Reviews in Agricultural Science
Online ISSN : 2187-090X
Unraveling the Potential UV-B Induced Gene Expression of the Primary and Secondary Metabolisms Against Environmental Stress in Shallot
Ani Widiastuti, Widhi D. Sawitri, Muhammad Idris, Valentina D.S. Handayani, Belinda Winona, Clarencia M. Silalahi, Deden D. Matra, Febri Doni, Aditya H. Setiyadi
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キーワード: plant defense mechanism, primary metabolic pathway, secondary metabolic pathway, shallot cultivar, UV-B-induced responses
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2024 年 12 巻 p. 111-127

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Abstract

Development of climate-resilient crops is adopted to cope with environmental stress. Activation of plant protective genes through radiation of ultraviolet-B (UV-B) has attracted more concerns in contributing to abiotic and biotic stress prevention. Plants exposed to a certain dose of UV-B irradiation give specific responses in growth and metabolite biosynthesis patterns. It has been interpreted that these responses in accumulation of primary and secondary metabolites improve plant tolerance to abiotic and biotic stresses. The potential use of UV-B light as a tool to enhance plant defense systems in agricultural practice has gained increasing interest. In terms of shallot as a plant model in this study, each cultivar exhibits complex responses to UV-B exposure at the transcription level of gene expression. The metabolic pathways in plants after UV-B exposure followed by abiotic and biotic stress are still unclear and necessary to be explored. This review provides a preliminary study of current understanding on UV-B-induced response and protective mechanism in shallot, particularly focusing on modulation of primary and secondary metabolic processes involved in pathogen and drought stress responses. In the primary metabolism, low intensity of UV-B exposure increases the sucrose phosphate synthase (SPS) expression in shallot Tuktuk cultivar. While in the secondary metabolic process, the expression level of lypoxigenase-2 (LOX-2) and cinnamyl alcohol dehydrogenase (CAD) are upregulated differently in two Indonesia shallot cultivars, Lokananta and Tuktuk. Upon the UV-B exposure to various types of stressors, such as Fusarium acutatum pathogen inoculation, the expression of LOX-2 is found to be upregulated in most of the exposures to resist the stress situation encountered. On the other hand, the expression of phenylalanine ammonia lyase (PAL) and chalcone synthase-A (CHS-A) are also upregulated through UV-B exposure followed by in vitro drought stress simulation. The gene encoding the secondary metabolites production, including the phenylpropanoid pathway products, is important to induce the protective mechanism in plant system. This mechanism assumes that UV-B plays a specific role as a prior exposure whereby a stimulus potentiates the defense mechanism. UV-B priming triggers biotic and abiotic tolerance by acting as warning signals at the transcription to phenotype levels.

1. Introduction

Shallot (Allium cepa L. Aggregatum-Group) is considered to have originated in Central Asia or Southeast Asia. In particular, shallot becomes a targeted crop to be improved since it is one of the priorities for horticultural crops in Indonesia. Shallot is a biennial plant, typically grown as annuals for its edible bulb, from the Amaryllidaceae family that has underground tubers. Environmental stress, i.e. abiotic and biotic stress in shallot, mainly causes the most severe yield losses and imposes a considerable economic burden [1, 2].

Drought is the most common and important environmental stress limiting the yield of many crops. Drought stress causes a broad range of physiological changes and impairments of metabolic processes, which result in the accumulation of reactive oxygen species (ROS), damages cell membranes, inhibits electron transfer, destroys chloroplast and thylakoid membrane structures, reduces the photosystem function, and finally decreases photosynthesis [3]. Shallots are particularly susceptible to drought stress. A lack of water causes a major effect on bulb development and yield at various growth stages. Thus, to increase shallot yield, a constant supply of water is needed. The number of bulbs per unit area and the quality of harvested bulbs are affected by irrigation water [4, 5].

For many years, fungicides have been broadly used to manage infection disease. In contrast, increasing the number of fungicide resistant among the Fusarium population becomes an emergent issue in the agriculture sector [6, 7]. Currently, twisted disease is the main biotic stress that affects shallot production and yield loss in Indonesia [8, 9]. Another problem with shallot cultivation from seed bulbs is possibly diminished the quality of shallot by accumulation of soil-borne disease as well as continuously impact to yield loss [9]. F. acutatum is one of pathogens causing twisted disease which is identified by symptoms of pale green or yellow leaves that grow longer and twisted, roots rot and dry, small bulb size, and the base of the bulb becomes white [8, 9, 10].

