Light stress
Light is one of the most important environmental factors affecting the accumulation of pigments during fruit ripening. Light effects can be categorised by duration (photoperiod), intensity (quantity), and quality (wavelength), all of which have been shown to affect pigment production. Both excess and inadequate light intensities and their fluctuations are collectively known as light stress. In addition, fluctuations in light wavelengths, especially excess of UV-light, can also cause light stress. Stress from non-optimal light conditions can cause alterations in pigment production (Zoratti et al . 2014). Plants convert photons of light through photosynthetic fixation of carbon dioxide into sugars. Light quality affects both photosynthetic rate and assimilation. Exquisite mechanisms have been developed to tolerate light stress, accumulation of pigments being one of the most important (Yang et al. 2019).
Little or moderate light stress can actually be beneficial for fruit quality by enhancing pigment concentration. On-tree apple experiments have shown that light stress induces anthocyanin production: these anthocyanins may reduce the amount of excess light as well as reducing the damage from the increased ROS produced to protect chlorophylls and carotenoids as part of the photooxidative machinery (Merzlyak & Chivkunova 2000). On-tree experiments have also shown that full spectra, including UV light, are essential for anthocyanin production (Henry‐Kirket al. 2018). Fruit bagging and shading experiments confirm the importance of direct exposure to light for biosynthesis of anthocyanins and carotenoids. Light exclusion results in transcriptional suppression of biosynthetic pathway genes and reduced accumulation of pigments (Downey, Dokoozlian & Krstic 2006; Saini & Keum 2018; Zhu et al. 2021; Zoratti et al. 2014). Whereas many fruits, like apples, have an absolute light requirement for anthocyanin biosynthesis (An et al. 2020a), there are species and cultivars that show no change in anthocyanin accumulation when in shaded conditions or any degradation of anthocyanins under high irradiation (Downey et al.2006; Zoratti et al. 2014). This indicates that there are different genetic regulation mechanisms for anthocyanin biosynthesis in some fruits, which are not fully understood.
Anthocyanins intercept and absorb light energy to avoid photodamage caused by excess light energy, directly scavenge free radicals and indirectly remove ROS by interacting with molecules in other signalling pathways (Li et al. 2019). In extreme high light conditions, anthocyanins play an important role in mitigating photoinhibition and photodamage. Naturally red-skinned pear species have been shown to maintain better photosynthetic capacity under high light and high temperature conditions, while some green-skinned pear cultivars increase skin anthocyanins in response to high light stress (Thomson, Turpin & Goodwin 2018).
In tomato, the accumulation of carotenoids during ripening is significantly influenced by light. Phytochrome induces degradation of phytochrome-interacting factor 1 (PIF1), a bHLH-type TF. In mature green tomato, PIF1 directly binds to the PIF-binding E-box PBE box of the PSY1 promoter of the carotenoid biosynthetic pathway, to repress carotenogenesis. During ripening, developmentally controlled degradation of chlorophylls reduces the self-shading effect, allowing phytochrome-mediated degradation of PIF1, which leads to depression of PSY1. This accelerates carotenoid biosynthesis and shifts the profile from xanthophyll, which is typical for leaves, to carotenes, mainly lycopene and β-carotene (Saini & Keum 2018). Exposure of tomato to excessive sunlight has been reported to inhibit the synthesis of lycopene (Brandt et al. 2006; Ilić & Fallik 2017). It has been proposed that ROS and redox status, combined with sugar and carbon status, integrate the stress response and photosynthetic metabolism, and so influencing the synthesis of carotenoids (Fanciullino, Bidel & Urban 2014). In Clementine (Citrus clementina ), accumulation of high amounts of soluble sugars through photosynthesis during the early stages of fruit development negatively influenced plastid development, which affected carotenoid accumulation, although later in fruit development, greater sugar accumulation increased carotenoid production (Fanciullinoet al. 2014; Saini & Keum 2018).
The quality of the light spectrum has been shown to affect fruit pigments. Treatments with UV-B and UV-C light during ripening or postharvest resulted in increased anthocyanin concentrations in many fruit species, including apple, peach, wine grape (Vitis spp.), and blueberry (Chen et al. 2021; Henry‐Kirk et al. 2018; Zoratti et al. 2014). Changes in carotenoid content following exposure to UV-light have also been reported in tomato (Giuntiniet al. 2005) and wine grape berries (Vitis vinifera ) (Joubert et al. 2016).
Solar UV-B radiation has extensive photobiological effects on plants: stress caused by UV-B is known to enhance the production of ROS, leading to damage of DNA, proteins and the photosynthetic apparatus. In plants, UV-B light is absorbed by tryptophan amino acid residues in the dimeric form of UV8 photoreceptor, leading to UVR8 monomerization and formation of a complex with CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), a known mediator of diverse light signals in plants interacting with regulators of both anthocyanin and carotenoid biosynthesis (Stanley & Yuan 2019; Zoratti et al. 2014). Plant pigments have an important role in protection of tissues against UV-radiation. For instance, anthocyanins and flavonols have been shown to accumulate in the epidermal tissues, such as fruit skin, to shield against excess UV-light (Zoratti et al. 2014). During photosynthesis, carotenoids harvest light energy and transfer this energy to chlorophylls through singlet-singlet excitation transfer, a lower energy state transfer. Excessive energy from chlorophylls is absorbed by carotenoids through triplet-triplet transfer, which is a higher energy state transfer essential for photo-protection. Carotenoids with more than eleven conjugated double bonds have a high capacity for quenching singlet oxygen produced under light stress (Maoka 2020).
Other light spectrum wavelengths have also been shown to influence the accumulation of fruit pigments and particularly red and blue wavelengths affect the biosynthesis of anthocyanins and carotenoids. Red or blue light treatment has resulted in a detectable increase in anthocyanin content in several fruit crops, including strawberries, grape, pear, apple, and cherry (Prunus avium ) (Kokalj et al. 2019a; Kokalj et al. 2019b; Koyama et al. 2012; Miao et al. 2016; Tao et al. 2018). Recently, both red and blue light were shown to increase anthocyanin biosynthesis during bilberry ripening (Samkumar et al. 2021; Samkumar et al. 2022). Interestingly, differences in the perception of red and blue light were detected between berries ripening whilst remaining attached to the mother plant, or when detached in Petri dishes. Transcriptomic analysis revealed differences in red and blue light signalling, leading to altered anthocyanin content in the ripe, treated berries, with red light increasing the anthocyanin content 12-fold compared with the control (Samkumar et al. 2021).
Many studies have shown that red light typically increases carotenoid biosynthesis in fruits, while blue light has less effect, although there are differences between species, cultivars and ripening stages. Spectral light quality experiments monitoring carotenoid biosynthesis in ripeningCapsicum annuum showed that red radiation was the most effective in increasing carotenoid accumulation, whereas green and blue radiation inhibited the formation of capsanthin, the major carotenoid influencing fruit colour (Lopez, Candela & Sabater 1986; Pola, Sugaya & Photchanachai 2019). Similar results have been shown in Citrus(Gong et al. 2021; Ma et al. 2012). In kumquat (Fortunella crassifolia ) fruit, a NAC family TF, FrCNAC22, was shown to mediate red light-induced carotenoid accumulation (Gonget al. 2021). Moreover, PIF1 regulation, following blue light perception, has been shown to act as a negative regulator of carotenoid biosynthesis (Gong et al. 2021).