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).