The exotic invasive Ambrosia artemisiifolia L. and a native co-occurring species in southern China, Urena lobata L., were compared to investigate the possible protective role of leaf antioxidant systems in the acclimation of invasive plants to different irradiance levels. Antioxidant activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) were examined under four irradiance regimes: 10% (dense shade), 30% (low irradiance), 55% (medium irradiance) and 100% (full irradiance). Free proline (Pro) content and the rate of lipid peroxidation in terms of malondialdehyde (MDA) content, glutathione reductase (GR), and tea polyphenols (TP) were also assessed under the different irradiance regimes. Antioxidant enzyme activity of SOD and CAT and the MDA, GR and TP contents for the two species increased with increasing irradiance levels. Invasive A. artemisiifolia was able to scavenge oxygen radicals more efficiently at higher irradiance levels by enhancing CAT activity and GR and TP contents although leaf SOD activity was not greatly enhanced. This exotic species also maintained normal physiological functions when subjected to low irradiance, which might be attributed to the increase in POD activity with decreasing irradiance levels. The higher efficiency of adaptive responses of antioxidant enzymes may protect plants from irradiance-induced stress and may contribute to the invasiveness of A. artemisiifolia in subtropical and tropical regions.
- Abiotic stress,
- Ambrosia artemisiifolia,
- antioxidative enzymes,
- common ragweed,
- invasive plants,
- lipid peroxidation,
- Urena lobata
Réponse antioxydant de l’herbe envahissante Ambrosia artemisiifolia L. à différents taux de flux énergétique
Dans le sud de la Chine, l’espèce exotique envahissante Ambrosia artemisiifolia L. a été comparée à une espèce indigène compagne, Urena lobata L., afin d’évaluer le rôle protecteur potentiel fourni par les systèmes antioxydants de la feuille lors de l’acclimatation des plantes envahissantes soumises à différents taux de flux énergétique. Les activités antioxydants de la superoxyde dismutase (SOD), de la peroxydase (POD) et de la catalase (CAT) ont été examinées sous quatre régimes de flux énergétique : 10 % (ombrage dense), 30 % (faible flux énergétique), 55 % (flux énergétique moyen) et 100 % (flux énergétique complet). Le contenu en proline libre (Pro) et le taux de peroxydation lipidique en termes de malonaldéhyde (MDA), de réductase de glutathion (RG) et de polyphénols de thé (PT) ont également été évalués pour différents taux de flux énergétique. Les activités enzymatiques antioxydantes de SOD et de CAT et les contenus en MDA, RG et PT des deux espèces ont augmenté avec l’augmentation des taux de flux énergétique. L’espèce invasive A. artemisiifolia était en mesure de récupérer les radicaux d’oxygène plus efficacement à un taux de flux énergétique plus élevé grâce à une activité accrue de la CAT et des contenus de RG et PT plus élevés, bien que l’activité de la SOD dans la feuille n’ait pas beaucoup augmentée. Cette espèce exotique a également maintenu des fonctions physiologiques normales lorsque soumise à de faible taux de flux énergétique, ce qui pourrait être attribuable à l’augmentation de l’activité de la POD en lien avec une diminution du taux de flux énergétique. Une plus grande efficacité des réactions adaptatives des enzymes antioxidants pourrait protéger les plantes du stress relié au flux énergétique et contribuer à l’envahissement de l’A. artemisiifolia dans les régions tropicales et subtropicales.
- Ambrosia artemisiifolia,
- enzymes antioxydants,
- flux énergétique,
- peroxydation lipidique,
- petite herbe à poux,
- plantes envahissantes,
- stress abiotique,
- Urena lobata
The dramatic increase in exotic plant invasions has resulted in substantial damage to the structure, biodiversity and function of numerous ecosystems worldwide (Mack et al. 2000). Invasive plants generally exhibit greater stress tolerance, they can acclimate to a wider range of environmental conditions (Alpert et al. 2000; Feng et al. 2007), and are able to make more efficient use of fluctuating resources than native species (Davis et al. 2000). Light is the most important resource for plants and it influences both vegetative and reproductive growth (Chazdon and Pearcy 1986; Demmig-Adams and Adams 1992; Poorter 2001; Feng 2008). Invasive species appear to be better suited than native species to capture and utilize light resources, particularly in high light environments such as frequently disturbed habitats (Williams and Black 1994; Pattison et al. 1998). Increased light capture and utilization efficiency of successful invaders have been attributed to their morphological and physiological traits. For instance, Pattison et al. (1998) found that invasive species are better able to adjust biomass allocation and photosynthetic capacities across different light regimes, yielding higher growth rates than native species. However, determining the specific mechanisms by which invasive plants acclimate to varying irradiance levels and possibly benefit from these adaptations is currently understudied.
