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Article

Light Quality Modulates Photosynthesis and Antioxidant Properties of B. vulgaris L. Plants from Seeds Irradiated with High-Energy Heavy Ions: Implications for Cultivation in Space

by
Ermenegilda Vitale
1,2,
Luigi Gennaro Izzo
2,
Chiara Amitrano
2,
Violeta Velikova
3,
Tsonko Tsonev
3,
Palma Simoniello
4,
Veronica De Micco
2 and
Carmen Arena
1,5,*
1
Department of Biology, University of Naples Federico II, Via Cinthia, 80126 Naples, Italy
2
Department of Agricultural Sciences, University of Naples Federico II, Via Università 100, 80055 Portici, Italy
3
Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., bl. 21, 1113 Sofia, Bulgaria
4
Department of Science and Technology, Parthenope University of Naples, Via Acton 38, 80133 Naples, Italy
5
BAT Center—Center for Studies on Bioinspired Agro-Environmental Technology, 80055 Portici, Italy
*
Author to whom correspondence should be addressed.
Plants 2022, 11(14), 1816; https://doi.org/10.3390/plants11141816
Submission received: 24 June 2022 / Revised: 6 July 2022 / Accepted: 7 July 2022 / Published: 10 July 2022
(This article belongs to the Special Issue The Impact of LED (Light-Emitting Diode) Spectra on Plant Growth and Quality)
Browse Figures
Versions Notes

Abstract

:
Beta vulgaris L. is a crop selected for cultivation in Space for its nutritional properties. However, exposure to ionizing radiation (IR) can alter plant photosynthetic performance and phytochemical production in the extraterrestrial environment. This study investigated if plant growth under different light quality regimes (FL—white fluorescent; RGB—red–green–blue; RB—red–blue) modifies the photosynthetic behavior and bioactive compound synthesis of plants sprouted by dry seeds irradiated with carbon or titanium high-energy ions. The study evidenced that: (i) the plant response depends on the type of heavyion; (ii) control and C-ion-irradiated plants were similar for photosynthetic pigment content and PSII photochemical efficiency, regardless of the LQ regime; (iii) under FL, net photosynthesis (AN) and water use efficiency (iWUE) declined in C- and Ti-ion plants compared to control, while the growth of irradiated plants under RGB and RB regimes offset these differences; (iv) the interaction Ti-ion× RB improved iWUE, and stimulated the production of pigments, carbohydrates, and antioxidants. The overall results highlighted that the cultivation of irradiated plants under specific LQ regimes effectively regulates photosynthesis and bioactive compound amounts in leaf edible tissues. In particular, the interaction Ti-ion × RB improved iWUE and increased pigments, carbohydrates, and antioxidant content.

Graphical Abstract

1. Introduction

The realization of Bioregenerative Life Support Systems (BLSSs) is crucial in considering future long-term human-crewed missions in Space. Transit vehicles, space stations, and platforms on Moon and Mars will include self-sustaining artificial eco-systems based on the balance between heterotrophs (humans and microorganisms) and autotrophs (plants or algae). In particular, higher plants significantly contribute to re-storing the resources in closed environments, regenerating and purifying air through CO2 absorption and O2 evolution and transpiration, as well as producing fresh food supplies for the crew [1,2,3,4].
Space is a harsh environment compared to Earth. Many factors may constrain the plant’s survival in the extraterrestrial environment, including altered gravity, the interaction between microgravity and fluid dynamics, ionizing radiation (IR), and modified pressure and temperature conditions. Among space factors, ionizing radiation represents the main hazard for the survival of life forms, including plants, in exploratory-class missions [5].
Understanding the effects of IR on photosynthetic apparatus and, in general, on plant metabolism is a prerequisite for cultivating plants in Space. IR may affect the photosynthetic process at different levels: from molecular, impacting light-harvesting complexes, reaction centers, and electron transport carriers, to physiological level by affecting primary and secondary photosynthetic metabolism, also through anatomical changes of leaf structure [6,7,8,9]. In addition, the radio-induced stress in plants triggers the production of a large variety of antioxidant compounds which are engaged in the detoxification of reactive oxygen species (ROS) and, at the same time, enriches the nutritional properties of plant tissues [4,10,11,12].
Generally, plant responses to IR depend on several variables, including species, phenological stage at the time of irradiation, dose, and radiation quality [5,6,13]. The space radiation environment consists of a wide variety of ion species with a continuous range of energies. The principal galactic cosmic rays (GCR) include high-energy protons, alpha particles, and heavy ions (HZE—high-energy nuclei component). Therefore, testing plant response to specific ions at proper acute doses is a vital prerequisite to assessing plant radiosensitivity and evaluating the suitability of different crops for cultivation in Space.
Carbon (C) and titanium (Ti) are among the heavy ions considered representative of HZE and are often used to simulate the GRC spectrum in ground-based experiments [14,15]. However, very little is known about titanium conversely to carbon ions. Early studies on animal models evidence that Ti-ions induce oxidative stress and genomic alterations associated with several health risks [16,17,18]. In plants, Ti-ions have been reported to improve starch mobilization towards actively growing tissues of eye bean seedlings and stimulate the production of antioxidants [19].
Therefore, the defining agricultural practices, as well as micro-environmental parameters, are essential for the selection of suitable crops for space farming. For example, plants have different requirements for light intensity, quality, and duration [3,20]. In particular, the light spectral composition affects not only germination [21], plant architecture, and leaf anatomy [22,23,24] but also physiological processes [25], such as stomatal opening regulation [26], photosynthesis [27,28,29], pigment synthesis [30,31], and ultimately biomass production [20,32,33,34]. Furthermore, specific light quality treatments during growth may also stimulate the resistance to diseases and abiotic stress (high temperature, nutritional deficiency, and heavy metals) [27,35,36,37], improving the synthesis of antioxidants [38] which, in turn, can enhance the nutritional quality of crops [39].
Based on this evidence, the modulation of the light spectrum is a promising tool for improving plant productivity in space farming [40,41,42,43], also representing a means to face the constraints of the space environment.
From this perspective, studying the interaction between space IR and light quality (LQ) is gaining interest in space research. Recent studies on crops evidenced that the interplay LQ/IR may elicit essential plant traits, such as dwarf growth, increased photosynthesis and nutritional value [44,45]. The present study aimed to deepen the knowledge of the interaction between high-LET (Linear Energy Transfer) ionizing radiation and LQ on chard (B. vulgaris L. var. cicla) plants focusing specifically on the photosynthetic process to assess the suitability of this species to be cultivated in Bioregenerative Life Support Systems (BLSSs). Chard was chosen for this study because it is considered a functional food [46], and for the high nutritional value of its leaves, rich in healthy secondary metabolites. Furthermore, its compact size and the great amount of edible biomass make it suitable for Space cultivation [3].
The specific aims of this study were to investigate: (i) how the exposure of chard seeds C and Ti heavy ions, representative particles of the galactic cosmic rays, may affect the photosynthetic metabolism of chard; (ii) how plant development under specific LQ regimes may modify the photosynthetic response to C and Ti irradiation; (iii) if and at what level the interaction between IR and specific LQ treatments may promote the production of functional metabolites which are beneficial as a supplement for the astronauts’ diet.

2. Results

2.1. Germination and Plant Biomass

Irradiation with C- and Ti-ions caused a significant increase in GP (100%) under FL light compared to not-irradiated control. RB light also determined a significant increase in GP after irradiation with C- (100%) and Ti-ions (75%). The same tendency to increase GP after irradiation was found under RGB light, but the values were significantly higher only in the case of C-ions (100%) compared to Ti and control treatments (Figure 1).
IR and LQ as the main factors did not significantly affect total biomass (TB) and shoot biomass (SB) (Table 1). Contrarily, the interaction IR × LQ was significant. More specifically, the RB regime induced an increase in TB and SB (p < 0.05) in plants from irradiated seeds (C 10-RB, Ti 10-RB) compared to the control (Ctrl-RB).

2.2. Gas Exchanges and Chlorophyll Fluorescence Emission Measurements

The IR and LQ regimes strongly affected the photosynthetic performance of B. vulgaris plants as single factors and in combination. AN and gS of C-10 and Ti-10 plants declined (p < 0.01) and NPQ were raised (p < 0.05), while iWUE, ϕPSII, and Fv/Fm did not change significantly compared to control (Table 2). LQ, as a single factor, reduced AN (p < 0.05), gS, and ϕPSII, (p < 0.01) in RGB and RB compared to FL plants and an increased iWUE(p < 0.05) and NPQ (p < 0.001) (Table 2). No variation was observed in Fv/Fm regardless of the IR treatments and LQ regimes (Table 2, Figure 2f).
The interaction IR × LQ (under FL regime) showed a significant decline of AN (p < 0.001), gS (p < 0.001), and iWUE (p < 0.05) in both C-10- and Ti-10-irradiated plants compared to control (Figure 2a–c).
Growth under RGB and RB regimes did not induce any differences in AN and iWUE among irradiated plants and respective controls (Figure 2a–c), while gS showed the lowest (p < 0.01) value in C10-RGB plants (Figure 2b).
Within the C-10 plant group, RGB and RB regimes reduced (p < 0.001) AN and gS compared to FL but did not influence iWUE (Figure 2a–c). In C-10 plants, AN was unaffected by LQ, while RGB and RB regimes induced a decline (p < 0.001) in gS and an increase (p < 0.05) of iWUE compared to FL (Figure 2a–c). Within the Ti-10 plant group, the RGB and RB light regimes enhanced AN (p < 0.05), gS (p < 0.05), and iWUE (p < 0.01) compared to FL (Figure 2a–c).
In all LQ regimes, ϕPSII and Fv/Fm ratio were not significantly affected by ionizing radiation. Contrary, among RB plants, Ti-ions significantly increased NPQ (Figure 2d–f). Within control plants, LQ regimes did not affect chard photochemistry. On the contrary, within the C-10 and Ti-10 plant groups, the RGB and RB regimes reduced (p < 0.01) ϕPSII and increased (p < 0.01) NPQ compared to FL. The strongest reduction of ϕPSII and the highest rise of NPQ were measured in Ti-10 RB plants (Figure 2d–f).

