1. Introduction
Mangroves located at the intertidal zones along tropical and subtropical latitudes are considered to be one of the most valuable and productive coastal ecosystems [1,2]. As unique marine ecosystems, mangrove ecosystems have the four distinct characteristics of high productivity, high return rate, high decomposition rate, and high resistance to extreme weather events and anthropogenic activities [3]. They also provide a variety of significant services, including acting as food sources and shelter for many terrestrial and marine species [4,5], protecting coastal areas from storms and floods [6], purifying the environment [7,8], and many other economic and ecological functions [9,10].
Even though mangroves are increasingly valued, forests are rapidly declining and 40% of the tropical mangroves have ecologically degraded over the last century [11]. Plenty of studies have investigated mangrove extinction due to anthropogenic activities such as aquaculture and urban development [12,13] and environmental changes such as extreme weather events, sea level rise affected by climate change, and plastic and microplastic pollution [14,15,16,17]. This loss causes a serious ecological problem and mangroves need urgent conservation to deal with further increases in climate change, which is expected to have a dramatic effect on coastal areas [18,19].
Mangrove estuaries are seawater mixing zones between freshwater and seawater. As a result, mangroves are subjected to stressful situations such as temperature change, salinity, water mixing, and human activities that cause hydrogen, eutrophication, etc., [20,21,22]. The photosynthesis and antioxidant functions of mangrove plants can be inhibited by low temperature and can even cause death [23]. Excessive salinity can result in an osmotic imbalance in mangrove organisms [24]. Inundation can affect the photosynthesis rate and the reactive oxygen production of mangrove plants [25]. Upwelling is an oceanic process in which deep, cold, saline, and nutrient-rich water is transported to the surface, and it plays an important role in coastal ecosystems [26,27,28]. Mangrove plants distributed at low tide level are frequently exposed to upwelling. The difference between an upwelling and non-upwelling area was examined in the tropical bay of Panama. First, although the air temperature is almost the same, the seawater temperature in the upwelling (25.61 °C) and non-upwelling (28.80 °C) areas was different. Second, the mangrove’s mean daily minimum mud in the upwelling (24.2 ± 0.07 °C) area was lower than that in the non-upwelling (25.6 ± 0.06 °C) area. These small but distinct differences caused a reduction in mangrove egg masses and capsules [29]. The upwelling phenomenon has also been reported in the eastern coast of Hainan Island, Leizhou Peninsula, and the Pearl River Estuary where mangroves are largely distributed [30,31]. In particular, the sea surface temperature in the east of Guangdong was as low as 22 °C during an upwelling event [32]. The studies of upwelling in these areas mainly focused on nutrient enrichment and phytoplankton and zooplankton changes [27,33,34]. There is still a lack of knowledge on the relationship between mangrove growth, distribution, and resistance with an air–sea temperature difference caused by upwelling. Hence, the research into the adaptability of mangrove plants to upwelling will provide a critical theoretical basis for mangrove protection.
Kandelia obovata is not only a dominant mangrove species along the south-eastern coast of China but also an important species for mangrove afforestation [35]. As a pioneer species, K. obovata is mainly distributed at low tide and middle tide zones, where it is frequently subjected to upwelling [36,37]. K. obovata can survive in areas with salinity of up to 27.58‰ [38]. Simultaneously, as a mangrove species successfully introduced to northernmost China, K. obovata can survive in unusually cold regions [39]. In mangrove growth and distribution, temperature is the main constraint. Upwelling has the dual characteristics of low temperature and high salinity. To determine the effect of upwelling on K. obovata seedlings, our study investigated the photosynthetic parameters, oxidative stress markers, and antioxidant system of their leaves in different upwelling temperature. Changes in physiological and biochemical characteristics demonstrated the special response mechanism of K. obovata to upwelling.
2. Materials and Methods
2.1. Seedling Collection and Treatment Conditions
Seedlings of well-developed K. obovata with no pests or diseases and similar length were collected from the nursery of the Qi’ao Island Mangrove Nature Reserve in Guangdong. They were transferred to sandy soil and grown using 1/2 Hoagland’s solution for one month to help the plants adapt to the new environment.
Following one month of acclimation in Hoagland nutrient solution, K. obovata seedlings were divided into three groups; each group contained ten seedlings. The second pair of fresh leaves was taken as the measurement material for each index, and three biological replicates were guaranteed. To simulate the upwelling, these three experimental groups were subject to three different levels of water temperature (25 °C (control), 13 °C, 5 °C) and the same air temperature (25 °C) for 12 h. In addition, the water salinity was maintained at 10‰.