Like other abiotic stresses, high irradiance levels may induce the production of a variety of active oxygen species (AOS) such as superoxide anion (O2-), hydrogen peroxide (H2O2), and hydroxyl (OH-) radicals (McCord 2000). Plants subjected to exposure to activated forms of oxygen and accumulation of free radicals may sustain damage to membranes and experience buildup of lipid peroxides (Smirnoff 1993; Hernández et al. 2000; Urquiaga and Leighton 2000). Cell membrane stability has been used to differentiate stress tolerant and stress susceptible varieties within crop plants (e.g. wheat) (Blum and Ebercon 1981; Bajji et al. 2002). In some cases, higher membrane stability has been correlated with increased performance or adaptation to stressful environmental conditions. Increases in the activity of antioxidant systems may help plants acclimate to irradiance stress (Grace and Logan 1996; Monk et al. 1989; Logan et al. 2006; Cheeseman 2007). Several studies have shown that plants produce antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APOX), catalase (CAT) and glutathione reductase (GR) to scavenge active oxygen species (Mishra et al. 1993; Ali et al. 2005; Kartashov et al. 2008), while relatively few studies have investigated the role of antioxidation in acclimation to irradiance of invasive plants.
Ambrosia artemisiifolia L. (common ragweed – Asteraceae), an herb species native to North America, was introduced into China in the 1930s and has extended its range from northern to southern China during the past three decades (Wan and Wang 1990; Qi et al. 2011). The latitudinal distribution of A. artemisiifolia in China ranges from 49°N to 24°N, covering more than 20 provinces and municipalities. Climate in northern regions is characterized as north-temperate, with mean annual air temperatures of 6-10°C and average annual precipitation of 530–680 mm, to subtropical in southern regions with mean annual air temperatures of 18–21°C and average annual precipitation of 1300–2400 mm. Moreover, about 54% of the annual solar radiation (4965 MJm‑2) received in northern regions occurs at temperatures above 10°C whereas in southern regions, 90% of annual solar radiation (4683 MJm‑2) occurs at these temperatures (climate data available from China Meteorological Data Sharing Service System, http://cdc.cma.gov.cn/index.jsp). With its rapid growth, plasticity and high reproductive output, A. artemisiifolia has successfully colonized disturbed habitats such as croplands and open, semi-natural and natural areas in Shaoguan, Jieyang and Huadu in the Guangdong province of southern China in recent years (Zeng et al. 2009). The presence of a wide range of spatially or temporally heterogeneous light environments in colonized regions provides an opportunity to assess the ecophysiological traits of A. artemisiifolia that may contribute to its invasive success, especially in the warmer subtropical regions of China. In a companion study, Zhong et al. (unpublished) observed enhanced morphological and photosynthetic physiological acclimation of A. artemisiifolia plants to a range of light regimes, particularly high irradiance levels. These adaptations were suggested to favour the recent invasive success of this exotic species in subtropical regions of China.
In this paper, we report on a comparative study of the exotic invader A. artemisiifolia and a native co-occurring species, Urena lobata L. (Caesar weed – Malvaceae) to determine their leaf antioxidant enzyme activity responses and malondialdehyde (MDA) content under different irradiance levels. These antioxidant enzymes and products play a key role in the scavenging of active oxygen species that damage the integrity and stability of plant cell membranes. We also evaluated differences between the two species in their antioxidant defense system, lipid peroxidation and irradiance capture efficiency. We used the native U. lobata in this study because it frequently co-occurs with A. artemisiifolia in disturbed, open habitats in southern China. We hypothesized that A. artemisiifolia exhibits a higher antioxidative capacity than U. lobata, and may receive increased protection from reactive oxygen species by increasing antioxidant enzyme activity, especially under extreme irradiance levels.
