“Metabolight”: how light spectra shape plant growth, development and metabolism

1 INTRODUCTION

Sunlight is the energy that powers life on our planet as photosynthesis is the “green engine” that converts the electromagnetic energy of sunlight into chemical energy by fixing carbon dioxide and water into sugars. Wavelengths of the electromagnetic spectrum absorbed by plants and used to drive photosynthesis can be grouped into (1) ultraviolet (UV) ranging from 100–400 nm (i.e. UV-A 100–280 nm; UV-B 280–315 nm; UV-C 315–400), a region in which photons are associated with potentially damaging high energy, (2) photosynthetically active radiation (PAR; 400–700 nm), corresponding to the wavebands that are principally absorbed by plant pigments to fuel the photosynthetic machinery, and (3) far-red (FR) light, associated with lower-energy photons.

From the first water-to-land transition and the consequent land colonization, plants had to face a set of variable life conditions, including the light environment. Being sessile organisms, they have adapted to light intensity (low/high), light fluctuation, and continuous light (at high latitude) and have evolved to efficiently perceive light quality, intensity, direction, and timing, then transmit and process the information received from light stimuli to optimize the plant development and behaviour (Carvalho et al., 2011). Through photoreceptors, namely phytochromes (dimeric chromopeptides that possess two photoconvertible forms for R and FR perception), cryptochromes (devoted to blue and UV absorption), and phototropin (flavoproteins mediating blue, UV and green light absorption), as well as UV-dedicated receptors (i.e., UV Resistance Locus 8 – UVR8, for sensing UV-A and UV-B) plants regulate photomorphogenesis, photoperiodicity and phototropism, but also maximize light harvesting in the context of competition with neighbouring plants or in shade condition in the understorey. (Rizzini et al., 2011; Landi et al., 2020; Rai et al., 2021). For example, phytochromes that are sensitive to variation in red/far red (R/FR) ratio (Falciatore & Bowler, 2005) are determinants in germination, de-etiolation, shade avoidance, and flowering responses in land plants (Mathews, 2006).

In terms of light harvesting and utilization, plants have evolved finely tuned and well-orchestrated mechanisms aimed at, on the one hand, maximizing light harvesting under suboptimal light conditions and, on the other hand, protecting the photosynthetic apparatus when light is in excess of what can be used for photosynthetic requirements (namely, photoinhibition) (Baker, 2008). In plants, light-harvesting pigments, chlorophyll a and b (which absorb principally in the red and blue regions of the solar spectrum) and the accessory pigments carotenoids (which extend the absorbed light to other wavelengths in the visible spectrum) are devoted to intercepting the sunlight and transferring electromagnetic energy to the reaction centers of both photosystems. The red and blue portions of the spectrum are the most absorbed by chlorophylls, but regardless of all the wavelengths of light they absorb, chlorophylls exclusively utilize red photons to drive water-splitting and ferredoxin-reducing photochemistry. (Björn et al., 2009). Indeed, the extra energy of a blue photon, according to the Planck equation (75% higher comparing a 400 vs a 700 nm photon), is dissipated as heat within subpicoseconds to the same energy level as red (Björn et al., 2009).

Curiously, the leaf's green appearance has spread the misconception that green light is poorly absorbed and utilized by the plant. Actually, green light (GL) plays a pivotal role in photosynthesis in the deepest mesophyll layers as well as in the understorey, where light is depleted in the red and blue regions due to absorbance by the overhanging leaves (Folta & Maruhnich, 2007; Brodersen & Vogelmann, 2010). Indeed, though red and blue are peaks for chlorophyll absorption, leaf reflectance, light scattering and energy loss via thermal dissipation dramatically reduce the efficiency of energy conversion to 4.6% in C3 and around 6% in C4 species (Zhu et al., 2008). Moreover, GL is also perceived by phytochromes and cryptochromes, reversing the effect of blue light, for example, in terms of stomatal regulation (Frechilla et al., 2000; Kim et al., 2004). Additionally, in red-leafed species, the effect of GL might be different due to the presence of red pigments (i.e., anthocyanins), which absorb preferentially (but not exclusively) in the green portion of the solar spectrum (Landi et al., 2021; Simkin et al., 2022).

In view of the above, in the last decade the management of light regimes and spectra has been explored to (1) promote plant growth and maximize biomass production in indoor cultivation (Jones, 2018; Stamford et al., 2023), (2) shape plant size and architecture (Li et al., 2000; Stapel et al., 2011), (3) improve the nutritional value of fruit and vegetables (Jones, 2018; He et al., 2022; Sarabi et al., 2022), (4) modulate the biosynthesis of targeted secondary metabolites (Lobiuc et al., 2017; Landi et al., 2020; Morello et al., 2022). Technical advancements in artificial lighting, i.e. the development of LED technology (Singh et al., 2015; Stamford et al., 2023) and new material developed for cover films (Cerny et al., 2003; Manja & Aoun, 2019; Zheng et al., 2020; Liu et al., 2022) have further improved the capacity of modifying the light environment perceived by the plant. In addition, there are some cases in which the modulation of the light regime may exert unwanted effects on plant performance, for example, the possible side effect of continuous light from streetlamps in urban environments (Matzke, 1936; Chaney, 2002; Ffrench-Constant et al., 2016; Massetti, 2018; Lo Piccolo et al., 2023); thus the new LED technology can be employed to minimize the light disturbance on urban trees physiology and phenology.

