TY - JOUR
AU - Peng, Changlian
AB - Abstract More intense, more frequent, and longer heat waves are expected in the future due to global warming, which could have dramatic ecological impacts. However, few studies have involved invasive species. The aims of this study were to examine the effect of extreme heating (40/35 °C for 30 d) on the growth and photosynthesis of an alien invasive species Wedelia trilobata and its indigenous congener (Wedelia chinensis) in South China, and to determine the development of this invasive species and its potential adaptive mechanism. In comparison with W. chinensis, W. trilobata suffered less inhibition of the relative growth rate (RGR) and biomass production due to high temperature, which was consistent with the changes of photosystem II (PSII) activity and net photosynthetic rate (Pn). High temperature caused a partial inhibition of PSII, but the adverse effect was more severe in W. chinensis. Measurement of the minimum fluorescence (Fo) versus temperature curves showed that W. trilobata had a higher inflexion temperature of Fo (Ti), indicating greater thermostability of the photosynthetic apparatus. Moreover, comparisons of absorbed light energy partitioning revealed that W. trilobata increased xanthophyll-dependent thermal dissipation (ΦNPQ) under high temperature, while retaining the higher fraction of absorbed light allocated to photochemistry (ΦPSII) relative to W. chinensis. The results suggest that the invasive W. trilobata has a high thermostability of its photosynthetic apparatus and an effective regulating mechanism in energy partitioning of PSII complexes to minimize potential damage and to retain greater capability for carbon assimilation. These factors confer greater heat stress tolerance compared with the native species. Therefore, the invasive W. trilobata may become more aggressive with the increasingly extreme heat climates. Chlorophyll fluorescence, high temperature, invasive species, photosynthesis, thermotolerance Introduction Invasion by exotic species is a major component of global environmental change (Vitousek et al., 1996; Dukes and Mooney, 1999; Vilà et al., 2006; Thuiller et al., 2007), and a likely cause of tremendous damage to worldwide economies and ecosystems (Pimentel et al., 2005). In addition, exotic species are capable of interacting with other elements of global change to alter biodiversity and ecosystem processes in invaded habitats (Dukes and Mooney, 1999; Ziska, 2003; Vilà et al., 2006). Global warming is one of the most important characteristics of global environmental change. In the last century, global mean temperatures have already risen by 0.74 °C, currently continuing to increase at ∼0.1 °C per decade (IPCC, 2007). Some exotic species, such as Spartina anglica and Cylindrospermopsis raciborskii (Woloszynska), and several tropical and warm-temperate agriculture weeds have been reported to exploit the new environmental conditions to expand their distribution into areas of high elevation (Patterson, 1995; Briand et al., 2004; Nehring and Hesse, 2008). In addition to a mean increase in annual temperature, extreme heat events (e.g. a heat wave or hot days) will become more frequent and severe over most land areas under future climate scenarios (Wagner, 1996; IPCC, 2007). These extreme events, though ephemeral, can cause dramatic ecological impacts which might be significantly greater than those associated with mean temperature increases (Karl et al., 1997). Sage and Kubien (2003) have reported that in natural systems, the significance of climate warming for C4 vegetation depends less on the mean increase in global temperature and more on the spatial and temporal variation of the temperature increase. Some researchers have examined the responses of plant species to heat waves (White et al., 2000, 2001; García-Plazaola et al., 2008; Wang et al., 2008). However, few studies have involved invasive species, so the ecological impact of extreme heat events on plant invasions remains unclear. Wedelia trilobata (L.) Hitchc. is a creeping herb native to tropical Central America, which has invaded many areas of the tropics and subtropics (Thaman, 1999). It has been listed as one of the world's 100 worst invasive alien species (IUCN, 2001). In the 1970s, W. trilobata was introduced into China as an ornamental groundcover, but it rapidly escaped from gardens to roadsides and plantations (Li and Xie, 2002). Thus, it has become recognized as a serious weed in southern China (Wu et al., 2005,b). Previous studies suggested that fast dispersal by vegetative propagation (Wu et al., 2005,a), high photosynthetic activity (Wu and Hu, 2004; Liu and Li, 2005), allelopathic potential (Vieira et al., 2001; Nie et al., 2004; Zhang et al., 2004), and energy-use efficiency (Song et