2.3. Plants Nutritional Traits and Bioactive Compounds

IR treatments and LQ regimes, as a single factor or interaction, determined a substantial variation in the concentration of photosynthetic pigment, total carbohydrate, proteins, and antioxidants (Table 3).
IR induced an increase (p < 0.001) in CHL and CAR concentration and a reduction (p < 0.01) in POL and ANTH in Ti-10 compared to Ctrl and C-10 plants. On the contrary, compared to control, C-10 plants showed comparable concentration of CHL, CAR, POL, and ANTH, lower (p < 0.05) CARB and PROT content, and higher (p < 0.001) level of TAC.
LQ as a single factor determined a reduction (p < 0.001) in CHL, CAR, and CARB under RGB and RB regimes (p < 0.001) compared to FL (Table 3), while for PROT and POL, the RGB plant group showed the lowest value. No significant difference was detected between FL and RB regimes. However, for ANTH and TAC, the different LQ regimes exerted diverse responses: RGB reduced (p < 0.01) ANTH content compared to FL and RB but increased TAC (p < 0.01).
The analysis of interactions IR × LQ highlighted that both control and irradiated plants are characterized by lower (p < 0.001) CHL and CAR content under RGB and RB than under FL regime (Figure 3a,b).
Total carbohydrate content was affected by IR and LQ; indeed, it decreased (p < 0.05) in irradiated plants under the FL regime compared to control, while under RB, in Ti-10 plants, it was higher than in control (Figure 3c). C-FL plants showed the highest (p < 0.001) concentration of carbohydrates. In irradiated C-10 plants, the highest increase (p < 0.001) of carbohydrates was obtained under RGB regime, whereas within the Ti-10 plant group, the highest (p < 0.001) carbohydrate concentration was determined under the RB regime (Figure 3c).
The interaction IR × LQ consistently affected the protein content. Within the control and Ti-10 plant group, the protein content was not affected by LQ regimes. On the contrary, in the C-10 Gy plant group, the protein amount declined (p < 0.05) under RGB and RB compared to FL (Figure 3d).
The comparison among control and irradiated plants at the same LQ regimes showed that the RGB reduced (p < 0.05) the total protein content in both irradiated plants compared to control. Otherwise, under FL and RB, the total protein concentration decreased only in Ti-10-FL (p < 0.05) and C-10-RB (p < 0.05) plants, respectively (Figure 3d).
The interaction IR × LQ indicated that polyphenols significantly declined (p < 0.001) in T-10 plants regardless of LQ quality (Figure 4a). Under the FL regime, anthocyanins decreased (p < 0.01) in T-10-FL plants compared to Ctrl-FL plants. Conversely, under RGB and RB regimes, no significant difference in anthocyanin level was found between control and irradiated plants (Figure 4b). In the Ctrl plant group, anthocyanin concentration was lower (p < 0.05) under RGB than under FL and RB, whereas in C-10 and Ti-10 irradiated groups, anthocyanin levels increased under RB compared to FL and RGB regimes (Figure 4b).
Finally, the total antioxidant capacity within the control group increased (p < 0.05) under the RGB compared to FL and RB plants; in the C-10 plant group, the highest (p < 0.01) value was measured under the RGB regime, while in the Ti-10 plant group, the highest values were found under both RGB and FL (Figure 4c). The comparison among control and irradiated plants under the same LQ regime evidenced that under FL and RGB, C-10 plants showed the highest values of TAC (p < 0.001, p < 0.01, respectively). On the other hand, the RB regime promoted (p < 0.01) TAC in Ti-10 plants (Figure 4c).

2.4. Heatmap Analysis

An overview of all measured parameters in response to heavy ions irradiation (C-10 and Ti-10) and the three LQ regimes (FL, RGB, and RB) is reported in Figure 5.
The heatmap identified two main clusters. The first cluster (I) included plants sprouted from control and C-10-irradiated seeds grown under the FL regime. The second cluster (II) was split into two sub-clusters: the first incorporated Ti-10 irradiated plants grown under FL and RGB regimes; the second included control and C-10 plants grown under RB, control, and C-10 plants grown under RGB and Ti-10 plants grown under RB. The heatmap indicated that control and C-10 irradiated plants showed a similar response for different physiological and biochemical attributes regardless of the LQ regime. In particular, under FL, plants exhibited the highest values of biomass, pigments, PSII photochemical efficiency, and antioxidant compounds. Within the Ti-10 group, RB plants were characterized by higher values of iWUE and NPQ than FL and RGB plants. Finally, the heatmap indicated that LQ regimes exerted different physiological responses in B. vulgaris plants irradiated with C- or Ti-ions.

3. Discussion

This work highlighted that a low dose of carbon and titanium heavy ions, delivered at the seed stage, may modify the B. vulgaris eco-physiological response (i.e., photosynthesis and accumulation of bioactive compounds) depending on different light quality regimes during growth. These results may have implications on controlled environment agriculture, especially in extreme environments such as Space.
In the view of space cultivation, seed germination could represent a critical step. Previous research demonstrated that seed responses to IR depend on the plant species and the type of ion. The seed irradiation with C-ions at the dose of 10 Gy, reduced the germination rate in rice and bean [6,47], whereas no variation occurred in spinach for doses up to 15 Gy [48]. Conversely, there is still little information about the effect of Ti-ions on different species. Ti-ions did not affect the germination of bean seeds at the dose of 10 Gy [6]. In B. vulgaris seeds, the irradiation with C-ions promoted the percentage germination (100%) compared to control and Ti-ions, regardless of the LQ regimes. These results indicated that more energetic C-ions likely favored seed tegument porosity which, in turn, may have promoted germination through a higher water permeability [4,49]. In control plants, the reduction of germination under RGB and RB light regimes could be ascribed to the higher incidence of blue wavelengths, which generally inactivate the phytochrome A involved in seed germination [50]. Moreover, the higher percentage germination found in Ctrl-RGB compared to Ctrl-RB seeds may be ascribed to the presence of green wavelength, which is known to promote germination through phytochrome [51].
Generally, the exposure of plants to IR determines a reduction of plant growth and biomass, inducing a more compact plant architecture [4,52,53,54,55]. On the other hand, the RB growth regime may produce an enhancement in biomass depending on the intrinsic characteristics of the species [31,56]. In our case, IR and LQ as single factors did not affect plant biomass, but their interaction produced significant differences under RB light regime. In particular, C and Ti-RB plants were characterized by higher edible biomass than control, representing a suitable trait for plants destined to grow in BLSSs.
Heavy ions and LQ regimes and their interaction deeply affected the photosynthetic activity in B. vulgaris. IR generally impaired AN, gS, and iWUE, regardless of the type of radiation and dose [52,57,58,59,60]. Moreover, these parameters are strictly interconnected, as CO2 uptake and water use follow the same route through stomata [61]. In control plants, leaf gas exchanges were sensitive to LQ, especially under RGB and RB regimes that strongly reduced AN and gS compared to FL. The seed irradiation with C-ion seemed to offset the effect LQ on AN, which resulted comparable under all regimes. It is hypothesized that in C-ion irradiated plants, the high intensity of red and blue wavelengths of RGB and RB regimes may have improved the stomatal control, ultimately resulting in the enhancement of iWUE. However, the occurrence of stomatal limitations due to the potentially detrimental effects of C heavy ions on photosynthetic machinery cannot be excluded. On the other hand, the seed irradiation with Ti-ion under RGB and RB regimes stimulated AN and gS compared to FL, determining, also in this case, an improvement of iWUE. In response to different LQ regimes during growth, leaves of irradiated plants have probably adopted adjustments in mesophyll traits and stomatal movements to improve photosynthesis and iWUE [45]. According to other authors, RB wavelengths, alone or supplemented with the green light that penetrates deeper inside the canopy, may have induced changes in leaf thickness, promoting the CO2 diffusion within chloroplasts [56,62,63,64,65,66]. In addition, the blue wavelengths, acting on the guard cells, stimulated the stomatal opening, improving leaf conductance and consequently, photosynthesis [26,67,68,69].
Both IR and LQ affected not only the dark but also the light phase of photosynthesis and, more specifically, the partitioning of light energy. In RGB and RB plants, the reduction of ϕPSII was consistent with the decline of AN and the rise of NPQ, indicating that the photosynthetic apparatus diverted the light energy in thermal dissipation mechanisms in conditions of reduced carbon assimilation [70]. On the contrary, in C-10-FL plants, the AN decline was accompanied by high values of ϕPSII. In this case, photochemical processes different from photosynthesis (i.e., photorespiration, Mehler reaction) occurred to avoid photoinhibition and photooxidative damage to photosystems. This response suggested that under C-irradiation, plants adopted a mechanism to optimize the PSII efficiency by transferring the excess light energy, which is potentially detrimental for photosystems to the other photochemical processes [71]. Control and Ti-ion-irradiated plants showed similar photochemical behavior. However, the higher NPQ measured in Ti-10 RB plants suggested that thermal dissipation processes were amplified under Ti irradiation and used as a safety valve against putative photoinhibition damages [72,73]. The absence of difference in the maximum quantum efficiency of PSII (Fv/Fm) among all treatments confirmed the efficiency of the different regulatory mechanisms of absorbed light induced by different heavy ion treatments.
The photochemical reactions observed in RGB- and RB-irradiated plants were consistent with the lower photosynthetic pigment content. The down-regulation of chlorophyll and carotenoid biosynthesis represents a safety strategy to avoid excessive light harvesting. Since the pigment reduction occurred in both control and irradiated plants, it may be argued that it depended on LQ more than IR. Indeed, red wavelengths, being photosynthetically more efficient, usually determined a photosynthetic pigment reduction in different species [31,66,73,74,75,76].
Our study pointed out that the FL-irradiated plants exhibited a reduced carbohydrate and protein production compared to the control consistent with the decline of photosynthesis. Previous studies performed on different plant species exposed to gamma rays demonstrated that depending on dose and plant phenological stage, the carbohydrate and protein levels may decrease, remain unchanged, or increase [13,52,77,78,79]. Generally, the higher dosage of gamma irradiation breaks down the seed proteins releasing more amino acids. This process may inhibit protein synthesis, thus inducing a decline in plant total protein content [78,80]. Besides IR, LQ can also modulate sugar and protein production. For instance, RB may induce a reduction in sugars [81] or an enhancement of the sugar and protein content in several species [31,82,83]. The intrinsic characteristics of the specific heavy ions may have produced a different behavior under the RB regime, which exerted a positive effect only when applied to Ti-ion-irradiated plants.
IR strongly influenced TPC, ANTH, and TAC, depending on ion type. While C-ions did not affect the concentration of anthocyanins and polyphenols compared to controls, Ti-ions reduced these compounds. To counteract the IR-induced oxidative stress and mitigate the risk of disease, a diet rich in polyphenols is essential for astronauts. Usually, phenolic compounds exert a screening function against high levels of solar radiation; protecting cell structures from photoinhibition damages [37,54,84,85] the same way, they offset the detrimental effects of IR [54,75,85,86,87]. The effects of IR on polyphenols and anthocyanins are controversial because some irradiated plants showed an enhancement after the exposure to gamma and X-rays or C-heavy ions [54,59,75,86], while other species exhibited a decline [54,85]. The different outcomes depend on the radiation quality and dose. In our study, Ti-ions induced a decline in polyphenols content regardless of the growth LQ regime.
The anthocyanin concentration was not only affected by IR but also by LQ.
In both C- and Ti-irradiated plants, the RB regime stimulated the anthocyanin synthesis compared to FL and RGB. The biosynthesis of anthocyanins is typically associated with blue light, but it may also be stimulated by red and green wavelengths [37,88]. It may be supposed that the higher intensity of red wavelengths in RB compared to the other regimes may have boosted the anthocyanin production, improving the nutritional properties of chard as observed for many crops [89,90,91]. Hence, the increase in anthocyanins may be considered a desirable feature for irradiated B. vulgaris plants.
Finally, C-ions irradiation determined a consistent rise of the total antioxidant capacity, which may be ascribed to the production of several different compounds characterized by antioxidant properties, as for other species, such as lettuce, irradiated with UV and gamma rays [75,92,93]. The antioxidant response of Ti-ion-irradiated plants was enhanced under RGB and RB regimes, confirming that red and blue supplemented with green wavelengths can promote the synthesis of free radical scavenger molecules. These compounds potentially improve the antioxidant capacity of chard plants and enhance their tolerance to stress conditions and nutrient quality [39,91,94,95]. Moreover, the high antioxidant content may be considered an added value, also for the use of chard as a supplement for astronauts’ diet.

