Introduction
Aluminum (Al) accounts for approximately 8% of the total metal content, which is one of the most abundant metal elements in the crust [1]. Al in soil exists as part of insoluble silicates or Al trioxide, which are generally harmless to plants. Soil acidification (pH < 5.5) increases the solubility of Al and converts it to the trivalent cation form (Al3+), which is highly toxic to organisms [2] and is one of the major factors limiting plant growth and development [3–5]. Micromolar concentrations of Al in soil are sufficient for inducing irreversible toxic symptoms in plants, such as the rapid overproduction of reactive oxygen species, leading to oxidative bursts. The significant decrease in the uptake of water and nutrients due to Al stress can adversely affect plants [6].
Al stress is an important abiotic factor restricting the normal development of plants growing in acidic soil and has become a global problem [7, 8]. In terms of its global distribution, acidic soil (39.5 × 109 hm2) primarily occurs in tropical, subtropical, and temperate regions. In China, acidic soil (total area of 2.03 × 107 hm2) is distributed in 14 provinces and regions, but especially in the southwestern part of the country [6]. Al toxicity, which is a major factor disrupting the growth of plants in acidic soil, has hindered plant growth and agricultural development in areas with acidic soil [9]. In addition, the increase in the frequency of acid rain has accelerated soil acidification, resulting in the activation of a large amount of Al in the soil, which has severely restricted plant growth and development [6, 10].
Photosynthesis, which directly contributes to energy conversion and use, involves a series of complex biochemical reactions that are highly sensitive to metals [11]. The light-dependent reactions produce NADPH, ATP, and oxygen after light energy is absorbed by photosystems II (PSII) and I (PSI) and photosynthetic electron transport and photophosphorylation are initiated [12]. Of these two photosystems, PSII extracts electrons from water to reduce QA, QB, the plastoquinone (PQ) pool, the cytochrome b6f complex, and plastocyanin (PC), whereas PSI oxidizes the reduced PC, which reduces the electron acceptors on the acceptor side of PSI [13, 14]. Changes to any part of this process will alter the electron transport chain, thereby affecting photosynthetic efficiency [14]. The decrease in plant growth and metabolism caused by Al stress is associated with the inhibition of photosynthetic activities due to changes in stomatal conductance, ribulose-1,5-bisphosphate carboxylase/oxygenase activity, and chlorophyll contents [15–17]. Al stress can currently be discovered to dramatically lower the chlorophyll content and net photosynthetic rate (Pn) of plants in a wide variety of plant species, such as tobacco [18], barley [19], maize [20], soybean [21], citrus [22], eucalyptus [23], tea [24]. Al toxicity impaired PSII photochemical activity by blocking electron transport between QA and QB, thus inhibiting photosynthesis in tobacco [18]. Reduced photosynthesis under Al stress is also associated with the inactivation of many chloroplast enzymes, which may be induced by oxidative stress [25]. High Al concentration increased the lipid peroxidation of soybean leaves, decreased cell membrane stability, changed the activity of superoxide dismutase (SOD), and then destroyed the system for detoxifying active oxygen species [21].
A technique that was recently developed for simultaneously measuring prompt chlorophyll fluorescence (PF), delayed chlorophyll fluorescence (DF), and modulated reflection of light at 820 nm (MR820nm) is convenient, flexible, and non-damaging to plants [26, 27]. When the dark reaction gives way to the light reaction, leaves release PF [14]. The subsequent reduction of electron acceptors on the acceptor side of PSII, in the PQ pool, and in the vicinity of PSI is linked to the redox state of the PSII reaction center (RC), which is dependent on PF [14]. When the light reaction gives way to the dark reaction, DF from leaves is produced [13]. This value reflects the recombination between the main electron acceptor QA− reduced by PSII in darkness and the oxidized donor (P680+) [28]. The MR820nm provides information regarding the electron transport mediated by PQ and PSI receptors, thereby indicating the changes in the redox state of PSI RCs and PC [29]. Therefore, the redox reaction of PSI can be analyzed by measuring the light reflection at 820 nm [30, 31]. Concurrent measurements of PF, DF, and MR820nm can yield complementary and parallel data regarding the composition or operation of the photosynthetic machinery [32]. Currently, the techniques have commonly been used in forestry [33], agriculture [34], horticulture [35], and other fields [36].
