmol/l EDTA and 2% (w/v) polyvinylpyrrolidone. The homogenate was centrifuged at 5000 g for 10 min, and the supernatant was used for the enzymatic assays. Superoxide dismutase (SOD) activity was assayed by monitoring the inhibition of photochemical reduction of nitro blue tetrazolium (NBT). One unit of SOD activity was defined as the amount of enzyme required to cause 50% inhibition of the reduction of NBT as monitored at 560 nm. The catalase (CAT) activity was measured according to the method of Beer and Sizer [28]. The reaction mixture (1.5 mL) consisted of 100 mmol/l phosphate buffer (pH 7.0), 0.1 mmol/l EDTA, 20 mmol/l H2O2, and 50 µL enzyme extract. The reaction was started by addition of the enzyme extract. The decrease in H2O2 was monitored at 240 nm and quantified by its molar extinction coefficient; one activity unit was expressed as the amount of H2O2 decreased per min and per gram of fresh weight. The peroxidase (POD) activity was determined in a 4 mL reaction mixture containing 1 mL of enzyme extract, 3.35 mM H2O2, 0.05% (v/v) guaiacol, and 100 mM sodium phosphate buffer (pH 6.0). The rate of increase in absorbance was measured at 470 nm within 2 min. A unit of POD activity (DA470) was defined as the change in absorbance per minute and per gram fresh weight (FW) of the tissue.

2.6. Quantitative Flavonoid Analysis

After six months of treatment, and prior to the final harvest, the plant material was sampled for flavonoid analysis according to Sultana et al. [29] and Tokusoglu et al. [30]. An amount of 3 g of 3rd to 5th fully expanded leaves in the top branch of each replicate were collected, frozen in liquid nitrogen and stored at −80 °C. Each sample was subsequently ground in liquid nitrogen and stored at −80 °C until analysis. Extraction/hydrolysis of flavonols was carried out following the method of Tokusoglu et al. [30]. Acidified methanol (25 mL) containing 1% (v/v) HCl and 0.5 mg mL−1 tertiary butylhydroquinone (TBHQ) was added to each plant sample (1 g). An amount of 5 mL HCl (1.0 M) was added, and the mixture was stirred at 90 °C under reflux for 2 h to obtain aglycons of flavonol glycosides. The extract was cooled to room temperature and centrifuged at 1500 g (5000 rpm) for 10 min. The upper layer was taken and sonicated for 5 min, to remove air. The final extract was filtered through a 0.45 mL (Millipore) filter, before injecting into HPLC. Analytical HPLC was conducted using a Shimadzu-20AT HPLC solvent delivery system and determined by Shimadzu photodiode array detector. Chromatography was carried out on a Shim-pack CLC-ODS with a gradient solvent system comprising solvent A [1.5% H3PO4] and solvent B [HOAc-CH3CN-H3PO4-H2O (20: 24: 1.5: 54.5)], then mixed using a linear gradient starting with 80% A, and decreasing to 33% A at 30 min, 10% A at 33 min, and 0% at 39.3 min. The concentrations of quercetin, myricetin, and kaempferol were determined by calibration with the standard. The concentration of total flavonol was the sum of quercetin, myricetin, and kaempferol. The flavonol ratio [(quercetin+myricetin)/ kaempferol] was also calculated.

2.7. Statistical Analysis

Analyses were performed with the software Statistical Package for the Social Science (SPSS) version 13.0. Data were log-transformed where necessary to ensure the assumptions of normality and homogeneity of variances. The main effect of cultivar, UV-B, and drought on all parameters were tested using three-way ANOVA. Individual treatment means were compared using the LSD (least significance difference) test.