Materials and Methods
Seeds of A. artemisiifolia and U. lobata were collected in late October 2009 from plants in several old fields that had at least 50% cover of A. artemisiifolia. The fields were located in the city of Shaoguan, province of Guangdong, China (24.8°N, 113.6°E). Typical climatological data for this climate region were described previously. Fully developed and average-sized seeds of the two species were selected and sown separately in seedbeds in a glasshouse on 6 March 2010. When seedlings of the two species were approximately 15 cm tall, uniform-sized seedlings were transplanted singly into clay pots (20 × 16 × 19 cm) that were filled with red lateritic soil collected from the 0 to 20 cm soil layer of an abandoned field near the experimental station. Seedlings were grown at 30% irradiance for 25 d. Shade houses (4 × 4 × 3 m each) were constructed and irradiance levels were created by covering the shade houses with different layers of black nylon shade netting, including no netting to allow 100% irradiance. The lower 30 cm of each shade house remained open to facilitate airflow and to maintain humidity and temperature levels as similar as possible between the shade houses. The relative irradiance in each shade house was estimated by comparing the integrated photosynthetic photon flux density (PPFD) in a shade house during a clear day with that in a shade house with no netting.
On 14 May 2010, when both A. artemisiifolia and U. lobata were in their branching stage, 30 plants from the two target species (15 individuals per species) were randomly selected and subjected to one of four irradiance treatments: (i) dense shade, (ii) low irradiance, (iii) medium irradiance, and (iv) full irradiance, corresponding to 10%, 30%, 55% and 100% irradiance, respectively. Seedlings were watered daily and a compound fertilizer (N:P2O5:K2O = 15:15:15%, Batian Eco-Engineering Company, Shenzhen, China) was applied at a rate of 2 g pot‑1 monthly. On 12 July 2010, the two species were in their late branching stage, although several individuals had initiated flowering. Five to eight fully expanded leaves of A. artemisiifolia and U. lobata individuals located at similar stem heights from the soil surface were collected from each treatment between 09:00 and 11:00 and subjected to enzymatic activity, protein and MDA content assays. Four replicates were used for each treatment. Leaf samples were rapidly fixed in liquid nitrogen, and stored at -70°C until the start of the assay.
For enzyme extracts, 1.0 g of fresh leaf samples were ground to a fine powder with liquid nitrogen and extracted with 50 mM phosphate buffer (pH 7.0). The extracts were centrifuged at 4°C for 30 min at 12 000×g and the resulting supernatants were collected and used for enzymatic activity, protein and MDA content assays.
The activity of SOD was determined by monitoring its ability to inhibit the photochemical reduction of nitroblue tetrazolium (NBT) at 560 nm (Beauchamp and Fridovich 1971). One unit of SOD was defined as the amount of enzyme necessary to inhibit the reduction of NBT by 50%. CAT and POD activity was determined using the methods described in Chance and Maehly (1955). To measure CAT activity, a decrease in absorbance at 240 nm following the decomposition of H2O2 was recorded, while for POD activity, the oxidation of guaiacol was recorded by the increase in absorbance at 470 nm. One unit of CAT or POD activity was defined as an absorbance change of 0.01 unit per min.
Lipid peroxidation was measured by the amount of MDA detected, a product of unsaturated fatty acid peroxidation. The MDA content was determined based on the thiobarbituric acid (TBA) reaction as described by Peever and Higgins (1989) with modification and measurements corrected for non-specific turbidity by substracting the absorbance at 532 nm. The concentration of MDA was calculated by using an extinction coefficient of 155 mM‑1 cm‑1 (Heath and Packer 1968). Free proline (Pro) content was determined spectrophotometrically at 520 nm following the method of Bates et al. (1973) and consisted in the colorimetric determination of the amount of coloured reaction product of proline with ninhydric acid. Proline concentration was determined using calibration curves from which the absorbance values recorded were converted to absolute amounts. GR content was determined by the reduction of 5,5’-dithiobis(2-nitrobenzoic acid) (DTNB) at 412 nm according to Li et al. (2009). The tea polyphenol (TP) content was measured according to Zhang et al. (2009).
Differences in antioxidant enzyme activities and the contents of MDA, GR and TP among the four irradiance levels for the two species were analyzed with variance analysis (ANOVA), and a post hoc test (Duncan’s multiple range test) was conducted at P < 0.05. Differences between A. artemisiifolia and U. lobata for a given irradiance level were detected using an independent sample t-test. Regression analyses were performed to examine the variations of leaf antioxidant system parameters under different levels of irradiance. All statistical analyses were performed using SPSS 17.0 (SPSS Inc., Chicago, IL, USA).
