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Article

UV-B Radiation in the Acclimatization Mechanism of Psidium guajava in Sunlight

by
Felipe G. Campos
,
Mariana O. Dantas
,
João P. M. Santos
,
Sophia S. Froes
,
João P. S. Gama
and
Carmen S. F. Boaro
*
Department of Biodiversity and Biostatistics, Institute of Biosciences, São Paulo State University (Unesp), Prof. Dr. Antônio Celso Wagner Zanin Street, 250, Botucatu 18618-689, São Paulo, Brazil
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(12), 1291; https://doi.org/10.3390/horticulturae9121291
Submission received: 26 September 2023 / Revised: 20 November 2023 / Accepted: 21 November 2023 / Published: 30 November 2023
(This article belongs to the Section Developmental Physiology, Biochemistry, and Molecular Biology)
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Abstract

:
The ozone layer (O3) is essential to the absorption and blocking of UV-B radiation, preventing a large portion from reaching the Earth’s surface. The degradation of the ozone layer (O3) caused by increased pollution has led to climate change exerting significant influence on natural ecosystems and has resulted in severe stress on the environment, such as an increase in UV-B radiation, which has deleterious effects on plant physiology. UV-B influences the protection pathways that increase compound production, leading to metabolic adjustments and promoting plant acclimatization. This study evaluated whether UV-B application prior to sunlight exposure induces anthocyanin synthesis, photochemical change, and carbohydrate profile modification, contributing to acclimatization in Psidium guajava seedlings. A higher concentration of H2O2 may have stimulated anthocyanin synthesis. Furthermore, greater instantaneous water use efficiency (iWUE), the absence of trehalose—a stress marker, and lower concentrations of glucose, fructose, and sucrose indicate that these plants acclimatize when exposed to full sun (30 days). Seedlings exposed to increased UV-B may be more resistant to the climate. The radiation can aid in water resource management with elevated carbohydrate concentrations. These conditions may enhance the success of P. guajava in the field. Therefore, it is suggested that UV-B application to seedlings of P. guajava promotes effective acclimatization, as it activates anthocyanin synthesis, inhibits trehalose accumulation, and increases iWUE. UV-B radiation, depending on its radiance, can be used as a technique in seedling production that can be implanted in anthropic environments.

