Abstract
Besides an essential source of energy, light provides environmental information to plants. Photosensory pathways are thought to have occurred early in plant evolution, probably at the time of the Archaeplastida ancestor, or perhaps even earlier. Manipulation of individual components of light perception and signaling networks in tomato (Solanum lycopersicum) affects the metabolism of ripening fruit at several levels. Most strikingly, recent experiments have shown that some of the molecular mechanisms originally devoted to sense and respond to environmental light cues have been re-adapted during evolution to provide plants with useful information on fruit ripening progression. In particular, the presence of chlorophylls in green fruit can strongly influence the spectral composition of the light filtered through the fruit pericarp. The concomitant changes in light quality can be perceived and transduced by phytochromes (PHYs) and PHY-interacting factors, respectively, to regulate gene expression and in turn modulate the production of carotenoids, a family of metabolites that are relevant for the final pigmentation of ripe fruits. We raise the hypothesis that the evolutionary recycling of light-signaling components to finely adjust pigmentation to the actual ripening stage of the fruit may have represented a selective advantage for primeval fleshy-fruited plants even before the extinction of dinosaurs.
Highlights
Light has a dual role in plants as an essential source of energy for driving photosynthesis and, on the other hand, as an environmental cue that modulates many aspects of plant biology such as photomorphogenesis, germination, phototropism, and entrainment of circadian rhythms (Chen et al, 2004; Jiao et al, 2007)
The ability to perceive and respond to light changes is mediated by a set of sophisticated photosensory pathways capable of discriminating the quality, intensity, duration, and direction of light (Moglich et al, 2010)
Multiple lines of evidence have exposed the relevance of fruit-localized photosensory pathways as important players in the regulation of fruit ripening and the potential of their manipulation to improve the nutritional quality of tomatoes (Azari et al, 2010)
Summary
Light has a dual role in plants as an essential source of energy for driving photosynthesis and, on the other hand, as an environmental cue that modulates many aspects of plant biology such as photomorphogenesis, germination, phototropism, and entrainment of circadian rhythms (Chen et al, 2004; Jiao et al, 2007). Photosensory pathways are thought to have occurred early in plant evolution, probably at the time of the Archaeplastida ancestor (i.e., the last common ancestor of glaucophyte, red algae, green algae and land plants) or perhaps even earlier, before the occurrence of the endosymbiotic event that gave rise to photosynthetic eukaryotes over more than a billion years ago (Duanmu et al, 2014; Mathews, 2014; Fortunato et al, 2015) Through the ages, these mechanisms diverged to play particular roles in different branches of the plant lineage, ranging from presumably acclimative roles in algae (Duanmu et al, 2014; Rockwell et al, 2014) to resource competition functions in land plants (Jiao et al, 2007). A large number of other fruits (including bananas, oranges, or peppers) lose chlorophylls and accumulate carotenoids during ripening, resulting in a characteristic pigmentation change (from green to yellow, orange or red) that acts as a visual signal informing animals when the fruit is ripe and healthy (Klee and Giovannoni, 2011)
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