Irradiance had a profound effect on the leaf antioxidant enzyme system and the contents of MDA, GR and TP, while species influenced the antioxidant enzyme system except for SOD. Irradiance accounted for at least 85% of the overall variance for measured antioxidant enzyme system parameters except for SOD. There were also significant interactions between irradiance and species except for MDA and SOD contents (Table 1). There were similar trends between A. artemisiifolia and U. lobata in terms of SOD activity in response to different irradiance regimes (Fig. 1A). With increasing irradiance levels, SOD activity in both species increased gradually (YSOD = 40.465 – 2.534X, R2 = 0.535, P = 0.001; Y’SOD = 42.863 – 2.539X, R2 = 0.571, P = 0.021, where YSOD and Y’SOD represent SOD activity of A. artemisiifolia and U. lobata, respectively, and X represents irradiance levels). Since SOD catalyzes superoxide free radical dismutation into H2O2 and O2, the increase in activity might signify the production of O2- during leaf exposure to the irradiance treatments. SOD activity in full sunlight increased by about 1.5-fold and 1.3-fold for A. artemisiifolia and U. lobata, respectively, compared with leaves subjected to the 10% irradiance treatment. For A. artemisiifolia, SOD activity at the three highest irradiance levels of 30%, 55% and 100% was greater than at the 10% level, while for U. lobata, SOD activity at the 100% and 55% irradiance levels was higher than at the 30% and 10% irradiance levels. There was no difference between the two species under the four irradiance levels. The maximum value of SOD activity for A. artemisiifolia was 42.33 unit min‑1 g‑1 FW, which is about 2.4% higher than that for U. lobata.
Growth at higher irradiance levels was associated with an increase in CAT activity in both A. artemisiifolia (YCAT = 2563.657 – 502.317X, R2 = 0.890, P = 0.000, where YCAT and X represent CAT activity and irradiance levels for A. artemisiifolia, respectively) and U. lobata (Y’CAT = 842.802 – 115.581X, R2 = 0.733, P = 0.000, where Y’CAT represents CAT activity of U. lobata). CAT activity in A. artemisiifolia and U. lobata at the 100% irradiance level was 3.5 and 2.6 times that at the 10% irradiance level, respectively. CAT activity in A. artemisiifolia was higher than that in U. lobata under all irradiance levels. CAT activity under the four irradiance levels was 23.8% to 42.7% higher for A. artemisiifolia than for U. lobata, indicating that the exotic invasive herb was better able to adapt to light stress via enhanced CAT activity (Fig. 1B).
Ambrosia artemisiifolia exhibited an increase in POD activity with decreasing irradiance levels (YPOD = 2.523 + 33.018X, R2 = 0.939, P = 0.000, where YPOD and X represent the POD activity and irradiance level in A. artemisiifolia, respectively), whereas U. lobata first displayed the same trend (Y’POD = 4.738 + 9.072X, R2 = 0.306, P = 0.026, where Y’POD represents POD activity in U. lobata), but POD activity decreased at the lowest irradiance level of 10% (Fig. 1C). The lowest POD activity value for A. artemisiifolia was 32.78 unit min‑1 g‑1 FW, which is about 28 times that of U. lobata, although both species had the lowest POD activity under the 100% irradiance treatment. POD activity of A. artemisiifolia at the four irradiance levels was 53.2% to 72.9% higher than for U. lobata. Ambrosia artemisiifolia clearly had greater POD activity for leaves grown under all irradiance regimes, with a peak value of 131.76 unit min‑1 g‑1 FW observed at the 10% irradiance level.
Ambrosia artemisiifolia and U. lobata exhibited similar patterns in MDA content, which increased with increasing irradiance levels and peaked in the full sunlight treatment (YMDA = 60.336 – 8.100X, R2 = 0.794, P = 0.000, Y’MDA = 59.002 – 10.400X, R2 = 0.758, P = 0.000, where YMDA and Y’MDA represent the MDA activity of A. artemisiifolia and U. lobata, respectively, and X represents the irradiance level). When compared with U. lobata, the MDA content in A. artemisiifolia leaves under the four irradiance treatments was 2.2% to 26.9% higher than in U. lobata leaves, with the highest differences observed under the 10% and 30% irradiance regimes (Fig. 2A).