1. Introduction

When it reaches the Earth, UV-C radiation (100–280 nm) can convert the molecular oxygen present in the stratosphere into ozone, creating an extensive layer. In lower levels of the atmosphere, UV-B radiation (280–315 nm), through photodissociation, produces reactive species of hydroxyl capable of reacting with natural pollutants, performing the ozone layer’s self-cleaning and maintaining stratospheric dynamics. The presence of anthropogenic pollutants such as hydrochlorofluorocarbons (HCFCs) and hydrofluorocarbons (HFCs) in the atmosphere halts ozone dissociation. Consequently, ozone layer degradation occurs, allowing the free transmittance of UV-B radiation toward the Earth’s surface [1]. However, the ozone layer is essential for the absorption and blocking of UV-B radiation, preventing a large portion from reaching the Earth’s surface [2].
The degradation of the ozone layer (O3) caused by increased pollution leads to climate change, exerting a significant influence on natural ecosystems and resulting in severe stress on the environment [3,4]. Among the consequences of these changes, there is an increase in ultraviolet B (UV-B) radiation, a critical abiotic factor that plays a determining role in plant growth and development, exerting deleterious effects on plant physiology, morphology, and biochemistry [5,6].
UV-B is associated with cell damage such as lipid peroxidation, DNA strand breaks, and hormone inactivation [5,7]. In addition, it can inhibit photosynthesis, negatively influence the functioning of crucial enzymes such as RuBisCO, and directly affect the photosystem, in turn reducing its efficiency and changing the rate of electron transport responsible for reactive oxygen species (ROS) formation [8,9].
ROS can damage the structural components of photosystem II, such as D1, D2, CP43, LHCII, and PsbH proteins present in thylakoid membranes, resulting in a low maximum quantum yield of PSII photochemistry (Fv/Fm) [10].
In addition to stimulating hydrogen peroxide formation (H2O2), UV-B radiation also stimulates the production and accumulation of abscisic acid (ABA) and nitric oxide (NO), molecules involved in promoting signaling for stomatal closure [11].
ROS are cytotoxic molecules and important signposts for specialized metabolites. UV-B radiation contributes to the synthesis and accumulation of ROS and, therefore, interferes with the growth, development, reproduction, and survival of plant organisms [3,12]. Under high concentrations of UV-B radiation, plants increase ROS production, which in excess causes the oxidation of biomolecules linked to enzymatic and non-enzymatic mechanisms [13,14].
Despite the deleterious effects of UV-B radiation, plants can also respond to the time and intensity of this radiation, which leads to acclimatization. Thus, in response to UV-B radiation and ROS plants produce efficient adaptation mechanisms, including the biosynthesis of specialized metabolites [15]. Among these metabolites, we can highlight phenolic compounds, a non-enzymatic mechanism of defense, due to their fundamental role as UV-B protective agents. The concentration of phenolic compounds in plants under UV-B stress is highly variable and depends on factors such as the plant species, radiation intensity, and exposure duration [16].
Several studies evaluated the influence of UV-B radiation on herbaceous plants and confirmed its effects on their specialized metabolism, with increased terpene levels and the synthesis of phenolic compounds that are related to abiotic and biotic stress defense [17,18].
The application of UV-B irradiation to Eucalyptus globulus promoted changes in the accumulation of sugars and the terpene profile, which may indicate changes in metabolism that contribute to this species’ acclimatization. UV-B radiation also influences protection pathways and can increase the production of compounds capable of absorbing it [19], promoting metabolic adjustments that can mitigate possible damage. Juvenile plants of E. globulus that received UV-B radiation showed no mortality or modification of carbohydrate content and terpenes, suggesting plant acclimatization [20].
Anthocyanin, one of these compounds, showed changes in expression under stress, with an increase in its concentration acting as a defense mechanism [21]. Synthesized from the phenylpropanoid pathway (PPP), anthocyanins accumulate in plant tissue and act by providing antioxidant activity that induces morphophysiological and metabolic acclimatization [22,23]. In these scenarios, plants may have a controlled ROS concentration.
Guava (Psidium guajava), a fruit tree belonging to the Myrtaceae family, is a C3 plant native to South Mexico and some regions in Central America, with leaves, bark, and roots that are important to the pharmaceutical and food industries [24,25]. Guava contributes to the economy of many countries in tropical and subtropical regions [24]. Its fruit is rich in phenols, triterpenes, tannins, flavonoids, saponins, carotenoids, lectins, vitamins, fibers, and fatty acids [26]. Moreover, its leaves contain an abundance of polyphenols and flavonoids, such as quercetin and anthocyanin [27], which have antioxidant properties [26] and act in plant defense against several factors, including UV-B light.
P. guajava cultivation occurs mostly in South Africa, India, Brazil, Venezuela, and Pakistan, which is the leading producer worldwide, producing 512.3 tons of fruit on 62.3 million hectares [28]. In Brazil, there is less production, with 22.630 ha of guava cultivation [29]. P. guajava is commercialized industrially as jams, juices, and pulp [30,31]. However, the species is often directed toward reforestation areas in Brazil [32]. Therefore, seedling production in guava plants is an important phase that influences the success and final production of the crop [33], as well as the restoration of degraded areas. Disturbances that occur naturally or from climatic changes can cause higher light intensity, promoting the initial establishment of P. guajava in degraded areas by creating a shaded environment beneficial to the growth of shadow-tolerant native species [34].
P. guajava grown under an irradiance of 1800 μmol m−2 s−1 photosynthetic photon flux density (PPFD) showed an increase in the concentration of anthocyanins and carotenoids, promoting the photoprotection of the photochemical apparatus, thus avoiding photoinhibition. This suggests that P. guajava plants can tolerate high irradiance, which could improve their growth [27].
Although the plant tolerates high light incidence, it is important to understand the response of guava plants as a consequence of increased UV-B incidence due to climate change. The response comprehension of the species to UV-B radiation can offer multiple perspectives, among them, the possibility of P. guajava seedling management with UV-B—contributing to their acclimatization—for both commercial orchard implementation and degraded area restoration. Under these conditions, plant acclimatization might be linked to phenolic compound synthesis and adjustments in the photosynthetic and carbohydrate profile. The aim of this study was to evaluate whether UV-B application prior to sunlight exposure induces anthocyanin synthesis, photochemical change, and carbohydrate profile modification, contributing to the acclimatization mechanism in Psidium guajava seedlings. The purpose of this study was to evaluate how UV-B radiation affects the signaling of the antioxidant system in the acclimatization of Psidium guajava seedlings under full sunlight.

2. Material and Methods

2.1. Growing Conditions

The experiment was conducted at the Unesp Biosciences Institute, Campus Botucatu, São Paulo, Brazil (geographic coordinates 22°49′10″ S, 48°24′35″ W, and 800 m average altitude). Guava (Psidium guajava) seedlings of 30 ± 5 cm height were transplanted in vases (2.6 L capacity) with TropStrato HT® (VidaVerde Inc., São Paulo, Brazil) substrate. Once in the vases, all seedlings were fertilized with nutrient solution number 2 by Hoagland and Arnon [35] and maintained for 30 days in a greenhouse before treatment application.
A growth chamber was used for UV-B radiation application, presenting medium values of temperature, relative humidity, and carbon concentrations of 25 ± 5 °C, 32 ± 2%, and 554.52 ± 50 µmol CO2 mol air−1, respectively. After 30 days in the greenhouse, the plants were moved to a growth chamber for UV-B radiation application. The growth chamber was equipped with UV-B lamps (model G15T8E®, Ushio Inc., Tokyo, Japan) with a wavelength between 280 and 360 nm (peak 305 to 310 nm) to provide 3000 ± 100 µW cm−2 s−1, and lamps to provide PPFD 396 ± 21 µmol m−2 s−1. The UV-B radiation was applied during the luminous period for two days (two periods of 13 h). A total of 48 h past the UV-B radiation period, the first evaluation was performed in the growth chamber.
Then, all plants were transferred to sunlight and were kept for 30 days with medium PPFD values of about 1149.13 ± 151 µmol m−2 s−1, temperature about 23.41 ± 2.4 °C, relative humidity about 32 ± 2%, and carbon concentrations about 400 ± 20 µmol CO2 mol air−1 in the sunlight. On the 30th day, the second evaluation was conducted of the sunlit plants. Two evaluations were made at 2 days (48 h after the UV-B radiation in the growth chamber) and 30 days after the UV-B radiation on the plants in sunlight.
The study was carried out in a completely randomized 2 × 2 factorial design with the application of UV-B radiation or not (UV-B or UV-B absent) and two evaluation times (2 and 30 days after UV-B radiation), with nine repetitions.
Photosynthetic parameters were measured with an Infra-Red Gas Analyzer, model GFS-3000 (Heinz Walz GmbH, Effeltrich, Germany), with a coupled portable modulated light fluorometer (LED-ARRAY/PAM-Module 3055-FL®, Heinz Walz GmbH, Effeltrich, Germany). The evaluations occurred between 9 a.m. and 11 a.m.