3. Results

3.1. Leaf Properties and Total Biomass

As shown in Figure 1, the chestnut rose cultivars Gui 7 exhibited higher leaf thickness (Figure 1A), but its leaf palisade/spongy tissue ratio, an important leaf structure, showed a similar level with cultivars Gui 2 under the control condition (ambient solar UV-B radiation; Figure 1b). In cultivars with thin leaves (Gui 2) leaf characteristics responded sensitively to solar UV-B radiation, whereby leaf thickness and palisade/spongy ratio reduced their values when solar UV-B was excluded (either under well-watered or under drought conditions; Figure 1A,B), but no changes in leaf thickness were observed in the cultivars of thicker leaves (Gui 7). Under mild drought, leaf palisade/spongy tissue ratio was reduced in both cultivars with ambient UV-B radiation and was further reduced under the UV-B exclusion condition (Figure 1b).
The biomass of both cultivars increased by UV-B exclusion under well-watered conditions, but was reduced by mild drought stress under ambient UV-B condition and further reduced when UV-B was excluded (Figure 1C). That is, the solar UV-B radiation moderated drought effects on total biomass in two cultivars.

3.2. Leaf Membrane Permeability, Proline and Ascorbic Acid Concentration

Leaf membrane value and leaf proline content were significantly affected by cultivar, UV-B, drought, and their interactions (Table 1). UV-B exclusion significantly decreased tissue electric conductivity (EC), a membrane permeability trait, under well-watered conditions, in particular in Gui 2, but increased significantly under drought in both cultivars (Figure 2A) which was what demonstrated that solar UV-B radiation moderated drought effects. Mild drought reduced EC under an ambient UV-B condition and increased EC under a UV-B exclusion condition.
Drought caused a significant accumulation of proline in both cultivars, either under ambient UV-B conditions or under UV-B exclusion. Thin leaf cultivars (Gui 2) were more responsive than the other cultivars to drought, resulting in an increase in proline levels. In contrast, UV-B exclusion induced a significant decrease in proline under both water regimes in Gui 7, but had little impact in Gui 2 (Figure 2B). UV-B exclusion decreased ascorbic acid (Asa) concentration only under drought conditions in Gui 2, but had little effect in Gui 7 (Figure 2C). Mild drought reduced Asa concentration only under UV-B exclusion conditions for both cultivars.

3.3. Flavonoid Compounds

Included in the group of non-enzymatic antioxidants, leaf flavonol derivatives were analyzed. Specifically, we focused on flavonol aglycones after acid hydrolysis in the chestnut rose, where the major flavonol compounds were kaempferol (K), quercetin (Q), and myricetin (M); with the later Q and M being dihydroxylated and trihydroxylated flavonoids in B-ring and the former K being their monohydroxylated counterpart. UV-B exclusion significantly decreased flavonol concentrations in both water regimes for two cultivars, especially in thin-leaf cultivars (Gui 2) and, meanwhile, the decrease was stronger in well-watered conditions than in drought (Figure 3a). On the contrary, drought significantly increased the concentration of total leaf flavonol derivatives. Gui 2 also showed a high total flavonol concentration under well-watered conditions.
The (myricetin+quercetin)/kaempferol ratio [(M+Q)/K] was significantly reduced by UV-B exclusion under well-watered conditions in both cultivars and was only reduced under drought conditions in thin-leaf cultivars (Gui2). Mild drought increased the (M+Q)/K ratio in both cultivars placed under UV-B exclusion conditions, and only increased this ratio under ambient UV-B condition in Gui 2 (Figure 3b).

3.4. Antioxidant Enzymes Activity

UV-B radiation and drought produced various effects on different antioxidant enzymes (Table 1, Figure 4). Despite the isolated drought stress causing little effects on SOD activity, when combined with UV-B exclusion, drought significantly decreased SOD activity, highlighting significant drought × UV-B exclusion interaction effects in both cultivars (Figure 4A). As for CAT activity, it significantly decreased by UV-B exclusion in both cultivars under both water regimes, and was more responsive in Gui 2 than in Gui 7 (Table 1, Figure 4B). POD activity was profoundly reduced by drought in both cultivars (Table 1, Figure 4C), but was not affected by mild drought.