Rhododendrons are well-known economically valuable ornamental flowers. There are approximately 967 known species of rhododendrons worldwide, including approximately 562 species in China, which is considered to be the country with the richest wild rhododendron resources [37, 38]. In China, rhododendrons are mainly distributed in the southwestern region, in which soil acidification is severe [38]. Rhododendrons can grow well in acidic soil with high Al concentrations, implying they may have evolved complex mechanisms that enable them to effectively cope with Al stress [39]. Due to the different genetic backgrounds, the morphology, traditional use, phytochemistry and pharmacology of different varieties of rhododendrons are very different, which may lead to the great differences in their physiology and biochemistry [40]. In order to examine the alterations in the photosynthetic electron transport chain of rhododendron seedlings exposed to Al stress, we evaluated PF, DF, and MR820nm concurrently in this work of Baijinpao and Kangnaixin, and revealed the changes of photochemical activity of different rhododendrons under Al stress.
Materials and methods
Plant materials and treatment
Experiment 1.
The experimental materials were 21 rhododendron cultivars (S1 Table) from Jiashan United Agricultural Technology Co., Ltd. Rhododendron seedlings were transplanted in red soil (pH 4.48) collected from Gaoligong Mountain in Yunnan province, China and then grown in an artificial climate incubator under the conditions of 25°C 16-h day/18°C 8-h night, relative humidity of 70% (± 5%), and a photosynthetic photon flux density (PPFD) of 600 μmol m−2 s−1. The plants were cultured for 15 days before the Al stress treatment to ensure they were acclimated to the artificial climate incubator conditions and were growing normally. For these cultivars, the seedlings were treated using a completely random design, with six biological replicates. The 12 rhododendron seedlings of each species were randomly divided into two equal groups with 6 seedlings in each group. One group was treated twice a week with 200 ml 0.5 mM AlCl3 solution. The AlCl3 solution was in ultrapure water. The other group (control) was treated with same solution without AlCl3. All seedlings were watered as needed with tap water the rest of the time to prevent drought stress.
Experiment 2.
Rhododendron hybridum cv. Kangnaixin and cv. Baijinpao were selected for further experiments. For both cultivars, the seedlings were treated using a completely random design, with six biological replicates. The 24 rhododendron seedlings of each species were randomly divided into two equal groups with 12 seedlings in each group. The remaining conditions were the same as those in the experiment 1.
Determination of leaf gas exchange parameter
For the analysis of gas exchange parameters, leaves were chosen from each seedling starting from the first fully unfolded leaf from top to bottom. The Li-6400 XT portable photosynthetic measurement system (LI-COR, Lincoln, USA) with a fluorescence fluorometer (6400–40 leaf chamber) was utilized for this purpose. The CO2 concentration was set at 400 μmol mol−1, the chamber temperature was set to 25°C, the leaf area was set to 2cm2, and the PPFD and gas flow rate were set to 800 μmol mol−1 and 300 μmol m−2 s−1 respectively [22, 35]. On days 0, 7, 14, and 21 after the Al stress treatment, the determination was performed.
Simultaneous measurement of PF, DF, and MR820nm
The Multifunctional Plant Efficiency Analyzer (M-PEA; Hansatech Instruments, Pentney, UK) was utilized for the simultaneous measurement of the leaf PF, DF, and MR820nm.
