1. Introduction
Kale (
Brassica oleracea var.
sabellica) is a leafy green vegetable of pronounced important nutritional value and agronomic utility. This vegetable is an abundant source of essential nutrients, including proteins, phytonutrients, antioxidants, and vitamins A, C, and K, as well as minerals, such as calcium, manganese, potassium, and iron [
1]. These qualities have contributed to the current high demand for kale production. Kale plants respond noticeably to its surrounding environment [
2]. Kale plants appropriate to grow in temperate climates with moderate sunlight exposure [
3]. Kale can be cultivated in a plant factory with artificial lighting (PFAL) to ensure consistent year-round and widespread kale production and to maintain its quality. PFAL is a closed system for planting that can modify environmental parameters to suit the cultivation of a specific crop, including temperature, humidity, light intensity, water, and CO
2 concentration. Such a system ensures the plants grow well, no matter the external conditions [
4].
There have been numerous attempts to enhance both the yield and nutrient content of kale grown in a PFAL. The addition of NO
3-N fertilizer to nutrient solutions has been shown to increase lutein and β-carotene levels [
5]. Increasing the CO
2 concentration to above that in the ambient atmosphere in the PFAL system has the potential to enhance the growth rate of plants by promoting the photosynthetic rate [
4]. Artificial lighting has proven to be effective in kale production due to its ease of implementation within the PFAL setting [
6]. An extension in the photoperiod has been shown to enhance pigment accumulation in kale [
7]. In addition, light conditions had a significant impact on the quantity and kind of phenolic components in kale [
6]. A specific light wavelength has the capacity to differentially trigger the secondary metabolic accumulation in kale. A light wavelength of 640 nm is optimal for activating the accumulation of chlorophyll a, chlorophyll b, and lutein, while a wavelength of 440 nm stimulates β-carotene accumulation [
8]. Furthermore, ultraviolet (UV) radiation has an impact on kale production. For example, UV-B radiation has been used successfully to increase the bioactive compounds in kale [
9]. In addition, the glucosinolate and soluble protein contents in Chinese kale were increased by using 10 and 15 W/m
2 UV-A for 10 days [
10].
The impact of UV-A radiation on plant growth has been reported to influence various aspects of plant development, metabolism, photosynthesis, and final biomass [
11,
12]. UV-A, encompassing wavelengths 315–400 nm, is defined as the invisible part of the solar spectrum that is the major component of the UV radiation reaching the Earth’s surface [
12,
13]. Other UV radiations are UV-B (280–315 nm), and UV-C (100–280 nm) [
13]. Among UV light, UV-A is crucial in plant photomorphogenesis and stress response [
14]. It was found that UV-A treatment could activate biomass accumulation in various plant species [
11], including kale [
6,
15]. Other studies focused on the treatment of UV-A radiation on kale production and the final yield quality, including the phytonutrients at harvest [
2,
6,
15]. However, there have been no published reports on the effects of UV-A radiation on various aspects of not only kale growth but also on changes in photosynthetic efficiency and leaf spectral reflectance. Understanding the physiological effects of UV-A on plant growth is essential for optimizing agricultural practices and enhancing crop production, particularly in plant factory systems. The current investigated the impact of different UV-A intensities on kale prior to harvest to elucidate the effectiveness of UV-A on promoting yield and phytonutrient accumulation through photosynthetic properties and leaf spectral reflectance under plant factory cultivation.
4. Discussion
The growth of the kale plants and their biomass were clear positive responses to the UV-A supplementation in this study. The shoot fresh weight was greater in response to the UV-A treatments than in the roots, as evidenced by the significantly higher fresh weight of the shoot compared to the control (
Table 1). It was evident that the dry weight biomass of both the shoots and roots increased when exposed to UV-A supplementation. The validity of these dry weights as indicators of the actual biomass was confirmed by the determination of the proportion of fresh weight to dry weight across the entire yield. This proportion indicated the moisture influence on the observed biomass, with the results showing that the ratio of fresh to dry weight proportions of the 5 and 10 W/m
2 UV-A treatments were lower than for the control and the 15 W/m
2 treatments, respectively (
Table 1). These results suggested that the total weight gain was not only affected by water content variations but also affected by others. Instead, the observed weight increase may have been caused by the presence of other components, such as insoluble solids, insoluble proteins, and/or other structural organisms in the biomass [
24,
25]. In the current study, the UV-A intensities of 5 and 10 W/m
2 produced greater increases in the biomass (shoot fresh weight, stem height, and canopy width) compared to the other intensities (
Table 1). The application of UV-A that lower or equal to 10 W/m
2 onto plants was indicated as mild UV-A treatment [
26]. Therefore, it could be inferred that incorporating low-intensity UV-A supplementation was more appropriate for enhancing the growth and biomass of kale grown in plant factory settings. This result was consistent with a study where 10 W/m
2 UV-A enhanced the biomass of Chinese kale baby-leaves [
10]. Furthermore, other studies have demonstrated the positive influence of UV-A on the enhancement of plant biomass in different plant species, such as lettuce [
27], sowthistle [
28], and black gram [
29].
