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Beyond the limits of photoperception: constitutively active PHYTOCHROME B2 overexpression as a means of improving fruit nutritional quality in tomato.

ABSTRACT: Photoreceptor engineering has recently emerged as a means for improving agronomically beneficial traits in crop species. Despite the central role played by the red/far-red photoreceptor phytochromes (PHYs) in controlling fruit physiology, the applicability of PHY engineering for increasing fleshy fruit nutritional content remains poorly exploited. In this study, we demonstrated that the fruit-specific overexpression of a constitutively active GAF domain Tyr252 -to-His PHYB2 mutant version (PHYB2Y252H ) significantly enhances the accumulation of multiple health-promoting antioxidants in tomato fruits, without negative collateral consequences on vegetative development. Compared with the native PHYB2 overexpression, PHYB2Y252H -overexpressing lines exhibited more extensive increments in transcript abundance of genes associated with fruit plastid development, chlorophyll biosynthesis and metabolic pathways responsible for the accumulation of antioxidant compounds. Accordingly, PHYB2Y252H -overexpressing fruits developed more chloroplasts containing voluminous grana at the green stage and overaccumulated carotenoids, tocopherols, flavonoids and ascorbate in ripe fruits compared with both wild-type and PHYB2-overexpressing lines. The impacts of PHYB2 or PHYB2Y252H overexpression on fruit primary metabolism were limited to a slight promotion in lipid biosynthesis and reduction in sugar accumulation. Altogether, these findings indicate that mutation-based adjustments in PHY properties represent a valuable photobiotechnological tool for tomato biofortification, highlighting the potential of photoreceptor engineering for improving quality traits in fleshy fruits.

SUBMITTER: Alves FRR

PROVIDER: S-EPMC7540714 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Beyond the limits of photoperception: constitutively active PHYTOCHROME B2 overexpression as a means of improving fruit nutritional quality in tomato.

Alves Frederico Rocha Rodrigues FRR Lira Bruno Silvestre BS Pikart Filipe Christian FC Monteiro Scarlet Santos SS Furlan Cláudia Maria CM Purgatto Eduardo E Pascoal Grazieli Benedetti GB Andrade Sónia Cristina da Silva SCDS Demarco Diego D Rossi Magdalena M Freschi Luciano L

Plant biotechnology journal 20200401 10

Photoreceptor engineering has recently emerged as a means for improving agronomically beneficial traits in crop species. Despite the central role played by the red/far-red photoreceptor phytochromes (PHYs) in controlling fruit physiology, the applicability of PHY engineering for increasing fleshy fruit nutritional content remains poorly exploited. In this study, we demonstrated that the fruit-specific overexpression of a constitutively active GAF domain Tyr<sup>252</sup> -to-His PHYB2 mutant ver ...[more]

PMID: 32068963

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Project description:BackgroundFruit maturation and ripening are genetically regulated processes that involve a complex interplay of plant hormones, growth regulators and multiple biological and environmental factors. Tomato (Solanum lycopersicum) has been used as a model of biological and genetic studies on the regulation of specific ripening pathways, including ethylene, carotenoid and cell wall metabolism. This model has also been used to investigate the functions of upstream signalling and transcriptional regulators. Thus far, many ripening-associated transcription factors that influence fruit development and ripening have been reported. NAC transcription factors are plant specific and play important roles in many stages of plant growth and development, such as lateral root formation, secondary cell wall synthesis, and embryo, floral organ, vegetative organ and fruit development.ResultsTissue-specific analysis by quantitative real-time PCR showed that SlNAC1 was highly accumulated in immature green fruits; the expression of SlNAC1 increased with fruit ripening till to the highest level at 7 d after the breaker stage. The overexpression of SlNAC1 resulted in reduced carotenoids by altering carotenoid pathway flux and decreasing ethylene synthesis mediated mainly by the reduced expression of ethylene biosynthetic genes of system-2, thus led to yellow or orange mature fruits. The results of yeast one-hybrid experiment demonstrated that SlNAC1 can interact with the regulatory regions of genes related lycopene and ethylene synthesis. These results also indicated that SlNAC1 inhibited fruit ripening by affecting ethylene synthesis and carotenoid accumulation in SlNAC1 overexpression lines. In addition, the overexpression of SlNAC1 reduced the firmness of the fruits and the thickness of the pericarp and produced more abscisic acid, resulting in the early softening of fruits. Hence, in SlNAC1 overexpression lines, both ethylene-dependent and abscisic acid-dependent pathways are regulated by SlNAC1 in fruit ripening regulatory network.ConclusionsSlNAC1 had a broad influence on tomato fruit ripening and regulated SlNAC1 overexpression tomato fruit ripening through both ethylene-dependent and abscisic acid-dependent pathways. Thus, this study provided new insights into the current model of tomato fruit ripening regulatory network.