2.2. Fluorescence of Chlorophyll a

The fluorescence of chlorophyll a in the dark was measured in fully expanded leaves dark-adapted for 30 min (leaves were left in the dark with aluminum paper around them) using a saturating irradiance of 4500 µmol m−2 s−1 PPFD. The maximum quantum yield of PSII photochemistry (Fv/Fm), non-photochemical quenching (NPQ), and minimum Chl a fluorescence in the dark-adapted state (Fo) were measured [36]. Chlorophyll a fluorescence in the light was evaluated in fully expanded leaves [37,38,39], with a saturating irradiance of 400 ± 8 µmol m−2 s−1 PPFD obtained through a light response curve [40]. The variables evaluated were the potential quantum efficiency of the open PSII center (Fv′/Fm′) energy fraction absorbed by the PSII antenna that is dissipated as heat (D), the energy fraction not dissipated in the antenna that cannot be used for the photochemistry stage (Ex), the electron transport rate (ETR), and the effective quantum efficiency of photosystem II (ΦPSII).

2.3. Gas Exchanges

The gas exchange, CO2 assimilation rate (Anet, μmol CO2 m−2 s−1), transpiration rate (E, mmol H2O m−2 s−1), stomatal conductance (gs, mmol m−2 s−1), and internal leaf CO2 concentration (Ci, μmol CO2 mol−1 ar) were determined. Instantaneous water use efficiency (iWUE, μmol CO2 (mmolH2O−1) was determined as the ratio between the CO2 assimilation rate and the transpiration rate (A/E). Ribulose 1,5-diphosphate carboxylase/oxygenase (RuBisCO) carboxylation efficiency, measured by the CO2 assimilation rate and internal CO2 concentration in the sub-stomatal chamber (Anet/Ci μmol m−2 s−1 Pa−1), were evaluated [39].

2.4. Foliar Pigments

Anthocyanin extraction was realized with 100 mg of crushed and frozen fresh leaves, using KCl (pH 1.0, Êxodo Científica®, São Paulo, Brazil) and sodium acetate (pH 4.5, Êxodo Científica®, São Paulo, Brazil). The obtained extracts of each pH were read at wavelengths of 520 and 700 nm, and the results were expressed in cyanidin-3-glucoside (anthocyanin) equivalents, mg g fresh weight−1 [27,41].
Carotenoids and chlorophyll a and b contents were determined [42] with Tris-(hydroxymethyl)-aminomethane (pH 7.8, Merk KGaA, Darmstadt, Germany) and acetone (Êxodo Científica®, São Paulo, Brazil) reagents. Leaves were macerated with an extractor solution and maintained in a freezer for one hour. Then, the extract was agitated and centrifuged (1000× g at 4 °C for five minutes). The supernatant readings were performed with a spectrophotometer (Bel Engineering®, model UV-M51, Milan, Italy) at wavelengths of 663 for chlorophyll a, 647 for chlorophyll b, and 470 nm for the carotenoids.

2.5. Hydrogen Peroxide, Lipid Peroxidation, and Total Phenolic Compounds

The H2O2 content was determined [43]. Frozen samples were used and reacted with phosphate buffer (0.1 M, pH 7.0) and potassium iodide 1 M. Then, the solutions were reacted for one hour in the dark. The measurements were performed with a spectrophotometer (Bel Engineering®, model UV-M51, Milan, Italy) at a wavelength of 390 nm.
Lipid peroxidation was determined [44]. The readings were made with a UV-visible spectrophotometer (Bel Engineering®, model UV-M51, Milan, Italy) at wavelengths of 560 and 600 nm. Total phenolic compounds were determined [45].

2.6. Carbohydrates

Total soluble sugar extraction [46], as well as its quantification [47], conformed to the methodology. For total quantification, the soluble sugar profile was evaluated using high-performance ion chromatography (Dionex ICS−5000+, Thermo Fisher Scientific Inc.®, Waltham, MA, USA) according to [48] methodology. All soluble sugar samples and standards were filtered with a 0.22 µm filter before being examined with a chromatography system outfitted with a quaternary pump, automated samples, an electrochemical detector DCS5000 (Thermo®), column P100 (Carbopack®, São Paulo, Brazil), and gold and Ag/AgCl reference electrodes. For 35 min, the eluent phases A, B, and C were 640 mM sodium hydroxide, 0.5 M sodium acetate, and ultrapure water, with a flow rate of 0.7 mL min−1. The injections of the samples were not repeated.