As sessile organisms, shallots have developed growth responses to deal with simultaneous changes in environmental conditions by modulating their physiological and biochemical changes. Light exerts a significant impact on how plants are protected against abiotic and biotic stresses. Recently, crops are often exposed to climate change effects, including ultraviolet-B (UV-B) irradiation. The challenge facing the agricultural sector nowadays is to discover an innovative solution to enhance crop productivity in the context of climate change. There are many studies indicating a negative effect of UV-B on plant growth, however, it remains a positive impact on plant defense systems against drought and pathogen stresses as the case study of abiotic and biotic adaptive responses, respectively [11]. Major abiotic stress arising from UV-B exposure leads the disease resistance in plants through activation of the response and expression of resistance genes so that plants are certainly more resistant and stronger against pathogen infection [12]. Understanding the impact of climate shift conditions in various plant defense systems has emerged as a strategy to design climate resilient crops in the future. Climate resilient crops are adopted to address the challenges associated with harsh climate conditions, as well as emerging plant diseases. In this review, we used shallot as a plant model to study UV-B induced gene transcriptional alterations in plant metabolic system.

UV-B light is electromagnetic wave radiation that comes from a small part of sunlight. UV irradiation consists of three wavelength clusters: UV-C (200–280 nm), UV-B (280–315 nm), and UV-A (315–400 nm) with only UV-A and part of UV-B reaching the Earth’s surface [13]. UV-B is part of UV irradiation that has a major impact on the environment and living things. The ozone layer absorbs most of the UV-B, but only about 0.15% of it passed the ozone layer and detected at the ground level. A shorter wavelength of UV implies greater energy and perhaps can be sufficient enough to damage the cells [14]. Under certain conditions, UV-B irradiation in plants has an impact on morphological changes, reproduction, photosynthesis, redox metabolism, hormone synthesis, primary and secondary metabolites [13, 15, 16, 17]. Interestingly, the effect of UV-B exposure will depend on the level of irradiation intensity and duration of UV-B exposure time. However, there is no exact determination for a low or high UV-B irradiation intensity as it depends on the specific plant response to trigger stress [15]. Several studies have been reported that UV-B intensity at maximum 3 μmol/m2/s or approximately 1.13 W/m2 (at the wavelength 310 nm) is still considered as medium intensity for activating photomorphogenic and defense related genes responses in Arabidopsis [15, 18, 19, 20, 21]. Hence, this report provides an elucidation of the role of UV-B exposure on shallot using UV-B fluorescence lamp (SPWFD24UB1PB, Panasonic Lighting Device, Co., Osaka, Japan) with wavelength peak at 310 nm.

Several studies have been proposed that UV-B exposure is one of treatments to overcome the issue of drought and crop disease prevention [22, 23, 24]. The activation of plant protective genes through UV-B exposure has been attracted more concerns to contribute to plant protection. Although several studies reported the gene expression regulation of UV-B irradiation, the plant defense mechanism in shallot remains unclear. Therefore, investigation of the protective genes that are activated in early UV-B induction is necessary to be explored. The UV-B exposure has resulted in a concomitant increase in expression of resistant genes and plant defense system. Based on this concept, it reveals that plants with UV-B treatment and exposed to adverse condition, such as environmental stress or certain pathogen, are capable to response and activate the defense mechanism faster than without UV-B irradiation treatment.

Application of UV-B exposure followed by various stress treatments, i.e. drought and pathogen inoculation, is able to initiate the activation of protective genes which modulate the secondary metabolites production to protect plants from the negative effects of abiotic and biotic stress. The phenylpropanoid pathway compounds are the most important secondary metabolites that have been identified as quercetin, kaempferol, anthocyanins, phenolic acids to reduce the negative effect of plant stressors [25, 26]. In addition, the activity of phytohormones, i.e., abscisic acid (ABA), salicylic acid (SA) and jasmonic acid (JA), is also influenced by UV-B, drought, and pathogen stresses [27, 28, 29].