4. Materials and Methods

4.1. Plant Material, Irradiation Procedure, and Experimental Design

Beta vulgaris L. var. cicla (white chard) is a widely cultivated crop, considered a functional food because of its high content of secondary metabolites, associated with some beneficial effects, including anti-tumoral activity [96]. Moreover, its compactness and high ratio of edible biomass/wastes make chard one of the candidates’ crops to be cultivated in the Space Greenhouses, designed as Closed Ecological Life Support Systems [3].
Dry chard seeds (n = 150) were divided into not-irradiated control (n = 50) and treated groups (n = 100). More specifically, 50 seeds were irradiated with carbonium (isotope 12C; E: 300 MeV/u (monoenergetic), LET: 13 keV/µm; dose rate 1 Gy/min), and 50 seeds with titanium (isotope 50Ti; E: 1000 MeV/u (monoenergetic), LET: 108 keV/µm; dose rate 1 Gy/min) at the dose of 10 Gy. In particular, C-ions are considered reference radiation and the dose of 10 Gy, being below the threshold for DNA damage, may not be lethal for plant development [19,97]. Seeds were collected into T25-flasks and the irradiation was performed using a pencil beam in a spread-out Bragg peak (SOBP), at the heavy-ion synchrotron (SIS) at the GSI Helmholtz zentrumfür Schwerionenforschung GmbH, (Darmstadt, Germany).
The seeds were maintained in the same storage and transport facilities to avoid bias due to different conditions during traveling. Irradiated and not-irradiated (control) seeds were then transferred to the laboratory and placed in Petri dishes on three layers of filter paper to follow the germination process. Both germination and plant cultivation took place in a climatized room under three different light regimens: (1) FL, provided by white fluorescent tubes (Lumilux L360W/640 and L360W/830, Osram, Germany); (2) RGB (red–green–blue) and (3) RB (red–blue) provided by red, green, and blue LEDs (Octa Light LTD, Bulgaria) with the following emission peaks: 630 nm red, 510 nm green, 440 nm blue. The spectral composition of LQ treatments (Figure 6a,b) was measured by a SR-3000A spectroradiometer at 10 nm resolution (Macam Photometrics Ltd., Livingston, Scotland, UK) at the top of the canopy.
The total photosynthetic photon flux density (PPFD) was fixed at 300 ± 5 µmol photons m−2s−1 at the canopy level for all LQ regimes. All plants were kept under air temperature of 25/20 °C (day/night), relative humidity 60–70%, and a photoperiod of 12 h. Plants were fertilized with tap water and Hoagland’s solution every two weeks.
The plant growth was followed up to 60 days after sowing (DAS) at the Plant Physiology and Genetics Institute of the Bulgarian Academy of Science (Sofia, Bulgaria). Gas exchanges and fluorescence emission measurements were carried out 60 days after sowing (DAS) on fully expanded leaves to assess how radiation may have affected the functionality of the photosynthetic apparatus and if the plant growth under different LQ may have influenced the plant photosynthetic behavior. In addition, at the end of the vegetative cycle (60 DAS), biometrical measurements, leaf functional traits, photosynthetic pigments, total carbohydrates, and antioxidant content were also determined on mature leaves as a proxy for carbon allocation and plant nutritional status. These analyses were performed at the Department of Biology of University Federico II of Naples (Italy).
Figure 7 displays the schema of the experimental design of the study.

4.2. Germination and Biometrical Measurements

The percentage of seed germination under FL, RGB, and RBLQ regimes was evaluated. Seeds were considered germinated when the root protruded from the seed coat. The percentage germination (GP) was calculated at 7 days after sowing (DAS), according to the formula:
GP7DAS = [(Number of germinated seeds after 7 days)/Total seed number] × 100
After germination, 10 control, 10 C—ion, and 10 Ti—ion—irradiated seedlings were sown in 3.0 L pots filled with peat soil. At the end of the experimental period, 60 DAS, total biomass (TB), and shoot biomass (SB) were determined on five plants for each treatment, weighing the whole plant and the shoot portion, respectively. The TB and SB were expressed as grams of fresh weight per plant (g FW plant−1).

4.3. Leaf Gas Exchange and Chlorophyll aFluorescence Emission Measurements

Leaf gas exchange was measured at 60 DAS on five fully expanded leaves from five plants per treatment (one leaf per plant) by a portable gas-exchange system (LCpro+, ADC BioScientific, UK). The middle part of the leaf was clamped into the 6.25 cm2 gas-exchange cuvette and exposed to a constant flow of 300 μmol s−1 of synthetic air (79% N2, 21% O2, and 400 µmol mol−1 CO2). Measurements were carried out at 25 ± 2 °C leaf temperature and 500 µmol m−2s−1 photosynthetic photon flux density (PPFD). The relative humidity in the leaf chamber was set at 50–60%. The intrinsic water use efficiency (iWUE) was calculated as a ratio between photosynthesis (AN) and stomatal conductance to water (gs). All gas-exchange parameters were recorded after reaching a steady-state, usually 7–10 min for each measurement, and calculated by the equations of von Caemmerer and Farquhar [98] with the software operating within the gas-exchange system.
Chlorophyll a fluorescence measurements were carried out on five fully expanded leaves from five plants per treatment (one leaf per plant) using a Fluorescence Monitoring System (FMS, Hansathech Instruments, King’s Lynn, UK). The determination of minimum (Fo) and maximum (Fm) fluorescence was carried out on 30 min dark adapted leaves. The maximum quantum yield of PSII photochemistry (Fv/Fm) was determined as (Fm−Fo)/Fm. The measurements in the light were carried out on leaves adapted to PPFD of 500 µmol m−2 s−1. A saturating pulse of 0.8 s with >6000 µmol photons m−2 s−1 was applied to determine the maximum (Fm’) and the steady-state (Fs) fluorescence in light adapted conditions. The quantum yield of PSII electron transport (ϕPSII) was calculated according to Genty et al. [99] as: ϕPSII = (Fm’ − Fs)/Fm’. The non-photochemical quenching (NPQ) was calculated as NPQ = (Fm− Fm’)/Fm’ [100].

