Tomatoes Turn Pale in the Heat: High Temperature Reduces Red and Green Pigmentation via Phytochromes Free

The gardeners among us know that direct sunlight is a prerequisite to obtain full-sized, bright red tomato (Solanum lycopersicum) fruits. Indeed, light increases the accumulation of yellow and red carotenoid pigments, particularly lycopene, in ripe tomato fruits while it also boosts chlorophyll levels in the green parts of the plant. At the molecular level, the accumulation of these pigments is regulated by multiple light signaling components, in particular the red/far-red light-sensing phytochrome photoreceptors and their immediate downstream targets, the PHYTOCHROME INTERACTING FACTORs (PIFs; Bianchetti et al., 2018; Gramegna et al., 2019; Rosado et al., 2019). Phytochromes act as a red/far-red light switch: upon red light perception, the inactive, red light-absorbing Pr form is converted into the biologically active Pfr form, which can in turn be inactivated by the absorption of far-red light. Active phytochromes elicit downstream responses in part by inhibiting and promoting the degradation of PIF transcription factors, thereby controlling gene expression in a light-dependent manner (Legris et al., 2017).

In Arabidopsis (Arabidopsis thaliana), phytochrome B (phyB) has been found to act not only as a photoreceptor but also as a temperature sensor. In addition to far-red light-induced photoconversion, Pfr can be inactivated by a relaxation process termed thermal reversion, as it is directly dependent on temperature; high ambient temperature speeds up this process and reduces phytochrome activity (Jung et al., 2016; Legris et al., 2016). Thermal reversion, or dark reversion, as it was originally called, has been observed for phytochromes of multiple species (Klose et al., 2020), but their control of developmental and physiological processes in response to ambient temperature has almost exclusively been investigated in Arabidopsis. In this issue of Plant Physiology, Bianchetti et al. (2020) show that phytochromes exert temperature-related functions in tomato, where they mediate the reduction in pigment accumulation at elevated temperatures.

Given the function of phyB as a thermosensor in Arabidopsis, the authors decided to investigate a putative role for the tomato phytochromes phyB1 and phyB2 in temperature-regulated processes. While elevated temperature reduced stem diameter, leaf area, and branching, these responses were still present in a phyB1B2 double mutant, suggesting that the respective developmental processes are not controlled by phyB-mediated temperature sensing. Since phytochromes are known to affect pigment accumulation in tomato, the authors then decided to focus their investigation on metabolic traits. Elevated temperature indeed reduced leaf chlorophyll and carotenoid content, which is accompanied by impaired chloroplast biogenesis and differentiation as well as by alteration in the chloroplast’s ultrastructure. These changes are at least partially mediated by a reduction of phytochrome activity, since a phyB1B2 double mutant showed constitutive reduction in pigment accumulation and chloroplast formation even when grown at low temperature. This observation is further corroborated by transcriptomic analyses, which revealed that heat reduces the expression of carotenoid biosynthesis genes while it promotes the expression of chlorophyll catabolic genes, both in a phyB1/B2-dependent manner (Fig. 1).

Figure 1.

Effects of the temperature-controlled activity of phytochromes on pigment metabolism in tomato. Elevated temperature shifts the balance from the active Pfr form to the inactive Pr form of phytochromes. Reduced phytochrome activity causes decreased accumulation of chlorophyll and carotenoids in both leaves and ripe fruits, and this drop is accompanied by the increased expression of chlorophyll catabolism genes (PHEOPHYTINASE [PPH], CHLOROPHYLLASE4 [CLH4], STAY-GREEN LIKE, and PHEOPHORBIDE A OXYGENASE [PAO]) as well as the decreased expression of carotenoid biosynthesis genes (GERANYLGERANYL DIPHOSPHATE SYNTHASE1 [GGPS1], GGPS2, PHYTOENE SYNTHASE [PSY1], and PHYTOENE DESATURASE [PDS]) and master regulators of fruit ripening (APETALA2a [AP2a] and NON-RIPENING [NOR]). Reproduced from Bianchetti et al. (2020), figure 7.

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When Bianchetti et al. (2020) investigated ripe tomato fruits, they found that levels of the carotenoid lycopene and its precursors specifically decreased in response to elevated temperature. Previous results showed that phyA and phyB2 are core regulators of lycopene biosynthesis in tomato fruits (Bianchetti et al., 2018), and indeed, lycopene accumulation was constitutively reduced in a phyAB1B2 triple mutant as well as in PHYA and PHYB2 RNA interference lines that knock down the respective PHY genes selectively in fruits. Lycopene levels also correlated with the expression of lycopene biosynthesis genes in these genotypes as well as with the expression of several master transcription factors known to control fruit ripening (Fig. 1).

Taken together, the results obtained by Bianchetti et al. (2020) show that, in tomato, phytochromes are key factors in metabolic responses to elevated temperature, suggesting that the phytochromes’ temperature-sensing capacity is of physiological relevance in species other than Arabidopsis. A recent study showed that tomato PIF4 also controls temperature responses, similar to its Arabidopsis counterpart (Rosado et al., 2019). It thus appears that the light- and temperature-sensing phytochrome-PIF module is conserved in tomato, highlighting the crucial role that these proteins play in sensing and reacting to the plant’s environment. Nevertheless, further investigation will be required to decipher the precise mechanisms of this regulatory module in tomato and other agriculturally relevant species and to reveal commonalities and differences when compared with the canonical Arabidopsis phytochrome signaling pathway.

LITERATURE CITED

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