On days 0, 7, 14, and 21 after the Al stress treatment, leaves were treated in darkness for 30 min before the analysis. The actinic light LED provide homogeneous illumination with an intensity of 5000 μmol photons m−2 s−1 for 60s. MR820 nm was measured separately with far-red light of 1000μmol photons m−2 s−1. For the simultaneous measurements, the light–dark transition was completed at 300 μs after the exposure, with PF and MR820nm signals recorded under light and then DF signals recorded in darkness. The wavelengths were 627±10 nm for the actinic light LED, 820±25 nm for the modulated light LED and 735±15 nm for the far-red light LED [14, 33]. Data were recorded with a variable rate: every 0.01ms from 0.01 to 0.3 ms, every 0.1ms from 0.3 to 3 ms, every 1 ms from 3 to 30 ms, every 10 ms from 30 to 300 ms, every 100 ms from 300 to 1000 ms [14, 33].
Fluorescence parameters were collected using the M-PEA. The parameters involved include the following: maximum quantum yield (at t = 0) for primary photochemistry (ϕPo), quantum yield (at t = 0) of energy dissipation (ϕDo), quantum yield (at t = 0) of electron transport (ϕEo), probability (at t = 0) that a trapped exciton moves an electron into the electron transport chain beyond QA-(ΨEo), absorption flux (of antenna Chls) per RC (ABS/CSm), trapped energy flux (leading to QA reduction) per RC (TRo/CSm), electron transport flux (further than QA−) per RC (ETo/CSm), total energy dissipated per reaction center (RC) (DIo/CSm), the efficiency of an electron beyond that reduced PSI acceptors (δRo), performance index for energy conservation from exciton to the reduction of PSI end acceptors (PItotal), performance index on an absorption basis (PIABS).
Statistical analysis
A two-factor analysis of variance (variety and Al stress treatment duration) was used. Using Duncan’s methods to analyze the significant difference among multiple sample groups. Data are herein provided as the average of six replicates ± standard error (SE). All data were processed and analyzed using SPSS 22.0 (IBM, Armonk, USA), with the default threshold for significance set at α = 0.05. The Origin 9.0 (Northampton, MA, USA) program was used for visualizing data.
Results
After 21 days of Al stress, the net photosynthetic rate (Pn) of was decreased in 21 rhododendron cultivars (Fig 1). The lines Kangnaixin and Wusedaqiao were the most tolerant cultivar, while the lines Juanzhiwu, Wangyue and Baijinpao were the most sensitive cultivar. Based on this result, we selected Baijinpao as an Al-sensitive rhododendron and Kangnaixin as an Al-resistant rhododendron for subsequent experiments.
[Figure omitted. See PDF.]
After 21 days of stress, Pn decreased by 38.5% in Baijinpao, whereas it did not decrease significantly in Kangnaixin. In Baijinpao and Kangnaixin, stomatal conductance (Gs) decreased significantly (by 34.45% and 20.58%, respectively), whereas intercellular CO2 concentration (Ci) increased significantly (by 32.68% and 12.24%, respectively) (Fig 2).
[Figure omitted. See PDF.]
(A). Pn, net photosynthetic rate; (B). Gs, stomatal conductance; (C). Ci, intercellular CO2 concentration. Duncan’s test was used to compare the changes between eight treatment combinations (two rhododendron cultivars × four Al treatment durations). Lowercase letters indicate P < 0.05.
During the Al stress treatment, the fluorescence intensity of the rhododendron leaves initially increased and then decreased, with typical O, J, I, and P points and the OJIP transient (Fig 3A and 3D). As the treatment time increased, the I and P points of Kangnaixin gradually decreased, and more significantly decreases were detected in the O, J, I, and P points of Baijinpao (Fig 3A and 3D).
[Figure omitted. See PDF.]
