TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato

Abstract Transglutaminases (TGases), which are widespread cross-linking enzymes in plants, play key roles in photosynthesis and abiotic/biotic stress responses; however, evidence concerning the genetics underlying how TGase improves the capability of photosynthesis and the mechanism of TGase-mediate...

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Main Authors: Min Zhong, Yu Wang, Kun Hou, Sheng Shu, Jin Sun, Shirong Guo
Format: Article
Language:English
Published: Oxford University Press 2019-08-01
Series:Horticulture Research
Online Access:https://doi.org/10.1038/s41438-019-0173-z
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author Min Zhong
Yu Wang
Kun Hou
Sheng Shu
Jin Sun
Shirong Guo
author_facet Min Zhong
Yu Wang
Kun Hou
Sheng Shu
Jin Sun
Shirong Guo
author_sort Min Zhong
collection DOAJ
description Abstract Transglutaminases (TGases), which are widespread cross-linking enzymes in plants, play key roles in photosynthesis and abiotic/biotic stress responses; however, evidence concerning the genetics underlying how TGase improves the capability of photosynthesis and the mechanism of TGase-mediated photosynthesis are not clear in this crop species. In this study, we clarified the function of TGase in the regulation of photosynthesis in tomato by comparing wild-type (WT) plants, tgase mutants generated by the CRISPR/Cas9 system and TGase-overexpressing (TGaseOE) plants. Our results showed that increasing the transcript level of TGase resulted in an enhanced net photosynthetic rate (Pn), whereas the tgase mutants presented significantly inhibited Pns and CO2 assimilation compared with the WT. Although the total RuBisCO activity was not affected by TGase, the initial and activation status of RuBisCO and the activity of RuBisCO activase (RCA) and fructose-1,6-bisphosphatase (FBPase) in TGaseOE plants were significantly higher than that in WT plants. Except for RuBisCO small subunit (RbcS), the transcription levels of Benson–Calvin cycle-related genes were positively related to the endogenous TGase activity. Furthermore, TGaseOE plants had higher protein levels of RuBisCO large subunit (RbcL) and RCA than did WT plants and showed a reduced redox status by enhancing the activity of dehydroascorbate reductase (DHAR) and glutathione reductase (GR), which was compromised in TGase-deficient plants. Overall, TGase positively regulated photosynthesis by maintaining the activation states of the Benson–Calvin cycle and inducing changes in cellular redox homeostasis in tomato.
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spelling doaj.art-e4ae5ca873c14db489215ffa469224332022-12-22T02:42:08ZengOxford University PressHorticulture Research2052-72762019-08-016111110.1038/s41438-019-0173-zTGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomatoMin Zhong0Yu Wang1Kun Hou2Sheng Shu3Jin Sun4Shirong Guo5Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural UniversityKey Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural UniversityKey Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural UniversityKey Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural UniversityKey Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural UniversityKey Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural UniversityAbstract Transglutaminases (TGases), which are widespread cross-linking enzymes in plants, play key roles in photosynthesis and abiotic/biotic stress responses; however, evidence concerning the genetics underlying how TGase improves the capability of photosynthesis and the mechanism of TGase-mediated photosynthesis are not clear in this crop species. In this study, we clarified the function of TGase in the regulation of photosynthesis in tomato by comparing wild-type (WT) plants, tgase mutants generated by the CRISPR/Cas9 system and TGase-overexpressing (TGaseOE) plants. Our results showed that increasing the transcript level of TGase resulted in an enhanced net photosynthetic rate (Pn), whereas the tgase mutants presented significantly inhibited Pns and CO2 assimilation compared with the WT. Although the total RuBisCO activity was not affected by TGase, the initial and activation status of RuBisCO and the activity of RuBisCO activase (RCA) and fructose-1,6-bisphosphatase (FBPase) in TGaseOE plants were significantly higher than that in WT plants. Except for RuBisCO small subunit (RbcS), the transcription levels of Benson–Calvin cycle-related genes were positively related to the endogenous TGase activity. Furthermore, TGaseOE plants had higher protein levels of RuBisCO large subunit (RbcL) and RCA than did WT plants and showed a reduced redox status by enhancing the activity of dehydroascorbate reductase (DHAR) and glutathione reductase (GR), which was compromised in TGase-deficient plants. Overall, TGase positively regulated photosynthesis by maintaining the activation states of the Benson–Calvin cycle and inducing changes in cellular redox homeostasis in tomato.https://doi.org/10.1038/s41438-019-0173-z
spellingShingle Min Zhong
Yu Wang
Kun Hou
Sheng Shu
Jin Sun
Shirong Guo
TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato
Horticulture Research
title TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato
title_full TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato
title_fullStr TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato
title_full_unstemmed TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato
title_short TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato
title_sort tgase positively regulates photosynthesis via activation of calvin cycle enzymes in tomato
url https://doi.org/10.1038/s41438-019-0173-z
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