The Pro content in A. artemisiifolia leaves decreased from the 100% to 55% irradiance treatments, then increased with decreasing irradiance (Fig. 2B). The highest Pro content (214.2 ug g‑1 FW) was observed at the 10% irradiance level, about 2.1 times that in the 100% irradiance treatment and 3.9 times that in the 55% irradiance treatment, thus indicating a higher Pro concentration due to irradiance stress. Urena lobata displayed a different trend from A. artemisiifolia in that Pro content increased in leaves subjected to the 55% irradiance level relative to full sunlight, then decreased at the 30% and 10% irradiance levels, reaching the lowest value of 27.0 ug g‑1 FW in the 10% irradiance treatment. Ambrosia artemisiifolia had higher Pro activity than U. lobata in all but the 55% irradiance treatment.
GR content in both A. artemisiifolia and U. lobata increased with increasing irradiance levels (Fig. 2C). The difference between minimum and maximum GR levels in the two species remained at approximately 4.7- to 2.8-fold, respectively. Ambrosia artemisiifolia had a higher GR content than U. lobata under the four irradiance levels, but especially in the 100% irradiance treatment, where the GR content in A. artemisiifolia leaves was 3.7 times greater than that in U. lobata leaves. Higher GR levels for A. artemisiifolia indicate that the enzyme provided more antioxidant protection in response to irradiance in comparison to U. lobata. Relative to full sunlight, the 10% irradiance treatment caused a 78.9% and 64.4% reduction in GR content in A. artemisiifolia and U. lobata leaves, respectively.
Increasing irradiance led to increased levels in TP content in both A. artemisiifolia and U. lobata (Fig. 2D). Under the four irradiance regimes, the TP content in A. artemisiifolia leaves was greater than in U. lobata leaves.
The preference of the exotic invader A. artemisiifolia for open, sunny habitats suggests a sensitivity to light intensity. In low light environments, the growth and reproduction of this species is generally lower than in high light environments, although these plants can tolerate low light conditions and are capable of reproducing (Bassett and Crompton 1975). In high light, warm environments such as the subtropical regions of China, growth and fitness may be favoured because of increased photosynthetic rates and the ability of plants to reduce plant cell membrane damage from light-induced active oxygen species. Consistent with this characterization, we found that A. artemisiifolia plants were more efficient at acclimating to the varying irradiance conditions than the native co-occurring species U. lobata. Based on the quantity of antioxidant enzymes and on the contents measured, this greater ability of A. artemisiifolia to acclimate to a range of irradiance levels was most evident at the highest irradiance level (100%), although acclimation to the lowest (10%) irradiance level was also suggested in several cases.
As a widely distributed enzyme in higher plants, one of the main functions of POD is associated with its role in the cells’ defense enzyme complex, which ensures the detoxification of activated oxygen forms. Higher POD levels have been observed in stress tolerant plant species, in which elevated POD activity protects the plants against oxidative damage (Scalet et al. 1995), whereas such activity has not been observed in sensitive plants (Peters et al. 1989). In our experiment, POD activity increased in both of our target species when subjected to low irradiance conditions, a response likely induced by increased levels of superoxide radicals resulting from a decline in SOD and CAT activity. This increase in POD activity was greater in A. artemisiifolia than in U. lobata, suggesting that A. artemisiifolia may be better able to survive and perform critical physiological functions, even at relatively low irradiance levels.
High SOD activity has been linked with stress tolerance in plants that survive treatments that enhance the production of O2- (Beauchamp and Fridovich 1971; Bowler et al. 1992). Increases in SOD activity has been observed in many plant species that have acclimated to temperature (Mishra et al. 1993), drought (Zhang and Kirkham 1994), or chilling stresses (Liu and Huang 2000). A similar higher SOD activity could be detected in our study in response to increasing irradiance. However, irradiance did not lead to a significant increase in SOD activity in A. artemisiifolia leaves relative to U. lobata leaves, suggesting that SOD may play a minor role in improving tolerance to irradiance stress in A. artemisiifolia plants. The comparatively lower SOD activity of A. artemisiifolia relative to U. lobata at the 55% and 10% irradiance levels does not imply that this exotic invasive species experienced more oxidative stress than the co-occurring native species since upon exposure to light, leaves of A. artemisiifolia exhibited higher activity of CAT enzymes as well as higher Pro, GR and TP contents than U. lobata, which points to specific non-enzymatic routes for the more effective conversion of O2- into H2O2 using antioxidants such as glutathione (GSH), ascorbate and phenol compounds (Asada 1999; Ali et al. 2005). Although the precise mechanism by which the activity of these enzymes is triggered remains to be determined, it might be assumed that CAT and POD enzymes as well as GR and TP contents are of equal importance in the detoxification of H2O2 in A. artemisiifolia leaves. This enhanced protection in A. artemisiifolia may reflect a more efficient antioxidative system given the higher CAT and POD enzyme activity and higher GR and TP contents.