4.4. Determinationof Photosynthetic Pigments and Antioxidants

Photosynthetic pigment and antioxidant contents were determined on five fresh leaves collected from five different plants (one leaf per plant) from each experimental condition.
The determination of the photosynthetic pigments content, namely total chlorophylls (a + b) and carotenoids (x + c), was performed according to Lichtenthaler [101]. Leaf samples of the known area (0.283 cm2) were homogenized in ice-cold 100% acetone using a mortar and pestle. The extracts were centrifuged at 5000 rpm for 5 min in a Labofuge GL (Heraeus Sepatech, Hanau, Germany). The sample absorbance was measured by a spectrophotometer (UV-VIS Cary 100; Agilent Technologies) at wavelengths of 470, 645, and 662 nm. Pigment concentration was expressed as µg cm−2.
The total polyphenol content was evaluated on fresh samples powdered in liquid nitrogen. Samples were extracted in 80% methanol at 4 °C, centrifuged at 11,000 rpm for 5 min. The soluble fraction was mixed with 10% Folin–Ciocâlteu solution, 1:1 v/v, and after 3 min, 700 mM Na2CO3 solution was added to the resulting mixture (1:5, v/v). Samples were incubated for 2 h in the darkness. The absorbance was measured at 765 nm with a spectrophotometer (UV-VIS Cary 100; Agilent Technologies). The total polyphenol amount was expressed as mg of Gallic Acid Equivalents g−1 FW (mg GAE g−1 FW) using a gallic acid standard curve.
The anthocyanin content was determined on fresh samples powdered in liquid nitrogen, treated with methanol 1% HCl solution and stored overnight at 4 °C. After adding 1:0.6 (v/v) ultra-pure water and chloroform at 1:1.6, v/v), samples were centrifuged at 11,000 rpm for 5 min. After mixing the supernatant with 1:1 (v/v) (60% (methanol 1% HCl) 40% ultra-pure water)solution, the absorbance was measured using a spectrophotometer (UV-VIS Cary 100, Agilent Technologies, Palo Alto, CA, USA) at 530 and 657 nm. The relative amount of anthocyanin was expressed as (A530—1/3A657) g−1 FW [102].
The antioxidant capacity was assessed by the Ferric Reducing Antioxidant Power (FRAP) assay, performed on fresh leaves powdered in liquid nitrogen, according to George et al. [103]. Briefly, the samples (0.250 g) were treated with methanol/water solution (60:40, v/v) and centrifuged at 14,000 rpm for 15 min at 4 °C. The extracts were mixed with the FRAP reagents (300 mM acetate buffer pH 3.6, 1:16.6 v/v; 10 mM tripyridyltriazine, TPTZ, in 40 mM HCl, 1:1.6 v/v; 12 mM FeCl3, 1:1.6 v/v) and incubated for 1 h in the dark. Then, the absorbance was read at 593 nm by a spectrophotometer (UV-VIS Cary 100; Agilent Technologies). The antioxidant capacity was calculated using a Trolox standard curve and expressed as µmol Trolox equivalents g−1 FW (µmol Trolox eq g−1 FW).

4.5. Total Soluble Carbohydrate Content and Protein Quantification

Total soluble carbohydrates were determined on five leaves for each treatment by the anthrone method, as reported in Hedge and Hofreiter [104]. The absorbance was measured at 630 nm using a spectrophotometer (UV-VIS Cary 100, Agilent Technologies, Palo Alto, CA, USA). The amount of soluble carbohydrates in the extracts was expressed as mg Glucose equivalents g−1 FW (mg Glu eq g−1 FW) using a Glucose standard curve.
Protein extraction was carried out on five fresh leaf samples ground in liquid nitrogen, according to Wang et al. [105]. Total protein content was quantified by Bradford colorimetric assay [106], measuring the sample absorbance at 595 nm by a spectrophotometer (UV-VIS Cary 100, Agilent Technologies, Palo Alto, CA, USA). Using a BSA standard curve, the protein concentration was expressed as µg BSA (bovine serum albumin) equivalents g−1 FW.

4.6. Statistical Analysis

Statistical data analysis was performed using SigmaPlot 12 software (Jandel Scientific, San Rafael, CA, USA). The effect of IR (C- and Ti-ions) and LQ regimes (FL, RGB, RB) on morphological, ecophysiological, and biochemical traits of chard plants were evaluated by processing data by two-way analysis of variance (ANOVA) followed by Duncan multiple comparison tests (p < 0.05). The Kolmogorov–Smirnov test was used to check the normality. When the interaction between the two factors (IR×LQ) was significant, data were further processed by applying one-way ANOVA, and multiple comparison tests were done with the Duncan test.
The overall parameters were visualized by a heatmap, plotted using the ClustVis program package (https://biit.cs.ut.ee/clustvis/online, accessed on 20 June 2022) and clustering both rows and columns with Euclidean distance and average linkage. In the heatmap, the numeric differences were evidenced by a color scale: red and blue indicate increasing and decreasing values, respectively.

5. Conclusions

The irradiation of dry chard seeds with carbon or titanium high-energy ions significantly modified the plant response to light quality. In particular, under the FL regime, gas exchanges of C- and Ti-ion-irradiated plants strongly declined compared to control. However, control and C-ion-irradiated plants showed a physiological performance higher than titanium plants in terms of for pigments content, PSII photochemical efficiency, and bioactive compounds.
The growth under RGB and RB regimes offset the differences of gas exchanges between control and C- and Ti-ion plants. C-ions induced the strongest antioxidant response regardless of light quality regimes. Furthermore, the interaction Ti-ion × RB was effective in improving iWUE, and the production of pigments, carbohydrates, and antioxidants.
The overall results indicate that by manipulating the interaction IR × LQ, it is possible to regulate the photosynthesis in order to obtain plants that are more performing in resource regeneration linked to gas exchanges (CO2 removal, O2 production) but also to modify the bioactive compound amounts in leaf edible tissues, which may result in a beneficial outcome for the astronauts’ diet.

Author Contributions

Conceptualization, C.A. (Carmen Arena) and V.D.M.; methodology, C.A. (Carmen Arena), V.V., T.T., E.V., C.A. (Chiara Amitrano), L.G.I. and P.S.; formal analysis, T.T. and E.V.; investigation, V.V., T.T., L.G.I., E.V., C.A. (Carmen Arena), P.S., and C.A. (Chiara Amitrano); resources, V.V. and C.A. (Carmen Arena); data curation, E.V., T.T. and C.A. (Carmen Arena); writing—original draft preparation, E.V. and C.A. (Carmen Arena); writing—review and editing, all the authors; supervision, C.A. (Carmen Arena), V.V. and V.D.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data supporting the results of this study are accessible from the corresponding author (C.A. (Carmen Arena)) upon reasonable request.