The process occurrences of plant defense mechanism begin with the photoreceptor UV resistance locus8 (UVR-8), which corresponds to integrate with transcriptional changes in plant protective mechanism. The UVR8, as a key signal that mediates light response to UV-B, regulates the expression of several genes involved in both flavonoid and alkaloid biosynthesis. According to previous report, it has been proved that accumulation of certain metabolites, such as flavonoids and alkaloids, has a direct mechanism in place to protect against pathogens [13, 15]. Thus, the objective of this study is to explore how plants perceive the UV-B light and alter plant specialized primary and secondary metabolites production. Further, we summarized the conclusion of numerous studies with respect to different UV-B application methods to improve plant resistance against biotic and abiotic challenges. In addition, exploration of supplemental UV-B light has a positive impact on designing climate resilient crops in the future.

2. Plant primary metabolism induced by UV-B irradiation

Several studies have been reported on the effect of UV-B irradiation and its implication on the production of endogenous phytohormones and compounds that have biological significance in plants [30, 31, 32]. However, the study on plant responses toward UV-B exposure to promote the primary metabolites biosynthesis is still limited.

In general, at low dose of UV-B exposure will activate UVR8 and drive to diversity of changes, such as alteration of plant morphology and specialized secondary metabolite biosynthesis [15]. In the case of shallot, morphological changes in response to UV-B exposure may appear in the form of bulb size. However, only one shallot cultivar, Tuktuk, showed an increment of bulb size after 6 hours UV-B exposure. Lokananta did not show such a morphological change in the presence or absence of UV-B exposure treatment (Fig. 1A). It was in good agreement with our study on transcriptional comparison between two cultivars, i.e., Tuktuk and Lokananta, in terms of primary metabolism pathway. By monitoring the transcriptional changes, sucrose phosphate synthase (SPS), as a representative gene in the primary metabolism pathway, revealed upregulated expression in Tuktuk after 6 hours UV-B exposure, while Lokananta did not (Fig. 1B). SPS plays an essential role for sucrose biosynthesis in higher plants and this soluble sugar can hydrolyze into sugar monomer to provide energy for plant growth and development. Each shallot cultivars may differ in their physiological characteristics. In Tuktuk, the expression SPS might be more responsive to UV-B and stimulate the accumulation of sucrose for distributing carbon source into shallot bulb. Since sucrose is considered as an osmoprotectant in plants, thus accumulation of sucrose along with other metabolites under UV-B exposure might lead to enhance ABA and secondary metabolite compounds [33].

Figure 1: Morphological (A) and Gene expression (B) of Tuktuk and Lokananta shallot after UV-B irradiation treatment (0 and 6 h after treatment)

On the other hand, ABA may work in concert with UV-B to facilitate the metabolic changes of primary metabolites into alkaloid and flavonoid compounds. Following UV-B exposure, sucrose can be oxidized through glycolytic pathway and the tricarboxylic acid (TCA) cycle. Since glycolysis can result in higher accumulation of adenosine triphosphate (ATP) content, the capacity of the plant to adapt to its surroundings under abiotic and biotic stress circumstances is unavoidably improved. The fundamental primary metabolites serve as precursors to secondary metabolites that increase plant resistance adaptability. In addition, shikimic acid is the initiator of secondary metabolism in higher plants, linking sugar metabolism to polyphenol metabolism. The flavonoid pathway is indirectly impacted by the activity of pathways involving phenylpropanoid substances linked with amino acid metabolism [34].

Phenolics, particularly flavonoids, are the biggest class of secondary metabolites found in plants and the most important for UV protection. We also discovered that UV-B light activates a number of gene encoding phenolic compound biosynthesis enzymes, including chalcone synthase (CHS) and cinnamyl alcohol dehydrogenase (CAD), which provides precursors for the downstream flavonoid metabolism pathway [35]. In Tuktuk, the expression of CHS and CAD exhibited in opposite from SPS. Conversely, Lokananta showed an upregulated of CHS and CAD, whereas the expression of SPS was apparently diminished (Fig.1A). The CAD is a specific enzyme involved in biosynthesis of monolignol that plays important role in cell wall lignification process [36, 37, 38]. These results demonstrated that the expression level of CAD gene is mostly influenced by UV-B irradiation as observed in Withania somnifera, Populus spp., and rice [39, 40, 41, 42]. Based on the results above, the different response between Lokananta and Tuktuk might be related to the physiological character of Lokananta which is more resistant to environmental stress compared to Tuktuk. A similar phenomenon was also found in rapeseed (Brassica napus) cultivars, which have different responses in gene expression for their response to submergence [43]. Another similar phenomenon was also observed in olive varieties and two rice subspecies under UV-B-induced photomorphogenic and stress responses [17, 44].

