Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits

Abstract Phytochomes and plant hormones have been emerging as important regulators of fleshy fruit biology and quality traits; however, the relevance of phytochrome-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. Here, we show that the deficiency in phyt...

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Autores principales: Ricardo Ernesto Bianchetti, Aline Bertinatto Cruz, Bruna Soares Oliveira, Diego Demarco, Eduardo Purgatto, Lázaro Eustáquio Pereira Peres, Magdalena Rossi, Luciano Freschi
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Publicado: Nature Portfolio 2017
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spelling oai:doaj.org-article:a8f10889df1743a2919ce649973b7ae62021-12-02T15:05:24ZPhytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits10.1038/s41598-017-08448-22045-2322https://doaj.org/article/a8f10889df1743a2919ce649973b7ae62017-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-08448-2https://doaj.org/toc/2045-2322Abstract Phytochomes and plant hormones have been emerging as important regulators of fleshy fruit biology and quality traits; however, the relevance of phytochrome-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. Here, we show that the deficiency in phytochrome chromophore phytochromobilin (PΦB) biosynthesis inhibits sugar accumulation in tomato (Solanum lycopersicum) fruits by transcriptionally downregulating sink- and starch biosynthesis-related enzymes, such as cell-wall invertases, sucrose transporters and ADP-glucose pyrophosphorylases. PΦB deficiency was also shown to repress fruit chloroplast biogenesis, which implicates more limited production of photoassimilates via fruit photosynthesis. Genetic and physiological data revealed the involvement of auxins and cytokinins in mediating the negative impact of PΦB deficiency on fruit sink strength and chloroplast formation. PΦB deficiency was shown to transcriptionally repress type-A TOMATO RESPONSE REGULATORs and AUXIN RESPONSE FACTORs both in pericarp and columella, suggesting active phytochrome-hormonal signaling crosstalk in these tissues. Data also revealed that PΦB deficiency influences fruit ripening by delaying the climacteric rise in ethylene production and signaling. Altogether, the data uncover the impact of phytochromobilin deficiency in fine-tuning sugar metabolism, chloroplast formation and the timing of fruit ripening and also reveal a link between auxins, cytokinins and phytochromes in regulating sugar import and accumulation in fruits.Ricardo Ernesto BianchettiAline Bertinatto CruzBruna Soares OliveiraDiego DemarcoEduardo PurgattoLázaro Eustáquio Pereira PeresMagdalena RossiLuciano FreschiNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-15 (2017)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Ricardo Ernesto Bianchetti
Aline Bertinatto Cruz
Bruna Soares Oliveira
Diego Demarco
Eduardo Purgatto
Lázaro Eustáquio Pereira Peres
Magdalena Rossi
Luciano Freschi
Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
description Abstract Phytochomes and plant hormones have been emerging as important regulators of fleshy fruit biology and quality traits; however, the relevance of phytochrome-hormonal signaling crosstalk in controlling fruit development and metabolism remains elusive. Here, we show that the deficiency in phytochrome chromophore phytochromobilin (PΦB) biosynthesis inhibits sugar accumulation in tomato (Solanum lycopersicum) fruits by transcriptionally downregulating sink- and starch biosynthesis-related enzymes, such as cell-wall invertases, sucrose transporters and ADP-glucose pyrophosphorylases. PΦB deficiency was also shown to repress fruit chloroplast biogenesis, which implicates more limited production of photoassimilates via fruit photosynthesis. Genetic and physiological data revealed the involvement of auxins and cytokinins in mediating the negative impact of PΦB deficiency on fruit sink strength and chloroplast formation. PΦB deficiency was shown to transcriptionally repress type-A TOMATO RESPONSE REGULATORs and AUXIN RESPONSE FACTORs both in pericarp and columella, suggesting active phytochrome-hormonal signaling crosstalk in these tissues. Data also revealed that PΦB deficiency influences fruit ripening by delaying the climacteric rise in ethylene production and signaling. Altogether, the data uncover the impact of phytochromobilin deficiency in fine-tuning sugar metabolism, chloroplast formation and the timing of fruit ripening and also reveal a link between auxins, cytokinins and phytochromes in regulating sugar import and accumulation in fruits.
format article
author Ricardo Ernesto Bianchetti
Aline Bertinatto Cruz
Bruna Soares Oliveira
Diego Demarco
Eduardo Purgatto
Lázaro Eustáquio Pereira Peres
Magdalena Rossi
Luciano Freschi
author_facet Ricardo Ernesto Bianchetti
Aline Bertinatto Cruz
Bruna Soares Oliveira
Diego Demarco
Eduardo Purgatto
Lázaro Eustáquio Pereira Peres
Magdalena Rossi
Luciano Freschi
author_sort Ricardo Ernesto Bianchetti
title Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
title_short Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
title_full Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
title_fullStr Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
title_full_unstemmed Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
title_sort phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruits
publisher Nature Portfolio
publishDate 2017
url https://doaj.org/article/a8f10889df1743a2919ce649973b7ae6
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