UV-A has demonstrated its ability to enhance plant growth through the process of photosynthesis [
11,
30]. One of the positive effects might be closely linked to the change in the photosynthetic pigment contents. Studies have shown that UV-A rapidly increased the chlorophyll contents in lettuce [
31], radish [
32], and canola [
33]. On the other hand, the pigment contents of eggplant leaves decreased after the plants had been treated with UV-A [
34]. However, the current investigations identified no significant changes in the pigment contents, including chlorophyll a, chlorophyll b, and carotenoids (
Table 2). As a result, there was no significant difference observed in the leaf greenness index (SPAD index), as shown in
Table 1. This result was consistent with the findings of Ahandani et al. [
35], who reported that the chlorophyll b content of
Dracocephalum moldavica did not respond significantly to UV-A exposure. Similarly, the influence of UV-A radiation stress on the pigment contents of pepper did not produce any significant differences. Another study suggested that the observed impact on the pigment contents could more likely be attributed to UV-B and UV-C radiation than to UV-A radiation [
36], perhaps because UV-B destroyed the chloroplast structure and enhanced chlorophyll degradation, as well as inhibiting chlorophyll synthesis more than UV-A [
36].
Numerous studies have focused on the impact of UV-B radiation on photosynthetic efficiency [
37,
38]. However, study on the effects of isolated UV-A radiation remains limited. The results of the current study showed that exposure to a 10 W/m
2 UV-A treatment resulted in an increase in the photosynthetic rate (
Figure 3a), which could be attributed to the heightened light absorption capacity of plant leaves in terms of UV-A wavelength, enhancing the availability of light for photosynthesis. This becomes more pronounced under conditions of limited light availability [
11,
39]. In this study, kale plants were grown under 200 µmol/m
2/s which was lower that the light saturation point of kale plant (884–978 µmol/m
2/s) [
40]. Therefore, the UV-A supplementation in this time might help to increase the photosynthetic rate in kale plants. The enhancement of P
n following UV-A treatment in the current study was consistent with a study on sorghum that reported that UV-A and UV-B promoted the photosynthetic rate in certain cultivars [
41]. The net carbon assimilation rate of barley was increased when exposed to UV-A radiation [
30]. Furthermore, the supplementation of UV-A radiation exhibited an impact on water use efficiency (
Figure 3e). This observation suggests that kale plants have improved ability to absorb and utilize water for growth and metabolic processes. Alternatively, it might indicate that the increased growth of kale resulted in a higher water uptake. In addition, there were no significant differences in the stomatal conductance and intercellular CO
2 concentration following UV-A exposure. This suggests that an increase in the photosynthetic rate is not primarily influenced by the concentration of carbon dioxide. The study of four Mediterranean plant species (
Daphne gnidium,
Pistacia lentiscus,
Ilex aquifolium, and
Laurus nobilis), showed that UV-A did not affect g
s under well watering conditions [
42]. Therefore, UV-A supplementation in this time might not alter stomatal properties because kale plants grown under adequate water.
The comparable values of F
v/F
m between the untreated and UV-A treated plants suggested that the intensity of UV-A radiation did not induce stress on the plants since F
v/F
m values that were higher than 0.8 indicated that plants were non-stress [
43]. According to Kolb et al. [
44], the F
v/F
m values of grape leaves were not different between exposure to pure visible light and to UV-A + visible light. In the current study, the quantum efficiency of photosystem II (Y(II)) reached its peak at an intensity of 10 W/m
2, which would be the optimal intensity for kale production. However, as the UV-A intensity increased to 15 W/m
2, the efficiency of photosystem II declined (
Figure 4b). The increase in Y(II) indicated that kale was able to absorb the UV-A for utilization in photosystem II, as evidenced by the increase in photochemical quenching (qP), as shown on
Figure 4c, where qP is the fraction of absorbed light energy that is used for photochemistry in photosynthesis [
16]. Photoreceptors that respond to UV-A might play a role in the signaling pathways that enhance PSII and photoprotective activities. Activation of these photoreceptors could lead to a more efficient use of absorbed light energy. In addition, the NPQ and ETR were not different in this study. The intensities used in this study were mild UV-A and did not trigger significant changes in NPQ. ETR measures the rate of photosynthetic electron transport to produce ATP and NADPH [
45]. Low intensities of UV-A might not directly interact with the electron transport chain components, resulting in little impact on ETR.