3.5. Plant Nutrition

Leaf N and P concentrations were increased by UV-B exclusion treatment in both cultivars, but these two major nutrient concentrations were significantly reduced by drought when solar UV-B radiation were excluded, although they were not affected under ambient UV-B radiation. Leaf K concentration was significantly affected by UV-B exclusion in both cultivars (Table 2), but was not affected by drought. Leaf Ca concentration significantly increased under UV-B exclusion or mild drought in both cultivars, and further increased with their combination. Opposite to the case of Ca2+ concentration, leaf Mg concentration ([Mg]) decreased under solar UV-B exclusion treatment in both cultivars, and somehow also decreased under drought (Gui 7, not significant) and was further reduced by drought and UV-B exclusion combination.
On the other hand, various changes in microelement concentrations were detected in both cultivars (Table 2). Compared with Gui 7, Gui 2 had higher values in Fe and Zn. UV-B exclusion significantly increased Fe concentration levels as well as Zn concentration levels in both cultivars only under well-watered conditions, whereas no consistent changes were observed under drought conditions or under the combination of drought × UV-B exclusion between those two cultivars for [Fe] and [Zn]. Leaf Mn concentration was not affected by UV-B exclusion or drought alone but increased by drought under UV-B exclusion conditions. Compared to the control, it was only under the combination of drought and UV-B exclusion that [Mn] decreased in Gui 2, whereas Gui 7 increased under either their separate or combined effects. These contrasting results between Gui 2 and Gui 7 show different cultivar × treatment interaction effects. Cu concentration levels were increased under UV-B exclusion condition in two cultivars, and whether drought was applied or not.