The present review summarizes the main findings related to morpho-anatomical, physiological and biochemical changes promoted by specific light regimes (Figure 1), i.e., the growth of plants in monochromatic environments (section 2), the use of light supplementation (section 3) as well as covering films with different features (photo-selective, light-extracting, diffusive, mulching films – section 4). In addition, in section 5, we depicted how streetlamp illumination may influence morpho-anatomy and physio-chemical attributes of urban trees with the aim of increasing awareness of the necessity of less-impacting streetlamp solutions.

2 MORPHO-ANATOMICAL TRAITS AND PLANT SECONDARY METABOLITES IN MONOCHROMATIC ENVIRONMENTS

The effect of monochromatic light (ML) on plant biomass, morpho-anatomical traits, and secondary metabolite production has been extensively investigated in the last decade. Table 1 and Figure 2 summarize the results from recent studies dealing with the effect of ML environments to unveil ML-triggered in planta metabolic changes, whose comprehension is crucial not only for improving horticultural crop yield and quality, as reviewed by Jones (2018), but also to photomodulate the synthesis of targeted bioactive compounds in medicinal plants, such as Cannabis sativa (Danziger & Bernstein, 2021; Wei et al., 2021; Morello et al., 2022), Withania somnifera (Adil et al., 2019), Scutellaria baicalensis (Zhang et al., 2022a), Aronia spp. (Szopa et al., 2018), Artemisia absinthium (Tariq et al., 2014), Moringa oleifera (Bajwa et al., 2023).

The effects of monochromatic red light (RL) and blue light (BL) environments have attracted intensive research. Under short photoperiods of red and blue light, cryptochromes and phyB act synergistically, but under continuous exposure to the same light field, the actions of phyB and cryptochrome can become independent and additive (Casal, 2000). Therefore, the behaviour of plants under monochromatic RL or BL is not easily predictable and, as depicted below, may lead to species-specific as well as dose-dependent responses (Ahmad et al., 2016; Kitayama et al., 2019; Khurshid et al., 2020; Izzo et al., 2021; Rong Sng et al., 2021; Wei et al., 2021; Carillo et al., 2022; Zhang et al., 2022a; Su et al., 2024). RL is able to enhance plant/callus biomass production, as observed in plants of Withania somnifera (Adil et al., 2019), C. sativa (Wei et al., 2021), Coriandum sativum (Nguyen et al., 2020), Lactuca sativa (Izzo et al., 2021), Mesembryanthemum crystallinum (Kim et al., 2018), I. aquatica (Kitayama et al., 2019), Scutellaria baicalensis (Zhang et al., 2022a), Brassica oleracea, (Sathasivam et al., 2023), callus of S. rabaudiana, (Ahmad et al., 2016) and in vitro cultures of Pistacea vera (Abdouli et al., 2023). Greater stem diameter, leaf area, leaf length, and overall plant weight are the most common morpho-anatomical traits observed after red light (RL) exposure, which explains the higher biomasses seen in plants exposed to this light condition. (Kim et al., 2018; Kitayama et al., 2019; Nguyen et al., 2020; Rong Sng et al., 2021; Carillo et al., 2022; Morello et al., 2022; Abdouli et al., 2023; Su et al., 2024; Wei et al., 2021). Given that phytochromes are present in two forms: the inactive form, which absorbs maximally in RL (Pr) and the active form, which absorbs maximally in far-red (FR) light (Pfr), the increase in plant biometric traits is conceivably related to a combination of increment of the active form of phytochromes as well as the interception of the most efficient wavebands for photosynthesis (McCree, 1972). RL is principally absorbed by PSII, whilst FR light is preferentially absorbed by PSI, so the use of monochromatic RL may lead to overexcitation of PSII. Therefore, neither of the two lights would be optimal for photosynthesis when applied alone, and the interaction between the two lights would be synergistic and has to be considered when growing plants under monochromatic RL (Zhen & van Iersel, 2017). Indeed, the supplementation of FR to white light (up to 40% of background light) can increase the canopy's gross photosynthesis by adding an equivalent amount of white photons (Zhen &Bugbee, 2020).

Though a huge body of evidence supports the accumulation of biomass in plants exposed to RL, contrasting results have emerged regarding the RL-dependent biosynthesis of secondary metabolites that are of utmost importance for human health. For example, Adil et al. (2019) found the highest content of chlorogenic acid and withaferin A in callus cultures of W. somnifera grown in an RL environment. These authors hypothesized that withanolides, such as withaferin A, are involved in the conversion of phenylalanine to cinnamic acid catalyzed by phenylalanine ammonia-lyase (PAL). This enzyme is activated under red light (RL), signalling the phenylpropanoid pathway to counteract oxidative stress by accumulating higher levels of withanolides (Adil et al., 2019). Enhancement of PAL activity, the key enzyme of the phenylpropanoid branch metabolism, promoted by RL might also explain the increase in anthocyanin and flavonol content in Vaccinium corymbosum callus cultures (Abou El-Dis et al., 2021). Zhang et al. (2022a) also observed an increased level of two other flavonoids, namely baicalein and wogonoside, in S. baicalensis seedlings supplied with RL. In the same study, a punctual transcriptome sequencing analysis demonstrated that RL induced a higher accumulation of flavonoids than other ML treatments. This effect was attributed to the upregulation of genes involved in flavonoid biosynthesis, such as PAL, cinnamate CoA ligase (CLL), chalcone synthase (CHS), flavonol synthase (FNS) and 8-O-methyl transferase (OMT). Moreover, the RL-promoted increased level of cytokinins may also contribute to the accumulation of phenolic compounds (Khurshid et al., 2020).