3. Plant secondary metabolism induced by UV-B irradiation

3.1 Gene expression associated with UV-B-Activated secondary metabolism in response to biotic stress

During their whole life, plants could not escape from any threats in their environment. Therefore, naturally plants are completed by advanced defense systems to thwart the detrimental effects of environmental stressor, particularly biotic stress. In plants, different responses in signaling pathways are linked to different ways, depending on types of stresses [45]. In nature, host-pathogen interaction is a mechanism involving the activation of a number of signals which produce a rapid resistance response from plants to pathogen attack [46]. Many studies reported the utilities of various types of elicitors through physical and biological treatments, i.e., hot water treatment [47, 48], UV-B irradiation [12, 15], and beneficial microbes [49, 50], to induce plant resistance against biotic stress. The SA, JA, and ethylene (ET) are known to be the main group of phytohormones that traditionally play a role in regulating plant resistance signals. Systemic acquired resistance (SAR) is known as a pathway that is mediated by SA, while induced systemic resistance (ISR) is mediated by JA/ET. Many genes related to plant resistance were known to be part of the SAR pathway, i.e., chitinase, peroxidase, and pathogen-related protein genes [29, 51, 52], while LOX gene is more correlated to JA/ET and ISR pathway [53, 54].

Plants exposed to UV-B light will adapt as a protective mechanism through elevating the resistance genes expression and induction of secondary metabolite compounds, such as flavonoids and jasmonic acid [15]. The previous studies on UV-B exposure treatment in cucumber, rice, lettuce, and broccoli have been used in various studies to improve the gene mechanism for resistance to diseases caused by biotic stress, i.e., fungi, viruses, bacteria, and insects [12, 53, 54]. UV-B irradiation treatment does not require special processing such as biological agents. Thus, the UV-B treatment would be easier application and more environmentally safe since the use of chemicals may reduce [13]. Plants that are exposed to UV-B adapt as a protective mechanism by inducing secondary metabolites such as flavonoids and jasmonic acid, therefore it has been used in many studies in an effort to improve the mechanisms of resistance genes against biotrophic diseases [53].

Many studies reveal the response on the plants between UV-B irradiation and pathogen attack [15, 53]. UV-B treatment or in combination with other challenges, such as pathogen inoculation, boosts the accumulation of antifungal metabolites for reducing disease. UV-B irradiation has a direct impact on increasing some resistance-related genes, including acidic endochitinase-2 (CHI2), ethylene receptor-2 (ETR2), and lipoxygenase-6 (LOX6) which are group of defense-related genes against powdery mildew disease in cucumber [12]. While in rice, UV-B irradiation followed by inoculation of Magnaporthe oryzae, a pathogen of blast disease, increased LOX and β-1,3-glucanase activity compared to UV-B treatment with no pathogen inoculation [55].

The LOX is one of the enzymes derived from the JA biosynthetic pathway that plays an important role as pathogen and environmental stress resistance, such as UV-B irradiation [15, 56]. In the case of shallot, Tuktuk and Lokananta cultivars, LOX2 gene expression constantly increased after UV-B irradiation treatment with intensity of 1.67 W/m2 (similar intensity with [57]), however it showed different patterns independently (Fig. 2).

The highest expression of LOX2 in Tuktuk and Lokananta were obtained after 45 and 180 minutes of UV-B treatment, respectively. Lokananta was registered as a resistant shallot cultivar against twisted disease, while there is no information about the disease resistance on Tuktuk. The LOX2 gene expression in Tuktuk increased remarkably during 45 min UV-B treatment, but immediately decreased and is stable during 180–360 min treatment. On the other hand, LOX2 gene expression in Lokananta increased slowly and peaked on 180 min treatment and decreased by the time. It possibly relates to the genetic character of Lokananta which is more resistant to twisted disease compared to Tuktuk.