Acknowledgments

The results presented here are based on the experiment SBio08_DeMicco per- formed at SIS18/Cave A at the GSI Helmholtz zentrum für Schwerionenforschung, Darmstadt (Germany) in the frame of FAIR Phase-0. The authors are grateful to Marco Durante, Head of the Biophysics Department at GSI Helmholtz zentrum für Schwerionenforschung for the irradiation of the samples, and for the scientific and technical support during the irradiation procedure.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Wolff, S.A.; Coelho, L.H.; Zabrodina, M.; Brinckmann, E.; Kittang, A.I. Plant mineral nutrition, gas exchanges and photosynthesis in space: A review. Adv. Space Res. 2013, 51, 465–475. [Google Scholar] [CrossRef]
  2. Wheeler, R.M. Agriculture for space: People and places paving the way. Open Agric. 2017, 2, 14–32. [Google Scholar] [CrossRef]
  3. Zabel, P. Designing a Closed Ecological Life Support System for Plants, Overview. In Handbook of Life Support Systems for Spacecraft and Extraterrestrial Habits; Seedhouse, E., Shayler, D., Eds.; Springer: Cham, Switzerland, 2018. [Google Scholar]
  4. Arena, C.; Vitale, E.; Hay Mele, B.; Cataletto, P.R.; Turano, M.; Simoniello, P.; De Micco, V. Suitability of Solanum lycopersicum L. ‘Microtom’ to be grown in Bioregenerative Life Support Systems: Exploring the effect of high-LET ionising radiation on photosynthesis, leaf structure and fruit traits. Plant Biol. 2019, 21, 615–626. [Google Scholar] [CrossRef] [PubMed]
  5. Arena, C.; De Micco, V.; De Maio, A. Growth alteration and leaf biochemical responses in Phaseolus vulgaris exposed to different doses of ionising radiation. Plant Biol. 2014, 161, 194–202. [Google Scholar] [CrossRef] [PubMed]
  6. De Micco, V.; Arena, C.; Pignalosa, D.; Durante, M. Effects of sparsely and densely ionizing radiation on plants. Radiat. Environ. Biophys. 2011, 50, 1–19. [Google Scholar] [CrossRef]
  7. Hwang, J.E.; Hwang, S.G.; Kim, S.E.; Lee, K.J.; Jang, C.S.; Kim, J.B.; Kim, S.H.; Ha, B.K.; Ahn, J.W.; Kang, S.Y.; et al. Transcriptome profiling in response to different types of ionizing radiation and identification of multiple radio marker genes in rice. Physiol. Plant. 2014, 150, 606–679. [Google Scholar] [CrossRef]
  8. Park, Y.C.; Kim, J.J.; Kim, D.S.; Jang, C.S. Rice RING E3 ligase may negatively regulate gamma-ray response to mediate the degradation of photosynthesis-related proteins. Planta 2015, 241, 1119–1129. [Google Scholar] [CrossRef]
  9. Arena, C.; Turano, M.; Hay Mele, B.; Cataletto, P.R.; Furia, M.; Pugliese, M.; De Micco, V. Anatomy, photochemical activity, and DNA polymorphism in leaves of dwarf tomato irradiated with X-rays. Biol. Plant. 2017, 61, 205–314. [Google Scholar] [CrossRef]
  10. Zaka, R.; Vandecasteele, C.M.; Misset, T.M. Effect of flow chronic doses of ionizing radiation on antioxidant enzymes and G6PDH activities in Stipacapillata (Poaceae). J. Exp. Bot. 2002, 53, 1979–1987. [Google Scholar] [CrossRef]
  11. Esnault, M.A.; Legue, F.; Chenal, C. Ionizing radiation: Advances in plant response. Environ. Exp. Bot. 2010, 68, 23–237. [Google Scholar] [CrossRef]
  12. Kim, J.H.; Moon, Y.R.; Lee, M.H.; Kim, J.H.; Wi, S.G.; Park, B.J.; Kim, C.S.; Chung, B.Y. Photosynthetic capacity of Arabidopsis Plants at the reproductive stage tolerates γ-irradiation. J. Radiat. Res. 2011, 52, 441–449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Jan, S.; Parween, T.; Siddiqqi, T.O.; Mahmooduzzafar. Effect of gamma radiation on morphological, biochemical, and physiological aspects of plants and plant products. Environ. Rev. 2012, 20, 17–39. [Google Scholar] [CrossRef] [Green Version]
  14. Schuy, C.; Weber, U.; Durante, M. Hybrid active-passive space radiation simulation concept for GSI and the future FAIR facility. Front. Phys. 2020, 8, 337. [Google Scholar] [CrossRef]
  15. Simonsen, L.C.; Slaba, T.C.; Guida, P.; Rusek, A. NASA’s first ground-based Galactic Cosmic Ray Simulator: Enabling a new era in space radiobiology research. PLoS Biol. 2020, 18, e3000669. [Google Scholar] [CrossRef]
  16. Jangiam, W.; Tungjai, M.; Rithidech, K.N. Induction of chronic oxidative stress, chronic inflammation and aberrant patterns of DNA methylation in the liver of titanium exposed CBA/Caj mice. Int. J. Radiat. Biol. 2015, 91, 389–398. [Google Scholar] [CrossRef]
  17. Rithidech, K.N.; Jangiam, W.; Tungjai, M.; Gordon, C.; Honikei, L.; Whorton, E.B. Induction of chronic inflammation and altered levels of DNA Hydroxymethylation in Somatic and Germinal tissue of CBA/CaJ Mice exposed to 48Ti ions. Front. Oncol. 2016, 6, 155. [Google Scholar] [CrossRef] [Green Version]
  18. Li, Z.; Jella, K.K.; Jaafar, L.; Li, S.; Park, S.; Story, M.D.; Wang, H.; Wang, Y.; Dynan, W.S. Exposure to galactic cosmic radiation compromises DNA repair and increases the potential for oncogenic chromosomal. Sci. Rep. 2018, 8, 11038. [Google Scholar] [CrossRef]
  19. De Micco, V.; De Francesco, S.; Amitrano, C.; Arena, C. Comparative Analysis of the Effect of Carbon- and Titanium-Ions Irradiation on Morpho-Anatomical and Biochemical Traits of Dolichosmelanophthalmus DC. Seedlings Aimed to Space Exploration. Plants 2021, 10, 2272. [Google Scholar] [CrossRef]
  20. Ouzounis, T.; Rosenqvist, E.; Ottesen, C.O. Spectral effects of artificial light on plant physiology and secondary metabolism: A review. HortScience 2015, 50, 1128–1135. [Google Scholar] [CrossRef] [Green Version]
  21. Barrero, J.M.; Jacobsen, J.V.; Talbot, M.J.; White, R.G.; Swain, S.M.; Garvin, D.F.; Gubler, F. Grain dormancy and light quality effects on germination in the model grass Brachypodium distachyon. New Phytol. 2012, 193, 376–386. [Google Scholar] [CrossRef]
  22. Liu, X.Y.; Guo, S.R.; Xu, Z.G.; Jiao, X.L.; Takafumi, T. Regulation of chloroplast ultrastructure, cross-section anatomy of leaves, and morphology of stomata of cherry tomato by light-emitting diodes. HortScience 2011, 45, 217–221. [Google Scholar]
  23. Singh, D.; Basu, C.; Meinhardt-Wollweber, M.; Roth, B. LEDs for energy efficient greenhouse lighting. Renew. Sust. Energ. Rev. 2015, 49, 139–147. [Google Scholar] [CrossRef] [Green Version]
  24. Izzo, L.G.; Mickens, M.A.; Aronne, G.; Gómez, C. Spectral effects of blue and red light on growth, anatomy, and physiology of lettuce. Physiol. Plant. 2021, 172, 2191–2202. [Google Scholar] [CrossRef]
  25. Olle, M.; Viršilė, A. The effects of light-emitting diode lighting on greenhouse plant growth and quality. Agric. Food Sci. 2013, 22, 223–234. [Google Scholar] [CrossRef]
  26. Goins, G.D.; Yorio, N.C.; Sanwo, M.M.; Brown, C.S. Photomorphogenesis, photosynthesis, and seed yield of wheat plants grown under red light-emitting diodes (LED) with and without supplemental blue light. J. Exp. Bot. 1997, 48, 1407–1413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Arena, C.; Tsonev, T.; Doneva, D.; De Micco, V.; Michelozzi, M.; Brunetti, C.; Centritto, M.; Fineschi, S.; Velikova, V.; Loreto, F. The effect of light quality on growth, photosynthesis, leaf anatomy and volatile isoprenoids of a monoterpene-emitting herbaceous species (Solanum lycopersicum L.) and an isoprene-emitting tree (Platanusorientalis L.). Environ. Exp. Bot. 2016, 130, 122–132. [Google Scholar] [CrossRef]
  28. Trouwborst, G.; Hogewoning, S.W.; van Kooten, O.; Harbinson, J.; van Ieperen, W. Plasticity of photosynthesis after the red-light syndrome in cucumber. Environ. Exp. Bot. 2016, 121, 12175–12182. [Google Scholar] [CrossRef]
  29. Izzo, L.G.; Hay Mele, B.; Vitale, L.; Vitale, E.; Arena, C. The role of monochromatic red and blue light in tomato early photomorphogenesis and photosynthetic traits. Environ. Exp. Bot. 2020, 179, 104195. [Google Scholar] [CrossRef]
  30. Fan, X.X.; Xu, Z.G.; Liu, X.Y.; Tang, C.M.; Wang, L.W.; Han, V.L. Effects of light intensity on the growth and leaf development of young tomato plants grown under a combination of red and blue light. Sci. Hortic. 2013, 153, 50–55. [Google Scholar] [CrossRef]
  31. Amitrano, C.; Vitale, E.; De Micco, V.; Arena, C. Light fertilization affects growth and photosynthesis in mung bean (Vigna radiata) plants. J. Environ. Account. Manag. 2018, 6, 295–304. [Google Scholar] [CrossRef]
  32. Li, Q.; Kubota, C. Effects of supplemental light quality on growth and phytochemicals of baby leaf lettuce. Environ. Exp. Bot. 2009, 67, 59–64. [Google Scholar] [CrossRef]
  33. Hernández, R.; Kubota, C. Physiological responses of cucumber seedlings under different blue and red photon flux ratios using LEDs. Environ. Exp. Bot. 2016, 121, 66–74. [Google Scholar] [CrossRef]
  34. Sams, C.E.; Kopsell, D.; Morrow, R.C. Light quality impacts on growth, flowering, mineral uptake and petal pigmentation of marigold. Proc. VIII Int. Symp. Light Hortic. 2016, 8, 139–145. [Google Scholar]
  35. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef]