RL also promoted the accumulation of ascorbic acid in C. sativum microgreens (Nguyen et al., 2020), targeted secondary metabolites in Eclipta alba such as amyrin, stigmasterol, luteolin, coumarin, eclalbatin, wedelolactone and derivatives (Khurshid et al., 2020) as well as carotenoids in petals of Crocus sativum (Moradi et al., 2022). Despite the generally positive impact of RL in terms of cannabinoid accumulation (Wei et al., 2021), some authors reported a reduction of this class of compounds in some C. sativa varieties after RL treatment, highlighting the importance of considering the genotype-dependent responses in terms of secondary metabolism modulation (Danziger & Bernstein, 2021; Morello et al., 2022).

Several studies have also analysed the effects of BL on plants, yielding interesting but occasionally contrasting results (Table 1). In terms of morpho-anatomical traits of plants treated with monochromatic BL, short petioles and shoots (with a reduction of plant height), leading to more compact plants characterized by increased leaf area and leaf thickness were observed (Izzo et al., 2021; Rong Sng, 2021; Carillo et al., 2022). In some studies, these changes translated into a reduction of the overall plant biomass (Zhang et al., 2022a; Wei et al., 2021). It is worth noting that such treatment led to enhanced inflorescence biomass in flowering crops (Wei et al., 2021; Orlando et al., 2023; Moradi et al., 2022). Rong Sng et al. (2021) analysed the morpho-anatomical traits of Lactuca sativa cv. Batavia plants grown for three weeks in a BL environment were found to have a higher leaf area and shorter petioles compared to lettuce grown in polychromatic or other MLs, such as RL and FR light. Accordingly, Carillo et al. (2022), analysing Petroselinum crispum microgreens grown in a chamber illuminated with BL, observed shorter internodes and more compact plants compared to those grown with other MLs or polychromatic lights. These authors attributed the inhibition of hypocotyl growth in plants exposed to BL to modifications in the cell wall structure, resulting in reduced turgor and finally leading to a slower plant growth rate (Carillo et al., 2022).

Another topic of research on the effect of a BL environment on plants is the possibility of increasing the inflorescence biomass. This phenomenon has been specifically observed in Cannabis sativa and C. sativus (Wei et al., 2021; Eftekhari et al., 2020; Moradi et al., 2022), suggesting a species-specific explanation for this feature. In C. sativa, it was observed that BL increased the photosynthate accumulation in the inflorescence, thereby reducing the vegetative growth and promoting inflorescence development and yield (Wei et al., 2021). Moradi et al. (2022) provided new insights, elucidating that the BL photoreceptor CRY is capable of initiating flowering by controlling the CRY2/coat protein 1(COP1) complex. COP1, in turn, affects the dehydration of CONSTANS (CO), a zinc-finger transcription factor able to trigger plants to flower.

It has long been known that in response to biotic and abiotic stressors, plants synthesize an arsenal of secondary metabolites. Exposure to a monochromatic BL can represent a “eustress” for plants, thus a stress that activates and stimulates plant responses, with positive consequences for plant development (Lichtenthaler, 1996), for example, the stimulation of the biosynthesis of those targeted secondary metabolites whose accumulation is strictly dependent on the applied narrowband light. As illustrated in Table 1, several studies reported an increase in the concentrations of key antioxidant molecules and enhanced antioxidant activity in seedlings and/or callus cultures grown under monochromatic BL (Ahmad et al., 2016; Kim et al., 2018; Kitazaki et al., 2018; Szopa et al., 2018; Asad Ullah et al., 2019; Kitayama et al., 2019; Nguyen et al., 2020; Usman et al., 2020; Anum et al., 2021; Yang et al., 2021; Biswal et al., 2022; Carillo et al., 2022; Moradi et al., 2022; Morello et al., 2022; Puccinelli et al., 2022; Bajwa et al., 2023; Eftekhari et al., 2023; Sathasivam et al., 2023; Su et al., 2024). The highest observed total phenolic content (TPC) and total flavonoid content (TFC) in plants exposed to BL can be attributed to the proximity of B and UV spectra wavelengths, thus promoting similar stimulatory effects on secondary metabolite biosynthesis (Abdouli et al., 2023). This observation is corroborated by Szopa et al. (2018), who noted the highest accumulation of neochlorogenic and protochatecuic acids in Aronia melanocarpa grown under BL and UV-A monochromatic environment. Simultaneously, other researchers confirmed that cryptochromes (blue and UV receptors) play a pivotal role in regulating the biosynthesis of secondary metabolites such as anthocyanins, cannabinoids and glucosinolates (Mickens et al., 2018; Wei et al., 2021; Yang et al., 2021; Morello et al., 2022; Sathasivam et al., 2023).