Figure 2: Gene expression pattern in Lokananta and Tuktuk cultivars in the treatment of UV-B irradiation with intensity of 1.67 W/m2 for LOX2 and CAD

Along with the data of LOX2 gene, CAD expression in shallot also showed cultivar dependent (Fig. 3). Tuktuk, which is supposed to be a more susceptible cultivar, CAD was expressed immediately after UV-B treatment and peaked at 45 min, but in Lokananta, the gene expression remains stable. The CAD enzymes function for lignin biosynthesis or lignification in plants that play a role in resistance mechanisms from pathogen infection and protect wounds in plant tissues [58].

Figure 3: Expression of LOX2 gene pattern under UV-B irradiation treatment and F. acutatum inoculation in Lokananta (A) and Tuktuk (B) Shallot cultivars. X0I0 : (-) UV-B and (-) F. acutatum; X0I1 : (-) UV-B and (+) F. acutatum; X1I0 : (+) UV-B and (-) F. acutatum; X1I1 : (+) UV-B and (+) F. acutatum. normalized to ACT expression. Vertical bars represent the mean ± SE

In this review, a study on shallot and LOX2 gene responses is used as physiological response and gene expression pattern for model in UV-B induced resistance against F. acutatum infection causing twisted disease, as a case study on the plant systemic disease. Figure 3 shows the expression levels of LOX2 during UV-B irradiation treatment followed by F. acutatum inoculation on shallots. Based on the result, there were different patterns of gene expression in Lokananta and Tuktuk cultivars. In Lokananta, LOX2 expression was increased remarkably on the same day of treatment (0-d) in plants treated by UV-B irradiation for 150 min – with no inoculation (X1I0), followed by the result on UV-B treatment continued by inoculation (X1I1). On 2-d, the expression of LOX2 was rapidly upregulated on UV-B treatment continued by F. acutatum inoculation (X1I1) and only F. acutatum treatment (X0I1). On 4- and 6-d, the expression of LOX2 was decreased significantly in all treatments with X1I0 treatment (UV-B irradiation with no inoculation) had higher expressions than other treatments. On those days, UV-B irradiation was followed by F. acutatum inoculation (XI1I) had down regulated of LOX2 expression in Lokananta. This indicates that on 2-d the gene was maximally expressed and decreased through time (Fig. 3A). While in Tuktuk, treatment of F. acutatum inoculation with no UV-B irradiation treatment (X0I1) had down regulated of LOX2 expression on the same day of treatment (0-d). The expression of LOX2 was upregulated on 2-d in all treatments, with UV-B irradiation only (X1I0) had the highest expression level. LOX2 regulation decreased over time afterwards, particularly on 6-d, the expression of LOX2 was down regulated on UV-B irradiation treatment (X1I0). On 6-d, plants treated with UV-B irradiation continued by F. acutatum inoculation had stable gene expression from 4-d (Fig. 3B).

Based on the results, priming mechanisms are reported in both Lokananta and Tuktuk cultivars under different mechanisms. In Lokananta, priming mechanism occurred on 2-d, which infected the F. acutatum after UV-B treatment could increase LOX2 gene expression in high level. However, the expression of LOX2 has maximally accumulated on 2-d and downregulated significantly by time. While in Tuktuk, the priming mechanism occurred soon after treatment and inoculation (0-d). Different from Lokananta, X1I1 treatment affects LOX2 gene expression in Tuktuk cultivar decreased and stable but not down regulated on 4-d and 6-d observation. Distinctive characteristics between Lokananta and Tuktuk cultivars affect the different resistance response between these two cultivars. Tuktuk is susceptible to Fusarium infection due to lower endogenous SA than Lokananta [9]. Thus, presumably causing Tuktuk to have fast response on 0-d as a defense mechanism.

Lipoxygenases initiate the lipid peroxidation process in the plant membrane system by attacking it directly and non-enzymatically. Several enzymes of the LOX-dependent peroxidase pathway are among the metabolites of lipid peroxidation. Thus, the regulation of different defense responses such as tissue necrosis, H2O2 production, hypersensitivity reactions, is also mediated by the LOX enzyme. Many molecules with antibacterial, signaling, or both properties can be synthesized via the LOX route. Stimulation of the LOX pathway results in the accumulation of hydroperoxides, which serve as the initial line of defense against pathogen infection [54]. The LOX gene is stated to be one of the important genes involved in cucumber resistance against powdery mildew [48]. Taken together from the expression of LOX2 and CAD, plant response against UV-B irradiation treatment possibly relates to its genotype character. Apart from the fact that genotype character affects plant response to UV-B irradiation, it is understood that UV-B treatment could be applied to help plants increase their defense against biotic stress.