  36. Tuteja, N.; Gill, S.S.; Tuteja, R. Plant responses to abiotic stresses: Shedding light on salt, drought, cold and heavy metal stress. In Omics and Plant Abiotic Stress Tolerance; Tuteja, N., Singh, S.G., Tuteja, R., Eds.; Bentham Science Publisher Ltd.: Sharjah, United Arab Emirates, 2011; Volume 3, pp. 39–64. [Google Scholar]
  37. Bian, Z.H.; Yang, Q.C.; Liu, W.K. Effects of light quality on the accumulation of phytochemicals in vegetables produced in controlled environments: A review. Sci. Food Agric. 2015, 95, 869–877. [Google Scholar] [CrossRef]
  38. Ohashi-Kaneko, K.; Matsuda, R.; Goto, E.; Fujiwara, K.; Kurata, K. Growth of rice plants under red light with or without supplemental blue light. Soil Sci. Plant Nutr. 2006, 52, 444–452. [Google Scholar] [CrossRef]
  39. Hasan, M.M.; Bashir, T.; Gosh, R.; Lee, S.K.; Bae, H. An Overview of LEDs’ Effects on the Production of Bioactive Compounds and Crop Quality. Molecules 2017, 12, 1420. [Google Scholar] [CrossRef] [Green Version]
  40. Massa, G.D.; Kim, H.H.; Wheeler, R.M.; Mitchell, C.A.; Cary, A. Plant productivity in response to LED lighting. Hortic. Sci. 2008, 43, 1951–1956. [Google Scholar] [CrossRef]
  41. Avercheva, O.; Berkovich, Y.A.; Smolyanina, S.; Bassarskaya, E.; Pogosyan, S.; Ptushenko, V.; Erokhin, A.; Zhigalova, T. Biochemical, photosynthetic and productive parameters of Chinese cabbage grown under blue–red LED assembly designed for space agriculture. Adv. Space Res. 2014, 53, 1574–1581. [Google Scholar] [CrossRef]
  42. Mitchell, C.A.; Dzakovich, M.P.; Gomez, C.; Lopez, R.; Burr, J.F.; Hernández, R.; Kubota, C.; Currey, C.J.; Meng, Q.; Runkle, E.S.; et al. Light-emitting diodes in horticulture. Hortic. Rev. 2015, 43, 1–87. [Google Scholar]
  43. Gómez, C.; Izzo, L.G. Increasing efficiency of crop production with LEDs. AIMS Agric. Food 2018, 3, 135–153. [Google Scholar] [CrossRef]
  44. De Micco, V.; Amitrano, C.; Vitaglione, P.; Ferracane, C.; Pugliese, M.; Arena, C. Effect of light quality and ionising radiation on morphological and nutraceutical traits of sprouts for astronauts’ diet. Acta Astronaut. 2021, 185, 188–197. [Google Scholar] [CrossRef]
  45. Vitale, E.; Vitale, L.; Costanzo, G.; Velikova, V.; Tsonev, T.; Simoniello, P.; De Micco, V.; Arena, C. Light Spectral Composition Influences Structural and Eco-Physiological Traits of Solanum lycopersicum L. cv. ‘Microtom’ in Response to High-LET Ionizing Radiation. Plants 2021, 10, 1752. [Google Scholar] [CrossRef] [PubMed]
  46. Ivanović, L.; Milašević, I.; Topalović, A.; Durović, D.; Mugoša, B.; Knežević, M.; Vrvić, M. Nutritional and phytochemical content of Swiss chard from Montenegro, under different fertilization and irrigation treatments. Br. Food J. 2018, 121, 411–425. [Google Scholar] [CrossRef]
  47. Sjahril, R.; Riadi, M.; Raffiundin, S.T.; Toriyama, K.; Abe, T.; Trisnawaty, A.R. Effect of heavy ion beam irradiation on germination of local Toraja rice seed (M1-M2) mutant generation. IOP Conference Series. Earth Environ. Sci. 2018, 157, 012046. [Google Scholar] [CrossRef]
  48. Komai, F.; Shikazono, N.; Tanaka, A. Sexual modification of female spinach seeds (Spinacia oleracea L.) by irradiation with ion particles. Plant Cell Rep. 2003, 21, 713–717. [Google Scholar] [CrossRef]
  49. Hammond, E.C.; Bridgers, K.; Berry, F.D. Germination, growth rates, and electron microscope analysis of tomato seeds flown on the LDEF. Radiat. Meas. 1996, 26, 851–861. [Google Scholar] [CrossRef] [Green Version]
  50. Barrero, J.M.; Downie, A.B.; Xu, Q.; Gubler, F. A Role for Barley Cryptochrome1 in Light Regulation of Grain Dormancy and Germination. Plant Cell 2014, 26, 1094–1104. [Google Scholar] [CrossRef] [Green Version]
  51. Shinomura, T.; Nagatani, A.; Hanzawa, H.; Kubota, M.; Watanabe, M.; Furuya, M. Action spectra for phytochrome A-and B- specific photoinduction of seed germination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 1996, 93, 8129–8133. [Google Scholar] [CrossRef] [Green Version]
  52. Thiede, M.E.; Link, S.O.; Fellows, R.J.; Beedlow, P.A. Effect of gamma radiation on stem diameter growth, carbon gain and biomass partitioning in Helianthus annus. Environ. Exp. Bot. 1995, 35, 33–41. [Google Scholar] [CrossRef]
  53. Honda, I.; Kikuchi, K.; Matsuo, S.; Fukuda, M.; Saito, H.; Ryuto, H.; Fukunishi, N.; Abe, T. Heavy-ion-induced mutants in sweet pepper isolated by M1 plant selection. Euphytica 2006, 152, 61–66. [Google Scholar] [CrossRef]
  54. De Micco, V.; Paradiso, R.; Aronne, G.; De Pascale, S.; Quarto, M.; Arena, C. Leaf Anatomy and Photochemical Behaviour of Solanum lycopersicum L. Plants from Seeds Irradiated with Low-LET Ionising Radiation. Sci. World J. 2014, 2014, 428141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Jo, Y.D.; Kim, S.H.; Hwang, J.E.; Kim, Y.S.; Kang, H.S.; Kim, S.W.; Kwon, S.J.; Ryu, J.; Kim, J.B.; Kang, S.Y. Construction of mutation populations by Gamma-ray and Carbon beam irradiated in Chili pepper (Capsicum annuum L.). Hortic. Environ. Biotchnol. 2016, 57, 606–614. [Google Scholar] [CrossRef]
  56. Kim, H.H.; Wheeler, R.M.; Sager, J.C.; Gains, G.D.; Naikane, J.H. Evaluation of lettuce growth using supplemental green light with red and blue light-emitting diodes in a controlled environment—A review of research at Kennedy Space Center. V International Symposium on Artificial Lighting in Horticulture. Acta Hortic. 2006, 711, 111–120. [Google Scholar] [CrossRef]
  57. Ursino, D.J.; Schefski, H.; McCabe, J. Radiation-induced changes in rate of photosynthetic CO2 uptake in soybean plants. Environ. Exp. Bot. 1977, 17, 27–34. [Google Scholar] [CrossRef]
  58. Jia, C.F.; Li, A.L. Effect of gamma radiation on mutant induction of Fagopyrum dibotrys Hara. Photosynthetica 2008, 46, 363–369. [Google Scholar] [CrossRef]
  59. Moghaddam, S.S.; Jaafar, H.; Ibrahim, R.; Rahmat, A.; Maheran, A.A.; Philip, E. Effects of Acute Gamma Irradiation on Physiological Traits and Flavonoid accumulation of Centella asiatica. Molecules 2011, 16, 4994–5007. [Google Scholar] [CrossRef] [Green Version]
  60. Fan, J.; Shi, M.; Huang, J.Z.; Xu, J.; Wang, Z.D.; Guo, D.P. Regulation of photosynthetic performance and antioxidant capacity by 60Co γ-irradiation in Zizania latifolia plants. J. Environ. Radioact. 2014, 129, 33–42. [Google Scholar] [CrossRef]
  61. Jones, H. What is water use efficiency. In Water Use Efficiency in Plant Biology? Bacon, M., Ed.; Blackwell Publishing: Hoboken, NJ, USA; CRC Press: Boca Raton, FL, USA, 2004. [Google Scholar]
  62. Sun, J.; Nishio, J.N.; Vofelmann, T.C. Green light drives CO2 fixation deep within leaves. Plant Cell Physiol. 1998, 39, 1020–1026. [Google Scholar] [CrossRef]
  63. Brodersen, C.R.; Vogelmann, T.C. Do changes in light direction affect absorption profiles in leaves? Funct. Plant Biol. 2010, 37, 403–412. [Google Scholar] [CrossRef]
  64. Terashima, I.; Hanba, Y.T.; Tholen, D.; Niinemets, U. Leaf Functional Anatomy in Relation to Photosynthesis. Plant Physiol. 2011, 155, 108–116. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Smith, H.L.; McAusland, L.; Murchie, E.H. Don’t ignore the green light: Exploring diverse roles in plant processes. J. Exp. Bot. 2017, 68, 2099–2110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Zhang, L.; Van-Labeke, M.C. Long-term effects of Red-and Blue-Light Emitting Diodes on leaf anatomy and photosynthetic efficiency of three ornamental pot plants. Front. Plant Sci. 2017, 8, 917. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  67. Akoyunoglou, G.; Anni, H. Blue light effect on chloroplast development in higher plants. In Blue Light Effects in Biological Systems; Senger, H., Ed.; Springer: Berlin, Germany, 1984; pp. 397–406. [Google Scholar]
  68. Sæbø, A.; Krekling, T.; Applegren, M. Light quality affects photosynthesis and leaf anatomy of birch plantlets in vitro. Plant Cell Tissue Org. Cult. 1995, 41, 177–185. [Google Scholar] [CrossRef]
  69. Brown, C.S.; Schuerger, A.C.; Sager, J.C. Growth and photomorphogenesis of pepper plants under red light-emitting diodes with supplemental blue or far-red lighting. J. Am. Soc. Hortic. Sci. 1995, 120, 808–813. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  70. Yang, L.Y.; Wang, L.T.; Ma, J.H.; Ma, E.D.; Li, J.Y.; Gong, M. Effect of light quality on growth and development, photosynthetic characteristics and content of carbohydrates in tobacco (Nicotiana tabacum L.) plants. Photosynthetica 2017, 55, 467–477. [Google Scholar] [CrossRef]
  71. Guidi, L.; Lo Piccolo, E.; Landi, M. Chlorophyll Fluorescence, Photoinhibition and Abiotic Stress: Does it Make Any Difference the Fact to Be a C3 or C4 Species? Front. Plant Sci. 2019, 10, 174. [Google Scholar] [CrossRef] [PubMed]
  72. Demmig-Adams, B.; Garab, G.; Adams, W.W.; Govindjee, U. Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria; Springer: Dordrecht, The Netherlands, 2014. [Google Scholar]