Although fewer studies are available on the use of monochromatic green (GL) environments (compared to those dealing with BL and RL), GL has been generally proven to exert negative effects on plant growth, as revealed by the impairment of several morpho-anatomical parameters, including a reduced leaf number and area in relation to stem weight as well as lower stomata density (Table 1). Furthermore, starch granules in the chloroplasts were fewer in number and smaller in size in plants grown under GL (Su et al., 2014). The biochemical parameters which have been most strongly affected by GL (compared to RL or BL) and contribute to the impairment of plant growth include lower chlorophyll content, reduced ribulose-1,5 bisphosphate carboxylase/oxygenase (Rubisco) activity and consequently, a decline in ETR and PSII efficiency (Landi et al., 2020).

In addition to this generalization, it is important to recognize that what is often described as a “monochromatic environment”, should more accurately be defined as a “narrowband light”, particularly for green light (GL). Indeed, supplementation with short- and long-wavelength GL may elicit different responses in plants (Dougher & Bugbee, 2007). Depending on the peak of the GL (usually ranging from 550 to 570), the absorbance by the inactive form of phytochrome (Pr) could be higher than that of Pfr. Therefore, the plant's responses may be derived from a trade-off between the effect of cryptochrome and phytochrome, which might explain why, in some cases, plants grown under green light have similar or even higher biomass yield (Pedroso et al., 2017; Amaki et al., 2011, respectively).

Biochemical modification triggered by GL also includes the secondary metabolism; for example, Adil et al. (2019) found that W. somnifera callus cultures grown in a monochromatic GL accumulated a higher withaferin A level than those grown with a cool white light, used as a control. Tariq et al. (2014) reported an increase in TPC and TFC, along with enhanced antioxidant activity in A. absinthium callus culture exposed to monochromatic GL compared to controls, i.e. callus culture grown in a cool white environment.

3 SUPPLEMENTAL LIGHTING WITH TARGETED WAVEBANDS

If monochromatic environments are used to stimulate targeted secondary metabolisms or are relevant in a vertical farming context for short-term applications (i.e., spouts, microgreens), the supplementation of solar light with narrowband lamps represents a feasible technique in greenhouse cultivation to be applied transiently or during a whole cultivation cycle. Nowadays, LEDs are the leading source of light in agriculture. Compared to traditional lighting methods, LEDs have energy efficiency implications as they (1) have up to 2.5-fold longer life span than HPS lamps, (2) have low energy consumption due to the low heat emissions and (3) can be efficiently designed for controlling the light spectrum, the intensity and the scheduling to fine-tuned their application based on the plant's needs (Bourget, 2008; Stamford et al., 2023).

In greenhouses, ML supplementation can increase the daylight intensity where daily light integral (DLI) is insufficient or extend the photoperiod by providing additional hours of illumination. The lighting enrichment by narrowband lamps can alter the spectral composition, capitalizing on the morphological, biochemical, and physiological responses connected with the exposure to specific monochromatic wavelengths. However, it is crucial to maintain a full-spectrum solar light background to ensure that plants receive all the necessary portions of the light spectrum. Selected wavebands can be applied individually or in combination, affecting plant productivity and morphology (Stamford et al., 2023). The consequences of light supplementation are not always consistent; in most cases, results are genotype-dependent but also attributable to the DLI provided, as well as the season/latitude where light supplementation is employed.

The impacts of narrowband light supplementation on plant development, physiology, and biochemistry are summarised in Table 2. Effects which are not related to the alteration of light quality by narrowband lights (i.e., effects merely related to increased light flux) have been omitted. In all the studies reported in Table 2, narrowband lights provided by LED lamps were employed because of their advantages over older light sources (Morrow, 2008) and, generally, a maximum intensity of up to 250 μmol m⁻² s⁻¹ was provided.

The supplementation of RL over sunlight increased plant productivity in strawberry (Lauria et al., 2023a) and mini cucumber (>200 μmol m⁻² s⁻¹; de Freitas et al., 2021) but decreased the yield in sweet pepper (Kim & Son 2022) and tomato (<100 μmol m⁻² s⁻¹; Kaiser et al., 2019). Similar results were observed when RL (<100 μmol m⁻² s⁻¹) was added before or after natural light exposure, resulting in increased strawberry fruit production (Choi et al., 2015) and plant development in cucumber and tomato (Wang et al., 2021, 2022, respectively). Despite the positive results observed in terms of productivity, supplemental RL often decreased net photosynthesis, reduced stomatal size, lowered Rubisco activity and decreased carbon export from the Calvin–Benson cycle in tomato (Kaiser et al., 2019), strawberry (Lauria et al., 2021, 2023c), and basil plants (Jensen et al., 2018; Lauria et al., 2023b). This reduction was associated with decreased PSII efficiency and PSII antenna's ability for energy conservation (Kaiser et al., 2019; Lauria et al., 2023c). Moreover, RL also led to a reduction in abscisic acid content in basil (Jensen et al., 2018). This behaviour could be partially explained by alterations in the expression of both PSII and PSI multiprotein complexes (Muneer et al., 2014). In contrast, when RL enrichment is applied in artificial lighting instead of over a natural background, even when RL is predominant, the observed effects are usually positive and consistent across different crops. In fact, it has been reported that a 2:1 to 4:1 red-to-blue (RL:BL) ratio, irrespectively of the fluence, enhances photosynthetic performances and increased net photosynthesis, transpiration rates and stomatal conductance in cucumber (Wang et al., 2021), mini cucumber (de Freitas et al., 2021), tomato (Wang et al., 2022; Zhang et al., 2022b) and Impatiens hybrida (Kobori et al., 2022).