2.2. Determination Method
2.2.1. Determination of Chlorophyll Content and Fluorescence Parameters
Chlorophyll a (Chl a) and chlorophyll b (Chl b) content were detected by spectrophotometry after 95% ethanol extraction [40]. Chlorophyll fluorescence parameters were measured using a fluorometer mini-PAM-Ⅱ (Walz, Germany) [41,42]. The following parameters were measured: ratio of variable and maximal fluorescence (Fv/Fm), effective quantum yield of photosystem Ⅱ (Y(Ⅱ)), electron transport rate (ETR), photochemical quenching coefficient (qP), and non-photochemical quenching coefficient (qN).
2.2.2. Determination of Soluble Sugar and Proline
The soluble protein content was measured by the method of Bradford using BSA as a standard [43]. The soluble sugar content was measured using anthrone colorimetry [44]. The concentration of proline was determined according to the Ninhydrin colorimetry by the assay kit (for plant) purchased from Nanjing Jiancheng Bioengineering Institute (Nanjing, China) [45].
2.2.3. Extraction and Assay of H2O2, MDA, SOD, POD, and CAT
Fresh leaf samples (roughly 1.0 g) were ground using an ice-cold mortar and pestle with 0.05 mol/L Tris hydrochloride buffer (PH 7.8) followed by centrifugation at 3500 rpm and 4 °C for 20 min [46]. The clear supernatant was collected for the measurement of hydrogen peroxide (H2O2), malondialdehyde activity (MDA), superoxide dismutase activity (SOD), peroxidase activity (POD), and catalase activity (CAT) following the instruments of the assay kit (for plant) purchased from Nanjing Jiancheng Bioengineering Institute (Nanjing, China).
The concentration of H2O2 was measured by monitoring the absorbance of the titanium–peroxide complex at 405 nm [47]. Lipid peroxidation was determined as the amount of MDA produced in the thiobarbituric acid (TBA) reaction [48]. The SOD activity was measured at 560 nm by the nitro-blue-tetrazolium (NBT) photoreduction method [49]. The POD activity was assayed at 470 nm using the guaiacol method [22]. The CAT activity was measured based on the hydrolysis reaction of H2O2 with CAT [49].
2.3. Statistical Analyses
Experimental data were presented as the mean ± SD. All data were verified for normality and homogeneity of variances with the Shapiro Wilk and Levene’s test, respectively. A one-way analysis of variance (ANOVA) and Tukey’s post hoc test were carried out to determine the significance of differences in the various leaf response indexes. p < 0.05 was considered a significant difference. The statistical analysis was performed in SPSS (version 18). Principal component analysis (PCA) was performed using Origin, and the variables were standardized to balance their impact on the weighting in the analysis.
3. Results
3.1. Changes in Photosynthetic Pigment and Fluorescence Parameters
The effect of decreasing temperature on the upwelling stress on chlorophyll contents and fluorescence parameters in K. obovata seedlings is shown in Table 1. A significant difference was only found in qN (p < 0.05). Photosynthetic pigments, Y(Ⅱ), ETR, qP, and Fv/Fm values displayed no significant differences among the groups.
3.2. Changes in H2O2 Production and MDA Content
To evaluate the oxidative stress in K. obovata seedlings under upwelling stress, the MDA and H2O2 contents were measured (Figure 1). The content of H2O2 increased significantly under 5 °C upwelling treatment (p < 0.05). Although with no statistical difference, the content of MDA showed a similar trend to H2O2 after the upwelling treatment.
3.3. Changes in Proline and Soluble Sugar Content
The changes in proline and soluble sugar contents in K. obovata seedlings under upwelling stress are shown in Figure 2. Proline content was significantly higher in the 5 °C treatment than in the control (p < 0.05). The content of soluble sugar decreased significantly with the upwelling treatment (p < 0.05), and there was no significant difference between the 13 °C and 5 °C treatments.
3.4. Changes in SOD, POD, and CAT Activity
The anti-oxidant enzymes activity of SOD, POD, and CAT are shown in Figure 3. No significant difference was detected in any of the analyzed parameters.