Catalase, which is localized in the peroxisomes of higher plants and functionally protects cells against H2O2-mediated damage, may play a significant role in the defense against oxidative stress since H2O2 can readily diffuse across the membranes (Bowler et al. 1992). Increase in CAT activity supposedly is an adaptive trait that may help overcome photooxidative damage by reducing the toxic levels of hydrogen peroxide produced during cell metabolism (Grace and Logan 1996; Willekens et al. 1997). In our study, the greater CAT activity, especially at the highest irradiance levels measured in A. artemisiifolia leaves compared with U. lobata leaves, suggests a more effective scavenging mechanism to remove highly damaging H2O2 from cells.
The quantity of MDA produced during peroxidation of membrane lipids is often used as an indicator of free radical damage to cell membranes under stress conditions (Premachandra et al. 1992). Therefore, irradiance stress may have resulted in more pronounced deleterious oxidative processes and lipid peroxidation in A. artemisiifolia than in U. lobata. However, accumulation rates of MDA with increasing irradiance in A. artemisiifolia were relatively lower than in U. lobata. From 10% irradiance to full sunlight, the MDA content in A. artemisiifolia increased 1.9-fold while that of U. lobata increased 2.5-fold, suggesting that U. lobata was more likely to suffer more oxidative damage under severe high light stress.
Consistent with other species experiencing environmental stresses (i.e. heat, drought, light), irradiance stress increased MDA content in both A. artemisiifolia and U. lobata, a response that may be attributable to the malfunction of the scavenging system, possibly leading to damage in the main cellular components (Monk et al. 1989). The relatively lower MDA accumulation rates under irradiance stress observed in A. artemisiifolia suggest slower lipid peroxidation development, thus providing more effective protection against oxidative damage since elevated CAT and POD activity as well as higher Pro, GR and TP concentrations were maintained compared with U. lobata.
Proline is generally assumed to serve as a carbon and nitrogen source for rapid recovery from stress and growth, a stabilizer for membranes and some macromolecules, and also a free radical scavenger (Jain et al. 2001). Accumulation of Pro under stress in many plant species has been correlated with stress tolerance, and its concentration has been shown to be generally higher in stress-tolerant plants (Ashraf and Foolad 2007). In our study, A. artemisiifolia accumulated about 7.9-fold and 1.9-fold more Pro than U. lobata at the 10% and 100% irradiance levels, respectively, making it less likely for A. artemisiifolia to be severely affected by low light availability or intense sunflecks. Similar to CAT, GR could also play a role in the control of endogenous hydrogen peroxide through an oxidoreduction cycle involving glutathione and ascorbate (Smith et al. 1989). Reduction in GR activity probably results in a decrease in the levels of reduced glutathione, which is known to be an important factor in preventing oxidative injuries (Alscher 1989). Therefore, the higher levels of GR content with increasing irradiance found in the present study may be helpful in protecting membranes from peroxidation damage by trapping oxygen radicals, especially in A. artemisiifolia.
In summary, irradiance stress (high or low light) induced oxidative injury in A. artemisiifolia and U. lobata plants. Both species exhibited defensive mechanisms under the various stress treatments to protect themselves against free radicals as highlighted by the varying activity of antioxidant enzymes, and the varying MDA, Pro and TP contents. These enhanced defense mechanisms ensured the detoxification of reactive oxygen species such as O2- or H2O2 that may be generated in light-stressed leaves. However, A. artemisiifolia has developed a particularly more efficient antioxidant enzyme system relative to the native species U. lobata that increases the likelihood of survival and continued development of plants experiencing stressful light conditions such as deep shade or full sunlight. In a companion study, Zhong et al. (unpublished) found that A. artemisiifolia performs especially well at high irradiance levels, exhibiting greater plasticity in morphological and photosynthetic traits such as specific leaf area, leaf area ratio and root:shoot ratio than the co-occurring native U. lobata. We applied these results to the current study and obtained support for A. artemisiifolia displaying a greater antioxidative capacity in adapting to an irradiance gradient than a co-occurring native species. These ecophysiological adaptive traits in A. artemisiifolia have likely contributed to the the successful invasion and range expansion of this species in many parts of temperate Europe (Fumanal et al. 2008), and also in subtropical regions such as observed recently in southern China (Wang et al. 2009; Qi et al. 2011). This better understanding of how acclimation to irradiance in A. artemisiifolia may affect its colonizing and invasive success will facilitate the prediction of future invasions and range transformations in relation to the projected climate change and general evolutionary potential of invasive plants (Clements and DiTommaso 2011; Sang et al. 2011).