Besides physiological effects, RL supplementation can also affect primary and secondary metabolism. Lower intensities of RL increased starch and sucrose (tomato; 125 μmol m⁻² s⁻¹; Zhang et al., 2022b) as well as glucose and fructose (sweet pepper; 71 μmol m⁻² s⁻¹; Kim & Son, 2022). These alterations could be related to the modulation of carbohydrate metabolism by phytochrome A and B (PHYA and PHYB), with PHYA promoting starch accumulation under a wide range of light conditions through a signalling cascade involving the plastidial nucleoside diphosphate kinase-2 (NDPK2) and glucose-1-phosphate adenylyltransferase small subunit (APS1) (Han et al., 2017). Conversely, Lauria et al. (2023a) observed that higher intensities (250 μmol m⁻² s⁻¹) of RL led to a reduction of sugars and organic acids content in strawberry fruits, suggesting that RL irradiation might accelerate glycolysis and tricarboxylic acid (TCA) cycle.

Regarding changes in secondary metabolism, supplemental RL has been shown to promote the accumulation of compounds belonging to different classes, including quercetin (I. hybrida cv. White; Kobori et al., 2022), ascorbic acid, carotenoids (sweet pepper; Kim & Son, 2022), anthocyanins (strawberry fruits; Lauria et al., 2023a), and xanthophylls (strawberry leaves; Lauria et al., 2021). After cold storage, tomato fruit treated with a pre-harvest ratio of 3:1 RL:BL showed increased lycopene and carotene contents (Appolloni et al., 2023). When RL was exclusively used to extend the photoperiod, an increase in chlorophyll content was reported in strawberry leaves and tomatoes (Choi et al., 2015, Wang et al., 2022, respectively), along with elevated carotenoid content in cucumber and tomatoes (Wang et al., 2021, 2022, respectively), higher carbohydrate levels in rocket salad (Sarabi et al., 2022), increased sugar content in strawberry fruit, cucumbers and tomatoes (Choi et al., 2015, Wang et al., 2021, 2022, respectively), and elevated flavonoid and tannin contents in rocket salad (Sarabi et al., 2022). Choi et al. (2015) also reported an increase in oxalic and malic acids, anthocyanins, and antioxidant activity in strawberry fruit, while Sarabi et al. (2022) noted a decrease in nitrate content and NH₄⁺ in Eruca sativa due to increased glutamine synthetase activity, which catalysed the conversion of NH₄⁺ into glutamine.

Although FR light is usually considered marginally in greenhouse cultivation, with a high R:FR ratio generally preferred (see section 3), some studies have reported impacts of supplemental FR light on the physiology, morpho-anatomy and both primary and secondary metabolisms of plants, for example, increased plant height (Taxus baccata; Chiocchio et al., 2022) and improved post-harvest cold tolerance in tomatoes (Affandi et al., 2020). When added to a background of supplemental wide-spectrum light, FR light increased the maximum quantum yield of PSII photochemistry, both in conditions of high and low R:FR ratio (Matysiak, 2021). Additionally, FR light supplementation promoted the accumulation of sucrose, glucose, fructose, and ascorbic acid in sweet pepper (Kim & Son, 2022).

A large body of experimental work explored the effect of supplemental BL on biomass, morpho-anatomical, and physiological responses, as well as its impact on both primary and secondary plant metabolism. The addition of 25–30% B light (approximately 100 μmol m⁻² s⁻¹) led to a reduction in triose phosphate use but correlates with an increase in photosynthetic capacity, quantum yield for CO₂ assimilation, and rates of daytime respiration in tomato (Kaiser et al., 2019, Kalaitzoglou et al., 2021). In cucumber, the supplementation with 180 μmol m⁻² s⁻¹ of BL increased net photosynthesis and transpiration rates (Yan et al., 2022). These improvements were likely caused by the enhancement in the activity/expression of key components of the photosynthetic process, such as Rubisco, cytochrome f complexes, chlorophylls, and light harvesting complexes proteins of PSII (Matsuda et al., 2004). Conversely, the application of higher intensity of BL (250 μmol m⁻² s⁻¹) might exert a detrimental effect on photosynthetic activity (strawberry; Lauria et al., 2021). This effect likely stemmed from BL influences on leaf physiology, possibly through the impact on chloroplast movement, as well a reduction in carbonic anhydrase activity (Momayyezi &Guy, 2017), which might explain the decrease in plant biomass and leaf area observed in some species (tomato; Kaiser et al., 2019; Kalaitzoglou et al., 2021; basil; Matysiak &Kowalski, 2019; Lauria et al., 2023b). Of note, BL has been reported to be more effective at opening stomata than RL (Vialet-Chabrand et al., 2021), which involves the release of stored energy and osmolytes from starch degradation or lipid metabolism (Horrer et al., 2016). As a consequence, BL resulted in greater stomatal conductance and transpiration rates in both green- and red-leafed basil (Jensen et al., 2018; Lauria et al., 2023b). However, BL-induced stomatal opening does not necessarily rely on higher photosynthesis, suggesting that the guard cell mitochondria play a key role in powering the BL response and that species-specific BL-induced stomatal, in terms of both rapidity and magnitude, must be considered (Vialet-Chabrand et al., 2021).