Project description:Salt stress generally induces important negative effects on tomato (Solanum lycopersicum) productivity but it may also cause a positive effect improving fruit quality, one of the greatest challenges in nowadays agriculture. Because of the genetic erosion of this horticultural species, the recovery of locally adapted landraces could play a very important role in avoiding, at least partially, production losses and simultaneously improving fruit quality. Two tomato landraces endemic of the Spanish Southeast area, characterized by the harsh climatic conditions of the Mediterranean basin, have been selected: Negro Yeste (NY) characterized by its dark-red colored fruits and Verdal (V), which fruits did not achieve the characteristic red color at ripening. Here the agronomic, physiological, and metabolic responses of these landraces were compared with the reference tomato commercial cv. Moneymaker (MM), in plants grown without salt (control) and with salt stress (100 mM NaCl) for 70 days. The higher salt tolerance of both landraces was mainly reflected in the fruit number, as NY only reduced the fruit number in salt stress by 20% whereas in MM it was reduced till 43%, and in V the fruit number even showed an increase of 33% with salt stress. An important fruit quality parameter is soluble solids content, which increases induced by salinity were significantly higher in both landraces (60 and 78% in NY and V, respectively) compared with MM (34%). Although both landraces showed a similar response in relation to the high chlorophyll accumulation detected in their fruits, the fruit metabolic profiles were very different. Increased carotenoids levels were found in NY fruits, especially lycopene in ripe fruit, and this characteristic was observed in both control and salt stress. Contrarily, the carotenoid biosynthesis pathway was disrupted in V ripe fruits, but other metabolites, such as Ca2+, mannose, formate, and glutamate were accumulated. These results highlight the potential of tomato landraces to improve nutritional fruit quality and maintain fruit yield stability under salt stress.

Project description:As a conserved kinase complex, sucrose non-fermenting-1-related protein kinase 1 (SnRK1) is a major regulator of plant growth and development. In our previous study, overexpression of MhSnRK1 in tomato (Solanum lycopersicum L.) modified fruit maturation: the transgenic fruit ripened earlier than the wild type (WT). However, the mechanism by which fruit maturation is regulated by SnRK1 is not clear; therefore, the test materials used were the transgenic tomato lines (OE-1, OE-3, and OE-4) overexpressing the coding gene of peach [Prunus persica (L.) Batsch] SNF1-related kinase ? subunit (PpSnRK1?). The activity of SnRK1 kinase in transgenic tomato lines OE-1, OE-3, and OE-4 was higher than that in the WT at different periods of fruit development; in the pink coloring period the SnRK1 kinase activity increased the most, with 23.5, 28.8, and 21.4% increases, respectively. The content of starch and soluble sugars in red ripe transgenic fruit significantly increased, while the soluble protein and titratable acid content decreased significantly. We also found that the tomatoes overexpressing PpSnRK1? matured approximately 10 days earlier than the WT. Moreover, the yeast-two-hybrid assay showed that PpSnRK1? interacted with the MADS-box transcription factor (TF) SIRIN, which acts as an essential regulator of tomato fruit ripening. The BiFC technology further validated the location of the PpSnRK1? interaction sites within the nucleus. The quantitative real-time PCR analysis showed that RIN expression was up-regulated by PpSnRK1? overexpression; the expression of RIN-targeted TF genes NOR and FUL1 increased during different stages of fruit development. The expression of key genes, ACS2, ACS4, and E8, in ethylene synthesis also changed accordingly, and the ethylene emitted by the red ripe fruit increased by 36.1-43.9% compared with the WT. These results suggest that PpSnRK1? interacts with SIRIN, increasing the expression of RIN, thereby regulating the expression of downstream ripening-related genes, finally promoting fruit ripening.

Dataset Information

Beyond the limits of photoperception: constitutively active PHYTOCHROME B2 overexpression as a means of improving fruit nutritional quality in tomato.

Publications

Beyond the limits of photoperception: constitutively active PHYTOCHROME B2 overexpression as a means of improving fruit nutritional quality in tomato.

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