Temperature stress
Temperature stresses, both below and above optimal growth temperatures, have been shown to affect plant pigment accumulation during fruit ripening. Although there is broad variation in what is the optimal temperature depending on species, cultivar and ecotype, heat stress can inhibit pigment biosynthesis in ripening fruits. Studies demonstrate that this is the case for both carotenoid and anthocyanin pigments (Gashu et al. 2022; Kliewer 1977; Lin‐Wang et al. 2011; Tomes 1963). When heat stress is moderate, the changes can be reversible, whereas severe episodes can cause irreversible changes to metabolites, resulting in crop failure.
Heat stress has been shown to inhibit anthocyanin biosynthesis in grape berry skin in controlled studies with temperatures higher than 30°C (Ryuet al. 2020; Yamane et al. 2006). Active inhibition and degradation of anthocyanin biosynthesis under high temperature conditions have also been reported in other fruits such as Malus profusion (Rehman et al. 2017) as well as in grape (Mohavedet al. 2016). Changes in ABA contents and in ABA/GA ratio have been associated with changes in anthocyanin concentrations under different temperature conditions (Ryu et al. 2020). Hot conditions during the growing season can dramatically reduce anthocyanin production in numerous apple cultivars, with an associated reduction in the transcription of the biosynthesis genes (Ubi et al . 2006) and the pathway regulating MYB TF, MYB10 (Lin-Wang et al . 2011). This appeared to be repression of anthocyanin activation, rather than an increase in transcription of known anthocyanin MYB repressors.
Almeida et al. (2021) found that ripe tomato fruit had better plasticity to restore carotenoids following a heat wave compared with tomatoes that experienced excessive heat during the breaker stage (when pink colour is just starting to develop). They concluded that heat-related transcriptional and posttranscriptional mis-regulation during early carotenogenesis affected the carotenoid composition in the ripe tomatoes. Moreover, upstream ripening regulators, such asCNR and NOR , were also affected by the heat treatments. The results also suggested that epigenetic mechanisms were mediating heat-induced transcriptional changes.
It is not only high temperatures that can be problematic for fruit colour. Low temperature conditions at around 4–10°C can cause stress in developing fruits because of ROS production and generation of malondialdehyde (MDA) in the cell, which can lead to severe membrane lipid peroxidation. Cold stress also promotes the accumulation of anthocyanin- and carotenoid-regulating phytohormones, ABA, jasmonates (JA), ethylene (ETH) and salicylic acid (SA) (He et al. 2022). ABA, JA and polyamines have been reported to be associated with low-temperature stress tolerance in apple fruitlets (Yoshikawa, Honda & Kondo 2007).
Lower temperatures have been observed to increase anthocyanin biosynthesis in many fruits, such as apples, table grapes, black currants (Ribes nigrum ), cloudberries (Rubus chamaemorus ), while anthocyanin accumulation is inhibited during heat stress (Chenet al. 2021; Downey et al. 2006; Martinussen et al.2010; Wang et al . 2018; Woznicki et al. 2015). The subsequent increase in anthocyanin concentration in fruit skin provides some tolerance to cold stress, for instance in mango (Sivankalyaniet al. 2016; Sudheeran et al. 2018). This production of anthocyanin at these lower temperatures is providing an alternative means to other ROS coping mechanisms which are compromised by cold. However, for other fruits such as strawberry, temperatures below 10°C have been shown to inhibit anthocyanin biosynthesis, a process mediated by MITOGEN-ACTIVATED PROTEIN KINASE3(FvMAPK3) (Mao et al. 2022).
Whereas high temperature clearly represses transcription of MYB10 in apple, the opposite is seen with low temperature in crabapple. In this case, the transcription of the MBW activation complex, including MYB10, bHLH3/33 and TTG1, is elevated, leading to increased anthocyanin production (Tian et al . 2015). Other TFs are involved in this response and Fang et al. (2019) showed that the zinc finger TF, MdBBX20, responds to low temperature via MdbHLH3 interaction, to drive anthocyanin production in a HY5-dependent manner.
Cold stress has been shown to affect carotenoid contents in fruits as a response to the production of ROS, in a species-specific manner. For example, higher lycopene contents have been shown to offer tolerance against cold stress in grapefruit (Citrus paradisi ) (Ladoet al. 2015), whereas in mango, carotenoid contents decreased under cold stress (Rosalie et al , 2018). In pepper (C. annuum ) fruit, Zhang et al. (2020) showed that CaATHB-12 , a member of the HD-ZIP I gene family, is one of the key regulators of fruit carotenoid content.
Diurnal temperature, with cool nights and warm days, is critical to optimal fruit colour in some species and a reduction in diurnal temperature range, as may become more evident with climate change, will impact anthocyanin in fruit peel, such as in apple (Qu & Zhou 2016). Clearly, optimal day and night temperatures help to produce high quality coloured fruit, while temperatures outside of this range often positively (cold) or negatively (excess heat) effect the concentration of colour.