4. Discussion

4.1. Complementary Effects of Antioxidant Property and Leaf Traits against UV-B and Drought Stress

In the present study, the thin-leaf chestnut rose cultivars (Gui 2) reached higher biomass and lower membrane permeability (MP) under non-stress conditions (-UVB; combined UV-B exclusion and well-watered condition); meanwhile, Gui 2 performed with lower biomass and higher MP under solar UV-B radiation and also under combined solar UV-B radiation with drought stress. This implies that the thin-leaf cultivars (Gui 2) take an opportunistic growth strategy, and it merits to understand how it responds to the environment conditions.
Many studies on leaf anatomy documented UV-B-induced thickness of lamina and palisade parenchyma in European aspen, Quercus rubra, Coffea arabica, Coffea canephorcucumber, Brassica napus [13,16,3132,33]. These increases in leaf and palisade parenchyma thickness might be due to expansion in cell numbers and greater cell elongation, which in turn, decrease the penetration of UV-B wavelengths to underlying tissues [34]. Previous studies on white clover and buckwheat also documented that plant tolerance to UV-B was positively related with their leaf thickness across different genotypes [9,15] (Hofmann et al., 2003; Yao et al., 2007 and 2008). Therefore, the increment of leaf thickness and leaf palisade/spongy tissue ratio help the thin-leaf cultivars (Gui 2) to tolerate solar UV-B radiation.
Osmoprotectant proline accumulation in response to drought stress has been frequently reported [35,36]. In our study, a greater increase in proline was observed in Gui 2, showing that Gui 2 is more responsive to drought than Gui 7 against osmotic pressure. On the other hand, UV-B exclusion also had a significant effect on proline decrease in Gui 7. According to Alexieva et al. [37], the removal of excess H+ that results from proline synthesis may have a positive effect on the reduction of the UV-B-induced damage. The different changes in proline contents indicate intra-specific responses.
Accumulation of flavonoids is a widely reported response to UV-B radiation that has been linked to UV-B absorption and radical scavenging [38]. We have also observed a decrease in flavonol derivative concentrations under exclusion of solar UV-B radiation (Figure 4a), as consistent with an earlier study in lettuce [39]. On the other hand, Morales et al. [40] reported a decrease in flavonoid concentration due to the lower expression of PAL and HYH genes. An earlier study showed that flavonoid content could be stimulated under high osmotic pressure [41]; an effect that in our study was also present when both cultivars were under UV-B exclusion conditions. Solar UV-B radiation, a major environmental factor on the synthesis of flavonoid compounds, modulated the drought effects on flavonol concentration in Chestnut rose, so that little enhancement by drought was observed in both cultivars. Furthermore, partly due to low leaf thickness, solar UV-B radiation caused higher enhancement of total flavonoid concentration in Gui 2, which could function in screening harmful UV-B radiation into the sensitive photosynthetic tissue to offset the shortage of thin leaf blades. A previous study demonstrated that the red lettuce with rich flavonoid compounds was less affected by ambient solar UV-B radiation in plant growth and photosynthetic parameters [38,41].
An increasing number of studies point out that differential UV-B favors B-ring-dihydroxylated or B-ring-trihydroxylated flavonoids over their monohydroxylated counterparts. This effect of UV-B has so far been found in rice, Petunia, and Brassica napus, what results in enhanced quercetin/kaempferol glycoside ratio [32,42]. Our study conforms with the evidence presented in these studies, as shown by the higher (M+Q)/K ratio [(myricetin+quercetin)/kaempferol ratios] found under either solar UV-B radiation or drought treatment, due to positive effects on myricetin and quercetin. Quercetin, myricetin, and kaempferol are respectively B-ring-dihydroxylated, B-ring-trihydroxylated, and B-ring-monohydroxylated flavonoids. Montesinos et al. [43] demonstrated a higher free radical antioxidant activity in ortho-dihydroxylated and ortho-trihydroxylated flavonoids, relative to their monohydroxylated equivalents. Therefore, the higher (M+Q)/K ratio is an important strategy against oxidative stress under drought or ambient UV-B condition.
It is well known that SOD quench O2.- to H2O2, and H2O2 can be further reduced to H2O by CAT, APX, or POD. In the present study, solar UV-B radiation increased SOD and CAT activities that resulted in increased stress defense in both cultivars, which is consistent with observations in peas, wheat, and soybean [19,44]. POD activity showed little variation under solar UV-B exclusion, meanwhile another antioxidative enzyme, CAT, played a central role under ambient UV-B radiation for quenching excess cytosol H2O2. A higher enhancement of CAT activity in thin-leaf cultivars Gui 2 under ambient UV-B radiation indicates that Gui 2 can respond more thoroughly to solar UV-B radiation, i.e., not only in non-enzyme antioxidant terms as above-mentioned but also in enzymatic antioxidant activity.
Overall, to counter the negative influence of lower leaf thickness under solar UV-B radiation, not only did Gui 2 increase its own leaf thickness but also performed with higher leaf palisade/spongy tissue ratio, total flavonol, and CAT enzyme activity relative to Gui 7. Moreover, the thin-leaf cultivars (Gui 2) exhibited higher enhancement of proline content and flavonol ratio (M+Q)/K under mild drought. Leaf thickness (one reciprocal indicator of specific leaf area) is known to be inversely related to the plant growth rate [45,46], which made thin-leaf cultivars of chestnut rose accumulate higher biomass under unstressed conditions. To offset the solar UV-B or drought effects, the thin-leaf cultivars showed higher responses in above-mentioned physiological traits, as well as complementary effects of antioxidant property and leaf traits against solar UV-B and drought stress.