al., 2009) are the principal factors explaining its successful invasion. In recent years, the frequency, duration, and severity of extreme heat stress in southern China have increased, accompanied by rising mean temperature. In this scenario, W. trilobata encounters severe high temperature stress in summer, as does its indigenous congener. The capacity for ecophysiological acclimation to heat stress might be critical for the survival and dispersal of plant seedlings. Since W. trilobata originates from tropical regions, it was hypothesized that it might have developed a suite of physiological characters that confer on it a greater ability to withstand acute heat events. High temperatures adversely affect plant growth in a number of ways, with photosynthesis considered as one of the most heat-sensitive processes (Berry and Björkman, 1980; Schrader et al., 2004). Photosystem II (PSII) is the critical site of damage by high temperatures (Allakhverdiev et al., 2008). High temperature >45 °C is known to damage PSII (Yamane et al., 1998; Sharkey, 2005). Moderate heat stress (e.g. 35–42 °C) has been reported to increase PSI cyclic electron flow (Pastenes and Horton, 1996; Bukhov et al., 1999; Zhang and Sharkey, 2009) and thylakoid proton conductance (Schrader et al., 2004) and reduces the photosynthetic rate (Feller et al., 1998), but its effect on PSII is only partial inhibition (Sun et al., 2007) and it is reversible (Sharkey, 2005). Possibly plants possess an effective regulatory system to protect photosynthesis from moderately high temperatures that do not damage PSII, such as down-regulation of PSII and thermal dissipation (Kato et al., 2003; Kornyeyev et al., 2004). Quantifying the fate of absorbed light energy is of importance for studying the response of the photosynthetic apparatus to environmental factors and the regulatory mechanisms involved in acclimation (Kornyeyev and Hendrikson, 2007). However, few studies have evaluated the effect of moderately high temperature on these aspects. Comparison of invasive species and native species is an efficient approach to identifying mechanisms of invasive plant success, and thus provides insight useful for predicting the development of local communities (Goldberg, 1987; Mack, 1996). In this study, the effects of simulated heat stress on the invasive W. trilobata and its indigenous congener [Wedelia chinensis (Osbeck.) Merr.] were compared. The main objectives were (i) to determine how simulated heat stress affects the growth of invasive W. trilobata and its indigenous congener W. chinensis, with a view to predicting the development of this invasive species in the future; and (ii) to characterize the acclimation of PSII in these two species to high temperature, in order to determine whether there is an existing specific photosynthetic regulatory mechanism in this invasive species enabling it to withstand high temperature. Materials and methods Plant materials and high temperature treatments Both plant species, W. trilobata and W. chinensis, were collected from Guangzhou, Guangdong Province, China. They share similar morphologies and life histories, and overlap in range. In contrast to W. trilobata, W. chinensis grows slowly and has not been found harmful to native plants or habitats in China. The experimental plant materials were grown from stem cuttings ∼5 cm long. After 2–4 weeks of propagation, uniform seedlings (∼10 cm tall) were selected and transplanted into pots containing a 1:1:1 mixture of river sand, pool mud, and peat. The high temperature treatments simulating either an extreme heat event or mild temperatures were conducted by using two growth chambers (RXZ-500, Ningbo Instruments, China). According to the reports on climate change of Guangdong, the number of high temperature days (≥35 °C) is >20 per year, and the maximum temperature can approach 40 °C in the summer (Composing Team for Assessment Report on Climate Change of Guangdong, 2007). The high temperature treatment was maintained at 40/35 °C (day/night), and the control was set at 28/23 °C (day/night), representing the annual average temperature of Guangzhou. The high temperature treatment lasted for 30 d. For each species, 12 individuals were randomly assigned to one growth chamber. In both chambers, the photosynthetically active irradiance was ∼200 μmol m−2 s−1 with a photoperiod of 12 h, and the relative humidity was ∼65%. All pots were watered daily to maintain the soil water content at ∼50%. Growth measurements Prior to the exposure to high temperature, six additional seedlings of each species of the same size as the experimental seedlings were harvested to determine the initial biomass. After 30 d of treatment, all plant materials were harvested and total biomass per individual was determined after drying for 72 