(A–C): Baijinpao. (D–F): Kangnaixin. (A and D): OJIP curves for the Al stress treatment period. (B and E): Vop = (Ft − Fo)/(Fm − Fo). (C and F): ΔVop = Vt (treatment) − Vop (control). Fo: initial fluorescence intensity when all reaction centers are fully open; FK/ FJ/ FI: fluorescence intensity at 300 μs/ 2 ms/ 30 ms; Fm: maximum fluorescence intensity.
After the OJIP data were normalized, the J, I, and P points of Baijinpao clearly increased, whereas obvious increases were detected for only the J and I points of Kangnaixin after 21 days of aluminum stress (Fig 3B and 3E). To facilitate the comparison, the OJIP curves were standardized (Fig 3C and 3F). The 21-day treatment of rhododendron seedlings with Al stress resulted in a significant increase in ΔVt (Fig 3C and 3F). The O to J and O to K points of the OJIP curve were normalized and the differences were calculated to obtain the L-band (Fig 4A and 4B) and K-band (Fig 4C and 4D). After 21 days under Al stress conditions, the K-band increased significantly. The response of Baijinpao to Al stress was significantly greater than that of Kangnaixin (Fig 4C and 4D). The L-band of Baijinpao increased, while that of Kangnaixin decreased (Fig 4A and 4B). After 21 days of the Al stress treatment, ϕPo, ϕEo, and ΨEo of Baijinpao decreased by 6.9%, 23.7%, and 20.1%, respectively, whereas ϕDo increased by 14.8% (Fig 5). For Kangnaixin, ϕPo and ϕDo did not change significantly, but ϕEo and ΨEo decreased by 12.9% and 12.4%, respectively (Fig 5). Compared with the control levels (0d), after 21 days of Al stress, ABS/CSm, TRo/CSm, and ETo/CSm of Baijinpao decreased by 7.2%, 6.7%, and 15.5%, respectively, but DIo/CSm increased by 32.2% (Fig 6). For Kangnaixin, DIo/CSm increased significantly by 32.2%, whereas others did not change significantly, (Fig 6). After the 21-day Al stress treatment, δRo, PItotal, and PIABS decreased in Baijinpao (by 13.2%, 68.3%, and 74.8%, respectively) and Kangnaixin (by 15.7%, 45.9%, and 55.8%, respectively) (Fig 7).
[Figure omitted. See PDF.]
Changes in the L-band and K-band of Baijinpao (left) and Kangnaixin (right) under Al stress conditions. (A and B): VOK = (Ft − Fo)/(FK − Fo); ΔVOK = VOK (treatment) − VOK (control). (C and D): VOJ = (Ft − Fo)/(FJ − Fo); ΔVOJ = VOJ (treatment) − VOJ (control).
[Figure omitted. See PDF.]
(A). ϕPo: Maximum quantum yield for primary photochemistry; (B). ϕDo: Quantum yield of energy dissipation; (C). ϕEo: Quantum yield of electron transport; (D). ΨEo: Probability that a trapped exciton moves an electron into the electron transport chain beyond QA-. Duncan’s test was used to compare the changes between eight treatment combinations (two rhododendron cultivars × four Al treatment durations). Lowercase letters indicate P < 0.05.
[Figure omitted. See PDF.]
(A). ABS/CSm, absorption flux (of antenna Chls) per RC; (B). TRo/CSm: trapped energy flux (leading to QA reduction) per RC; (C). ETo/CSm: electron transport flux (further than QA−) per RC; (D). DIo/CSm:,total energy dissipated per reaction center (RC). Duncan’s test was used to compare the changes between eight treatment combinations (two rhododendron cultivars × four Al treatment durations). Lowercase letters indicate P < 0.05.
[Figure omitted. See PDF.]
(A). δRo, the efficiency of an electron beyond that reduced PSI acceptors; (B). PItotal, the performance index for energy conservation from exciton to the reduction of PSI end acceptors; (C). PIABS: the performance index on an absorption basis. Duncan’s test was used to compare the changes between eight treatment combinations (two rhododendron cultivars × four Al treatment durations). Lowercase letters indicate P < 0.05.