Supplemental BL (250 μmol m⁻² s⁻¹) also increased primary metabolite content in strawberry fruit, mainly organic acids, sugars, and amino acids (Lauria et al., 2023a) and promoted changes to the secondary metabolism, such as increasing flavonoid content in a plethora of species including green basil (Taulavuori et al., 2016; Matysiak & Kowalski, 2019; Lauria et al., 2023b) red-leafed sweet basil (Matysiak & Kowalski, 2019; Lauria et al., 2023b), lamb's lettuce and garden rocket (Matysiak &Kowalski, 2019), red-leafed lettuce (Taulavuori et al., 2016), and tomato (He et al., 2022). BL also promoted the accumulation of phenolic content in red-leafed lettuce, tomato and strawberry (Taulavuori et al., 2016, He et al., 2022, Lauria et al., 2023a, respectively) as well as anthocyanins in red-leafed basil (Lauria et al., 2023b). Indeed, BL has been shown to overexpress the transcript levels of genes encoding PAL and flavonoid-3′-hydroxylase, with the former playing a key role in flavonoid biosynthesis by channelling primary metabolites into this secondary pathway (Thwe et al., 2014). In other cases, BL was also reported to increase antioxidative capacity, level of lycopene, vitamin C, free amino acids, and soluble sugars (e.g. tomato; He et al., 2022) and promote the decrease in nitrate and NH₄⁺, likely due to the stimulated activity of nitrate metabolism enzymes (E. sativa; Sarabi et al., 2022).

To date, little research has explored the impact of supplementing GL in the greenhouse environment. Despite an increase in stomatal number, supplemental GL led to a decrease in stomatal conductance and, consequently, in internal CO₂ concentration in both green- and red-leafed basil, thereby positively influencing water use efficiency (Lauria et al., 2023b). Regarding secondary metabolism changes, some studies have reported that GL increases xanthophyll content at high intensities after a single day of supplementation (strawberry leaves; Lauria et al., 2021), increases primary metabolites and phenolics in strawberry fruit (Lauria et al., 2023a), and enhances the flavonoid metabolism in red-leafed basil after long-term treatment (Lauria et al., 2023b). However, the few studies on the effect of supplemental GL on secondary metabolism make it challenging to draw general conclusions.

In addition to the aspects mentioned above, recent experiments have also explored the possibilities of supplementing additional hours of narrowband light during the night. Supplemental hours of both BL and yellow (Y) light during nighttime showed positive effects in terms of biomass, photosynthesis, and secondary metabolite production in Anoectochilus roxburghi, while RL, GL, and white light decreased secondary metabolite content (30 μmol m⁻² s⁻¹; Wang et al., 2018). Similarly, in strawberry plantlets, additional hours of BL during the night positively affect flowering and biomass, while R light revealed the opposite effect (Magar et al., 2018). The authors hypothesize that a BL increase in the cytokinin levels stimulates flowering, while the inhibition of this process was potentially connected with the RL activation of endogenous gibberellins. Moreover, Lin (2000) reported the control of flower induction genes (i.e., FLOWER LOCUS T and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1) by cryptochrome and phytochrome in Arabidopsis. Further investigations may shed light on whether night supplementation can represent a feasible greenhouse technique for improving the quality of horticultural crops. If it is proven to offer benefits in terms of yields or nutraceutical properties, it could potentially replace daytime light supplementation, thereby reducing lamp energy costs.

4 LIGHT MODULATION THROUGH COVERING MATERIALS

Among all the covering materials used in agriculture, those able to modulate the light spectrum and covered to some extent in literature are (1) films which can exclude specific undesirable wavebands, (2) photo-selective coloured shading nets and films which can considerably modify the full light spectrum, (3) photo-converting films with fluorescent dyes and the ability to induce a photonic shift toward more desirable wavebands, (4) and light-diffusing plastic films which can alter light distribution inside the greenhouses (Figure 3). Lastly, plants can also be influenced by light modification induced by coloured mulching films, which can alter the reflectance of the light spectrum.

5 LIGHT DISTURBANCE: THE CASE OF STREETLAMP ILLUMINATION ON TREES

Although there are benefits to supplemental lighting in greenhouse cultivation, artificial illumination may negatively affect plant physiology. This is particularly evident in urban areas, where streetlamps extend the “day length” throughout the night. In our cities, light pollution has constantly risen by around 6% per year over the last decades to facilitate human activities (Hölker et al., 2010), altering animal behaviour, like herbivores and pollinators, and affecting plant phenology, growth, and resource allocation (Lian et al., 2021; Liu et al., 2021; Lo Piccolo et al., 2023). The first observations of this phenomenon on plants occurred in the first half of the 20th century when Matzke (1936) observed a delay in leaf senescence in trees growing in close proximity to streetlamps (e.g., in Populus canadensis and Platanus × acerifolia individuals). Subsequently, Chaney (2002), compiled a comprehensive table detailing the susceptibility of woody plants to the influence of illumination from streetlamps. However, since then, only a handful of studies have investigated the repercussions of light pollution on trees, and even fewer have explored the physio-chemical traits of plants illuminated by streetlamps at night. Furthermore, no one has ever studied the long-term effect of night illumination on tree health and ecosystem services. Consequently, much of the real amplitude of this phenomenon remains to be thoroughly understood and elucidated.

