Transcriptional regulation of tocopherol biosynthesis in tomato

LEANDRO QUADRANA; JULIANA ALMEIDA; SANTIAGO OTAIZA; TOMAS DUFFY; JUNIA V. CORRÊA DA SILVA; FABIANA DE GODOY; RAMÓN ASIS; LUISA BERMÚDEZ; ALISDAIR R. FERNIE; FERNANDO CARRARI; MAGDALENA ROSSI

PLANT MOLECULAR BIOLOGY

SPRINGER

Lugar: Berlin; Año: 2013 vol. 81 p. 309 - 325

0167-4412

Tocopherols, compounds with vitamin E (VTE) activity, are potent lipid-soluble antioxidants synthesized only by photosynthetic organisms. Their biosynthesis requires the condensation of phytyl-diphosphate and homogentisate, derived from the methylerythritol phosphate and shikimate pathways, respectively. These metabolic pathways are central in plant chloroplast metabolism and are involved in the biosynthesis of important molecules such as chlorophyll, carotenoids, aromatic aminoacids and prenylquinones. In the last decade, few studies have provided insights into the regulation of VTE biosynthesis and its accumulation. However, the pathway regulatory mechanism/s at mRNA level remains unclear. We have recently identified a collection of tomato genes involved in tocopherol biosynthesis. In this work, by combining a dedicated qPCR array platform, tocopherol profiles and coregulation network and neural clustering analyses, we found that tocopherol biosynthesis is tightly controlled both temporally and spatially while total tocopherol content remains constant. These analyses exposed 18 key genes highly associated with VTE content in leaves and fruits. Moreover, genomic analyses of promoter regions suggested that the expression of the tocopherol-core pathway genes is trancriptionally coregulated with specific genes of the upstream pathways. Whilst the transcriptional profiles of the precursor pathway genes would suggest an increase in VTE content across fruit development, the geranylgeranyl-phosphate reductase (ggdr) appeared as a limiting step for the isoprenoid precursor availability. As a proof of concept, by analyzing a collection of Andean landrace tomato genotypes, the role of the pinpointed genes in determining fruit tocopherol content was confirmed. The results uncovered a finely tuned regulation able to shift the precursor pathways controlling substrate influx for VTE biosynthesis and overcoming endogenous competition for intermediates. The whole set of data allowed to propose that 1-deoxy-D-xylulose-5-phosphate synthase and ggdr encoding genes, which determine phytyl-diphosphate availability, together with enzyme encoding genes involved in chlorophyll-derived phytol metabolism appear as the most plausible targets to be engineered aiming to improve tomato fruit nutritional value.