  73. Hamdani, S.; Khan, N.; Perveen, S.; Qu, M.; Jiang, J.; Govindjee, U.; Zhu, X.G. Changes in the photosynthesis properties and photoprotection capacity in rise (Oryza sativa) grown under red, blue, or white light. Photosynth. Res. 2019, 139, 107–121. [Google Scholar] [CrossRef]
  74. Sood, S.; Gupta, V.; Tripathy, B.C. Photoregulation of the greening process of wheat seedlings grown in red light. Plant Mol. Biol. 2005, 59, 269–287. [Google Scholar] [CrossRef]
  75. Fan, X. Antioxidant capacity of fresh-cut vegetables exposed to ionizing radiation. J. Sci. Food Agric. 2005, 85, 995–1000. [Google Scholar] [CrossRef]
  76. Liu, Y.; Wang, T.; Fang, S.; Zhou, M.; Qin, J. Responses of Morphology, Gas Exchange, Photochemical Activity of Photosystem II, and Antioxidant Balance in Cyclocaryapaliurus to Light Spectra. Front. Plant Sci. 2018, 9, 1704. [Google Scholar] [CrossRef] [Green Version]
  77. Stajner, D.; Milosevic, M.; Popovic, B.M. Irradiation effects on phenolic content, lipid and protein oxidation and scavenger ability of soybean seeds. Int. J. Mol. Sci. 2007, 8, 618–627. [Google Scholar] [CrossRef] [Green Version]
  78. Kiong, A.L.P.; Lai, A.G.; Hussein, S.; Harun, A.R. Physiological Responses of Orthosiphon stamineus Plantles to Gamma Irradiation. Am. Eurasian J. Sustain. Agric. 2008, 2, 135–149. [Google Scholar]
  79. El-Beltagi, H.S.; Ahmed, O.K.; El-Desouky, W. Effect of low doses γ-irradiation on oxidative stress and secondary metabolites production of rosemary (Rosmarinus officinalis L.) callus culture. Radiat. Phys. Chem. 2011, 80, 968–976. [Google Scholar] [CrossRef]
  80. Hammeed, A.; Shah, T.M.; Atta, B.M.; Haq, M.A.; Sayed, H. Gamma Irradiation effects on seed germination and growth, protein content, peroxidase and protease activity, lipid peroxidation in Desi and Kabuli Chickpea. Pak. J. Bot. 2008, 40, 1033–1041. [Google Scholar]
  81. Chen, Q.F.; Ya, H.Y.; Feng, Y.R.; Jiao, Z. Expression of the Key Genes Involved in ABA Biosynthesis in Rice Implanted by Ion Beam. Appl. Biochem. Biotechnol. 2014, 173, 239–247. [Google Scholar] [CrossRef]
  82. Zhang, L.; Liu, S.; Zhang, Z.; Yang, R.; Yang, X. Dynamic effects of different light qualities on pea sprouts quality. North. Hortic. 2010, 8, 4–7. [Google Scholar]
  83. Li, H.; Tang, C.; Xu, Z.; Liu, X.; Han, X. Effects of Different Light Sources on the Growth of Non-heading Chinese Cabbage (Brassica campestris L.). J. Agric. Sci. 2012, 4, 262–273. [Google Scholar] [CrossRef] [Green Version]
  84. Lattanzio, V.; Kroon, P.A.; Quideau, S. Plant phenolics—Secondary metabolites with diverse functions. In Recent Advances in Polyphenol Research; Daay, F., Lattanzio, V., Eds.; Wiley-Blackwell: Oxford, UK, 2008; pp. 1–35. [Google Scholar]
  85. De Micco, V.; Arena, C.; Aronne, G. Anatomical alterations of Phaseolus vulgaris L. mature leaves irradiated with X-rays. Plant Biol. 2014, 16, 187–193. [Google Scholar] [CrossRef]
  86. He, J.; Dong, L.; Lixia, Y.; Wenjian, L. Pigment analysis of color-leaf mutant in Wanderig Jew (Tradescantiafluminensis) irradiated by carbon ions. Nucl. Sci. Techol. 2011, 22, 77–83. [Google Scholar]
  87. Arena, C.; De Micco, V.; Aronne, G.; Pugliese, M.; Virzo, A.; De Maio, A. Response of Phaseolus vulgaris L. plants to low-LET ionisingradiation: Growth and oxidative stress. Acta Astronaut. 2013, 91, 107–114. [Google Scholar] [CrossRef]
  88. Lekkham, P.; Srilaong, V.; Pongprasert, N.; Kondo, S. Anthocyanin concentration and antioxidant activity in light-emitting diode (LED)-treated apples in a greenhouse environmental control system. Fruits 2016, 71, 269–274. [Google Scholar] [CrossRef] [Green Version]
  89. Agarwal, A.; Gupta, S.D.; Barman, M.; Mitra, A. Photosynthetic apparatus plays a central role in photosensitive physiological acclimations affecting spinach (Spinacia oleracea L.) growth in response to blue and red photon flux ratios. Environ. Exp. Bot. 2018, 156, 170–182. [Google Scholar] [CrossRef]
  90. Lobiuc, A.; Vasilache, V.; Pintilie, O.; Stoleru, T.; Burducea, M.; Oroian, M.; Zamfirache, M.M. Blue and Red LED Illumination Improves Growth and Bioactive Compounds Content in Acyanic and Cyanic OciumBasilicum L. Microgreens. Molecules 2017, 22, 2111. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  91. Livadariu, O.; Raiciu, D.; Maximilian, C.; Capitanu, E. Studies regarding treatments of LED-s emitted light on sprouting hemp (Cannabis sativa L.). Rom. Biotechnol. Lett. 2018, 24, 485–490. [Google Scholar] [CrossRef]
  92. Alothman, M.; Bhat, R.; Karim, A.A. Effects of radiation processing on phytochemicals and antioxidants in plant procedure. Trends Food Sci. Technol. 2009, 20, 201–212. [Google Scholar] [CrossRef]
  93. Sallam, E.M.; Anwar, M.M. Antioxidant Activity of some Extracts from Gamma irradiated Purslane (Portulaca oleracea) Plant. Int. J. Agric. Biol. 2017, 19, 48–52. [Google Scholar] [CrossRef]
  94. Ohashi-Kaneko, K.; Takase, M.; Kon, N.; Fukiwara, K.; Kurata, K. Effect of light quality in leaf lettuce, spinach and komatsuna. Environ. Control Biol. 2007, 45, 189–198. [Google Scholar] [CrossRef] [Green Version]
  95. Samuolienė, G.; Urbanovičiūtė, A.; Brazaitytė, A.; Šabajevienė, G.; Sakalauskaitė, J.; Duchovskis, P. The impact of LED illumination on antioxidant properties of sprouted seeds. Cent. Eur. J. Biol. 2011, 6, 68–74. [Google Scholar] [CrossRef]
  96. Ninfali, P.; Angelino, D. Nutritional and functional potential of Beta vulgariscicla and rubra. Fitoterapia 2013, 89, 188–199. [Google Scholar] [CrossRef]
  97. Kazama, Y.; Hirano, T.; Saito, H.; Liu, Y.; Ohbu, S.; Hayashi, Y.; Abe, T. Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. Plant Biol. 2011, 11, 161. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. von Caemmerer, S.; Farquhar, G.D. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 1981, 153, 376–387. [Google Scholar] [CrossRef] [PubMed]
  99. Genty, B.; Briantais, J.M.; Baker, N.R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 1989, 990, 87–92. [Google Scholar] [CrossRef]
  100. Bilger, W.; Björkman, O. Temperature dependence of violaxanthin deepoxidation and nonphotochemical fluorescence quenching in intact leaves of Gossypium kirsutum L. and Malva parviflora L. Planta 1991, 184, 226–234. [Google Scholar] [CrossRef]
  101. Lichtentaler, H.K. Chlorophylls and Carotenoids: Pigments of photosynthetic biomembranes. Meth. Enzymol. 1987, 148, 350–382. [Google Scholar]
  102. Mancinelli, A.L.; Yang, C.P.H.; Lindquist, P.; Anderson, O.R.; Rabino, I. Photocontrol of Anthocyanin Synthesis. Plant Physiol. 1975, 55, 251–257. [Google Scholar] [CrossRef] [Green Version]
  103. George, B.; Kaur, C.; Khurdiya, D.S.; Kapoor, H.C. Antioxidants in tomato (Lycopersicumesculentum) as a function of genotype. Food Chem. 2004, 84, 45–51. [Google Scholar] [CrossRef]
  104. Hedge, J.E.; Hofreiter, B.T. Carbohydrate chemistry. In Methods in Carbohydrate Chemistry; Whistler, R.L., Be Miller, J.N., Eds.; Academic Press: New York, NY, USA, 1962; Volume 17. [Google Scholar]
  105. Wang, W.; Vignani, R.; Scali, M.; Cresti, M. A universal and rapid protocol for protein extraction from recalcitrant plant tissue for proteomic analysis. J. Electrophor. 2006, 27, 2782–2786. [Google Scholar] [CrossRef]
  106. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
Plants 11 01816 g001 550
Figure 1. Percentage germination (GP) of Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds of B. vulgaris under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 50). Different letters indicate statistically significant differences among treatments according to one-way ANOVA (p < 0.05).
Figure 1. Percentage germination (GP) of Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds of B. vulgaris under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 50). Different letters indicate statistically significant differences among treatments according to one-way ANOVA (p < 0.05).
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Plants 11 01816 g002 550
Figure 2. (a) Net CO2 assimilation, AN; (b) stomatal conductance, gS; (c) intrinsic water use efficiency, iWUE; (d) quantum yield of PSII electron transport, ϕPSII; (e) non-photochemical quenching, NPQ; (f) maximum PSII photochemical efficiency, Fv/Fm of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red–green–blue (RGB) and red-blue (RB) light quality regimes (n = 5). Different letters indicate statistically significant differences among light treatments according to one-way ANOVA (p < 0.05).
Figure 2. (a) Net CO2 assimilation, AN; (b) stomatal conductance, gS; (c) intrinsic water use efficiency, iWUE; (d) quantum yield of PSII electron transport, ϕPSII; (e) non-photochemical quenching, NPQ; (f) maximum PSII photochemical efficiency, Fv/Fm of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red–green–blue (RGB) and red-blue (RB) light quality regimes (n = 5). Different letters indicate statistically significant differences among light treatments according to one-way ANOVA (p < 0.05).