2.7. Statistical Analysis

Data were subjected to Levene’s test to ensure variance homogeneity and the Kolmogorov–Smirnov normality test. The F test was used to analyze the variance and when there was significance (p < 0.05) the means were compared using the Tukey test and SigmaPlot® statistical tool.
The heatmap was created using the software MetaboAnalyst® v5.0 (Québec, QC, Canada, https://www.metaboanalyst.ca/ accessed on 5 May 2023) [49]. Variables were standardized and the Euclidean distance between treatments was considered.
The F values and the significance of the variables evaluated can be observed in Supplementary Table S1.

3. Results and Discussion

3.1. Fluorescence of Chlorophyll a

UV-B radiation has the potential to damage the PSII, destroying structural compounds such as D1, D2, CP43, LHCII, and PsbH proteins present in thylakoid membranes, resulting in a low maximum quantum yield of PSII photochemistry (Fv/Fm) and a decrease in the light capture [10]. The decrease in Fv/Fm can indicate dynamic photoinhibition when the regeneration of those protein components occurs in the dark period. However, when the damage is very severe the regeneration does not occur, resulting in chronic photoinhibition [50]. The photosynthetic metabolism has mechanisms that promote photoprotection to avoid chronic photoinhibition, such as energy dissipation in the form of heat by the complex antenna [51], avoiding damage to PSII structural compounds [52].
Guava (Psidium guajava) seedlings 2 days after UV-B application and UV-B absent showed higher maximum quantum productivity of photosystem II (Fv/Fm) relative to plants evaluated 30 days after (Figure 1A). However, the results remained within the expected range for the species as found by Ortiz et al. [53], around 0.7 and 0.8. The application of UV-B radiation caused dynamic photoinhibition in guava seedlings in the present study. The application of radiation did not cause a decrease in Fv/Fm, which was 0.7, with changes observed only when the plants were exposed to sunlight radiation 30 days after applying UV-B (Figure 1A).
There was no difference in energy dissipation in the form of heat between treatments, as revealed by non-photochemical quenching (NPQ, Figure 1B). However, when maintained in sunlight for 30 days after UV-B application, guava seedlings showed higher NPQ (Figure 1B), which may have been responsible for dissipating excess light radiation [51], without triggering the dissipation in the form of fluorescence (Fo) (Table S1). Based on the results, plants displayed a photosynthetic metabolic photoprotection of the seedlings with D1 protein regeneration (Figure 2A–C).
P. guajava seedlings that received UV-B showed lower Fv’/Fm’ (Figure 3A). Also, lower Fv’/Fm’ was observed in plants 30 days after starting the treatments (Figure 3B).
Higher ETR and ΦPSII were observed in the first evaluation compared to 30 days after UV-B application (Figure 3C,D). These results confirmed expectations for a controlled environment that provides sufficient and stable photosynthetically active photon flux density (PPFD) in relation to sunlight conditions, allowing maximum efficiency of the photosystem. In sunlight, the PPFD was 2.75 times greater than that observed two days after UV-B application.
Ex in plants two days after UV-B application was 1.3 times higher in relation to Ex in the second evaluation (30 days) (Figure 2A) and had a lower heat dissipation (Figure 2B), indicating the accumulation of energy not dissipated in the antenna and neutralized, since ΦPSII did not differ between treatments with and without UV-B (Figure 3D).
These plants showed higher D (Figure 2C), which indicates the dissipation of excess energy in the form of heat via the antenna complex to minimize damage to the photosystem [8,19]. This condition indicates a loss of electron transport capacity, resulting in a reduction in the synthesis of NADPH + H+ (ΦPSII) from the greater light intensity of sunlight (30 days after UV-B application) in cultivated plants. This light intensity had a greater effect on reducing electron transport than the application of UV-B radiation.
This behavior indicated that the xanthophyll cycle may have contributed to the photoprotective process of these plants [54] dissipating energy in the form of heat (D), as observed in the plants that received UV-B two days after UV-B application (Figure 2C). It should be noted that, although the supply of UV-B radiation was approximately four times greater to P. guajava, this species was more resistant than Solanum melongena cv. Nápoli [8]. P. guajava did not undergo severe photochemical damage, triggering the photoprotection pathways, as seen with D (Figure 2C), and revealing dynamic photoinhibition. These results suggest the importance of studies involving UV-B, as different species display different results.
Higher ETR and ΦPSII were observed in the first evaluation compared to 30 days after UV-B application (Figure 3C,D). These results confirmed expectations for a controlled environment that provides sufficient and stable photosynthetically active photon flux density (PPFD) in relation to sunlight conditions, allowing maximum efficiency of the photosystem. In sunlight, PPFD was 2.75 times greater than that observed two days after UV-B application.
Two days after UV-B application, Ex in plants was 1.3 times higher in relation to Ex in the second evaluation (30 days) (Figure 2A), indicating the accumulation of energy not dissipated in the antenna and neutralized, since ΦPSII did not differ between treatments with and without UV-B (Figure 3).
A minor light capture observed in plants exposed to UV-B can be explained by its greater dissipation in the form of heat by the antennas (Figure 2C and Figure 3A). The greater efficiency of photosystem II may be a reflection of the greater concentration of CO2 present in the growth chamber, generating a greater demand for photochemical energy for its reduction [55].
Therefore, P. guajava may present itself as a resistant species from a photochemical point of view, able to develop even in conditions of climate change, such as damage to the ozone layer and increased UV-B irradiation [13].