3.5. Principal Component Analysis (PCA)
A two-dimensional data matrix, where each row corresponded to a sample at a different upwelling temperature and each column corresponded to a response variable, was employed for principal component analysis (PCA). The results of the correlation coefficient (mostly > 0.3) confirmed the adequacy of the dataset for PCA (Figure 4). The PCA generated eight principal components, and the first two principal components with eigenvalues >1 accounted for 66.01% of total variation (Table 2). PC1 explained 47.86% of the total variance. It was most highly correlated with MDA, H2O2, SOD, soluble sugar, Y(Ⅱ), and ETR. PC1 could be described as the oxidative damage factor, which reflected the accumulation and scavenge system of oxidative stress markers. PC2 described 18.15% of the variance, mainly influenced by the chlorophyll contents (Figure 5). PC2 could be described as the photosynthetic efficiency factor, which showed the strength of the photosynthetic capacity.
4. Discussion
4.1. Response of the Photosynthetic System of K. obovata Seedlings to Upwelling
Chlorophyll is a critical biomolecule in photosynthesis, absorbing light and transforming light energy [50]. Previous studies have shown that the chlorophyll content of K. obovata was decreased under abiotic stress, such as low temperature, high salinity, and flooding [51,52,53]. However, in our study, despite the absence of significant differences for Chl a and Chl b content, their contents were increased under treatment (Table 1). As the leaves were exposed to the air temperature (25 °C), and the roots were exposed to low-temperature upwelling directly, this phenomenon might be a type of response strategy to the air–water temperature difference: increasing chlorophyll content to produce more carbon-based defensive chemicals, thus alleviating root stress [54].
Chlorophyll fluorescence analysis technology is often used in plant photosynthesis mechanism and stress resistance physiology [55]. The value of qN significantly increased under treatment. This is similar to a study where the qN value increased in cucumber and sweet pepper at 4 °C temperature exposure [56]. Our result showed that upwelling treatment induced qN and enhanced the photoprotective mechanism. The Fv/Fm values of all the seedlings obtained in this study were close to 0.8, showing that impairment in plant health status did not occur [57]. The values of Y(Ⅱ), ETR, and qP values showed a decrease compared to the control but no significant change. These results demonstrated that the original light energy capture efficiency in the PS Ⅱ reaction center decreased slightly but was still maintained at a regular level [42]. Combining the chlorophyll content changes with chlorophyll fluorescence analysis, the photosynthetic system of K. obovata seedlings was not seriously damaged, and it could be speculated that K. obovata seedlings can adapt to short-term upwelling stress through different energy allocation strategies for roots and leaves.
4.2. Membrane Damage and Oxidative Stress of K. obovata Seedlings under Upwelling
Mangrove subjected to abiotic stress can experience oxidative damage [47]. Changes in the content of MDA and H2O2 in plants are important indicators of oxidative stress. H2O2 is one of the most significant reactive oxygen species (ROS), and its overproduction promotes lipid oxidation and increases MDA content [58,59]. In the present study, MDA and H2O2 content increased under treatment (Figure 1). In addition, the content of H2O2 significantly increased in the 5 °C treatment (p < 0.05). Similar to the research in strawberry seedlings, MDA and H2O2 increased at low temperatures [60]. The results showed that upwelling could induce H2O2 accumulation and, thus, increase MDA content, resulting in cell membrane damage. This indicates that K. obovata seedlings were somewhat damaged by upwelling stress, and the injury increased as the upwelling temperature decreased.
4.3. Response of Antioxidant Mechanisms of K. obovata Seedlings to Upwelling
In order to scavenge excess ROS and alleviate abiotic stress, plants generate antioxidant mechanisms to protect themselves including enzymatic and non-enzymatic antioxidant response systems [61]. In the enzymatic system, SOD converts free O2– radicals to H2O2 and O2, POD and CAT scavenge the accumulated H2O2 to nontoxic levels or form water and O2 [62,63]. In non-enzymatic antioxidant systems, ascorbate, proline, and soluble sugar can reduce the damaging effect of ROS [64].
In the present study, SOD and POD activity showed a slight increase though no significant difference. Interestingly, the opposite change was observed in CAT activity. The CAT activity decreased under upwelling stress, which was consistent with figleaf gourd under low temperature [65]. This phenomenon might be explained by the fact that K. obovata was a chilling-adaptive plant and had a certain adaptability to low temperature upwelling. In addition, the enzymatic systems of POD and CAT have a shifting peak regulation to reduce ROS accumulation [66]. POD mainly functioned in the early stage of stress, while the 12 h upwelling treatment did not reach the response time of CAT. Therefore, POD and CAT showed a different trend in our study. At the same time, the contents of H2O2 and MDA remained at a rather high level. All these findings indicate that the antioxidant enzyme activities could not maintain the balance between ROS production and elimination.