4.2. Solar UV-B Radiation Primes Chestnut Rose Plants with Increased Antioxidative Capacity against Drought Stress

Under UV-B exclusion condition, moderate drought caused a marked reduction in total biomass but promoted membrane permeability. However, drought-induced negative effects were significantly alleviated when solar UV-B radiation were applied (D treatment). Robson et al. [47] also observed that solar UV-B radiation ameliorated plant phenotype under drought stress such as plant height, leaf production, and leaf length in silver birch.
Drought-induced reduction of antioxidants was also observed in ascorbic acid content (Gui 2) and SOD activity (both cultivars) under the UV-B exclusion condition. However, these two antioxidative parameters were reversed and increased when applied by solar UV-B radiation. In both the two cultivars, drought induced increases in two additional parameters under the UV-B exclusion condition, i.e., total flavonol content and CAT enzyme activity, which were promoted further in their amplitude when subjected to solar UV-B radiation. This amelioration, attributed to solar UV-B radiation, reveals its priming effects on chestnut rose plants with increased tolerance to environmental stress.
Leaf ascorbic acid (Asa), a non-enzyme antioxidant, tends to decrease under drought via synthesis inhibition [47], showing that Asa content might also increase to some extent under solar UV-B radiation in some genotypes, like that of Gui 2. A previous study on cucumber and common buckwheat also validated the UV-B-induced enhancement effect on leaf Asa concentration [15].
Mátai et al. [48] found that UV-B radiation reinforced antioxidant responses to drought in Nicotiana benthamiana leaves when receiving supplementary irradiation. Thomas et al. [49] revealed that UV-B priming on seedlings alleviated the negative effect of NaCl and drought stress via the induction of non-enzymatic antioxidants, antioxidant enzyme activity, and stress-responsive proteins. Our results are consistent with the conclusion of Mátai et al. [48] and Thomas et al. [49]. Furthermore, in our study, solar UV-B radiation primed the chestnut rose plants with a higher level of total flavonols content, endowing chestnut rose plants with additional antioxidant properties. The exception to the above comes with the change in POD enzyme activity, which was pronouncedly reduced, independently of whether UV-B radiation was applied or not. POD enzyme catalyzes the H2O2-dependent oxidation of phenol substrate, whereas long term drought might make the phenol to be consumed, resulting in the reduction of POD activity, as shown in the present study and previous report by Vincent et al. [50].

4.3. Complementary Effects of Solar UV-B Radiation and Drought on Nutrition Balance in Chestnut Rose Plants

Despite significant reduction in macroelement nutrition under drought and UV-B exclusion conditions (e.g., N, P, K, and Mg concentrations), macroelements in drought-stressed plants maintain comparable concentration levels with the control when supplied with solar UV-B radiation, indicating the stabilizing effects of UV-B. Few studies reported UV-B × drought interaction effects on plant nutrition balance. Lu et al. [51] observed that N concentration maintained or increased in the control under combined UV-B and drought treatments. Recently, it has been found that nitrogen and phosphorus absorption can be improved via the regulation of the nitrate transporter NRT2.1 and phosphate regulator (phosphorus starvation response 1), when HY5 transcription is up-regulated. As HY5 can be upregulated by ambient UV-B radiation [52], solar UV-B radiation can therefore reverse the nutrition reduction caused by drought. In addition, the moderate drought applied in the present study may have stimulated the root system to increase root area [26].
Leaf K and Mg concentration were also reduced by solar UV-B exclusion, which means that solar UV-B radiation is beneficial to the absorption of K+ and Mg2+. In an earlier study, Yue et al. [53] observed increases in K+ and Mg2+ concentrations in leaves of Triticum aestivum plants exposed to elevated UV-B radiation. Reduction in Mg2+ absorption by drought was widely reported [54], which is consistent with our study. In an earlier study reported by Chimphango et al. [55], they found that Mg concentration increased under enhanced UV-B radiation in legume plants such as Cyclopia maculata, Glycine max, and Lupinus luteus. Solar UV-B-induced absorption of Mg can effectively avoid the insufficiency of Mg nutrition. As for potassium, K plays a key role in osmotic adjustment capacity, especially under drought or salt condition [56], so solar UV-B-induced [K+] absorption can help chestnut rose plants acclimate drought stress, often occurring in the Karst region.
As a calciphile species, chestnut rose increased its plant Ca levels under moderate drought conditions. It is not yet known whether this is a typical characteristic of calciphile species. Ca levels can be reduced under UV-B radiation, as reported in the present study and previous reports [57]. However, the increase in Ca levels by moderate drought can effectively avoid Ca reduction when exposed to solar UV-B radiation, showing their complementary effects.
As for microelement nutrition, Fe, Cu, and Zn concentration levels were reduced by solar UV-B radiation. A study on barley with iron deficiency showed that UV-B radiation may develop a high level of oxidative stress [58], reducing Zn or Cu levels, which can ultimately affect plant growth or its antioxidative capacity [59]. Moderate drought stabilized these microelement levels in chestnut rose. More recently, Guo et al. [60] reported that when iron was insufficient during the circadian cycle, HY5 promoted iron uptake via the systemic activation of FER expression, so that HY5 expression can be induced under the combination of both solar UV-B and drought. The stabilizing mechanism that controls microelement nutrition under combined solar UV-B × drought merits further research in chestnut rose.
It should be noticed that, compared with the other cultivars, thin-leaf Gui 2 had higher nutrition levels under different conditions, such as for N, P, Ca, Fe, Cu, and Zn, so this supported higher biomass when optimal environmental conditions were present.