In plants, photoreceptors (i.e., phytochromes, cryptochromes, and phototropins) are pivotal for regulating circadian rhythms based on external light stimuli, perceiving seasonal changes, controlling the repair and recovery of plant physiological functions, and inducing the onset of flowering and dormancy (Björn, 2015; Kong & Zheng, 2020). In this framework, it seems obvious that night streetlamp illumination could influence plant circadian rhythms by interfering/stimulating photoreceptors (Bennie et al., 2016; Bennie et al., 2017). The light emission spectrum of streetlamp illumination can vary greatly depending on the technology (Bennie et al., 2016). In the urban environment, the most common streetlamp solutions used in the past were High-Pressure Sodium (HPS) lamps, with high irradiance peaks in the R spectrum, which are highly likely to interfere with plant phytochromes. However, more recently, HPS lamps have been gradually replaced by LED lamps, causing different problems for tree metabolism, as these lamps have an additional peak in the B light emission spectrum (Lo Piccolo et al., 2023), which interferes with plant cryptochromes. These photoreceptors regulate stem growth, flowering time, stomatal opening, circadian clock, and other UV/BL-driven responses (Wang & Lin, 2020). Among others, one of the main reactions triggered by cryptochrome is the BL-induced stomatal response, which occurs at low light intensities and is often considered independent of photosynthesis (Vialet-Chabrand et al., 2021). However, some studies demonstrated that the intensity of RL over BL influences the magnitude of the stomatal response (Shimazaki et al., 2007), considering that this ratio varies during the day and plants experience a high BL:RL at dawn and before dusk (Matthews et al., 2020). Therefore RL:BL, as well as the addition of GL on the streetlamp spectra (which is opposite the effect of BL on cryptochromes; Johkan et al., 2012; Landi et al., 2020) should be considered to develop less impacting streetlamps on tree species.

To date, information on the effects of specific streetlamp technologies on plant physiology is scarce, largely due to the lack of investigation into different streetlamp technologies and the species-specific nature of these effects. Therefore, the following text will discuss the general impacts of nocturnal illumination by streetlamps on trees. Table 8 outlines the multiple effects on plant phenology and physiology due to streetlamp illumination on trees.

In general, nocturnal illumination by streetlamps leads to a delay in the autumn leaf fall and the entry into winter dormancy, as was observed in P. canadensis and P. occidentalis (Matzke 1936), P. × acerifolia (Massetti, 2018; Lo Piccolo et al., 2023), Rhus typhina (Tuhárska et al., 2014; Škvareninová et al., 2017) and Acer pseudoplatanus (Škvareninová et al., 2017) (Figure 4). These delays could potentially have adverse consequences for deciduous trees, especially in the presence of frosts, which may damage leaves and buds.

On the contrary, no alterations in the tree phenology were observed in Betula pendula and Tilia × platyphyllos (Sarala et al., 2013, Lo Piccolo et al., 2023, respectively). These differential responses among tree species could be due to the species-specific sensitivity to external stimuli, as winter dormancy can be influenced by factors such as photoperiod and temperature, or the combination of both (Zhang et al., 2020). Lo Piccolo et al. (2023) observed that the entry into winter dormancy of T. × platiphyllos was less influenced by the altered photoperiod, suggesting that external environmental temperatures played a more significant role in regulating dormancy induction than the photoperiod. On the other hand, in the case of B. pendula, both photoperiod and temperature can influence the onset of winter dormancy (Junttila et al., 2003, Li et al., 2003b). Therefore, the absence of an influence in tree phenology observed by Sarala et al. (2013) could be due to the low light intensity tested (0.16 μmol m⁻² s⁻¹ at the sampling point).

A 13-year-long investigation conducted in the UK on spatially referenced budburst data from four deciduous tree species, matched with satellite imagery of night-time, unveils that streetlamp night illumination anticipate bud burst by 7.5 days on brighter areas affecting particularly later-budding species (Ffrench-Constant et al., 2016). Similarly, an experiment with four tree and four shrub species found that all the species investigated were influenced by artificial light at night and developed buds faster than the control group (Czaja & Kołton, 2022). Moreover, it was reported that night light pollution could lead to an anticipated start of the growing season in the climatically temperate regions of the USA, though in colder or hotter regions, environmental temperatures have a predominant role in the induction of the spring phenology (Zheng et al., 2021). On the contrary, Lian et al. (2021), observed a delay in leaf burst in Alnus glutinosa, B. pendula and F. excelsior grown in light-polluted areas in Europe between 1991–2015. The apparent contradictions in these findings may be due to the fact that little research has been performed on the interactive effects of urban environmental temperatures (e.g., heat islands) and streetlamp illumination (e.g., if it heats, its light spectrum, its brightness) on urban tree phenology. Lian et al. (2021) suggested that while temperature plays a dominant role in shifts in plant phenological phases, the delaying effect of artificial light pollution is evident when considering these interactions.