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Plants 11 01816 g003 550
Figure 3. (a) Total chlorophylls; (b) total carotenoids; (c) total carbohydrates; (d) total proteins of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 5). Different letters indicate statistically significant differences among treatments according to one-way ANOVA (p < 0.05).
Figure 3. (a) Total chlorophylls; (b) total carotenoids; (c) total carbohydrates; (d) total proteins of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 5). Different letters indicate statistically significant differences among treatments according to one-way ANOVA (p < 0.05).
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Plants 11 01816 g004 550
Figure 4. (a) Total polyphenol; (b) anthocyanin content; (c) total antioxidant capacity of B. vulgaris plants sprouted from Control (C) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 5). Different letters indicate statistically significant differences among treatments according to one-way ANOVA (p < 0.05).
Figure 4. (a) Total polyphenol; (b) anthocyanin content; (c) total antioxidant capacity of B. vulgaris plants sprouted from Control (C) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 5). Different letters indicate statistically significant differences among treatments according to one-way ANOVA (p < 0.05).
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Figure 5. Cluster heatmap analysis summarizing morphological, eco-physiological, and biochemical parameters of Beta vulgaris L. cv cicla plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red-green-blue (RGB) and red-blue (RB) LQ regimes. Numeric differences within the data matrix are shownby the color scale: light blue and dark blue indicate increasing and decreasing values, respectively. Parameters are clustered in the rows; sample groups are clustered in the columns by the two independent factors: IR treatment and LQ regimes.
Figure 5. Cluster heatmap analysis summarizing morphological, eco-physiological, and biochemical parameters of Beta vulgaris L. cv cicla plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy), and Titanium (Ti-10 Gy) seeds and grown under white fluorescent (FL), red-green-blue (RGB) and red-blue (RB) LQ regimes. Numeric differences within the data matrix are shownby the color scale: light blue and dark blue indicate increasing and decreasing values, respectively. Parameters are clustered in the rows; sample groups are clustered in the columns by the two independent factors: IR treatment and LQ regimes.
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Plants 11 01816 g006 550
Figure 6. (a) Spectral distributions in the relative energy of the light quality regimes used in the study: FL—white fluorescent tubes; LED RGB—red–green–blue; LED RB—red–blue. Photon flux density: 300 µmol m−2s−1; (b) Particular of growth chambers with RGB (front) and RB (back) light quality regimes.
Figure 6. (a) Spectral distributions in the relative energy of the light quality regimes used in the study: FL—white fluorescent tubes; LED RGB—red–green–blue; LED RB—red–blue. Photon flux density: 300 µmol m−2s−1; (b) Particular of growth chambers with RGB (front) and RB (back) light quality regimes.
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Figure 7. Schema of the experimental design created with BioRender.com (accessed on 2 May 2022).
Figure 7. Schema of the experimental design created with BioRender.com (accessed on 2 May 2022).
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Table
Table 1. Analysis of variance and comparison of means for total biomass (TB) and shoot biomass (SB) of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds, and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes.
Table 1. Analysis of variance and comparison of means for total biomass (TB) and shoot biomass (SB) of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds, and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes.
TBSB
IR
Ctrl25 a21 a
C-1027 a21 a
Ti-1027 a21 a
LQ
FL29 a23 a
RGB24 a19 a
RB26 a21 a
IR × LQ
Ctrl-FL31 a25 a
Ctrl-RGB28 a24 a
Ctrl-RB17 b14 b
C 10-FL28 a22 a
C 10-RGB25 a21 a
C 10-RB26 a21 a
Ti 10-FL30 a22 a
Ti 10-RGB23 a19 a
Ti 10-RB29 a22 a
Significance
IRNSNS
LQNSNS
IR × LQ**
TB—Total biomass, g FW plant−1; SB—Shoot biomass, g FW plant−1. Different letters in each column indicate significant differences according to Duncan’s test (p < 0.05). NS—not significant; * p < 0.05.
Table
Table 2. Analysis of variance and comparison of means for net CO2 assimilation (AN), stomatal conductance to water (gS), intrinsic water use efficiency (iWUE), quantum yield of PSII electron transport, ϕPSII, non-photochemical quenching (NPQ), maximum PSII photochemical efficiency, (Fv/Fm) of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds, and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes.
Table 2. Analysis of variance and comparison of means for net CO2 assimilation (AN), stomatal conductance to water (gS), intrinsic water use efficiency (iWUE), quantum yield of PSII electron transport, ϕPSII, non-photochemical quenching (NPQ), maximum PSII photochemical efficiency, (Fv/Fm) of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds, and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes.
ANgsiWUEϕPSIINPQFv/Fm
IR
Ctrl9.1 a0.16 a59 a0.34 a2.4 b0.76 a
C-106.7 b0.13 b53 a0.34 a2.7 a0.75 a
Ti-106.4 b0.13 b56 a0.29 a2.8 a0.74 a
LQ
FL7.9 a0.16 a48 b0.38 a2.2 b0.75 a
RGB7.4 b0.14 b55 b0.31 b2.8 a0.75 a
RB6.8 c0.12 c65 a0.28 b2.9 a0.75 a
Significance
IR******NSNS**NS
LQ**********NS
IR × LQ******NSNS***NS
AN—net CO2 assimilation (µmol CO2 m−2 s−1); gS—stomatal conductance to water (mol H2O m−2s−1), iWUE—intrinsic water use efficiency (µmol CO2 mol−1 H2O); ϕPSII—quantum yield of PSII electron transport; NPQ—non-photochemical quenching; Fv/Fm—maximum PSII photochemical efficiency. Different letters in the columns indicate significant differences according to Duncan’s test (p < 0.05). NS—not significant; * p < 0.05; ** p < 0.01; *** p < 0.001.
Table
Table 3. Analysis of variance and comparison of means for chlorophylls (CHL), carotenoids (CAR), carbohydrates (CARB), proteins (PROT), polyphenols (POL), anthocyanins (ANTH), and total antioxidant capacity (TAC) of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds, and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 5).
Table 3. Analysis of variance and comparison of means for chlorophylls (CHL), carotenoids (CAR), carbohydrates (CARB), proteins (PROT), polyphenols (POL), anthocyanins (ANTH), and total antioxidant capacity (TAC) of B. vulgaris plants sprouted from Control (Ctrl) and irradiated Carbon (C-10 Gy) and Titanium (Ti-10 Gy) seeds, and grown under white fluorescent (FL), red–green–blue (RGB) and red–blue (RB) light quality regimes (n = 5).
CHLCARCARBPROTPOLANTHTAC
IR
Ctrl38 b5.7 b36 a480 a0.91 a2.8 a2.8 c
C-1041 b6.7 b33 b347 b0.94 a2.9 a4.1 a
Ti-1047 a8.4 a31 b321 b0.47 b2.0 b3.3 b
LQ
FL54 a8.8 a42 a427 a0.81 a2.5 b3.0 b
RGB37 b5.7 b33 b337 b0.70 b1.9 c4.3 a
RB36 b5.9 b26 c381 a0.80 a3.3 a2.9 b
Significance
IR*******************
LQ*****************
IR × LQ*************NS***
CHL—Chlorophylls (µg cm−2); CAR—Carotenoids (µg cm−2); CARB—Carbohydrates (mg GLU eq g−1 FW); PROT—Proteins (µg BSA eq g−1 FW); POL—Polyphenols (mg GAE g−1 FW); ANTH—Anthocyanins ((A530-1/3A657) g−1 FW); TAC—Total antioxidant capacity (µmol Trolox eq g−1 FW). Different letters in each column indicate significant differences according to Duncan’s test (p < 0.05). NS—not significant; * p < 0.05; ** p < 0.01; *** p < 0.001.
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Vitale, E.; Izzo, L.G.; Amitrano, C.; Velikova, V.; Tsonev, T.; Simoniello, P.; De Micco, V.; Arena, C. Light Quality Modulates Photosynthesis and Antioxidant Properties of B. vulgaris L. Plants from Seeds Irradiated with High-Energy Heavy Ions: Implications for Cultivation in Space. Plants 2022, 11, 1816. https://doi.org/10.3390/plants11141816

AMA Style

Vitale E, Izzo LG, Amitrano C, Velikova V, Tsonev T, Simoniello P, De Micco V, Arena C. Light Quality Modulates Photosynthesis and Antioxidant Properties of B. vulgaris L. Plants from Seeds Irradiated with High-Energy Heavy Ions: Implications for Cultivation in Space. Plants. 2022; 11(14):1816. https://doi.org/10.3390/plants11141816

Chicago/Turabian Style

Vitale, Ermenegilda, Luigi Gennaro Izzo, Chiara Amitrano, Violeta Velikova, Tsonko Tsonev, Palma Simoniello, Veronica De Micco, and Carmen Arena. 2022. "Light Quality Modulates Photosynthesis and Antioxidant Properties of B. vulgaris L. Plants from Seeds Irradiated with High-Energy Heavy Ions: Implications for Cultivation in Space" Plants 11, no. 14: 1816. https://doi.org/10.3390/plants11141816

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