3.2. Gas Exchanges

The UV-B radiation of 3000 µW cm−2 s−1, applied for 13 h on two days, affected the gas exchanges of P. guajava seedlings.
P. guajava plants grown with UV-B application two days after treatment showed lower CO2 assimilation (Anet). Seedlings in sunlight (30 days) showed no Anet difference (Figure 4A). A study on eggplant plants (Solanum melongena cv. Nápoli) exposed to UV-B radiation (7.07 W m−2 for 6 h on 49 days) determined that the lower Anet was possibly influenced by the decreased number and length of chloroplasts [8]. Although the differences among species and applied radiation intensity levels were smaller than in this study, similar results were observed in P. guajava plants two days after UV-B application, when there was a decrease in Anet.
The decrease in E and gs (Figure 4B–D) in plants that received UV-B may be the result of morphophysiological changes in number, size [8], and stomatal opening [7,53], contributing to the lower Anet. UV-B induces the production of abscisic acid (ABA) and consequent hydrogen peroxide (H2O2). UV-B is perceived by the photoreceiver UVR8, which induces the expression of ELONGATED HYPOCOTYL5 (HY5) and HY5 HOMOLOG (HYH) genes, which stimulate the production of NO. The NO—activated by SLAC1, K+ canals inhibition, and Cl− canals activation—promotes water output and stomatal closure [11].
The water use efficiency (iWUE) did not differ between treatments with and without UV-B and between evaluation periods (Table S1), which suggests that P. guajava seedlings after a UV-B treatment of 3000 µW cm−2 s−1 applied in two 13 h cycles for two consecutive days may show a higher resistance to a second stress, for example, hydric stress, as they are able to resist the lack of water. Plants that face several challenges can quickly form their responses, indicating the efficiency of their survival strategies [56]. Confrontation mechanisms against these challenges may be related to the accumulation of molecules such as H2O2, nitric oxide, and ABA, which control the stomatal opening [11].
Despite the greater accumulation of CO2 in the growth chamber, which equaled 544.52 ± 50 µmol CO2 mol air−1, there was no increase in Anet/Ci in plants with the application of UV-B (Figure 4E); however, at 30 days after the application of UV-B an increase in Anet/Ci was observed (Figure 4F). When inhibited by UV-B, a carboxylation enzyme can function as an oxygenase, which alters the consumption of NADPH + H+ [55]. Baker et al. [55] reported that the dynamic photoinhibition caused by UV-B radiation leads to a reduction in CO2 assimilation, which is reflected in an increase in carbon in the substomatal chamber (Ci) (Figure 4G).
However, 30 days after the treatment application, regardless of whether plants received UV-B or not, there was no difference in Anet values. The same results were observed in a study conducted with the application of UV-B (12 kJ m−2) for two days on Eucalyptus globulus [17], suggesting that species from the same family are resistant to UV-B.
In this study, the application of UV-B decreased most of the variables involved in the gas exchange. The results suggest that the accumulation of energy in the photosystem (ΦPSII) of plants subjected to UV-B may have activated the oxygenase function of the RuBisCO enzyme, directing the use of NADP + H+ to photorespiration as a form of photoprotection [57].

3.3. Foliar Pigments

The concentration of anthocyanins in the leaves of P. guajava seedlings two days after treatment application was higher in plants without UV-B (Figure 5A). The previous application of UV-B radiation resulted in a higher leaf anthocyanin concentration 30 days after irradiation when the plants were evaluated in sunlight, suggesting the possibility of acclimatization to the field (Figure 5A).
There was no difference in the concentration of carotenoids in guava plants treated or not treated with UV-B radiation at both evaluations (Figure 5B), suggesting efficient dissipation of excessive radiation (D and NPQ) incident on the antenna complex (Figure 1B and Figure 2A).
There were no differences in chlorophyll a and b contents in plants subjected or not subjected to UV-B (Figure 5C,D). However, their concentrations were higher 2 days after the application of the treatments, while the chla/chlb ratio was higher at 30 days (Figure 5C–E). The results of the present study are in agreement with those of Sisson and Caldewell [58], who found no variation in the chlorophyll a content. The authors suggested that the decrease in the photosynthetic rate did not occur due to pigment degradation, but rather due to stomatal closure with lower stomatal conductance and transpiration. This also agrees with our results. In the present study, the decrease in the photosynthetic rate could be due to stomatal closure and oxygenase activation of the RuBisCO enzyme [51].
The prevention of chlorophyll degradation may be related to the lower anthocyanin accumulation in plants subjected to UV-B, suggesting that the latter pigment may have assisted the antioxidant system due to reactive oxygen species neutralization, excess light filtration, or reflection. These results are in agreement with Shi et al. [59].
A study reported a lack of response between treatments with and without UV-B, which suggests an irradiation dose below the stress threshold that causes no critical damage to plant pigments or Fv/Fm [60]. The results of the present study are partially in line with those of Mannucci et al. [60] since our results showed moderate stress for the photochemical phase with the activation of photoprotection mechanisms such as energy dissipation in the form of heat (D), photorespiration, and the action of anthocyanins.
After 30 days, the metabolic adjustments observed in plants that received UV-B provided the conditions for acclimatization. Two days after the treatments were applied, the increase in chlorophyll b, as an accessory pigment, must have protected photosystem II from degradation (Figure 5D). At 30 days after irradiation, the higher chlorophyll a/b ratio suggests less need to activate the protection pathway carried out by chlorophyll b, maintaining energy dissipation (D) (Figure 2A).