5. Conclusions

The cultivar Gui 2 with thinner leaves was more responsive to environmental factors such as drought and solar UV-B radiation, while in Gui 7 the responses were generally smaller. Gui 2 grew better than Gui 7 in response to UV-B exclusion under well-watered conditions, underlining the opportunistic growth strategy of Gui 2. Offsetting the negative influence of lower leaf thickness under solar UV-B radiation, Gui 2 performed better than Gui 7, the former reaching higher enhancements in leaf palisade/spongy tissue ratio, CAT activity, and flavonoid compounds than Gui 7. On the other hand, ambient UV-B radiation in effect modified the adverse impact caused by drought in both cultivars, improving total biomass and reducing membrane penetration. This modification might be related with the improved antioxidant enzyme capacity as explained by higher enzyme activity (SOD and CAT) and higher non-enzyme antioxidant concentration (flavonol aglycones and proline) under ambient UV-B radiation conditions. Finally, solar UV-B radiation effectively reversed nutrient reduction in chestnut rose plants, such as in N, P, Mg, Zn, and Cu. Given that the majority of studies on plant responses to water deficit were conducted in controlled environments without solar UV-B radiation, drought effects may have been exaggerated due to the exclusion of mitigation effects of solar UV-B radiation. Our study showed that solar UV-B radiation plays an important role for chestnut rose to tolerate drought stress, which occurs frequently in the Karst region, by modulating its antioxidative capacity and nutrition balance.