At 21 days after the Al stress treatment, there were changes in the MR820nm curve of the rhododendron, with a slight decrease in the lowest point (Fig 8A and 8B). As the treatment period progressed, the maximum slope of decrease in the MR/MR0 transient (Vox) increased, whereas the maximum slope of increase in the MR/MR0 transient (Vred) decreased (Fig 8C and 8D). At 21 days after starting the Al stress treatment, Vox increased by 16.8% and 11.2% for Baijinpao and Kangnaixin, respectively. Conversely, Vred decreased by 50.4% and 26% for Baijinpao and Kangnaixin, respectively (Fig 8C and 8D).
[Figure omitted. See PDF.]
(A/B): Effect of Al treatment on the MR820nm curves of Baijinpao/Kangnaixin. (C): Vox, oxidation rate of PSI. (D): Vred, PSI reduction rate. Duncan’s test was used to compare the changes between eight treatment combinations (two rhododendron cultivars × four Al treatment durations). Lowercase letters indicate P < 0.05.
The construction of DF induction curves was based on the fluorescence signals measured at 20 μs (Fig 9A and 9B). Significant changes in the DF curves of the rhododendron seedlings were detected after 21 days of the Al stress treatment. There were significant decreases at the I1 point for Baijinpao and Kangnaixin, and the I2 point for Baijinpao also decreased (Fig 9A and 9B). Both I1/I2 and (I1 − D2)/D2 decreased significantly as the Al stress treatment progressed. After 21 days under Al stress conditions, I1/I2 and (I1 − D2)/D2 of Baijinpao decreased by 24.34% and 29.2%, respectively, which were larger than the corresponding decreases observed in Kangnaixin (by 15.15% and 19%, respectively) (Fig 9C and 9D).
[Figure omitted. See PDF.]
(A): Effects of Al stress on the DF curves of Baijinpao. (B): Effects of Al stress on the DF curves of Kangnaixin; I1: maximum value; I2: second peak value; D2: minimum value. Duncan’s test was used to compare the changes between eight treatment combinations (two rhododendron cultivars × four Al treatment durations). Lowercase letters indicate P < 0.05.
Discussion
In our study, Al stress treatment decreased Pn and Gs, but increased Ci, in both rhododendron cultivars (Fig 2), suggesting that the decline in Pn was caused by a non-stomatal factor [22, 41], which aligns with previous studies conducted on eucalyptus and citrus plants [23]. In addition, the Al stress-induced decrease in Pn was more significant in Baijinpao than in Kangnaixin, which indicated that Kangnaixin is more resistant to Al than Baijinpao.
When light irradiates the leaves of plants, the intensity of fluorescence emitted rises from the lowest point (O-point) to the highest point (P-point), which can be divided into three stages (O-J, J-I, and I-P) [42]. These phases can reflect the three different reduction processes in the electron transport chain [43]. There were obvious changes in the OJIP curve (Fig 3) as the Al stress treatment time increased, especially at 21 days, with the entire photosynthetic electron transport chain in the rhododendron seedlings damaged. After normalizing the OJIP data, we detected an increase of the J-point, but a decrease of the P-point, in both cultivars. Recent studies have demonstrated that an increase in the J-point may be due to a decrease in the electron transport efficiency at QA, while a decrease in the P-point may be due to an increase in the non-radiative dissipation of PSII antenna pigments, a decrease in antenna pigment contents, a decrease in the PSII RC activities, damages to the PSI receptor side, or the denaturation and degradation of chlorophyll proteins [44]. In addition, an increase in the K-band may reflect the photoinhibition of PSII donors, which has been widely used as a specific indicator of the degradation of the oxygen-evolving complex (OEC) [45]. The increase of K band can be observed under many abiotic stresses [46, 47]. In the current study, the K-band increased during the Al stress treatment of both rhododendron cultivars, indicative of the Al stress induced OEC damage of PSII, ultimately resulting in decreased electron transport on the donor side of PSII. The increase of K-band was greater for Baijinpao than for Kangnaixin, indicating the donor-side electron transfer was weaker in Baijinpao than in Kangnaixin. The L-band reflects the energy connectivity among PSII units or between the antenna and the PSII RCs, with an increase in the connectivity indicative of an increase in damage [48, 49]. At 21 days after starting the Al stress treatment, the L-band of Baijinpao and Kangnaixin increased and decreased significantly, respectively (Fig 4), indicating the greater damage to PSII in Baijinpao than in Kangnaixin (Fig 4A, 4B).
