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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| Format: | Article |
| Language: | English |
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Nature Portfolio
2017-08-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-017-08448-2 |
| _version_ | 1818344249370869760 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-13T16:43:28Z |
| format | Article |
| id | doaj.art-a8f10889df1743a2919ce649973b7ae6 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-13T16:43:28Z |
| publishDate | 2017-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-a8f10889df1743a2919ce649973b7ae62022-12-21T23:38:13ZengNature PortfolioScientific Reports2045-23222017-08-017111510.1038/s41598-017-08448-2Phytochromobilin deficiency impairs sugar metabolism through the regulation of cytokinin and auxin signaling in tomato fruitsRicardo Ernesto Bianchetti0Aline Bertinatto Cruz1Bruna Soares Oliveira2Diego Demarco3Eduardo Purgatto4Lázaro Eustáquio Pereira Peres5Magdalena Rossi6Luciano Freschi7Departamento de Botânica, Instituto de Biociências, Universidade de São PauloDepartamento de Botânica, Instituto de Biociências, Universidade de São PauloDepartamento de Botânica, Instituto de Biociências, Universidade de São PauloDepartamento de Botânica, Instituto de Biociências, Universidade de São PauloDepartamento de Alimentos e Nutrição Experimental, Faculdade de Ciências Farmacêuticas, Universidade de São PauloDepartamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São PauloDepartamento de Botânica, Instituto de Biociências, Universidade de São PauloDepartamento de Botânica, Instituto de Biociências, Universidade de São PauloAbstract 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.https://doi.org/10.1038/s41598-017-08448-2 |
| spellingShingle | 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 Scientific Reports |
| title | 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_short | 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 |
| url | https://doi.org/10.1038/s41598-017-08448-2 |
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