In the present research, we studied the response of P. graveolens to UV and PAR in terms of growth, yield, phenol and flavonoid contents, antioxidant capacity and essential oil composition. Our results proof that high PAR intensity declined the length and width of leaf and the height of plant, resulting in formation of dense and dwarf plants. Corresponding findings have been previously reported for Dianthus caryophyllus L. (Hlatshwayo and Wahome, 2010), Hordeum vulgare L. (Klem et al., 2012), Pelargonium zonale (L.) L'Hér. ex Aiton (Vidović et al., 2015) Rosmarinus officinalis L. (Raffo et al., 2020), which produced lower leaf area and plant height in the presence of high PAR intensity. However, similar to our results, plant dry weight were positively affected by PAR induction. As reported in previous studies, the high PAR intensity generally increased plant dry matter, and this effect is probably linked to the induced photosynthetic activity resulting in increased carbon fixation (Raffo et al., 2020). On the other hand, increasing leaf area in plants exposed to low PAR intensity can be interpreted as a kind of adaptation strategy to maximize the capture rate of radiant energy (Givnish, 1998).
Results showed different growth responses between plants exposed to enriched UV-A and enriched UV-B, as enriched UV-A radiation was more compatible and favorable for P. graveolens. Enriched UV-B irradiation was associated with reduced plant height, leaf expansion and fresh and dry weight of aerial part. These findings are in accordance with the earlier reported studies on UV-A and UV-B effects (Shayganfar et al., 2018; Mumivand et al., 2021d). Reduction in growth and yield of plants exposed to enhanced UV-B irradiation is mostly due to the negative effects of high UV-B on photosynthesis (especially photochemical efficiency of PSII) and chloroplast ultrastructure, DNA damage as well as the indole acetic acid photo-oxidative destruction (Klem et al., 2012; Matsuura, et al., 2013; Hui et al., 2014). Moreover, reduction of growth and yield of plant with UV-B irradiation was higher under low PAR intensity than high PAR intensity, confirming that UV-B irradiation and high PAR synergistically motivate defense systems in plant. As a support to our results, it has been previously demonstrated that blue light may ameliorate UV-B adverse effects (Vidović et al., 2015). Corresponding findings have been previously published for two barley varieties, where negative influences of enriched UV-B radiation on morphology and growth of plant were largely alleviated by high PAR intensity (Klem et al., 2012). As noted in that study, high PAR intensity prevented negative UV-B influence on the extent of light absorption, carboxylation activity as well as photochemical efficiency.
Increasing evidence suggests that plants exposure to excessive amounts of UV-B radiation quite often leads to overproduction of reactive oxygen species (ROS) in plant cells, due to impairing the photosynthetic machinery (Shayganfar et al., 2018). Plant cells are usually preserved against the adverse influences of ROS by a concerted action of both enzymatic and non-enzymatic antioxidant constituents. The antioxidants compounds act synergistically to scavenge increased level of ROS and mitigate stress (Mumivand et al., 2023). Previous studies reported that UV-B promotes the activities of antioxidant compounds, such as α-tocopherol, flavonoids, carotenoids and phenolics, which play important roles as defenses against ROS (Klem et al., 2012; Müller et al., 2013; Müller et al., 2015). As noted in the present study, the amount of total phenols and flavonoids and antioxidant activity of P. graveolens strongly increased with the UV-B radiation. Of all groups of secondary metabolites, phenolic compounds, especially flavonoids, are considered as the most related for UV-B defense. Therefore, it can be concluded that plant produces higher amount of these secondary metabolites to counteract the effects of UV-B irradiation. On the contrary, UV-A radiation did neither significantly influence total phenol and flavonoid contents nor antioxidant activity. Results demonstrated that high PAR intensity also induced the contents of total phenol and flavonoids in plant irrespective of UV treatment. Moreover, the combination of high PAR intensity and enhanced UV-B led, not only to further increases in total flavonoid content, but also in the antioxidant capacity. Therefore, it was found that PAR and UV-B had an increasable influence on the accumulation of flavonoids as UV-absorbing compounds
It is commonly acknowledged that epidermally located flavonoids, as photoprotective pigments, reduce the penetration of short wavelengths of solar radiation (280–450 nm) into leaves (Burchard et al., 2008), thus efficiently protect the photosynthetic apparatus from high PAR intensity and UV-B irradiation and prevent photo-oxidative damage (Müller et al., 2013). It has also been reported that flavonoids are endogenous regulators of transport and oxidation rates of indole acetic acid (Jansen, 2002). Therefore, further increase in flavonoid accumulation by UV-B and PAR irradiance could attribute to their roles as defense and signal compounds for protecting the plants. Furthermore, our findings demonstrated the negative relationship between flavonoids concentration and growth and yield of the plant.
We have shown that both high PAR and enhanced UV-B particularly increased the essential oil content and yield of P. graveolens. In accordance with this observation, an increased essential oil content of the plants exposed to higher PAR intensity has been reported in Aeollanthus suaveolens Mart. ex Spreng. (Barbosa et al., 2021), R. officinalis (Raffo et al., 2020), Eclipta alba (L.) Hassk. (Rai and Agrawal, 2020), and has been commonly ascribed to the induced photosynthetic activity and corresponding rate of basic metabolites. The higher accumulation of plant secondary metabolites in response to high PAR intensity could also be explained by the ecological functions of these compounds as a part of a plant defense mechanism against high light intensity (Raffo et al., 2020). Differently from what observed in this research, shading of solar radiation has been associated to the increased essential oil content of some species, due to the protection conferred by shading against the very intense radiation stress (Degani et al., 2016; Mousavinik et al., 2016).