h in an oven set at 70 °C. The relative growth rate (RGR) was calculated as the net dry matter increase per unit dry mass per day (mg g−1 d−1) averaged over 30 d. Chlorophyll fluorescence and gas exchange measurements During the high temperature treatment, chlorophyll (Chl) fluorescence parameters were measured in situ continually at 2–3 d intervals with a portable pulse-modulated fluorimeter PAM-2100 (Walz, Efeltrich, Gemany). Leaf samples were dark adapted for 15 min before measurements of the minimum (Fo) and maximal fluorescence (Fm). The maximal photochemical efficiency of PSII (Fv/Fm) was calculated as Fv/Fm=(Fm–Fo)/Fm (Schreiber et al., 1986). The steady-state (Fs) and maximum fluorescence (Fm′) in the light-adapted state were measured under an actinic light irradiance of 200 μmol m−2 s−1. The effective photochemical efficiency of PSII (ΦPSII) was calculated as ΦPSII=(Fm′–Fs)/Fm′ (Genty et al., 1989). The total electron transport rate through PSII (ETR) was estimated according to Krall and Edwards (1992): ETR=ΦPSII×PPFD×A×0.5, where A is the leaf absorptance, which was estimated as 0.84. The factor 0.5 was based on the assumption of an equal distribution of photons between PSI and PSII. Incident irradiance was measured with a quantum sensor. After heat stress, gas exchange was measured concurrently with Chl fluorescence on the same leaves with a portable photosynthesis measuring system (Li-6400, Portable Photosynthesis System, Li-Cor, Lincoln, NE, USA). Partitioning of the absorbed light energy was estimated according to the model proposed by Hendrickson et al. (2004). The allocation of photons absorbed by the PSII antennae to photosynthetic electron transport and PSII photochemistry was estimated as ΦPSII=1–(Fs/Fm′). The quantum efficiency of regulated ΔpH- and/or xanthophyll-dependent non-photochemical dissipation processes within the PSII antennae (ΦNPQ) was calculated as: ΦNPQ=(Fs/Fm′)–(Fs/Fm). Constitutive non-photochemical energy dissipation and fluorescence was calculated as: Φf,D=Fs/Fm (Cailly et al., 1996). The temperature-dependent increase in minimal florescence in the dark (Fo versus T curve) was determined as described by Lin et al. (2005). The third and fourth mature leaves from 4-week-old plants grown at the ambient temperature were used for this experiment. Before the measurement of Fo, leaf samples were dark adapted for 15 min at 25 °C. Then leaf discs were placed in a water bath of 25–80 °C, in which the temperature was increased continuously at 2 °C min−1, and the corresponding Fo was recorded at 0.02 s intervals with a PAM-2100. The inflexion temperature at which Fo began to rise sharply (Ti) and the peak temperature (Tp) were recorded. Measurements of physiological characteristics After the high temperature treatment, the mature and fully expanded leaves were collected for pigments analysis. The Chl content was quantified using the procedure described by Arnon (1949). Xanthophyll cycle pigments were extracted with ice-cold 100% acetone from leaf tissue that had been frozen in liquid nitrogen immediately after detachment and ground in a mortar. The extract was analysed using an HPLC system (Agilent 1100LC, Germany) according to the method described by Gilmore and Yamamoto (1991). The de-epoxidation state (DES) of the xanthophyll cycle was calculated as (Z+0.5×A)/(V+A+Z), where V, A, and Z correspond to the concentration of violaxanthin, antheraxanthin, and zeaxanthin, respectively (Gilmore and Yamamoto, 1993). In order to measure the cell membrane leakage rate, leaves [0.2 g fresh weight (FW)] of the two species were immersed in double-distilled water for 1.5 h at room temperature, followed by a 30 min boiling treatment. The conductivity of a solution of leaked electrolytes before (Lt) and after boiling (Lo) was determined using a DDS-11C conductometer (Shanghai Dapu Instruments, Shanghai, China). Membrane leakage rate was defined as Lt/Lo and expressed as a percentage (Vieira Santos et al., 2001). For extraction and determination of heat-stable protein, leaves (0.5 g FW) were ground and extracted in an ice bath with 5 ml of pre-cooled phosphate buffer (pH 7.0). The homogenate was heated in boiling water for 15 min, and then placed into an ice bath to cool for 30 min. After centrifugation at 4 °C, 13 000 g for 15 min, the content of the heat-stable protein in the supernatant was measured using Coomassie brilliant blue (Bradford, 1976). The content of the heat-stable protein was expressed as a percentage of the total soluble protein. In order to assess total antioxidative capability, 50% ethanol extracts were prepared from the leaves of the two Wedelia species (0.1 g FW), followed by centrifugation at 4 °C and 5000 g for 15 min. The supernatant was mixed with coloured DPPH· (1.1-diphenyl-2-picrylhy-drazyl) solution. The