Abstract
Plastids are organelles responsible for essential aspects of plant development, including carbon fixation and synthesis of several secondary metabolites. Chloroplast differentiation and activity are highly regulated by light, and several proteins involved in these processes have been characterised. Such is the case of the GOLDEN 2-LIKE (GLK) transcription factors, which induces the expression of genes related to chloroplast differentiation and photosynthesis. The tomato (Solanum lycopersicum) genome harbours two copies of this gene, SlGLK1 and SlGLK2, each with distinct expression patterns. While the former predominates in leaves, the latter is mainly expressed in fruits, precisely at the pedicel region. During tomato domestication, the selection of fruits with uniform ripening fixed the mutation Slglk2, nowadays present in most cultivated varieties, what penalised fruit metabolic composition. In this study, we investigated how SlGLK2 is regulated by light, auxin and cytokinin and determined the effect of SlGLK2 on tocopherol (vitamin E) and sugar metabolism, which are components of the fruit nutritional and industrial quality. To achieve this, transcriptional profiling and biochemical analysis were performed throughout fruit development and ripening from SlGLK2, Slglk2, SlGLK2-overexpressing genotypes, as well as from phytochrome and hormonal deficient mutants. The results revealed that SlGLK2 expression is regulated by phytochrome-mediated light perception, yet this gene can induce chloroplast differentiation even in a phytochrome-independent manner. Moreover, auxin was found to be a negative regulator of SlGLK2 expression, while SlGLK2 enhances cytokinin responsiveness. Additionally, SlGLK2 enhanced chlorophyll content in immature green fruits, leading to an increment in tocopherol level in ripe fruits. Finally, SlGLK2 overexpression resulted in higher total soluble solid content, possibly by the regulation of sugar metabolism enzyme-encoding genes. The results obtained here shed light on the regulatory network that interconnects SlGLK2, phytohormones and light signal, promoting the plastidial activity and consequently, influencing the quality of tomato fruit.
Highlights
Plastids are organelles with a great diversity of shapes and functions that are found in all photosynthetic eukaryotes
A different profile was observed in au-SlGLK2 genotype fruits, in which the highest amount of SlGLK2 transcripts was verified at IG5 stage
The deficiency in the PHY-mediated light perception characteristic of the au-SlGLK2 led to increased levels of SlGLK2 transcript at immature green stages and decreased amounts from Br stage onwards compared to the wild-type genotype
Summary
Plastids are organelles with a great diversity of shapes and functions that are found in all photosynthetic eukaryotes. The proper development of fruit chloroplast impacts nutritional quality, by affecting the content of photoassimilates and of secondary metabolites Another plastid-synthesised family of compounds with important nutraceutical value for human health, yet less studied, are the tocopherols [14,15, 16, 17], for which the consequences of SlGLK2 loss of function in tomato fruit remains unexplored. Many aspects of GLK regulation and effects over the metabolism of important nutraceutical compounds remain elusive To fill this gap, the transcriptional profile of SlGLK2 and the tocopherol and sugar contents were addressed in tomato fruits from wild-type (i.e. SlGLK2), Slglk, PHY-deficient aurea (auSlGLK2) and au-Slglk overexpressing SlGLK2 genotypes. The results expanded the knowledge regarding the complex regulatory network that controls chloroplast biogenesis and showed that SlGLK2 positively impacts tomato fruit quality in a light- and auxin-dependent manner
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