3 THE STRESS Response: a brief overview
When plants are subjected to sufficient environmental stress, reduction-oxidation (redox) reactions occur (Figure 2). Under normal conditions, partially reduced or activated forms of oxygen, known as ROS, are generated, but at a rate that can be managed by the plant’s ROS-scavenging machinery. Under highly stressful conditions, this redox homeostasis can become unbalanced, and these highly reactive molecules can cause cellular damage. As cellular ROS concentrations increase, for example with extreme temperature or drought, damage can afflict DNA, RNA, membranes and ultimately destroy the cell itself (Mittler 2002). As oxygen is produced during photosynthesis, the chloroplastic photosynthetic machinery, particularly in leaves, is the site of much of the ensuing ROS (Foyer 2018). In green developing fruit, where active photosynthesis is driving metabolism, this can still apply, but as the fruit ripens, ROS can be generated in other organelles, particularly mitochondria (Schertl & Braun 2014). This rise in respiratory sourced ROS, may occur when the common chloroplast/chromoplast shift removes the central mechanisms for coping with ROS: the xanthophyll (and other carotenoid) cycles embedded within the photosynthetic machinery.
Since these redox reactions are inevitable in an oxygenated world, plants have had to evolve coping mechanisms. One mechanism is enzymatic, with enzymes such as superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase, monohydroascorbate (MDHAR) and dehydroascorbate reductase (DHAR)(Das & Roychoudhury 2014). The other major mechanism involves the non-enzymatic antioxidants such as ascorbic acid (AsA) and numerous polyphenols and terpenes (Decroset al. 2019). AsA is an important scavenger of reactive oxygen and in a scenario where stress leads to a reduction in photosynthesis and an increase in photooxidative damage and ROS production, AsA production may be enhanced. AsA production does not directly affect the colour of fruit and will not be covered in this review, but nevertheless it is interesting to consider that the same signals that mediate changes in the concentration of AsA in fruit, may also mediate changes in polyphenol and terpene production. The polyphenols include flavonoids such as catechin, quercetin and anthocyanins, while terpenes include the pigmented carotenoids lycopene and β-carotene. It is clear then, that these plant pigments have a role in fruit beyond facilitating seed dispersal since there is good evidence for the induction of red pigmentation in vegetative tissues directly in response to ROS production. Plants have evolved this pigmentation to act as sunscreens and antioxidants and alleviate stresses from damaging environmental conditions (Davies et al . 2022).
The amount of ROS will also affect the concentrations of plant hormones, including abscisic acid (ABA), brassinosteroids (BRs), auxin and gibberellins (GAs). Phytohormones play a major role in ripening, with ethylene and ABA having key roles in climacteric and non-climacteric fruits, respectively (Fenn & Giovannoni 2021). Both ethylene and ABA play dual roles in the fruit, being not only linked with ripening, but also with the stress response (Husain et al. 2020; Leng, Yuan & Guo 2013). Several studies have shown a connection between increased content of fruit ABA, as a response to stress or at onset of fruit ripening, and the accumulation of anthocyanins (Jia et al. 2011; Karppinen et al. 2018; Wheeler et al. 2009; Zifkinet al. 2012). It has been suggested that accumulation of ABA inside the cell induces downstream signalling involving ROS and calcium as secondary messengers, resulting in activation of the TFs controlling the anthocyanin biosynthetic pathway (Vighi et al. 2019). Phytohormones can also interact, sometimes antagonistically such as has been shown for ABA and ethylene, but sometimes positively through providing an enhanced response to abiotic stresses (Müller 2021).
In this review, we concentrate on the major environmental stressors that influence pigment carotenoid and anthocyanin production in fruit crops. Chlorophyll accumulation and degradation also contribute to fruit colour, particularly before ripening occurs, but this falls outside the scope of this review. While betalains are also important plant pigments, they are most commonly found in leaves, flowers, tubers and only quite rarely found in fruit, such as in prickly pear (Opuntia ficus-indica ) and dragon fruit/pitaya (Hylocereus costaricensis ) (Cheok et al . 2022). They too are elevated in response to various environmental stresses: this has recently been well reviewed (Davieset al. 2018; Li et al. 2019) and will not be covered here.