decrease of coloured DPPH· solution absorbance was measured at 525 nm using a spectrophotometer (UV-2450, Shimadzu, Japan) as described by Peng et al. (2000). Total antioxidative capability was expressed as the scavenging amount of an organic free radical DPPH· per g FW of leaves. Statistical analysis All statistical tests were performed using SPSS 11.5 software (SPSS Inc., USA). A two-way analysis of variance (ANOVA) was performed to evaluate the main effects and interactive effect of high temperature and species on measured variables. Treatment means were compared to determine if means of the dependent variable were significant at the 0.05 probability level with the least significant difference (LSD) post-hoc analysis. Results RGR was significantly affected by species, high temperature, and their interaction (Table 1). Wedelia chinensis exposed to high temperature exhibited a significant decrease in RGR. However, the RGR of W. trilobata was not significantly changed by high temperature (Fig. 1A). High temperature-induced changes in RGR were associated with a consistent trend in the total biomass. The total biomass was affected significantly by species and high temperature (Table 1). A significant decrease of total biomass was found in W. chinensis by the high temperature treatment, whereas no significant change occurred in W. trilobata (Fig. 1B). Table 1. Results from two-way ANOVA (F value) for treatment effects on plant individual variables Variables  Species  High temperature  Species×high temperature  Biomass  104.1**  8.08**  2.23ns  RGR  56.34**  34.98**  20.77**  Fv/Fm  33.21**  300.0**  16.96**  Fo  16.72**  195.8**  14.64**  ETR  0.77ns  773.5**  4.32*  ΦPSII  1.99ns  350.2**  2.88ns  ΦNPQ  0.55ns  220.7**  0.22ns  Φf,D  19.64**  1.22ns  18.54**  Pn  6.03*  37.30**  14.22**  Variables  Species  High temperature  Species×high temperature  Biomass  104.1**  8.08**  2.23ns  RGR  56.34**  34.98**  20.77**  Fv/Fm  33.21**  300.0**  16.96**  Fo  16.72**  195.8**  14.64**  ETR  0.77ns  773.5**  4.32*  ΦPSII  1.99ns  350.2**  2.88ns  ΦNPQ  0.55ns  220.7**  0.22ns  Φf,D  19.64**  1.22ns  18.54**  Pn  6.03*  37.30**  14.22**  Significance levels: ns, P >0.05; *P <0.05; **P <0.01. View Large Fig. 1. View largeDownload slide Effects of simulated heat events on the relative growth rate (RGR) (A) and total biomass (B) of the invasive Wedelia trilobata and the native Wedelia chinensis. Error bars represent 1 SE. Means with a common letter do not differ from each other based on LSD post-hoc analysis at the P=0.05 level. Fig. 1. View largeDownload slide Effects of simulated heat events on the relative growth rate (RGR) (A) and total biomass (B) of the invasive Wedelia trilobata and the native Wedelia chinensis. Error bars represent 1 SE. Means with a common letter do not differ from each other based on LSD post-hoc analysis at the P=0.05 level. As shown in Table 2, high temperature influenced various physiological processes in these two species. High temperature decreased the total Chl content of W. chinensis, but increased that of W. trilobata. The Chl a/b ratio was decreased under 40/35 °C in both species. It indicated that the Chl, especially Chl a, was sensitive to high temperature. In addition, high temperature increased the carotenoid content of W. trilobata, but did not affect that of W. chinensis. Exposure to high temperature resulted in a trend toward a decrease in the content of heat-stable proteins, but this was not significantly different in the two species at high temperature. The membrane leakage rate is a relevant index reflecting the degree of impaired membrane function. High temperature induced an increase in the membrane leakage rate of both Wedelia species, suggesting that their plasma membranes, and possibly also their chloroplast envelope membranes, were damaged to some extent. After high temperature treatment, the membrane leakage rate of W. chinensis was significantly higher than that of W. trilobata. Measurement of scavenging of the DPPH· free radicals is a rapid, simple, sensitive, and practical assay for evaluating antioxidant capacity in plants (Peng et al., 2000). In this respect, these two species exhibited different responses to high temperature. The DPPH· scavenging capacity of invasive W. trilobata declined by 29.6%, whereas that of W. chinensis exhibited an increase of 22.0%. After the heat treatment, these two species reached a similar level of DPPH· scavenging capacity. Table 2. Total chlorophyll (Chl) content, Chl a/b ratio, carotenoid content, heat-stable protein content, membrane leakage rate, and DPPH· scavenging capacity in leaves of invasive Wedelia trilobata and native Wedelia chinensis at 28/23 °C and 40/35 °C. Variable  Wedelia trilobata   Wedelia chinensis     28/23 °C  