3.4. Hydrogen Peroxide, Lipid Peroxidation, and Total Phenolic Compounds

The hydrogen peroxide (H2O2) concentration showed no difference between the treatments at two days (Figure 6A). At 30 days after treatment application, the concentration was higher in plants subjected to UV-B. In the second evaluation, a higher concentration of H2O2 was observed in the plants at two days (Figure 6A). The higher concentration of H2O2 30 days after the treatment application can be explained by reactive species involvement in the signaling cascade of events and signal maintenance for acclimatization, according to studies involving the stress response of hydrogen peroxide [61,62] or its application [63,64]. The accumulation of ROS is a sign of oxidative stress; H2O2 is relevant because, in addition to its pro-oxidative function, it participates in the signaling pathway of metabolites such as phenolic compounds, which help to overcome stress conditions [60]. The results agree with the anthocyanin accumulation in the present study (Figure 5A). Our results show an increase in the H2O2 concentration in plants without UV-B at 30 days, indicating that, even in sunlight, UV-B radiation can cause oxidative stress by increasing ROS, as Ruuhola et al. [14] reported.
Regardless of the evaluation time, UV-B resulted in greater lipid peroxidation (Figure 6B). These results are in line with a previous study [65] which recorded lipid peroxidation as indicative of membrane damage, generating malondialdehyde (MDA), a molecule that indicates stress and free radical formation [4].
The total phenol content was higher without UV-B and at 30 days after treatment application (Figure 6C,D). This may be explained by the antioxidant system action, which uses phenols (anthocyanins) as electron donors to neutralize hydrogen peroxide, with a higher concentration in sunlight (30 days) and with UV-B compared to non-irradiated plants (Figure 5A). The most effective defense mechanism against UV-B is the compound’s biosynthesis, which is capable of absorbing radiation such as flavonoids and other phenolic compounds [19]. Phenolic compounds also act to protect against ROS, and a study found an increase in their content when a plant is exposed to UV-B radiation [65]. In the present study, there was no increase in phenolic compounds when evaluations were carried out, indicating their utilization and degradation. In addition, soluble phenols can be used to protect the cell wall [60].

3.5. Carbohydrates

The evaluation carried out two days after UV-B application revealed an increase in glucose and fructose concentrations (Figure 7A,B). Sucrose degradation can generate an abscisic acid (ABA) signal, which inhibits photoassimilate translocation to the drain tissues, compromising growth and retaining sugars in the leaves. It acts as a signalizer of the biosynthesis of defense compounds by a specialized metabolism to combat the deleterious effects of UV-B radiation and can contribute to acclimatization [66].
Thirty days after irradiation, there was an increase in trehalose in plants without UV-B and a degradation of sucrose in plants with and without UV-B (Figure 7C,D). Plants not submitted to UV-B and kept in sunlight for 30 days had higher concentrations of trehalose, glucose, and fructose (Figure 7A–C). The presence of trehalose in sunlight plants is a stress indicator [67]. It should be noted that the natural environment also emits UV-B radiation, which can contribute to stress.
When transferred to sunlight, the plants subjected to UV-B lacked trehalose and their glucose and fructose concentrations did not change (Figure 7A,B), suggesting that these plants were already acclimatized.
The concentration of total sugars showed no difference between the treatments at two days (Figure 7E). In sunlight (30 days), the concentration was higher with UV-B. During evaluation periods, the concentration of total sugars was higher in sunlight (30 days) with UV-B (Figure 7). These plants may be more successful in the field. Thus, the application of UV-B may contribute to the acclimatization of seedlings in the field.

3.6. Heatmap

Two clusters were formed in the heatmap, one grouping plants at 2 days and the other plants at 30 days after the UV-B was applied (Figure 8).
At two days, plants that received UV-B showed a positive correlation for NPQ, Fv/Fm, Ex, Ci, chlorophyll a, chlorophyll b, sucrose, fructose, glucose, and mannose. UV-B radiation, which is highly energetic [19], did not cause damage to the photosystems, since the dissipation of non-photochemical energy protected the photosystem. The higher Ex did not result in ROS accumulation. The negative correlation with anthocyanins and phenolic compounds suggests that these compounds are used to neutralize ROS [27], thus preventing chlorophyll degradation. The positive correlation observed among sucrose, fructose, glucose, and mannose suggests metabolic adjustment and the direction of photoassimilates to cope with UV-B stress [20].
Two days after treatment without UV-B, there was a positive correlation among Fv’/Fm’, ΦPSII, Fo, chlorophyll a, chlorophyll b, Anet, carotenoid, anthocyanin, sucrose, and mannose. The higher concentration of CO2 present in the growth chamber may have generated a greater demand for reducing agents [55], promoting greater photochemical efficiency and high fluorescence dissipation as a protective form [19] and preventing the degradation of chlorophylls, carotenoids, and anthocyanins, with a positive correlation between sucrose and mannose.
Thirty days after application, plants that received UV-B showed a high positive correlation between iWUE, chlorophyll a/b, and MDA, and a positive correlation among ΦPSII, H2O2, NPQ, total soluble carbohydrate, anthocyanin, Fo, and E. The effective quantum efficiency and photochemical quenching of these plants may have been responsible for the synthesis of NADPH + H+; the dissipation of non-photochemical energy and fluorescence resulted in the protection of the chla/chlb ratio [51]. The higher concentration of H2O2 may have stimulated the anthocyanin synthesis pathway [68], explaining the higher concentration of this pigment. In addition, the greater efficiency of water use, trehalose absence, a stress marker, and the lower concentrations of glucose, fructose, and sucrose indicate that these plants acclimatized more quickly when exposed to sunlight (30 days).
At 30 days, the plants without UV-B application showed a high correlation between ETR, phenolic compounds, and trehalose, and a positive correlation among carotenoids, gs, Anet/Ci, H2O2, D, and E. Despite the high rate of electron transport and RuBisCO activity, no positive correlation was observed among sucrose, fructose, glucose, and mannose. However, the positive correlations between trehalose, carotenoids, and phenolic compounds may indicate a metabolic adjustment in response to the high light intensity environment [27,69]. The greater dissipation of energy by the antennas confirms the excess incidence, suggesting the plants are in the process of acclimatizing.
In this context, we suggest that the prior application of UV-B radiation promotes more effective acclimatization, since it triggers anthocyanin synthesis, inhibits the accumulation of trehalose, and increases instant water usage efficiency; additionally, UV-B may be indicated as a treatment for the production of seedlings to be planted in anthropized environments.