Leaf reflectance was measured to calculate to the spectral indices. Some spectral indices could be related to plant biomass and plant stress. The NDVI and NDRE are generally applied to monitor environmental stress in plants [
46,
47], where a higher NDVI indicates that the plant is experiencing low stress [
46]. In addition, it has been reported that some spectral indices could refer to phytonutrient contents, such as glucosinolates, with kale containing a high level of glucosinolates with high leaf reflectance at 425 nm [
2]. Among the spectral indices, the NPQI calculated from leaf reflectance at 415 and 435 nm were close to 425 nm. Furthermore, Soengas et al. [
48] found that a low NPQI was associated with high glucosinolate contents. The current study found that supplementation with 10 and 15 W/m
2 of UV-A resulted in lower values of NPQI than for the control (
Figure 5c). This might indicate that UV-A could increase glucosinolates in kale. Kale containing a high level of glucosinolate has been reported to have high leaf reflectance in the range 700–1000 nm [
2], which could be used to calculate various spectral indices, such as the NDVI, NDRE, SIPI, SR, and WI. The current study found that supplementation using 10 and 15 W/m
2 of UV-A not only produced lower values for the NPQI but also for the SR, PRI, and NDRE than the control (
Figure 5b, c, d, f). On the other hand, the addition of 15 W/m
2 of UV-A significantly increased the WI compared to the control (
Figure 5g). These results were consistent with Soengas et al. [
48], who reported that kales containing high glucosinolates had low values for the PRI, NDVI, NDRE, SIPI, SR, and NPQI but had high WI values.
The phytochemical profiles of kale (total vitamin C, nitrate, soluble protein, and total phenolic content) were notably impacted by UV-A supplementation, particularly at an intensity of 10 W/m
2. Under this condition, UV-A treatment resulted in a significant enhancement of several aspects of the phytochemical profile (increased total vitamin C content, elevated soluble protein content, and higher levels of total phenolic content), as shown in
Figure 5a, c, d. Conversely, UV-A treatment reduced the nitrate content in the kale yield (
Figure 5b). A study in pea sprouts noted that UV-A exposure induced the regulation of vitamin C catabolism genes in plants, resulting in increased vitamin C accumulation [
49]. The augmentation of vitamin C levels provides a protective effect against heightened levels of reactive oxygen species (ROS) and DNA strand breaks induced by exposure to UV-A radiation [
50]. The increase in vitamin C content affected by UV exposure aligns with the findings of a study on mung bean sprouts subjected to UV-B treatment [
51], as well as the investigation by He et al. [
52] on the impact of UV-A supplementation in plant factory settings on lettuce production. The total phenolic had been reported to be higher after exposed to UV radiation in the tomatoes study [
53]. Plants can produce more phenolic compounds when exposed to UV radiation, which function as UV-absorbing pigments, effectively protecting plant tissues from direct UV radiation and diminishing the infiltration of harmful UV radiation [
54,
55]. UV radiation has been documented to participate in the photolysis of nitrate ions [
56], which explains the reduction in nitrate content following exposure to UV treatments in the result of this study (
Figure 5b). These findings align with the research by He et al. [
52] who examined the nitrate content of ‘Red butter’ lettuce grown in the plant factory reduced following the increases of UV-A supplementation intensities. Nevertheless, it is important to note that the effect of UV-A on nitrate content can vary across different plant species, with some species not exhibiting a significant impact. Furthermore, UV exposure could induce the production of stress proteins and activate defense mechanisms [
57,
58], resulting in temporary increases in soluble protein content as the plant responds to UV-induced stress. Additionally, it has been observed that there is an increase in soluble protein levels through the activation of antioxidant enzymes. These enzymes are crucial in mitigating the harmful effects of ROS induced by UV radiation exposure [
59,
60,
61]. Therefore, the increase of soluble protein in kale after exposure to UV-A in this study might caused from these reasons.