In the non-enzymatic antioxidant systems, proline plays an important role in scavenging ROS, maintaining osmotic pressure balance, and regulating complex metabolic processes [67]. Soluble sugar, as an important metabolite in plants, also helps to increase osmotic pressure, provides energy and substrate, and induces other physiological and biochemical processes [68]. Proline accumulation in plant tissues under abiotic stress conditions leads to osmotic regulation [69], and this is consistent with our results. However, the soluble sugar content significantly decreased under treatment in our study (p < 0.05). This result was different to alfalfa seedlings [70] and broccoli seedlings [71], when exposed to low temperature. The decrease in soluble sugar content might be because the K. obovata seedlings did not respond in time under the short-term stress, so they needed to consume the stored soluble sugar to generate energy to adapt to upwelling stress, which occurred in bamboo and sweet persimmon [72,73]. Another possible reason could be that the roots were directly exposed to upwelling to cause stress; thus, the leaves consumed the stored soluble sugar to enhance the ability to maintain homeostasis. It could be concluded that K. obovata seedlings alleviate upwelling stress by stimulating enzyme activities, producing osmotic adjustment substances, and generating more energy.
4.4. Relationship between Upwelling Treatment and K. obovata Seedling Response
As the stress response mechanism of plants is sophisticated, a multivariate analysis method must be used to evaluate the comprehensive stress response index [74]. In our study, PCA was implemented to further explore the relationship between upwelling treatment and the K. obovata seedlings’ response mechanism. PC1 was mainly correlated with H2O2 and MDA (positively) as well as soluble sugar (negatively). The results indicated that under upwelling stress, excessive H2O2 and MDA were accumulated in the leaves of K. obovata, and soluble sugar was consumed to resist the stress. Oxidative stress markers (MDA and H2O2) were more sensitive to low temperature, which was unanimous with the results of one-way ANOVA (Figure 1). PC2 was principally determined by chlorophyll content (positively), demonstrating that upwelling treatment enhanced photosynthesis to synthesize more energy to resist stress. In the PCA biplot (Figure 5), the samples of the group treated with 5 °C are located on the right of the figure, whereas the control group is located on the left side of the figure. This separation suggests that the upwelling temperature significantly affected the response mechanism of K. obovata. With the decrease in upwelling temperature, the response of K. obovata seedlings was more obvious. Comparatively, chlorophyll content, H2O2, MDA, SOD, POD, Fv/Fm, and qN increased more significantly at low temperatures. The increase in soluble sugar, ETR, Y(Ⅱ), and CAT were more striking at high temperatures. These results might not only be due to the temperature of upwelling but also to the water–air difference especially for the inconsistent trend for soluble sugar and chlorophyll content compared with former studies [75,76]. In conclusion, PCA revealed the effect of different upwelling temperatures on K. obovata seedlings. A lower upwelling temperature caused more intense response on K. obovata seedlings. The oxidative damage factor and photochemical efficiency factor could be used as the main evaluation indexes of the upwelling resistance of K. obovata. These indicators are also in the stress response systems of other mangrove plants, such as Sonneratia apetala, Bruguiera gymnorhiza, and Kandelia candel (L.) Druce [47,77,78].
5. Conclusions
In this study, chlorophyll content, chlorophyll fluorescence parameters (except qN), H2O2 production, MDA content, SOD activity, POD activity, and proline content increased, while CAT activity, qN value, and soluble sugar content decreased in the seedling leaves of K. obovata under short-term upwelling. The lower the upwelling temperature was, the more obvious the changes were.
The results showed that the leaves of K. obovata can enhance photosynthesis by increasing the chlorophyll content and consume stored soluble sugar to produce more organic substances to alleviate the stress of the air–water temperature difference caused by upwelling. When encountering upwelling, H2O2 and MDA accumulation was observed in K. obovata and caused oxidative stress, which would be alleviated by increased antioxidant enzymes (SOD and POD) and osmotic adjustment substances (proline). The PCA results supported the notion that the chlorophyll content, oxidative stress markers, osmotic adjustment substance, and antioxidant enzymes had different responses to low temperature upwelling. As for the limitation of the experimental conditions, our experiments only revealed the stress response of mangroves to short-term upwelling (12 h). Through improving experimental facilities, we will further study the response of mangroves to long-term upwelling stress in order to better explore the resistance mechanisms of mangroves to upwelling.