Author Contributions

D.L., J.L. (Jielin Li) and Y.W., investigation and analysis; J.L. (Jianxun Luo), methodology; Y.M., resource and material; W.L., software; L.G.R., writing—review and editing; Y.Y.; supervision, conceptualization, writing and project administration. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by Sichuan Innovative Talent Program (2020JDRC0065) and Jiangsu Forestry Science and Technology Innovation and Promotion Project “Integrated promotion of new technology on ecological shelterbelt construction for difficult coastal areas of Jiangsu Province” (LYKJ(2020)01). as well as by National Scientific Foundation in China (No. 30800127 and No.30972341).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We would like to thank Lijun Wang for useful discussions regarding the data interpretation as well as fund supports.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 00050 g001 550
Figure 1. Leaf thickness (A), leaf palisade/spongy tissue ratio (B) and plant above-ground biomass (C) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate a significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
Figure 1. Leaf thickness (A), leaf palisade/spongy tissue ratio (B) and plant above-ground biomass (C) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate a significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
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Forests 14 00050 g002a 550Forests 14 00050 g002b 550
Figure 2. Leaf electrolyte conductance (A), leaf proline concentration (B) and leaf total ascorbic acid concentration (C) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate the significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
Figure 2. Leaf electrolyte conductance (A), leaf proline concentration (B) and leaf total ascorbic acid concentration (C) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate the significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
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Figure 3. Concentration of leaf total flavonol aglycones (Kaempferol+QuercetinMyricetin) measured after acid hydrolysis (A) and Flavonol ratio (M+Q)/K [(myricetin+quercetin) /kaempferol ratio] (B) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
Figure 3. Concentration of leaf total flavonol aglycones (Kaempferol+QuercetinMyricetin) measured after acid hydrolysis (A) and Flavonol ratio (M+Q)/K [(myricetin+quercetin) /kaempferol ratio] (B) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
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Figure 4. Leaf SOD activity (A), CAT activity (B), and POD activity (C) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
Figure 4. Leaf SOD activity (A), CAT activity (B), and POD activity (C) of two Chestnut rose cultivars under different water regimes and solar UV-B treatments. Values are mean ± SD. Different letters above the bars indicate significant difference between treatments at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion.
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Table
Table 1. F-values and significance levels for three-way ANOVAs of the effect of cultivar, drought, UV-B, and their interaction on growth and physiological properties in Chestnut rose. C, cultivar; D, drought; U, UV-B. P/S ratio, leaf palisade/spongy tissue ratio; EC, leaf electrolyte conductance; Asa, leaf total ascorbic acid concentration. ns, not significant.
Table 1. F-values and significance levels for three-way ANOVAs of the effect of cultivar, drought, UV-B, and their interaction on growth and physiological properties in Chestnut rose. C, cultivar; D, drought; U, UV-B. P/S ratio, leaf palisade/spongy tissue ratio; EC, leaf electrolyte conductance; Asa, leaf total ascorbic acid concentration. ns, not significant.
Leaf ThicknessP/S RatioBiomassECProlineAsaSODCATPODTotal FlavonolFlavonol Ratio (M+Q)/K
C107.2 ***6.8 *163.1 ***691.1 ***5426.7 ***16.0 ***1.66 ns10.5 **1.0 ns0.653 ns40.4 ***
D16.0 ***7.9 *8066.8 ***14.5 **12,305.8 ***38.3 ***81.54 ***3.4 ns166.4 ***137.5 ***167.5 ***
U11.5 **
2.127 ns		54.0 ***74.8 ***192.4 ***669.0 ***0.25 ns875.13 ***706.0 ***7.0 *950.2 ***68.9 ***
C×D2.1 ns1.4 ns208.3 ***195.3 ***3966.8 ***2.54 ns1.14 ns26.8 ***0.05 ns1.124 ns14.4 **
C×U4.2 ns132 **95.5 ***278.1 *469.7 ***15.6 ***1.09 ns78.7 ***3.6 ns238.5 ***34.7 ***
D×U2.6 ns6.8 *998.7 ***1223.9 ***68.9 ***6.8 *171.6 ***16.7 ***0.02 ns52.6 ***0.052 ns
C×D×U
FS×C×T		1.8 ns11.6 **111.5 ***78.0 ***63.0 ***0.26 ns0.99 ns20.8 ***2.1 ns44.7 ***64.3 ***
*, **, *** indicate significant difference between treatments at p < 0.05, p < 0.01, p < 0.001, respectively.
Table
Table 2. The concentration of different nutrition elements of two Chestnut rose cultivars under different water regimes and UV-B treatments. Values shown are mean ±SD. Values within a column followed by the same letter do not differ significantly at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion. Significance level (ANOVA): C, cultivar effect; D, drought effect; U, UV-B effect; C × D, cultivar×drought interaction; C × U, cultivar×UV-B interaction; U × D, drought × UV-B interaction; C × D × U, cultivar×drought×UV-B interaction. ns, not significant.
Table 2. The concentration of different nutrition elements of two Chestnut rose cultivars under different water regimes and UV-B treatments. Values shown are mean ±SD. Values within a column followed by the same letter do not differ significantly at p < 0.05 level by LSD pairwise comparisons. Control, ambient UV-B; –UV-B, UV-B exclusion; D, drought with ambient UV-B; –UV-B+D, drought with UV-B exclusion. Significance level (ANOVA): C, cultivar effect; D, drought effect; U, UV-B effect; C × D, cultivar×drought interaction; C × U, cultivar×UV-B interaction; U × D, drought × UV-B interaction; C × D × U, cultivar×drought×UV-B interaction. ns, not significant.
Caltivars TreatmentsN (mg/g)P (mg/g)K (%DW)Ca (ug/g)Mg (ug/g)Fe (ug/g)Mn (ug/g)Cu (ug/g)Zn (ug/g)
Gui 2 Control3.87 ± 0.13 b0.34 ± 0.017 b1.23 ± 0.07 a6329 ± 178.9 d1188 ± 46.57 a108.4 ± 10.8 c50.80 ± 6.1 ab7.20 ± 0.73 b8.40 ± 0.31 b
-UV-B4.05 ± 0.12 a0.37 ± 0.017 a1.02 ± 0.09 b7671 ± 307.5c991 ± 27.8 b289.2 ± 17.0 a47.65 ± 2.7 b9.85 ± 1.10 a9.30 ± 0.44 a
D3.71 ± 0.12 b0.33 ± 0.024 b1.08 ± 0.09 ab9183 ± 313.2 b931 ± 33.78 bc162.3 ± 9.6 b45.15 ± 3.7 b7.80 ± 0.37 ab7.95 ± 0.31 c
-UV-B + D3.37 ± 0.13 c0.29 ± 0.012 c1.02 ± 0.09 b10,000 ± 190.8 a899 ± 17.35 c148.3 ± 14.2 b56.90 ± 4.5 a9.05 ± 0.65 a7.75 ± 0.69 c
Gui 7Control3.51 ± 0.10 b0.23 ± 0.01 b1.07 ± 0.17 a7162 ± 237.0 d1058 ± 33.0 a57.5 ± 5.6 c61.8 ± 7.2 b6.65 ± 0.79 b4.65 ± 0.35 c
-UV-B3.77 ± 0.12 a0.27 ± 0.024 a0.93 ± 0.09 b8371 ± 419.0 c994 ± 27.6 b100.7 ± 11.8 b67.0 ± 4.7 b7.90 ± 0.62 ab5.40 ± 0.45 b
D3.44 ± 0.17 b0.22 ± 0.023 b1.01 ± 0.11 ab9014 ± 256.5 b1008 ± 40.4 a153.5 ± 8.1 a64.5 ± 4.4 b6.80 ± 0.82 b6.75 ± 0.28 a
-UV-B + D3.04 ± 0.13 c0.20 ± 0.026 c0.89 ± 0.10 b10535 ± 493.0 a892 ± 47.8 c102.4 ± 6.5 b80.2 ± 3.5 a8.65 ± 0.37 a5.50 ± 0.44 b
C******ns*********ns***
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U**************ns*****
C × Dnsnsnsns******nsns***
C × Unsnsnsns******nsns***
D × U****nsnsns******nsns
C × D × Unsnsnsns******nsns***
*, **, *** indicate significant difference between treatments at p< 0.05, p < 0.01, p < 0.001, respectively.
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MDPI and ACS Style

