Photosynthetic Capacity, Antioxidant Activity and Molecular Responses in Parthenocissus Quinquefolia (L.) Planch Under High Temperature Stress and Subsequent Recovery

Abstract

Photosynthetic capacity and photosystem II (PSII) activity decreased with increasing temperature, whereas antioxidant enzyme activity showed the opposite trend. High temperature stress induced a significant increase in Φf,D, and D1 protein turnover rate. Photosynthetic capacity, PSII activity, and antioxidant enzyme levels in plants treated at 35 and 40°C were restored to control levels upon stress relief, whereas those in plants grown at 45°C were only partially restored. Therefore, the temperature limit for heat tolerance in Parthenocissus quinquefolia is between 40 and 45°C. Further, it was observed that antioxidant enzymes were crucial for high-temperature stress resistance in P. quinquefolia, with DEGP1 protein playing a major role in the rapid turnover of D1 protein for PSII repair. Parthenocissus quinquefolia (Vitaceae) is considered as an important climbing woody species for three-dimensional greening due to its advantage of high coverage and rapid growth (Emerine et al. 2013). However, global warming poses an increasingly serious threat to this kind of plant species growing on walls (Islam 2015). Photosystem II (PSII) activity is commonly used as an indicator of plant health status in warm environments (Chen et al. 2017). Non-regulated thermal energy loss (\uf046f,D) reflects photodamage happened to PSII (Osório et al. 2013). Antioxidant enzyme, such as catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD), can eliminate superoxide free radicals (O) and hydrogen peroxide (H2O2). Previous studies have confirmed that the decrease of PSII activity at high temperature is caused by the inhibition of PSII repair which is closely related to D1 protein turnover (Li et al. 2017). However, most of this research focused on economically important crops, whereas a few studies have been conducted on lianas. In this study, responses of photosynthetic capacity, the antioxidant system, and related proteins in P. quinquefolia to elucidate the effects of heat on this species were investigated. Experiments were conducted at North China University of Science and Technology, China (39°37′ N; 118°37′ E). The uniform two-year-old P. quinquefolia plants with 10 15 fully expanded leaves were divided into four groups (five replicates per group), and each group was subjected to either 25 (control) 35, 40 or 45°C for 1 d (from 09:00 to 16:00 hrs). After the stress period, each group was returned to control treatment conditions for 2 d. All parameters were collected at the end of the stress period, and after the 2 d recovery period. Net photosynthetic rate (Pn), the maximum quantum yield of PSII photochemistry (Fv/Fm), actual quantum yield of PSII *Author for correspondence: <[email protected]>. Hebei Key Laboratory of Mining Development and Security Technology, Tangshan 063000, China. DOI: https://doi.org/10.3329/bjb.v50i2.54103 434 XUE-TAO AND FU-PING PHOTOSYNTHETIC CAPACITY, ANTIOXIDANT ACTIVITY 435 photochemistry (\uf046PSII), and non-regulated thermal energy loss (\uf046f,D) were measured and calculated according to Lazár (2015). Malondialdehyde (MDA) content, and POD, SOD, and CAT activities were measured as described by Chen et al. (2017). The identification of proteins was based on multiple reaction monitoring (MRM) (Wang et al. 2016). All data were expressed as means ± standard errors of five replicates. One-way ANOVA was performed using the SPSS version 19.0 software (IBM, Chicago, IL, USA) and Duncan’s multiple comparison (p < 0.05) test was used to determine significant differences among means. Table 2. Effect of high temperature on relative protein abundance of D1, D2 and DegPs and FtsHs protease families in leaves of Parthenocissus quinquefolia. Protein accession Fold-change Plant species Protein description HS RC O22609 1.4592 1.1701 A. thaliana Protease Do-like 1, chloroplastic GN=DEGP1 PE=1 SV=2 Q0ZJ40 1.0339 1.067 V. vinifera Photosystem II protein D1 GN=psbA PE=3 SV=1 Q39102 1.1805 0.8091 A. thaliana ATP-dependent zinc metalloprotease FTSH 1, chloroplastic GN=FTSH1 PE=1 SV=2 Q39444 1.1805 0.8091 C. annuum ATP-dependent zinc metalloprotease FTSH, chloroplastic (Fragment) GN=FTSH PE=2 SV=1 Q655S1 1.0952 0.6005 O. sativa. japonica ATP-dependent zinc metalloprotease FTSH 2, chloroplastic GN=FTSH2 PE=3 SV=1 Q8W585 1.0925 0.569 A. thaliana ATP-dependent zinc metalloprotease FTSH 8, chloroplastic GN=FTSH8 PE=1 SV=1 Q9FH02 1.1805 0.8091 A. thaliana ATP-dependent zinc metalloprotease FTSH 5, chloroplastic GN=FTSH5 PE=1 SV=1 HS and RC represent high temperature stress and recovery, respectively. With increasing temperature, leaf Pn and the ΦPSII decreased (Table 1). This indicated that the photosynthetic capacity and photosynthetic efficiency of PSII reaction centers were negatively affected by high temperature stress (Feng et al. 2014, Haque et al. 2014). The decrease in Fv/Fm was slight at 35 and 40°C but significant at 45°C (4.18%). This indicated that significant inhibition occurred at PSII reaction centers at 45°C. Moreover, the Φf,D showed an increasing trend with increasing temperature. This indicated that photodamage are still inevitable when ambient temperature exceeds the suitable temperature range for plant growth (Osório et al. 2013). During recovery, chlorophyll fluorescence parameters were restored to pre-stress levels at temperatures lower than 45°C, which indicated that the PSII activity of P. quinquefolia tolerated 40°C. High temperature induced membrane-lipid peroxidation damage in P. quinquefolia and increased antioxidant enzyme activity, which helped plants to overcome oxidative stress. Interestingly, SOD content showed an initial increase followed by a decrease with increasing temperature (Table 1), thus suggesting that the synthesis of H2O2 was inhibited and that the 45°C temperature treatment exceeded the capacity of the antioxidant system of P. quinquefolia (Sgobba et al. 2015). During the stress period, a significant increase was observed in DegP1, FtsH, FtsH1, and FtsH5 levels (Table 2). This indicated that the turnover rate of D1 protein was enhanced and that DegP1 played a major role in D1 turnover for the repair of PSII (Li et al. 2017). FtsH, FtsH1, 436 XUE-TAO AND FU-PING FtsH2, FtsH5 and FtsH8 levels decreased significantly upon stress relief compared to those under stress, indicating that the turnover rate of D1 protein decreased. It is inferred that D1 protein turnover did not play a major role at this stage. 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