Several studies have been conducted to examine the effect of UV-B irradiation on the induction of plant resistance to disease stress, which is shown in Table 1, such as research in UV-B irradiation on rice against which increase LOX and β-1,3-glucanase genes. Those genes play important role in rice resistance Magnaporthe oryzae [55]. Similar results were also found in research from [12] that UV-B irradiation increased the expression of the LOX6 gene which functions as a defense gene against powdery mildew disease in cucumber. The research in Table 1 provides data along based on the explanation above and with our study in shallot, proposing the potency of UV-B irradiation treatment to increase shallot resistance against plant disease needs to be explored further.

Table 1: Examples of UV-B induced resistance against plant disease

No. Host plant Treatment Plant disease Effect Ref.
1. Cucumber UV-B 15 µW/cm2, 4 h a day Powdery mildew
(Podosphaera xanthii)		 Increased functional LOX6 gene expression as a defense gene against powdery mildew [12]
2. Rose UV-B during 2 h at night day (0.5–1 KJ/m2, 0.065–0.14 W/m2, 2 h, 265–385 nm) Powdery mildew
(Podosphaera pannosa)		 Lowered the disease occurrence [15]
3. Strawberry UV-B (0.864–2.03 KJ/m2; 0.08–0.188 W/m2, 3 h, 280–315 nm) powdery mildew
(Podosphaera aphanis)		 Lowered the standard amount of fungicide application [15]
4. Arabidopsis UV-B 5.5 KJ/m2 for 4 h Gray mold
(Botrytis cinerea)		 Increased the plant resilience [22]
5. Rice UV-B 310 nm Blast disease
(Magnaporthe oryzae)		 Increased the LOX and
β-1,3 glucanase		 [55]
6. Lettuce UV-B 312 nm Downy mildew
(Bremia lactucae)		 Reduction of disease by the number of conidia [74]
7. Tomato, cucumber (seedlings) 50 mW/m2 and 100 mW/m2, 2 h a day Two types of powdery mildew
(Podosphaera xanthii, Pseudoidium neolycopersici)		 UV-B control was logically equivalent to the conventional control by chemicals [75]
8. Shallot (seedlings) 1.67 W/m2, 150 min optimum (max 6 h), daytime Twisted disease
(Fusarium acutatum)		 Increased the LOX2 gene expression This study

3.2 Gene expression associated with UV-B-Activated secondary metabolism in response to abiotic stress

Plants produce a variety of secondary metabolites for improving their adaptability to survive under harsh environments, i.e., drought, salinity, high light intensity and temperature. Recently, researchers explored the potential of UV-B for improving plant tolerance for abiotic stress. Preliminary research on the use of UV-B in plant assembly was conducted using Arabidopsis as molecular genetic model plants. Based on this study, the UVR8 was identified as UV-B photoreceptors [15,17]. UVR8 photoreceptor is 150 kDa proteins and appear as inactive homodimers in the cytoplasm expressed throughout plant organs, such as roots, leaves, petals, and shoots UVR8 interacts with the transcription factor WRKY DNA-binding protein36 (WKRY36) which plays a role in the transcription process of elongated hypocotyl5 (HY5). Furthermore, UVR8 monomers also interact with and suppress transcription factors BRI1-EMS-suppressor1 (BES1) and BES1-interacting MYC-LIKE1 (BIM1), which are gene activators of the response to brassinosteroids [12].