Conceptualization, M.W., Y.W., J.D. and X.L.; methodology, M.W. and X.L.; software, X.L.; writing—original draft preparation, X.L.; writing—review and editing, M.W.; data curation, X.L.; funding acquisition, M.W. and Y.W. All authors have read and agreed to the published version of the manuscript.
This research was supported by the National Natural Science Foundation of China (31971480), Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (No. GML2019ZD0303) and Innovation Academy of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences (ISEE2019ZR02 and ISEE2018ZD02).
Not applicable.
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The authors declare no conflict of interest.
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Enlarge this image.Figure 1. Effect of upwelling on MDA and H2O2 content in the leaves of K.obovata. (a) MDA, malondialdehyde activity; (b) H2O2, hydrogen peroxide. Values are presented as mean ± SD, and bars with different letters indicate significant differences (p < 0.05).
Enlarge this image.Figure 2. Effect of upwelling on the proline and soluble sugar content in the leaves of K. obovata. (a) Proline; (b) soluble sugar. Values are presented as mean ± SD, and bars with different letters indicate significant differences (p < 0.05).
Enlarge this image.Figure 3. Effect of upwelling on SOD, POD, and CAT activity in the leaves of K. obovata. (a) SOD, superoxide dismutase; (b) POD, peroxidase; and (c) CAT, catalase. Values are presented as mean ± SD, and no significant differences were detected in these parameters (p < 0.05).
Enlarge this image.Figure 4. Matrix of correlation for response indexes of K. obovata seedlings under upwelling. MDA, malondialdehyde activity; H2O2, hydrogen peroxide; POD, peroxidase; CAT, catalase; SOD, superoxide dismutase; Chl a, chlorophyll a; Chl b, chlorophyll b; Fv/Fm, ratio of variable and maximal fluorescence; Y(Ⅱ), effective quantum yield of photosystem Ⅱ; ETR, electron transport rate; qP, photochemical quenching coefficient; qN, non-photochemical quenching coefficient.
Enlarge this image.Figure 5. Principal component analysis biplot for PC1 and PC2. MDA, malondialdehyde activity; H2O2, hydrogen peroxide; POD, peroxidase; CAT, catalase; SOD, superoxide dismutase; Chl a, chlorophyll a; Chl b, chlorophyll b; Fv/Fm, ratio of variable and maximal fluorescence; Y(Ⅱ), effective quantum yield of photosystem Ⅱ; ETR, electron transport rate; qP, photochemical quenching coefficient; qN, non-photochemical quenching coefficient.
Effect of upwelling on chlorophyll contents and fluorescence parameters in the leaves of K. obovata.
| Control | Treated | |||
|---|---|---|---|---|
| 25 °C | 13 °C | 5 °C | p-Value | |
| Photosynthetic pigments, mg/L | ||||
| Chlorophyll a | 7.458 ± 1.045 | 8.358 ± 1.769 | 7.611 ± 1.817 | 0.767 |
| Chlorophyll b | 2.902 ± 0.613 | 3.179 ± 0.584 | 2.856 ± 0.545 | 0.772 |
| Photosynthetic fluorescence parameters | ||||
| Y(Ⅱ) | 0.387 ± 0.047 | 0.348 ± 0.041 | 0.324 ± 0.021 | 0.197 |
| ETR | 70.233 ± 8.451 | 63 ± 7.375 | 58.633 ± 3.88 | 0.193 |
| qP | 0.542 ± 0.061 | 0.542 ± 0.066 | 0.504 ± 0.054 | 0.692 |
| qN | 0.459 ± 0.02 b | 0.659 ± 0.017 a | 0.678 ± 0.041 a | 0.000 |
| Fv/Fm | 0.833 ± 0.003 | 0.842 ± 0.003 | 0.845 ± 0.011 | 0.120 |
Notes: Values are presented as mean ± SD, and bars with different letters indicate significant differences (p < 0.05). Chl a, chlorophyll a; Chl b, chlorophyll b; Fv/Fm, ratio of variable and maximal fluorescence; Y(Ⅱ), effective quantum yield of photosystem Ⅱ; ETR, electron transport rate; qP, photochemical quenching coefficient; qN, non-photochemical quenching coefficient.
Principal component analysis eigenvalues for response indexes of K. obovata seedlings under upwelling.
| PC1 | PC2 | PC3 | |
|---|---|---|---|
| Eigenvalue | 6.700 | 2.541 | 1.875 |
| Proportion % | 47.86 | 18.15 | 13.39 |
| Cumulative % | 47.86 | 66.01 | 79.4 |
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