40/35 °C  28/23 °C  40/35 °C  Total Chl (μg cm−2)  35.29±1.48 c  52.80±1.43 ab  54.72±2.34 a  48.19±1.23 b  Chl a/b ratio  2.77±0.02 a  2.55±0.01 b  2.70±0.08 a  2.37±0.01 c  Carotenoid (μg cm−2)  3.30±0.13 b  4.54±0.09 a  4.74±0.21 a  4.78±0.14 a  Heat-stable protein content (%)  10.37±0.60 a  9.35±0.70 ab  9.32±0.20 ab  7.83±0.10 b  Membrane leakage rate (%)  14.10±0.65 c  17.17±0.25 b  12.80±0.23 d  19.78±0.24 a  DPPH· scavenging capacity (mg DPPH· g−1 FW)  44.16±2.19 a  31.09±1.90 b  25.46±1.11 c  31.07±1.27 b  Variable  Wedelia trilobata   Wedelia chinensis     28/23 °C  40/35 °C  28/23 °C  40/35 °C  Total Chl (μg cm−2)  35.29±1.48 c  52.80±1.43 ab  54.72±2.34 a  48.19±1.23 b  Chl a/b ratio  2.77±0.02 a  2.55±0.01 b  2.70±0.08 a  2.37±0.01 c  Carotenoid (μg cm−2)  3.30±0.13 b  4.54±0.09 a  4.74±0.21 a  4.78±0.14 a  Heat-stable protein content (%)  10.37±0.60 a  9.35±0.70 ab  9.32±0.20 ab  7.83±0.10 b  Membrane leakage rate (%)  14.10±0.65 c  17.17±0.25 b  12.80±0.23 d  19.78±0.24 a  DPPH· scavenging capacity (mg DPPH· g−1 FW)  44.16±2.19 a  31.09±1.90 b  25.46±1.11 c  31.07±1.27 b  Data are means ±1 SE. For each variable, means labelled with the same letter are not significantly different according to LSD post-hoc analysis at the P=0.05 level. View Large The maximal photochemical efficiency of PSII (Fv/Fm) and the minimum fluorescence (Fo) were significantly affected by species, high temperature, and their interactive effect (Table 1). Upon exposure to high temperature, an obvious decreasing trend of Fv/Fm was observed in both Wedelia species (Fig. 2A). Within the first 2 d, Fv/Fm underwent a sudden decline, followed by a slight recovery between 3 d and 12 d, and a continuous decrease beyond 12 d. Although there was no significant difference between the two species before the heat treatment, high temperature magnified the discrepancy of Fv/Fm between them. After treatment for 30 d, W. trilobata exhibited higher Fv/Fm than W. chinensis (P <0.001). While Fv/Fm decreased, these two species showed an increase in Fo with the duration of heat treatment (Fig. 2B). After the heat treatment for 30 d, Fo was increased by 31.3% and 48.2% in W. trilobata and W. chinensis, respectively. Fig. 2. View largeDownload slide Changes in the maximal photochemical efficiency of PSII (Fv/Fm) (A), the minimum fluorescence (Fo) (B), the effective photochemical efficiency of PSII (ΦPSII) (C), and the total electron transport rate (ETR) (D) of invasive Wedelia trilobata and the native Wedelia chinensis during heat stress. Error bars represent 1 SE. Fig. 2. View largeDownload slide Changes in the maximal photochemical efficiency of PSII (Fv/Fm) (A), the minimum fluorescence (Fo) (B), the effective photochemical efficiency of PSII (ΦPSII) (C), and the total electron transport rate (ETR) (D) of invasive Wedelia trilobata and the native Wedelia chinensis during heat stress. Error bars represent 1 SE. High temperature had significant effects on ΦPSII and ETR (Table 1). Both species exhibited a similar decreasing trend in ΦPSII and ETR (Fig. 2C, D). The dynamic changes of ΦPSII and ETR during heat treatment seemed to involve two stages of alteration. In the first stage (within the first 12 d), ΦPSII and ETR declined slowly and there was no significant difference between these two species. In the second stage (beyond 12 d), W. chinensis exhibited a relatively fast decrease in ΦPSII and ETR compared with W. trilobata. High temperature had significant effects on the energy partitioning of absorbed light to photochemical conversion (ΦPSII) and thermal dissipation via ΔpH- and xanthophyll-dependent energy quenching (ΦNPQ) (Table 1). The estimated energy partitioning of absorbed light to the various pathways indicated that the photochemistry fraction (ΦPSII) was significantly decreased by high temperature (P <0.001), while the thermal dissipation fraction (ΦNPQ) was increased in both species (P <0.001) (Fig. 3). In contrast, Φf,D, the combined fraction of absorbed light energy dissipated constitutively as heat in a light-independent manner and as Chl fluorescence, showed different response patterns to high temperature in these two species. The invasive W. trilobata exhibited a significant decrease in Φf,D (P = 0.045), whereas the native W. chinensis showed an increase (P=0.001) (Fig. 3). Under high temperature, the constitutive energy dissipation (Φf,D) was significantly lower in W. trilobata than in W. chinensis (P <0.001). Fig. 3. View largeDownload slide Effects of simulated heat events on the energy partitioning of absorbed light to photochemical process (ΦPSII), ΔpH- and xanthophyll-dependent thermal dissipation (ΦNPQ), and the sum of fluorescence and constitutive thermal dissipation (Φf,D) of the invasive Wedelia trilobata and the native Wedelia chinensis. Fig. 