Plants were irradiated with UV-B to activate protective genes to produce secondary metabolites that can be acted as protection compounds for sequence of abiotic stress. Under UV-B-induced response in plants, there are two signaling pathways which were activated by UV-B, i.e., low-intensity of UV-B-induced photomorphogenesis signaling response and high-intensity of UV-B-induced stress response. Several studies have found that phenylalanine ammonia-lyase (PAL) activity increases in response to UV and drought [25]. Besides PAL, CHS is one of other key genes in the phenylpropanoid pathway which was activated under UV-B and drought [19, 20, 59, 60, 61]. UV-B radiation plays an important role for chestnut roses to help in drought stress, which occurred in the Karst region, by modifying its antioxidant capacity and nutrition balance [26]. Based on the explanation by [34] and [62], plants under UV-B and drought exhibited a notable up-regulation of specific acclimation-associated metabolites, i.e., flavonoids, anthocyanins, and phenols under the phenylpropanoid pathway.

Besides the activation of phenylpropanoid pathway, UV (including UV-B) and drought also activated the biosynthesis of JA, which included LOX2, activator of JA biosynthesis found in Arabidopsis [62, 63]. Previous research was found that many genes, including LOX2, was activated under UV-B-induced photomorphogenic and stress responses [17, 21, 64, 65]. In shallot, based on our preliminary results, it was found that expression level of LOX2 was also affected by UV-B (exposure time; 30 and 150 min, intensity; 1.67 W/m2), followed by water stress treatment using polyethylene-glycol 6000 (PEG6000) during six days observation (data is not shown). Genes related to JA biosynthesis become interesting to be explored deeper in this sequence environmental treatments for developing resilience species for the future climate change scenario.

The use of UV-B as a priming factor for inducing plant protective mechanisms has also become an interesting topic in plant science. It was well known that UV-B was a eustress factor where UV-B activates several mechanisms of plant defenses pathways.

4. General discussions: Potency of UV-B irradiation to develop climate-resilient crop

Climate change has become an environmental issue that cannot be avoided in recent years. The productivity of cultivated plants is very vulnerable to climate change because it can cause plants to experience environmental stress, including biotic and abiotic stress. It is estimated that climate change can reduce agricultural productivity by up to 30% and will also be accompanied by an increase in pathogen attacks on plants. The solution to overcome the impact of climate change which affects crop productivity is the need to modify production processes and agricultural management. Currently, the climate resilient crop concept is recommended as a strategy to overcome the decline in crop productivity due to climate change. The climate resilient crop strategy is an effort to cultivate plants to be able to adapt to various environmental stresses due to climate change [66, 67, 68].

UV-B irradiation is a natural inducer of defense mechanisms in plants that are capable of influencing internal factors, such as genes and hormones related to plant resistance mechanisms [13, 15, 53]. In the case of plant disease, one of the resistance-related genes induced by UV-B was LOX2, a potential marker gene for the jasmonic acid (JA) synthesis pathway [15]. UV-B irradiation was able to activate LOX2, which acts as a plant resistance to pathogen-induced diseases, anti-inflammatory, and lipid protection [69]. LOX or lipoxygenase enzymes are active due to stresses, such as UV-B irradiation and pathogen infection, and it will cause galacto-lipase and phospholipase mechanisms to occur, resulting in the release of polysaturated fatty acids (PUFA) from the lipid membrane and forming LOX. Furthermore, LOX will catalyze PUFA hydroperoxides, which are reactive molecules that can be easily converted by various enzymes in the defense mechanism. PUFA hydroperoxides will synthesize three other main enzymes such as allene oxide synthase (AOS), divinyl ether synthase (DES), and hydroperoxide lyase which play a role in defense metabolism in large quantities for plants [56].

Several variables affect the quality of UV-B irradiation and play a role in the resistance-related genes induction. Duration is one of the important variables in UV-B irradiation research that affects increasing plant defense mechanisms [15]. It has been reported that duration of the UV-B irradiation can induce a plant’s response, such as photomorphogenic and stress response that are not mutually exclusive [57]. Mostly, short term exposures increase metabolic secondary higher than long term exposure of UV-B. Based on [15], a short duration of UV-B irradiation has more positive effects than a long duration, such as gene expression level, has been shown. Short-term UV-B exposure of mature postharvest lemon was able to induce a natural fruit defense enhancement response by mechanical/chemical modification of flavedo tissue that prevents the spread of Penicillium digitatum [70].

Many studies describing methods for developing climate resilient crops, including heat stress treatment, showed increasing expression of pathogen resistance related genes [29, 51]. Although many studies describe the negative effects of climate change on plant growth, some report the effects of UV-B as a potential plant defense mechanism against pathogen attacks [22, 23]. This has also been reported in cucumber plants where the defense mechanism elicited by UV-B irradiation [12].