4. Conclusions

Psidium guajava seedlings can be resistant to climate change with an increase in UV-B. The radiation can help to provide better water resource management with elevated carbohydrate concentration. These conditions may improve the likelihood of success of P. guajava in the field. Therefore, we suggest that the application of UV-B to P. guajava seedlings promotes effective acclimatization, as it activates the synthesis of anthocyanins, inhibits the accumulation of trehalose, and maintains iWUE. UV-B radiance, depending on its intensity, can be used as a technique in the production of seedlings implanted in anthropic environments.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae9121291/s1, Table S1: F values and significance of the variables. Maximum quantum yield of Photosystem II efficiency (Fv/Fm); (B) non-photochemical quenching (NPQ); fluorescence in the dark-adapted state (Fo); potential quantum efficiency of open PSII center (Fv′/Fm′) energy fraction absorbed by PSII antenna that is dissipated as heat (D); energy fraction not dissipated in the antenna that cannot be used for photochemistry stage (Ex); electron transport rate (ETR); effective quantum efficiency of photosystem II (ΦPSII); CO2 assimilation rate (Anet); transpiration rate (E); stomatal conductance (gs); and Ribulose 1,5-diphosphate carboxylase/oxygenase (RuBisCO) carboxylation efficiency (Anet/Ci); anthocyanin (Anthoc.); carotenoids (Carot.); chlorophylls a and b (Chl a and Chl b); Chla/Chlb; hydrogen peroxide (H2O2); Lipid peroxidation (MDA); Total phenolic compounds (TPC); glucose; fructose; mannose; trehalose; sucrose; total soluble carbohydrates (TSC).

Author Contributions

Conceptualization, F.G.C. and C.S.F.B.; methodology, F.G.C., M.O.D. and C.S.F.B.; validation, C.S.F.B.; formal analysis, C.S.F.B.; investigation, F.G.C., M.O.D. and C.S.F.B.; resources, C.S.F.B.; data curation, F.G.C. and C.S.F.B.; writing—original draft preparation, F.G.C., J.P.M.S., S.S.F., J.P.S.G., M.O.D. and C.S.F.B.; writing—review and editing, F.G.C., J.P.M.S., S.S.F., J.P.S.G., M.O.D. and C.S.F.B.; visualization, F.G.C., M.O.D. and C.S.F.B.; supervision, C.S.F.B.; project administration, C.S.F.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financed in part by Pro-Rectory of Research (PROPe-Unesp) to support scientific publication (Unesp—PROPe/PROPEG 01/2023).

Data Availability Statement

The data presented in this study are available in article and Supplementary Materials.

Acknowledgments

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES).

Conflicts of Interest

The authors declare no conflict of interest.