The ϕPo, ϕEo, ΨEo, and ϕDo parameters are related to the energy allocation ratio. The ϕPo indicates the PSII RC’s capacity to absorb photons and then collect energy [49]. The significant decreases in ϕEo and ΨEo indicate that Al stress inhibited the transfer of photosynthetic electrons beyond QA (Fig 5) [50]. Additionally, ABS/CSm, TRo/CSm, ETo/CSm, and DIo/CSm are associated with energy distribution per unit cross-sectional area and RC density [32, 51]. As the Al stress treatment proceeded, ABS/CSm, TRo/CSm, and ETo/CSm decreased significantly in Baijinpao. However, a significant increase in DIo/CSm was detected for both rhododendron cultivars (Fig 6). Earlier studies indicated that stress-induced decreases in ABS/CSm, TRo/CSm, and ETo/CSm may be associated with the degradation or deactivation of RCs, possibly as part of a mechanism protecting plants from stress [52, 53]. The RC-associated activation of the defense mechanism that leads to the dissipation of excess excitation energy in leaves in a timely manner, which is indicated by an increase in DIo/CSm, helps to minimize the damage to plants [48]. A recent study confirmed δRo is a semi-quantitative index useful for determining the relative change in PSI [14]. In this study, δRo decreased significantly in response to Al stress treatment of the two rhododendron cultivars, implying the exposure to Al stress destroys photochemical activity of PSI. Furthermore, PItotal has been used to indicate the overall activity of PSII, PSI, and the intersystem electron transport chain, whereas PIABS has been used to reflect the functional activity of PSII based on ABS absorption [54, 55]. In this study, both PItotal and PIABS decreased significantly, and the decrease Baijinpao was more significant than Kangnaixin, indicating that Al stress inhibited the overall activity of PSII, PSI, and the intersystem electron transport chain more in Baijinpao than in Kangnaixin (Fig 7).
Changes in MR820nm represent alterations to the redox state of PC and P700 [36, 56, 57]. Therefore, measuring MR820nm signals can fill in some of the “blind spots” associated with PF measurements [26, 56]. The MR820nm analysis indicated that in response to an increase in the duration of the Al stress treatment, the later the lowest point of the MR/MR0 curve for the two rhododendron cultivars occurred, the Vox increased, and the Vred decreased. Vox can be used to evaluate the activity of PSI, Vred can be used to evaluate the cyclic electron transport activity [58]. Under Al stress, the increase in Vox meant that the oxidation rate of PC and P700 increased. The decrease in Vred meant that the re-reduction rates of P700+ and PC+ decreased, which was related to the suppression of PSI, possibly because an insufficient number of electrons were transferred to PSI during the Al stress treatment [33, 36]. In addition, after Al stress, compared with Kangnaixin, the Vox of Baijinpao had no significantly change, while the Vred of Baijinpao was significantly decreased (Fig 8). This showed that compared with Kangnaixin, the oxidation rate of PC and P700 of Baijinpao was not much different, while the re-reduction rate of PC+ and P700+ of Baijinpao is slower. Thus, under Al stress, the cyclic electron transport activity of Kangnaixin was higher and showed faster cyclic electron transport around PSI. High cyclic electron transport activity can protects PSII from excess light by producing ΔpH, which is necessary to form non-photochemical quenching [59], and may also maintain the Calvin cycle by balancing ATP/NADPH [60]. These may be the reasons why Kangnaixin has a stronger Al tolerance.