In the literature, there are conflicting reports regarding the effect of streetlamp illumination on leaf pigments of urban trees, which, again, suggests the species-specificity of this response. Kwak et al. (2018) reported that leaves of plants exposed to streetlamp illumination rapidly turned yellow and fell. In contrast, Sarala et al. (2023) found no significant differences in leaf chlorophyll content in B. pendula trees exposed to streetlamps, whilst Li et al. (2019) reported higher values in leaf chlorophyll content in Cinnamomum camphora. Interactions between external light signals and the endogenous plant circadian clock regulate chlorophyll biosynthesis and breakdown. For instance, the conversion from protochlorophyllide to chlorophyllide is light-dependent, thus, this control mechanism leads to decreased chlorophyll synthesis at night and increased synthesis during the day (Kobayashi & Masuda, 2019; Kumar et al., 2020; Suzuki & Bauer, 1995). Lo Piccolo et al. (2023) argued that nighttime lighting provided by streetlamps hampered the natural decrease in chlorophyll biosynthesis during the night, thus explaining the higher chlorophyll content in the leaves of trees grown under streetlamp illumination and possibly increasing the demand for N assimilation by the leaves. This assumption agrees with the observations of Liu et al. (2021), who reported low N concentrations in the roots and wood of trees illuminated by streetlamps, probably due to an increased demand for N assimilation by leaves and, subsequently, more chlorophyll biosynthesis. The contrasting results reported by Kwak et al. (2018) were probably linked to a premature leaf senescence phenomenon stemming from oxidative damage produced by high levels of ROS, such as O₂⁻ and H₂O₂, which led to increased lipid peroxidation and membrane permeability under artificial night illumination.

Nighttime illumination, if of sufficient intensity, can induce plants to photosynthesise during nocturnal hours (Lo Piccolo et al., 2021, 2023; Kwak et al., 2018), although the observed values of net photosynthesis (P_n) were lower than those at sunrise. Kwak et al. (2017) suggested that artificial nighttime light may unbalance the endogenous circadian levels of ABA, resulting in stomatal opening. The reduced P_n values at dawn may also be related to impairment of the photosynthetic machinery. Indeed, as observed in Populus alba, the greatest reductions in PSII performances were observed at dawn, where the lack of starch degradation during the night and the relative impairment in the sinking capacity, which may induce a feedback limitation, thus impairing linear electron transport flow, also evidenced by the downregulation of two ferredoxin nitrite/sulphite reductase domains (Lo Piccolo et al., 2024). Furthermore, the abundance of light-harvesting complex (LCHII) of PSII also exhibited a reduction in L. tulipifera (Kwak et al., 2017). Nocturnal alterations in photosynthesis due to streetlamp lighting can alter the primary metabolism of illuminated leaves, consequently impairing the source/sink balance. Kwak et al. (2017) observed a carbon starvation phenomenon in the leaves of L. tulipifera, resulting from reduced daytime accumulation and decreased nighttime starch degradation. Liu et al. (2021) observed an increase in starch and total soluble sugar concentrations in Acer truncatum and Quercus mongolica in streetlamp-lighted trees due to an accelerated translocation of carbon to sinks (i.e., new shoots that remained active even during the winter; Lo Piccolo et al., 2023).

The few observations obtained from the literature regarding leaf primary metabolism and carbon content suggest that tree species may adopt different strategies in response to nighttime streetlamp illumination, emphasising differences in susceptibility to artificial night lighting and highlighting the fact that this topic still needs to be fully elucidated.

All of the aforementioned reports highlight the deep influence of streetlamp lighting on urban trees. However, it is important to note that streetlamps do not only affect trees but also grass species, inducing vegetation changes in biomass and plant cover over time (i.e., Agrostis tenuis, Anthoxanthum odoratum and Holcus lanatus; Bennie et al., 2017).

To strike a balance between citizen safety and the well-being of urban vegetation, more research is required to fully understand both the annual and long-term impacts that urban illumination has on ecosystem functioning. It is necessary to investigate the effects of different streetlamp technologies, test innovative light spectra enriched with green and orange wavelengths and provide a comprehensive list of tree species susceptibility to artificial nocturnal lighting. Such research could help urban planners select the proper tree species for roadside avenues and lessen the impact of lighting solutions in our cities without compromising the fundamental need for citizen safety.

6 CONCLUSION AND PERSPECTIVES

The capabilities of new light technologies and cutting-edge materials for covering films to improve plant growth as well as metabolic performance have been increasingly exploited. The trade-off between costs and benefits (which goes beyond the aim of the present review) has to be considered and contextualized for each species. However, it is undeniable that “photomodulation” is a powerful tool to shape plant morpho-anatomical and metabolic features, though a lot of aspects still need to be investigated. For example, improving light use efficiency by the plant, even in condition of fluctuating light, is a frontier topic of investigation to feed a constantly growing population. On the other hand, artificial lighting may exert negative side effects, i.e. light pollution in urban environments, posing the urgent need for less-impacting streetlamp spectra on tree physiology. Besides the methodologies for light management proposed herein, some others for which the research and application are in their infancy are still worth mentioning. For example, root illumination in hydroponic cultivation (Cabrera et al., 2022) and fruit bagging (i.e. the use of coloured plastic films; Ali et al., 2021) could be proficiently used as an unconventional method to promote the quality and development of horticultural species. To date, few reports are available on these topics, and few details are provided regarding the spectra supplied to plants, which makes the result unreliable for drawing any solid and consistent conclusions. Thus, scientists and growers have nowadays a unique opportunity to contribute to generating knowledge on existing products for light management, while companies have the possibility to extend the portfolio of available products through cutting-edge innovation on light technologies and photomodulating materials.