Figure 4 proposed the use of UV-B irradiation to increase plant resistance against biotic and abiotic stresses in shallot plants as a plant model. Based on the previous study, some genes related to plant resistance increased after UV-B treatment to protect plants against disease and drought stress. LOX2 gene is confirmed to increase in the UV-B treatment and pathogen infection. The increase in LOX gene expression is caused by epigenetic modifications that affect changes in gene expression as one of the plant responses in the face of stress, both abiotic and biotic. One type of epigenetics that occurs is non-coding RNA or also called RNA associated silencing. Due to stress, changes occur in RNA so that RNA regulates gene expression negatively through RNA interference mechanisms. After that, the formation of small interfering RNA (siRNA) plays an important role in influencing plant gene expression since it improves memory from the influence of stress that has been experienced in previous situations to subsequent situations. This is also referred to as priming, where plants produce memorization signal of environmental experiences as an increased response to repeated stress, which drives to increased resistance and adaptation to pathogens and other stresses [71]. Plants experiencing stress will respond by increasing resistance genes which causing priming mechanism, so that the further stressor will be more quickly responded by higher increasing of resistance genes expression. Taken together from all studies in UV-B induced resistance, it is assumed that UV-B has a priming effect to prepare plants in the ready state to respond to any following stress.

Plant responses to UV-B and environmental multiple stress are an important research focus currently related to global climate change. UV-B is an abiotic factor that works as eustress, where UV-B activates genes that encourage plants to be more adaptive and tolerant of other environmental stresses such as drought (osmotic). In this case, UV-B can function as a priming that prepares plants to be able to withstand environmental stress conditions. UV-B exposure was given in the first stage, followed by drought stress treatment in the next stage. UV-B and drought stress work synergistically in inducing protective mechanisms in plants either simultaneously or sequentially, UV-B followed by drought stress or vice versa [72, 73].

Figure 4: Propose of climate resilient crop on shallot induced by UV-B irradiation treatment through plant defense mechanism. After UV-B irradiation treatment (1.67 W/m2; max 150 minutes) on shallot tissue culture, LOX2 gene expression increased and contributed to the plant protection against environmental stress both biotic and abiotic. Further deep study on plant defense mechanism activated by UV-B irradiation will contribute to developing a climate resilient crop in the future.

The study of UV-B irradiation is one of the scientific aspects that needs to be developed more broadly in the agricultural field. The number of problems in decreased production and quality due to disease is one of the serious problems that require problem solving. Through the development of UV-B irradiation, it provides long-term prospects for improving the characteristics of plant resistance to disease and abiotic stress through both primary and secondary metabolism. Previous research showed that the two shallot cultivars responded differently in defense related genes of LOX2 gene expression after UV-B irradiation treatment. Further deep research to observe the relationship of primary and secondary metabolism induced by UV-B to raise plant tolerance against biotic and abiotic stress. Above all, this novel finding is important to conduct further study in how to apply this specific character as plant resistance response against stress to assembly climate resilient crops.

5. Conclusion

Based on the explanations above related to the potential of UV-B used in improving plant resistance to environmental stress, it was concluded that; plants respond to the presence of UV-B through UVR8 photoreceptor, dependent or independently, which will activate the primary and secondary metabolism pathways for protective function; several genes, i.e., SPS, LOX, CHS and CAD, were investigated in shallots that show distinguishing features to abiotic and biotic stresses responses after UV-B irradiation; the SPS gene is an interesting gene to be explored for understanding the role of primary metabolism function in coping with environmental stress after UV-B irradiation; the LOX gene on shallot is consistently gave the responses into environmental stress due to its involvement in JA biosynthesis pathway, which has different pattern between shallot cultivars after UV-B treatment and improved its resistance; under the intensive research on UV-B irradiation as priming and eustressors, the potency of UV-B to be used in agriculture for developing climate resilient crops in promising for the future climate change scenarios.

Acknowledgments

Authors express the deepest gratitude to Universitas Gadjah Mada, Indonesia, which financially support this research through Indonesian Collaboration Research Grant 2023 (RKI 2023) No. 2641/UNI/DITLIT/Dit-Lit/PT.01.03/2023.

References
 
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