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Horticulturae 09 01291 g001
Figure 1. (A) Maximum quantum yield of photosystem II efficiency (Fv/Fm) and (B) non-photochemical quenching (NPQ) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 9).
Figure 1. (A) Maximum quantum yield of photosystem II efficiency (Fv/Fm) and (B) non-photochemical quenching (NPQ) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 9).
Horticulturae 09 01291 g001
Horticulturae 09 01291 g002
Figure 2. (A) Fraction of dissipated excitation energy in the antenna that cannot be used for the photochemical phase (Ex), and (B,C) light fraction absorbed by the PSII antenna that is dissipated as heat (D) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05 (n = 9).
Figure 2. (A) Fraction of dissipated excitation energy in the antenna that cannot be used for the photochemical phase (Ex), and (B,C) light fraction absorbed by the PSII antenna that is dissipated as heat (D) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05 (n = 9).
Horticulturae 09 01291 g002
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Figure 3. (A,B) Photosystem II efficiency (Fv’/Fm’); (C) electron transport rate (ETR); and (D) effective quantum yield (ΦPSII) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05, (n = 9).
Figure 3. (A,B) Photosystem II efficiency (Fv’/Fm’); (C) electron transport rate (ETR); and (D) effective quantum yield (ΦPSII) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05, (n = 9).
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Figure 4. (A) Carbon assimilation (Anet); (B) transpiration (E); (C,D) stomatal conductance (gs); (E,F) efficiency of RuBisCO activity (Anet/Ci); (G) internal leaf CO2 concentration (Ci) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 9).
Figure 4. (A) Carbon assimilation (Anet); (B) transpiration (E); (C,D) stomatal conductance (gs); (E,F) efficiency of RuBisCO activity (Anet/Ci); (G) internal leaf CO2 concentration (Ci) in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 9).
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Figure 5. (A) Anthocyanin content; (B) carotenoids content; (C) chlorophyll a; (D) chlorophyll b; and (E) chlorophyll a/chlorophyll b in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 6).
Figure 5. (A) Anthocyanin content; (B) carotenoids content; (C) chlorophyll a; (D) chlorophyll b; and (E) chlorophyll a/chlorophyll b in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 6).
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Figure 6. (A) Hydrogen peroxide content; (B) lipid peroxidation; and (C,D) total phenolic compounds in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 6).
Figure 6. (A) Hydrogen peroxide content; (B) lipid peroxidation; and (C,D) total phenolic compounds in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 6).
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Figure 7. (A) Glucose; (B) fructose; (C) trehalose; (D) sucrose; (E) total soluble carbohydrates in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 4).
Figure 7. (A) Glucose; (B) fructose; (C) trehalose; (D) sucrose; (E) total soluble carbohydrates in Psidium guajava plants evaluated at 2 and 30 days after UV-B radiation application—with UV-B and without (UV-B absent). Means followed by the same letter do not differ from each other according to the Tukey test, p < 0.05. Capital letters compare averages between the application and absence of UV-B, and lowercase letters compare averages of the evaluation seasons (n = 4).
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Figure 8. Hierarchical cluster analysis presented as a heatmap of evaluations of maximum quantum yield of photosystem II efficiency (Fv/Fm); non-photochemical quenching (NPQ); minimum fluorescence (Fo); photosystem II efficiency (Fv’/Fm’); electron transport rate (ETR); effective quantum yield (ΦPSII, yield); fraction of dissipated excitation energy in the antenna that cannot be used for photochemical phase (Ex); light fraction absorbed by the PSII antenna that is dissipated as heat (D); carbon assimilation (Anet); transpiration (E); stomatal conductance (gs); carbon intern content (Ci); instant water usage efficiency (iWUE); efficiency of RuBisCO activity (Anet/Ci); contents of anthocyanin, carotenoids, and chlorophyll a and b (Chl a, Chl b); and the relation between chlorophyll a/chlorophyll b, hydrogen peroxide (H2O2), lipid peroxidation (MDA) phenolic compounds, contents of glucose, fructose, mannose, trehalose, and sucrose, and total soluble carbohydrates (total soluble carb) in Psidium guajava plants evaluated at 2 (GC) and 30 days (S) after UV-B radiation application—UV-B and UV-B absent (n = 3).
Figure 8. Hierarchical cluster analysis presented as a heatmap of evaluations of maximum quantum yield of photosystem II efficiency (Fv/Fm); non-photochemical quenching (NPQ); minimum fluorescence (Fo); photosystem II efficiency (Fv’/Fm’); electron transport rate (ETR); effective quantum yield (ΦPSII, yield); fraction of dissipated excitation energy in the antenna that cannot be used for photochemical phase (Ex); light fraction absorbed by the PSII antenna that is dissipated as heat (D); carbon assimilation (Anet); transpiration (E); stomatal conductance (gs); carbon intern content (Ci); instant water usage efficiency (iWUE); efficiency of RuBisCO activity (Anet/Ci); contents of anthocyanin, carotenoids, and chlorophyll a and b (Chl a, Chl b); and the relation between chlorophyll a/chlorophyll b, hydrogen peroxide (H2O2), lipid peroxidation (MDA) phenolic compounds, contents of glucose, fructose, mannose, trehalose, and sucrose, and total soluble carbohydrates (total soluble carb) in Psidium guajava plants evaluated at 2 (GC) and 30 days (S) after UV-B radiation application—UV-B and UV-B absent (n = 3).
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MDPI and ACS Style

Campos, F.G.; Dantas, M.O.; Santos, J.P.M.; Froes, S.S.; Gama, J.P.S.; Boaro, C.S.F. UV-B Radiation in the Acclimatization Mechanism of Psidium guajava in Sunlight. Horticulturae 2023, 9, 1291. https://doi.org/10.3390/horticulturae9121291

AMA Style

Campos FG, Dantas MO, Santos JPM, Froes SS, Gama JPS, Boaro CSF. UV-B Radiation in the Acclimatization Mechanism of Psidium guajava in Sunlight. Horticulturae. 2023; 9(12):1291. https://doi.org/10.3390/horticulturae9121291

Chicago/Turabian Style

Campos, Felipe G., Mariana O. Dantas, João P. M. Santos, Sophia S. Froes, João P. S. Gama, and Carmen S. F. Boaro. 2023. "UV-B Radiation in the Acclimatization Mechanism of Psidium guajava in Sunlight" Horticulturae 9, no. 12: 1291. https://doi.org/10.3390/horticulturae9121291

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