3. View largeDownload slide Effects of simulated heat events on the energy partitioning of absorbed light to photochemical process (ΦPSII), ΔpH- and xanthophyll-dependent thermal dissipation (ΦNPQ), and the sum of fluorescence and constitutive thermal dissipation (Φf,D) of the invasive Wedelia trilobata and the native Wedelia chinensis. Leaf net photosynthetic rate (Pn) was affected significantly by species, high temperature, and their interaction (Table 1). Measured under high temperature, Pn showed a significant decrease of 82.0% in the native W. chinensis, while that in the invasive W. trilobata exhibited only a decrease of 21.9% which was not statistically significant (Fig. 4). Fig. 4. View largeDownload slide Effects of simulated heat events on the net photosynthetic rate (Pn) of the invasive Wedelia trilobata and the native Wedelia chinensis. Error bars represent 1 SE. Means with a common letter do not differ from each other based on LSD post-hoc analysis at the P=0.05 level. Fig. 4. View largeDownload slide Effects of simulated heat events on the net photosynthetic rate (Pn) of the invasive Wedelia trilobata and the native Wedelia chinensis. Error bars represent 1 SE. Means with a common letter do not differ from each other based on LSD post-hoc analysis at the P=0.05 level. Exposure to high temperature resulted in a trend toward an increase of the total xanthophyll cycle pigments pool (V+A+Z) in both species (Fig. 5A). Furthermore, W. trilobata exhibited a significant increase in the DES of the xanthophyll cycle under high temperature, whereas no obvious change was observed in W. chinensis (Fig. 5B). Fig. 5. View largeDownload slide Effects of simulated heat events on the total amounts of xanthophyll cycle pigments (A) and the de-epoxidation state (B) in the leaves of the invasive Wedelia trilobata and the native Wedelia chinensis. Error bars represent 1 SE. Means with a common letter do not differ from each other based on LSD post-hoc analysis at the P=0.05 level. Fig. 5. View largeDownload slide Effects of simulated heat events on the total amounts of xanthophyll cycle pigments (A) and the de-epoxidation state (B) in the leaves of the invasive Wedelia trilobata and the native Wedelia chinensis. Error bars represent 1 SE. Means with a common letter do not differ from each other based on LSD post-hoc analysis at the P=0.05 level. Figure 6A shows the Fo versus T curves in the leaves of W. trilobata and W. chinensis. With the continuous increase in temperature, Fo versus T curves showed a pattern similar to a parabola. The inflexion temperature (Ti) at which Fo began to rise sharply corresponds to the beginning of irreversible injury of photosynthetic membranes. Wedelai trilobata exhibited a higher inflexion temperature for Fo (48.0 °C) than W. chinensis (44.6 °C) (Fig. 6B). As shown in Fig. 6C, the peak temperature for Fo (Tp) in W. trilobata was also significantly higher (54.5 °C) than in W. chinensis (51.2 °C). Fig. 6. View largeDownload slide The Fo versus. temperature curves (A), inflexion temperature (Ti) (B), and peak temperature (Tp) (C) in leaves of the invasive Wedelia trilobata and the native Wedelia chinensis. **P <0.01. Fig. 6. View largeDownload slide The Fo versus. temperature curves (A), inflexion temperature (Ti) (B), and peak temperature (Tp) (C) in leaves of the invasive Wedelia trilobata and the native Wedelia chinensis. **P <0.01. Discussion Plant growth, photosynthesis, and photochemical efficiency High temperature adversely affects various physiological processes which can reduce plant growth, survival, and, consequently, crop yield (Boyer, 1982). However, the relative inhibition varies greatly among plant species (Stasik and Jones, 2007), such differences having important consequences for plant competition. Following a short-term exposure to high temperature, the growth of two Wedelia species was restricted to a varying degree. In particular, W. chinensis was more strongly inhibited in RGR and total biomass production compared with W. trilobata (Fig. 1). Photosynthesis is recognized as the most important determinant of plant growth; its responses and adaptation to the environment enable plants to exist and develop under various temperature conditions. Although high temperature decreased the net photosynthetic rate, W. trilobata exhibited a significantly higher Pn than W. chinensis (Fig. 4), which is consistent with the changes in RGR and biomass under heat stress. High temperature did not decrease pigment content, and induced a smaller increase in membrane leakage in W. trilobata compared with W. chinensis (Table 2). These results indicated that the invasive W. trilobata had greater thermotolerance. Under field conditions, high temperature often accompanies high irradiance, drought, and other