The essential oil yield of oil-bearing plants is thoroughly dependent on the plant biomass and percentage of essential oil (Mumivand et al., 2021b). The extent of increasing the essential oil content due to enriched UV-B irradiation was higher than that of decreasing the leaf dry weight. For this reason, the essential oil yield of the plant was promoted by enhanced UV-B treatment. Thus, the induced amount of essential oil content is the dominant factor in determining an increased essential oil yield in P. graveolens. Results showing UV-B-induced incitement of production of essential oil is in accordance with observations of previous reports on other medicinal plants such as Acorus calamus L. (Kumari et al., 2009), Ocimum sanctum L. (Kumari and Agrawal, 2011), Thymus spp. (Shayganfar et al., 2018)d alba (Rai and Agrawal, 2020). Rai and Agrawal (2020) reported that the content of E. alba essential oil was increased under continuous UV-B irradiation, while reduced under intermittent UVB irradiation. Kumari and Agrawal (2011) have concluded that exposure of UV-B is a substantial need for the development and filling of the oil glands or glandular trichomes in O. sanctum, resulting in the boosting of the essential oil secretion. One of the roles of essential oils is participation in defensive mechanisms in response to environmental stresses, and their production is associated with abiotic factors such as nutrient deficiency, salt stress, water scarcity, temperature, light intensity, and UV irradiation. (Wang et al., 2019; Mumivand et al., 2021a). Thus, increasing the essential oil content of rose-geranium to induce plant tolerance to UV-B irradiation and its oxidative stress seems reasonable. In this study, enhanced UV-A irradiation made no change in essential oil content and yield of plant. This result was inconsistent with finding reported by Mumivand et al., (2021d) in thyme, who mentioned a positive effect of enhanced UV-A irradiation on the essential oil production of the studied species. These differences in the responses of the plants could be due to factors including the inherent characteristics of the species, plant origin, climatic conditions, extraction methods, storage conditions, and dose and duration of UV-B irradiation (Morshedloo et al., 2021; Mumivand et al., 2021d).
A change in essential oil composition under both UV-B irradiance and PAR intensity has been demonstrated in a majority of papers, although in some cases it remains constant. In the present study, the data show that the UV irradiation and PAR intensity significantly affected the essential oil constituents of P. graveolens. High PAR intensity increased the amount of geraniol in essential oil, leading to a slight reduction of C/G ratio. Furthermore, significant decrease in C/G ratio was observed in the enriched UV-B irradiation in comparison with ambient UV. The C/G ratio is a key index characterizing the quality of the essential oil in rose-geranium for the perfume industry (Saxena et al., 2008). C/G ratio of 1:1–3:1 give the economic value to rose-geranium essential oil (Verma et al., 2010). However, it believes that essential oils with a C/G ratio higher than 3:1 is have poor quality for the perfume industry (Peterson et al., 2006). Considering that the lower C/G ratio is the most important indicator of the high economic value of rose-geranium essential oil, reducing C/G ratio under enriched UV-B radiation and/or high PAR is likely to be favorable.
Significant increase was observed in the percentage of geraniol under enriched UV-B treatment. While, under low PAR intensity, neral and citronellyl formate showed increment in plants exposed to enhanced UV-B. On the other hand, under high PAR intensity, caryophyllene oxide showed reduction following enhanced UV-B exposure. Citronellol and β-elemene both found to be declined in P. graveolens essential oil when plants were exposed to enriched UV-B. On the contrary, under low PAR intensity, enhanced UV-A radiation was positive for high citronellol content. It is hypothesized that such modification in secondary metabolites biosynthesis is necessary for plant adaptation to biotic and abiotic stresses such as PAR intensity and UV-B radiation (Manukyan, 2013). The effect of PAR and UV-B on essential oil components is likely due to its effects on modulating the expression of genes involved in phenylpropanoids and terpenoids biosynthetic pathways (Kumari et al., 2009). A slight change in enzymatic activity may lead to an increase or decrease in certain compounds and make a change in the composition of essential oil (Figueiredo et al., 2008). Citronellol and geraniol, as the major constituents of P. graveolens essential oil, are alcoholic monoterpenes synthesized by the biosynthetic pathway of methylerythritol-4-phosphate (MEP) (Saxena et al., 2008; Verma et al., 2010). The precursor supplies (IPP and DMAPP) is a limiting factor in the biosynthesis of monoterpenes from the plastidial MEP pathway (Dolzhenko et al., 2010). Considering the fact that monoterpenes are synthesized in plastids, any chloroplast damage induced by UV-B and/or high PAR may lead to change in monoterpene biosynthesis. It has been shown that UV-B altered expression of genes involved in essential oil biosynthesis in peppermint, subsequently made change in essential oil composition (Dolzhenko et al., 2010; Alagupalamuthirsolai et al., 2019). Many publications report the change in essential oil composition under UV-B exposure or PAR intensity. For example, in lemongrass, UV-B exposure increased the essential oil content. Furthermore, the proportion of Z-citral, geraniol formate, polyol, linalyl formate was also significantly changed following UV-B treatment (Kumari et al., 2009). Rai and Agrawal (2020) also reported significant increment in some medicinally important constituents of E. alba essential oil such as α-terpineol, δ-cadinene, methyl linoleate, linolenic acid and myristic acid amide exposed to continuous UV-B irradiation. The findings obtained from the study of Raffo et al., (2020) on R. officinalis demonstrated that the relative percentages of camphene, α-pinene, myrcene, 1,8-cineole, β-pinene, α-terpinene, β-caryophyllene and α-phellandrene enhanced in plants exposed to 50% sunlight, whereas camphor, 3-carene, terpinen-4-ol, borneol, verbenone, α-terpineol, and humulene showed lowered abundances in this treatment.