The DF induction kinetics of the two rhododendron cultivars were significantly affected by Al stress (Fig 9). The I1 point of DF is related to the increase of the transmembrane potential of the thylakoid membrane and the accumulation of the luminescent group Z+P680QAQB− caused by PSI oxidation [61, 62]. The appearance of I2 is related to the accumulation of Z+P680QA−QB− during the reduction of PQ [63]. The I1/I2 ratio is related to the electron transport capacity of the donor side of PSII [14, 64]. (I1−D2) /D2 changes are similar to I1/I2, which reflects the electron transfer rate on the acceptor side of PSII [63, 64]. In the current study, I1 and I1/I2 of both cultivars decreased significantly, indicating the decrease in the electron transport capacity of the PSII donor side. Additionally, the significant decrease in the (I1 − D2)/D2 value may be related to the loss of PSII activity and the functional impairment of PSI. The changes of curve and the decreases of parameters in the DF kinetic were more obvious for Baijinpao than for Kangnaixin, suggesting the electron transport in Baijinpao than in Kangnaixin under Al stress conditions was more severely damaged.
In conclusion, in this study, the Pn and Gs rhododendron leaves were decreased and Ci was increased under Al stress, indicating that the photosynthetic performance of leaves was decreased by non-stomatal factors. Changes in the L-band and K-band and decreases in (I1−D2) /D2 and I1/I2 indicated that the electron transfer rate on the PSII acceptor side was inhibited. The δRo was significantly decreased, which indicated that the photochemical activity of PSI was destroyed by Al stress. The results of MR820 showed that under Al stress, the oxidation rate of PC and P700 increased, and the re-reduction rate of P700+ and PC+ decreased. Compared with Kangnaixin, the Pn of Baijinpao decreased more significantly, the donor-side electron transfer efficiency was inhibited more seriously, and the overall functional activity of PSII, PSI and intersystem electron transfer chain was damaged more seriously under Al stress. Therefore, Kangnaixin performed better than Baijinpao under Al stress and had a higher tolerance to Al.
Supporting information
S1 Table. Rhododendron cultivars used in experiments.
https://doi.org/10.1371/journal.pone.0305133.s001
(XLSX)
Citation: Zhang J, Xu Y, Lu K, Gong Z, Weng Z, Shu P, et al. (2024) Differences in gas exchange, chlorophyll fluorescence, and modulated reflection of light at 820 nm between two rhododendron cultivars under aluminum stress conditions. PLoS ONE 19(6): e0305133. https://doi.org/10.1371/journal.pone.0305133
About the Authors:
Jing Zhang
Contributed equally to this work with: Jing Zhang, Yanxia Xu
Roles: Conceptualization, Data curation, Methodology, Writing – original draft, Writing – review & editing
Affiliation: Jiyang College, Zhejiang A&F University, Zhuji, China
Yanxia Xu
Contributed equally to this work with: Jing Zhang, Yanxia Xu
Roles: Conceptualization, Writing – review & editing
Affiliation: Jiyang College, Zhejiang A&F University, Zhuji, China
Kaixing Lu
Roles: Methodology
Affiliation: Ningbo Key Laboratory of Agricultural Germplasm Resources Mining and Environmental Regulation, College of Science and Technology, Ningbo University, Ningbo, China
Zhengyu Gong
Roles: Resources
Affiliation: Ecological Forestry Development Center of Suichang County, Suichang, China
Zhenming Weng
Roles: Resources
Affiliation: Ecological Forestry Development Center of Suichang County, Suichang, China
Pengzhou Shu
Roles: Software
Affiliation: Jiyang College, Zhejiang A&F University, Zhuji, China
Yujia Chen
Roles: Software
Affiliation: Jiyang College, Zhejiang A&F University, Zhuji, China
Songheng Jin
Roles: Funding acquisition
Affiliation: Jiyang College, Zhejiang A&F University, Zhuji, China
Xueqin Li
Roles: Conceptualization, Data curation, Methodology, Writing – original draft, Writing – review & editing
E-mail: [email protected]
Affiliation: Jiyang College, Zhejiang A&F University, Zhuji, China
ORICD: https://orcid.org/0009-0007-7848-8244
[/RAW_REF_TEXT]
1. Chandra J, Keshavkant S. Mechanisms underlying the phytotoxicity and genotoxicity of aluminum and their alleviation strategies: A review. Chemosphere. 2021;278:130384. pmid:33819888
2. Rengel Z. Aluminium cycling in the soil-plant-animal-human continuum. Biometals. 2004;17(6):669–89. pmid:15689110
3. Muhammad N, Zvobgo G, Zhang GP. A review: The beneficial effects and possible mechanisms of aluminum on plant growth in acidic soil. J Integr Agric. 2019;18(7):1518–28.
