Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature
In plants, the trehalose biosynthetic pathway plays key roles in the regulation of carbon allocation and stress adaptation. Engineering of the pathway holds great promise to increase the stress resilience of crop plants. The synthesis of trehalose proceeds by a two-step pathway in which a trehalose-...
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| Format: | Article |
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MDPI AG
2022-09-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/19/11436 |
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| author | Mohanna Mollavali Frederik Börnke |
| author_facet | Mohanna Mollavali Frederik Börnke |
| author_sort | Mohanna Mollavali |
| collection | DOAJ |
| description | In plants, the trehalose biosynthetic pathway plays key roles in the regulation of carbon allocation and stress adaptation. Engineering of the pathway holds great promise to increase the stress resilience of crop plants. The synthesis of trehalose proceeds by a two-step pathway in which a trehalose-phosphate synthase (TPS) uses UDP-glucose and glucose-6-phosphate to produce trehalose-6 phosphate (T6P) that is subsequently dephosphorylated by trehalose-6 phosphate phosphatase (TPP). While plants usually do not accumulate high amounts of trehalose, their genome encodes large families of putative trehalose biosynthesis genes, with many members lacking obvious enzymatic activity. Thus, the function of putative trehalose biosynthetic proteins in plants is only vaguely understood. To gain a deeper insight into the role of trehalose biosynthetic proteins in crops, we assessed the enzymatic activity of the TPS/TPP family from tomato (<i>Solanum lycopersicum</i> L.) and investigated their expression pattern in different tissues as well as in response to temperature shifts. From the 10 TPS isoforms tested, only the 2 proteins belonging to class I showed enzymatic activity, while all 5 TPP isoforms investigated were catalytically active. Most of the <i>TPS/TPP</i> family members showed the highest expression in mature leaves, and promoter–reporter gene studies suggest that the two class I <i>TPS</i> genes have largely overlapping expression patterns within the vasculature, with only subtle differences in expression in fruits and flowers. The majority of tomato <i>TPS/TPP</i> genes were induced by heat stress, and individual family members also responded to cold. This suggests that trehalose biosynthetic pathway genes could play an important role during temperature stress adaptation. In summary, our study represents a further step toward the exploitation of the <i>TPS</i> and <i>TPP</i> gene families for the improvement of tomato stress resistance. |
| first_indexed | 2024-03-09T21:40:05Z |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T21:40:05Z |
| publishDate | 2022-09-01 |
| publisher | MDPI AG |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-5c51796a222e47459433f4a4dad24f4e2023-11-23T20:33:11ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123191143610.3390/ijms231911436Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to TemperatureMohanna Mollavali0Frederik Börnke1Plant Metabolism Group, Leibniz-Institute of Vegetable and Ornamental Crops (IGZ), Theodor-Echtermeyer Weg 1, 14979 Großbeeren, GermanyPlant Metabolism Group, Leibniz-Institute of Vegetable and Ornamental Crops (IGZ), Theodor-Echtermeyer Weg 1, 14979 Großbeeren, GermanyIn plants, the trehalose biosynthetic pathway plays key roles in the regulation of carbon allocation and stress adaptation. Engineering of the pathway holds great promise to increase the stress resilience of crop plants. The synthesis of trehalose proceeds by a two-step pathway in which a trehalose-phosphate synthase (TPS) uses UDP-glucose and glucose-6-phosphate to produce trehalose-6 phosphate (T6P) that is subsequently dephosphorylated by trehalose-6 phosphate phosphatase (TPP). While plants usually do not accumulate high amounts of trehalose, their genome encodes large families of putative trehalose biosynthesis genes, with many members lacking obvious enzymatic activity. Thus, the function of putative trehalose biosynthetic proteins in plants is only vaguely understood. To gain a deeper insight into the role of trehalose biosynthetic proteins in crops, we assessed the enzymatic activity of the TPS/TPP family from tomato (<i>Solanum lycopersicum</i> L.) and investigated their expression pattern in different tissues as well as in response to temperature shifts. From the 10 TPS isoforms tested, only the 2 proteins belonging to class I showed enzymatic activity, while all 5 TPP isoforms investigated were catalytically active. Most of the <i>TPS/TPP</i> family members showed the highest expression in mature leaves, and promoter–reporter gene studies suggest that the two class I <i>TPS</i> genes have largely overlapping expression patterns within the vasculature, with only subtle differences in expression in fruits and flowers. The majority of tomato <i>TPS/TPP</i> genes were induced by heat stress, and individual family members also responded to cold. This suggests that trehalose biosynthetic pathway genes could play an important role during temperature stress adaptation. In summary, our study represents a further step toward the exploitation of the <i>TPS</i> and <i>TPP</i> gene families for the improvement of tomato stress resistance.https://www.mdpi.com/1422-0067/23/19/11436trehalose metabolismheat stress<i>Solanum lycopersicum</i>yeast complementation |
| spellingShingle | Mohanna Mollavali Frederik Börnke Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature International Journal of Molecular Sciences trehalose metabolism heat stress <i>Solanum lycopersicum</i> yeast complementation |
| title | Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature |
| title_full | Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature |
| title_fullStr | Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature |
| title_full_unstemmed | Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature |
| title_short | Characterization of Trehalose-6-Phosphate Synthase and Trehalose-6-Phosphate Phosphatase Genes of Tomato (<i>Solanum lycopersicum</i> L.) and Analysis of Their Differential Expression in Response to Temperature |
| title_sort | characterization of trehalose 6 phosphate synthase and trehalose 6 phosphate phosphatase genes of tomato i solanum lycopersicum i l and analysis of their differential expression in response to temperature |
| topic | trehalose metabolism heat stress <i>Solanum lycopersicum</i> yeast complementation |
| url | https://www.mdpi.com/1422-0067/23/19/11436 |
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