This research was financially supported by the National Natural Science Foundation of China (No. U1131006, No. 30770403), the Doctoral Fund of the Ministry of Education of China (No. 200805640012, No. 20124404110009). Z. Qin and D.-J. Mao contributed equally to this work. We thank anonymous referees for their valuable comments on the manuscript.
- Ali, M.B., E.J. Hahn, and K.Y. Paek. 2005. Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. Environ. Exp. Bot. 54 : 109-120.
- Alpert, P., E. Bone, and C. Holzapfel. 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect. Plant Ecol. Evol. Syst. 3 : 52-66.
- Alscher, R.G. 1989. Biosynthesis and antioxidant function of glutathione in plants. Physiol. Plant. 77 : 457-464.
- Asada, K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 : 601-639.
- Ashraf, M., and M.R. Foolad. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ. Exp. Bot. 59 : 206-216.
- Bajji, M., J.-M. Kinet, and S. Lutts. 2002. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul. 36 : 61-70.
- Bassett, I.J., and C.W. Crompton. 1975. The biology of Canadian weeds: 11. Ambrosia artemisiifolia L. and A. psilostachya DC. Can. J. Plant Sci. 55 : 463-476.
- Bates, L.S., R.P. Waldren, and I.D. Teare. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39 : 205-207.
- Beauchamp, C., and I. Fridovich. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44 : 276-287.
- Blum, A., and A. Ebercon. 1981. Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci. 21 : 43-47.
- Bowler, C., M.V. Montagu, and D. Inze. 1992. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 : 83-116.
- Chance, B., and A.C. Maehly. 1955. Assay of catalases and peroxidases. Methods Enzymol. 2 : 764-775.
- Chazdon, R.L., and R.W. Pearcy. 1986. Photosynthetic responses to light variation in rainforest species. I. Induction under constant and fluctuating light conditions. Oecologia 69 : 517-523.
- Cheeseman, J.M. 2007. Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 1 : 4-15.
- Clements, D.R., and A. DiTommaso. 2011. Climate change and weed adaptation: can evolution of invasive plants lead to greater range expansion than forecasted? Weed Res. 51 : 227-240.
- Davis, M.A., J.P. Grime, and K. Thompson. 2000. Fluctuating resources in plant communities: a general theory of invasibility. J. Ecol. 88 : 528-534.
- Demmig-Adams, B., and W.W. Adams. 1992. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 : 599-626.
- Feng, Y.L. 2008. Photosynthesis, nitrogen allocation and specific leaf area in invasive Eupatorium adenophorum and native Eupatorium japonicum grown at different irradiances. Physiol. Plant. 133 : 318-326.
- Feng, Y.L., H. Auge, and S.K. Ebeling. 2007. Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153 : 501-510.
- Fumanal, B., C. Girod, G. Fried, F. Bretagnolle, and B. Chauvel. 2008. Can the large ecological amplitude of Ambrosia artemisiifolia explain its invasive success in France? Weed Res. 48 : 349-359.
- Grace, S.C., and B.A. Logan. 1996. Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol. 112 : 1631-1640.
- Heath, R.L., and L. Packer. 1968. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125 : 189-198.
- Hernández, J.A., A. Jiménez, P. Mullineaux, and F. Sevilia. 2000. Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ. 23 : 853-862.
- Jain, M., G. Mathur, S. Koul, and N.B. Sarin. 2001. Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogaea L.). Plant Cell Rep. 20 : 463-468.
- Kartashov, A., N. Radyukina, Y. Ivanov, P. Pahkovskii, N. Shvyakova, and V. Kuznetsov. 2008. Role of antioxidant systems in wild plant adaptation to salt stress. Russ. J. Plant Physiol. 55 : 463-468.