Luo, D.; Li, J.; Luo, J.; Ma, Y.; Wang, Y.; Liu, W.; Rodriguez, L.G.; Yao, Y. Responses to Solar UV-B Exclusion and Drought Stress in Two Cultivars of Chestnut Rose with Different Leaf Thickness. Forests 2023, 14, 50. https://doi.org/10.3390/f14010050

AMA Style

Luo D, Li J, Luo J, Ma Y, Wang Y, Liu W, Rodriguez LG, Yao Y. Responses to Solar UV-B Exclusion and Drought Stress in Two Cultivars of Chestnut Rose with Different Leaf Thickness. Forests. 2023; 14(1):50. https://doi.org/10.3390/f14010050

Chicago/Turabian Style

Luo, Dapeng, Jielin Li, Jianxun Luo, Yan Ma, Yongzhi Wang, Wei Liu, Lucas Gutierrez Rodriguez, and Yinan Yao. 2023. "Responses to Solar UV-B Exclusion and Drought Stress in Two Cultivars of Chestnut Rose with Different Leaf Thickness" Forests 14, no. 1: 50. https://doi.org/10.3390/f14010050

APA Style

Luo, D., Li, J., Luo, J., Ma, Y., Wang, Y., Liu, W., Rodriguez, L. G., & Yao, Y. (2023). Responses to Solar UV-B Exclusion and Drought Stress in Two Cultivars of Chestnut Rose with Different Leaf Thickness. Forests, 14(1), 50. https://doi.org/10.3390/f14010050

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