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-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.

Comparative transcriptome analysis reveals gene network regulation of TGase-induced thermotolerance in tomato

“…FBPase enzyme contributes a key role for the regeneration of ribulose-1,5-bisphosphate (RuBP) in the Calvin cycle. Our recent research showed that TGaseOE plants significantly elevated both FBPase activity and its encoding gene expression and the speed of electron transport for the production of RuBP is more in comparison to WT plants under optimal growth conditions (Zhong et al, 2019a). Similarly, our results showed that TGaseOE plants had higher expression level of FBPase both in control and heat stress (Table S8).…”

“…Ailsa Craig) seedlings were used as test material in this experiment. Two independent homozygous TGase overexpressed (TGaseOE) lines were obtained from our laboratory (Zhong et al, 2019a). Germinated seeds were sown in a 50-holes seedling tray filled with peat and vermiculite mixture (2:1, v:v) and transferred to it artificial growth chamber.…”

“…Indeed, overexpression of TGase from maize in Arabidopsis extends the stroma thylakoid network, increases linear electron flow and threshold of photoprotection (Ioannidis et al, 2016). The initial and activation status of RuBisCO, RuBisCO activity and FBPase activity (Fructose-1, 6-bisphosphatase) increases with an increase of TGase activity, resulted in elevating the net photosynthetic rate (Zhong et al, 2019a). Furthermore, TGase interacts with cytoskeleton regulates the apical growth of pollen tube and mediates the process of self-incompatibility (Del Duca et al, 2013;Mandrone et al, 2019).…”

Mercury-Induced Phytotoxicity and Responses in Upland Cotton (Gossypium hirsutum L.) Seedlings

“…Thus, reduction of biomass under Hg stress may be the consequence of reduction in photosynthesis pigments and following blocking of photosynthesis. Declined Pn may result from the inhibition of relevant reaction steps in the Benson-Calvin cycle and rubisco activity influenced by these contaminants [31]. Moreover, a decrease in Pn could be due to stomatal closing.…”

S-Glycosylation of Fluensulfone in Tomatoes: An Important Way of Fluensulfone Metabolism

“…9 After germination, seedlings were hydroponically grown in Hoagland's nutrient solution at a temperature of 25/20 °C (day/ night), a light intensity of 200 μmol m −2 s −1 , and a 12/12 h day/night rhythm. 12 Six tomato seedlings with approximative growth at two-leaf stage were transplanted in each 2 L plastic pot; the nutrient solution was renewed every 2 days. 12 When the seedlings were in the three-leaf one-heart stage, the acute toxicity test set the root exposure concentrations of 0, 2, 4, 6, and 8 mg/L FSF for 24 h. 2,8,13 The long-term experiment with continuous exposure for 7 d set a series of concentrations of 0, 0.5, 1, and 2 mg/L in the nutrient solutions.…”