environmental stress, and thus heat stress is further aggravated. It is expected to intensify the negative impact on the native W. chinensis to some extent. Therefore, it was inferred that the invasive W. trilobata may become more aggressive in a warmer world in future. PSII is particularly sensitive to high temperature (Berry and Björkman, 1980; Thompson et al., 1989; Mamedov et al., 1993). Exposure to a short-term high temperature treatment resulted in significant changes in PSII function in these two Wedelia species. An obvious decreasing trend of Fv/Fm was observed in these two species, while the value of Fo was increased under high temperature in the later stages of the treatment (Fig. 2). These changes in Fv/Fm and Fo are considered to be reliable diagnostic indicators of photoinhibition (Maxwell and Johnson, 2000). The present results are consistent with the evidence of Sun et al. (2007), which demonstrated that moderate high temperature stress causes a partial inhibition of PSII. Further, the adverse effect was more severe in native W. chinensis. After 30 d of heat stress, the invasive W. trilobata showed higher ΦPSII and ETR than W. chinensis (Fig. 2C, D). All the above results show that the invasive species maintained relatively high activity of PSII under high temperature conditions. High thermal stability of the photosynthetic apparatus High thermostability of the photosynthetic apparatus is conducive to the maintenance of PSII function at a high temperature. The temperature-dependent increase in minimal florescence in the dark (the Fo versus T curve) has been routinely used to estimate the thermostability of the photosynthetic apparatus (Schreiber and Berry, 1977; Schreiber and Bilger, 1987; Froux et al., 2004; Weng and Lai, 2005). The temperature at which Fo began to rise sharply (Ti) is the critical point which indicates that irreversible injury has begun in the photosynthetic membrane (Georgieva and Yordanov, 1993). In this study, W. trilobata exhibited higher Ti than W. chinensis (Fig. 6B), suggesting that W. trilobata has a greater thermostability of its photosynthetic apparatus. Previous studies reported that moderate heat causes thylakoid membranes to become leaky (Schrader et al., 2004). In the present study, W. trilobata displayed a smaller Fo increase following high temperature exposure than W. chinensis (Fig. 2B), suggesting a greater thermostability of thylakoid membranes in this invasive species. Additional experimental evidence is necessary to test this hypothesis further. Partitioning of absorbed light energy High temperature could accelerate photoinhibition by inducing an imbalance between light energy absorption and utilization. When the energy absorbed is in excess of the amount that can be used for carbon fixation, it could lead to the production of reactive oxygen species, which can damage the photosynthetic apparatus (Osmond, 1994; Müller et al., 2001). In this study, the native W. chinensis exhibited significant decreases in total Chl content and the Chl a/b ratio under high temperature (Table 2), which is considered as an avoidance mechanism to reduce light absorption (Ishida et al., 2000). In contrast, invasive W. trilobata had greater thermal tolerance; its leaves under high temperature became greener, with increased total Chl content (Table 2). Thermal dissipation of excess excitation energy is an important photoprotective mechanism that plants have evolved to cope with excess absorbed light. Several models have been proposed to quantify the partitioning of total absorbed energy by PSII between the various processes of photochemistry and thermal dissipation (Demmig-Adams et al., 1996; Hendrickson et al., 2004; Kramer et al., 2004), which is of significant importance for studying the response of the photosynthetic apparatus to high temperature and the regulatory mechanisms involved in acclimation. In the present study, the partitioning of the absorbed light to various pathways in control and heat-stressed plants was estimated according to the method of Hendrickson et al. (2004). For both Wedelia species, the fraction partitioned to photochemistry (ΦPSII) decreased with rising temperature (Fig. 3), presumably because Rubisco activase-mediated activation of Rubisco was inhibited at the higher temperature (Feller et al., 1998). However, it is noteworthy that W. trilobata exhibited a relatively higher ΦPSII following high temperature treatment (Fig. 2C), which resulted in more electron flow through PSII (ETR) compared with the native species (Fig. 2D). This result suggests that this invasive species had a greater capacity for energy utilization under high temperature. Any small improvement in energy utilization has a cumulative effect over a growing season, ameliorating the growth inhibition of