Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato

Bianchetti, Ricardo Ernesto; Lira, Bruno Silvestre; Monteiro, Scarlet Santos; Demarco, Diego; Purgatto, Eduardo; Rothan, Christophe; Rossi, Magdalena; Freschi, Luciano

doi:10.1093/jxb/ery145

Cited by 63 publications

(79 citation statements)

References 78 publications

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Section: Discussionmentioning

confidence: 99%

“…On the contrary, silencing of the negative regulators of light signalling SlDDB1 and SlCUL4 led to a significant increment in the number of plastids that resulted in enhanced carotenoid and flavonoid accumulation during ripening (Wang et al, 2008). In particular, a positive role of PHYdependent light response cascade in fruit carotenogenesis has been demonstrated (Alba, Cordonnier-Pratt, & Pratt, 2000;Bianchetti et al, 2018;Llorente et al, 2016). Tocopherol biosynthesis is highly dependent on Chl degradationderived phytol (Almeida et al, 2016), and consequently, the rising of tocopherol content from MG to the ripe stage of fruit development correlates with the amount of Chl right before the onset of ripening.…”

Section: Discussionmentioning

confidence: 99%

“…Considering that light has a central role in regulating chloroplast activity and differentiation during tomato fruit ripening (Cocaliadis, Fernández‐Muñoz, Pons, Orzaez, & Granell, ) and that tocopherols are photosynthesis‐related compounds synthesized in the plastids, it is expected that light also affects the accumulation of fruit tocopherols, as already demonstrated for carotenoids (Llorente et al, ). The red/far‐red light perception via PHYTOCHROMES (PHYs) plays a central role in controlling fruit development and ripening (Bianchetti et al, , ; Gupta et al, ). Functional PHYs are homodimers with each polypeptide (apoprotein) associated with the linear tetrapyrrole chromophore phytochromobilin (PϕB).…”

Section: Introductionmentioning

confidence: 99%

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PHYTOCHROME‐INTERACTING FACTOR 3 mediates light‐dependent induction of tocopherol biosynthesis during tomato fruit ripening

Gramegna

Rosado

Carranza

et al. 2018

Plant Cell & Environment

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Tocopherols are important antioxidants exclusively produced in plastids that protect the photosynthetic apparatus from oxidative stress. These compounds with vitamin E activity are also essential dietary nutrients for humans. Although the tocopherol biosynthetic pathway has been elucidated, the mechanisms that regulate tocopherol production and accumulation remain elusive. Here, we investigated the regulatory mechanism underlying tocopherol biosynthesis during ripening in tomato fruits, which are an important source of vitamin E. Our results show that ripening under light conditions increases tocopherol fruit content in a phytochrome‐dependent manner by the transcriptional regulation of biosynthetic genes. Moreover, we show that light‐controlled expression of the GERANYLGERANYL DIPHOSPHATE REDUCTASE (SlGGDR) gene, responsible for the synthesis of the central tocopherol precursor phytyl diphosphate, is mediated by PHYTOCHROME‐INTERACTING FACTOR 3 (SlPIF3). In the absence of light, SlPIF3 physically interacts with the promoter of SlGGDR, down‐regulating its expression. By contrast, light activation of phytochromes prevents the interaction between SlPIF3 and the SlGGDR promoter, leading to transcriptional derepression and higher availability of the PDP precursor for tocopherol biosynthesis. The unraveled mechanism provides a new strategy to manipulate fruit metabolism towards improving tomato nutritional quality.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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PHYTOCHROME‐INTERACTING FACTOR 3 mediates light‐dependent induction of tocopherol biosynthesis during tomato fruit ripening

Gramegna

Rosado

Carranza

et al. 2018

Plant Cell & Environment

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“…In tomato, five PHY-encoding genes, namely PHYA, PHYB1, PHYB2, PHYE and PHYF, have been identified (Alba et al, 2000a). PHYB2 is the most expressed in tomato fruits (Bianchetti et al, 2017;Hauser et al, 1997;Pratt et al, 1995) and a major regulator of fruit chloroplast maturation and carotenoid accumulation (Bianchetti et al, 2018;Gupta et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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

Alves

Lira

Pikart

et al. 2020

Plant Biotechnology Journal

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Summary 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.

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“…The Solanum lycopersicum genome harbours ve PHYencoding genes: PHYA, PHYB1, PHYB2, PHYE and PHYF 22 . Previous studies have shown that PHYA, PHYB1 and PHYB2 are major regulators of fruit chloroplast maturation and nutraceutical compound accumulation [23][24][25][26] . In this work, the genome-wide transcriptome and methylome were comprehensively analysed in fruits from phyA and phyB1B2 null mutants, revealing that PHY-dependent DNA demethylation is a crucial stimulus for triggering ripening-associated gene expression.…”

Section: Introductionmentioning

confidence: 99%

Phytochromes B1/B2 Are Major Regulators of Ripening-associated Epigenome Reprogramming in Tomato Fruits

Bianchetti

Bellora

Haro

et al. 2020

Preprint

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Phytochrome-mediated light and temperature perception has been shown to be a major regulator of fruit development. Furthermore, chromatin remodelling via DNA demethylation has been described as a crucial mechanism behind the fruit ripening process; however, the molecular basis underlying the triggering of this epigenetic modification remains largely unknown. Here, through integrative analyses of the methylome, siRNAome and transcriptome of tomato fruits from phyA and phyB1B2 null mutants, we report that PHYB1 and PHYB2 control genome-wide DNA methylation during fruit development. The experimental evidence indicates that PHYB1B2 signal transduction is mediated by the coordinated expression of DNA methylases/demethylases, histone-modifying enzymes and chromatin remodelling factors, resulting in the transcriptional regulation of photosynthetic and ripening-associated genes. This new level of understanding provides insights into the orchestration of epigenetic mechanisms in response to environmental cues affecting agronomical traits.

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Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato

Abstract: Fruit-localized phytochromes and their downstream signaling cascades not only modulate chloroplast biogenesis in immature tomato fruits but also regulate sugar and carotenoid accumulation, two essential features of tomato fruit quality.

Cited by 63 publications

References 78 publications

PHYTOCHROME‐INTERACTING FACTOR 3 mediates light‐dependent induction of tocopherol biosynthesis during tomato fruit ripening

PHYTOCHROME‐INTERACTING FACTOR 3 mediates light‐dependent induction of tocopherol biosynthesis during tomato fruit ripening

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

Phytochromes B1/B2 Are Major Regulators of Ripening-associated Epigenome Reprogramming in Tomato Fruits

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