- Li, L., N.H. Li, S.M. Jiang, J.Y. Leng, and X.Q. Wang. 2009. Experiment guidance of plant physiology module. Science Press, Beijing, China.
- Liu, X., and B. Huang. 2000. Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Sci. 40 : 503-510.
- Logan, B., D. Kornyeyev, J. Hardison, and A. Holaday. 2006. The role of antioxidant enzymes in photoprotection. Photosynth. Res. 88 : 119-132.
- Mack, R.N., D. Simberloff, W.M. Lonsdale, H. Evans, M. Clout, and F.A. Bazzaz. 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10 : 689-710.
- McCord, J.M. 2000. The evolution of free radicals and oxidative stress. Am. J. Med. 108 : 652-659.
- Mishra, N.P., R.K. Mishra, and G.S. Singhal. 1993. Changes in the activities of anti-oxidant enzymes during exposure of intact wheat leaves to strong visible light at different temperatures in the presence of protein synthesis inhibitors. Plant Physiol. 102 : 903-910.
- Monk, L.S., K.V. Fagerstedt, and R.M.M. Crawford. 1989. Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Physiol. Plant. 76 : 456-459.
- Pattison, R.R., G. Goldstein, and A. Ares. 1998. Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117 : 449-459.
- Peever, T., and V. Higgins. 1989. Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum. Plant Physiol. 90 : 867-875.
- Peters, J.L., F.J. Castillo, and R.L. Heath. 1989. Alteration of extracellular enzymes in pinto bean leaves upon exposure to air pollutants, ozone and sulfur dioxide. Plant Physiol. 89 : 159-164.
- Poorter, L. 2001. Light-dependent changes in biomass allocation and their importance for growth of rain forest tree species. Funct. Ecol. 15 : 113-123.
- Premachandra, G.S., H. Saneoka, K. Fujita, and S. Ogata. 1992. Leaf water relations, osmotic adjustment, cell membrane stability, epicuticular wax load and growth as affected by increasing water deficits in sorghum. J. Exp. Bot. 43 : 1569-1576.
- Qi, G.J., D.C. Huang, Y. Gao, L. Wang, X.-Y. Shao, J-X. Sun, and L.-H. Lv. 2011. Occurrence and distribution of Ambrosia antemisiifolia [artemisiifolia] and its two natural enemies in Guangdong province. Chin. J. Appl. Entomol. 48 : 197-201.
- Sang, W., X. Liu, and J.C. Axmacher. 2011. Germination and emergence of Ambrosia artemisiifolia L. under changing environmental conditions in China. Plant Species Biol. 26 : 125-133.
- Scalet, M., R. Federico, M.C. Guido, and F. Manes. 1995. Peroxidase activity and polyamine changes in response to ozone and simulated acid rain in Aleppo pine needles. Environ. Exp. Bot. 35 : 417-425.
- Smirnoff, N. 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125 : 27-58.
- Smith, I.K., T.L. Vierheller, and C.A. Thorne. 1989. Properties and functions of glutathione reductase in plants. Physiol. Plant. 77 : 449-456.
- Urquiaga, I., and F. Leighton. 2000. Plant polyphenol antioxidants and oxidative stress. Biol. Res. 33 : 55-64.
- Wan, F.H., and R. Wang. 1990. Overview of biological control of Ambrosia artemisiifolia. Chin. Weed Sci. 4 : 45-48.
- Wang, F., R.J. Wang, P.D. Zhuang, Q. Guo, and Z.-R. Li. 2009. Present status and management strategies of alien invasive plants in Guangdong province. Chin. J. Ecol. 28 : 2088-2093.
- Willekens, H., S. Chamnogpol, M. Davey, M. Schraudner, C. Langebartels, M. Van Montagu, D. Inzé, and W. Van Camp. 1997. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 16 : 4806-4816.
- Williams, D.G., and R.A. Black. 1994. Drought response of a native and introduced Hawaiian grass. Oecologia 97 : 512-519.
- Zeng, X.F., X.D. Lin, H.Y. Qiu, and X.Y. Zhuang. 2009. Investigation on alien plants in E. Guangdong. J. Fujian For. Sci. Tech. 36 : 174-179.
- Zhang, J., and M.B. Kirkham. 1994. Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol. 35 : 785-791.
- Zhang, Y.S., X. Huang, and Y.F. Cheng. 2009. The instructor’s manual for plant physiology. Senior Education Press, Beijing, China.