invasive W. trilobata under high temperature. Concomitantly, the fraction of the regulated ΔpH- and xanthophyll-dependent thermal dissipation process (ΦNPQ) was significantly increased by high temperature in both Wedelia species (Fig. 3). This result is partly associated with the increased trend towards the xanthophyll cycle pigment pool (V+A+Z) (Fig. 5A). In comparison with W. chinensis, W. trilobata had a smaller xanthophyll pool size at both the control and elevated temperature. A previous study reported that plants with higher thermotolerance have a smaller xanthophyll pool size (Tsai and Hsu, 2009). Furthermore, high temperature enhanced the DES of the xanthophyll cycle in W. trilobata, whereas no obvious change was observed in W. chinensis (Fig. 5B). This differential effect resulted in the slightly higher ΦNPQ fraction in W. trilobata (despite a smaller xanthophyll pool size) than that in W. chinensis under high temperature, which could offer more photoprotection to this invasive species. For W. chinensis, high temperature did not enhance its DES, but significantly increased its DPPH· scavenging capacity. It is deduced that the major protective mechanism against photodamage may be different for the two plant species; an elevated antioxidative capacity may be the predominant protective mechanism in W. chinensis, whereas W. trilobata might not need to enhance its antioxidative capacity. In this respect, it is interesting to note that in W. trilobata ΦPSII decreased from 73.1% to 61.9% on transition to the high temperature regime (Fig. 3, top), a percentage decrease similar to that of Pn (Fig. 4, left). In contrast, in W. chinensis ΦPSII decreased from 73.3% to 59.8% on acclimation to the high temperature regime (Fig. 3, bottom), a percentage decrease vastly smaller than that of Pn (Fig. 4, right). Conceivably, the ‘missing’ electron flow (the component of the ETR not coupled to Pn) that had gone through PSII in W. chinensis but not reflected in net carbon assimilation could have been diverted to antioxidative activity or other alternative electron pathways. The proportion of constitutive thermal dissipation (Φf,D) showed different responses to high temperature between these two species; Φf,D decreased slightly in W. trilobata, while it increased slightly in W. cheninsis (Fig. 3). Since Φf,D represents an inevitable energy loss, the invasive species seems to have an advantage over the native species in having a slightly lower Φf,D in the high temperature regime. The present results revealed that the invasive W. trilobata could regulate energy partitioning in PSII complexes to minimize damaging potential and retain a great capability for carbon assimilation. For the invasive W. trilobata, the effective regulation of energy partitioning around PSII might be an alternative acclimation mechanism to withstand high temperature. In conclusion, the invasive W. trilobata has a relatively high thermostability of its photosynthetic apparatus and an adaptive regulation in energy partitioning in PSII complexes, which confer on it a greater ability than the native species to withstand heat stress. The invasive W. trilobata is likely to become more aggressive with the increasingly extreme heat climates. Furthermore, it should be noted that W. trilobata originates from the tropics of Central America, where the mean temperature is higher than in the invaded land in South China. In a long-term evolution process, W. trilobata has developed an adaptive capacity to withstand high temperature. Some previous studies have demonstrated that low elevation species have a higher thermal tolerance than high elevation species (Loik and Harte, 1996). The present results lead to the conclusion that those exotic species whose native habitats are warmer than their introduced ranges would have an advantage in an increasingly extreme heat climate. We thank Professor Zhifang Lin (South China Botanical Garden) for her constructive comments on the manuscript. This work was supported by the National Natural Science Foundation of China (30870385), National Basic Research Program of China (973 Program) (2009CB118504), the Natural Science Foundation of Guangdong Province (8451063101000535), China Postdoctoral Science Foundation (20080440766), and the Australian Research Council (DP1093827). 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TI - Acclimation of photosystem II to high temperature in two Wedelia species from different geographical origins: implications for biological invasions upon global warming
JF - Journal of Experimental Botany
DO - 10.1093/jxb/erq220
DA - 2010-07-13
UR - https://www.deepdyve.com/lp/oxford-university-press/acclimation-of-photosystem-ii-to-high-temperature-in-two-wedelia-QTsQJU6rlk
SP - 4087
EP - 4096
VL - 61
IS - 14
DP - DeepDyve
ER -