4. Yao H, Zhang S, Zhou W, Liu Y, Liu Y, Wu Y. The effects of exogenous malic acid in relieving aluminum toxicity in Pinus massoniana. Int J Phytorem. 2020;22(6):669–678. pmid:32138521
5. Zhang Z, Liu D, Meng H, Li S, Wang S, Xiao Z, et al. Magnesium alleviates aluminum toxicity by promoting polar auxin transport and distribution and root alkalization in the root apex in populus. Plant Soil. 2020;448(1):565–585.
6. Chauhan DK, Yadav V, Vaculík M, Gassmann W, Pike S, Arif N, et al. Aluminum toxicity and aluminum stress-induced physiological tolerance responses in higher plants. Crit Rev Biotechnol. 2021;41(5):715–730. pmid:33866893
7. Duan L, Chen X, Ma X, Zhao B, Larssen T, Wang S, et al. Atmospheric S and N deposition relates to increasing riverine transport of S and N in southwest China: Implications for soil acidification. Environ Pollut. 2016;218:1191–1199. pmid:27589892
8. Tao L, Li FB, Liu CS, Feng XH, Gu LL, Wang BR, et al. Mitigation of soil acidification through changes in soil mineralogy due to long-term fertilization in southern China. CATENA. 2019;174:227–234.
9. Kopittke PM. Role of phytohormones in aluminium rhizotoxicity. Plant Cell Environ. 2016;39(10):2319–2328. pmid:27352002
10. Ling Y, Liu HY, Zhang XT, Wei SQ. Characteristics of typical soils acidification and effects of heavy metal speciation and availability in Southwest China. Environmental Science. 2023;441:376–386. pmid:36635825
11. Su C, Jiang Y, Yang Y, Zhang W, Xu Q. Responses of duckweed (Lemna minor L.) to aluminum stress: Physiological and proteomics analyses. Ecotoxicol Environ Saf. 2019;170:127–140. pmid:30529611
12. Zhang WT, Li PM. Application of simultaneous measurements of instantaneous and delayed chlorophyll fluorescence and 820 nm light reflection dynamics in photosynthesis studies. Acta Biophysica Sinica. 2015;31(3):221–229.
13. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta. 2010;1797(6–7):1313–1326. pmid:20226756
14. Wang J, Liu Y, Xu Y, Chen W, Han Y, Wang GG, et al. Sexual differences in gas exchange and chlorophyll fluorescence of Torreya grandis under drought stress. Trees. 2021;36(1):283–294.
15. Rahman MA, Lee SH, Ji HC, Kabir AH, Jones CS, Lee KW. Importance of Mineral Nutrition for Mitigating Aluminum Toxicity in Plants on Acidic Soils: Current Status and Opportunities. Int J Mol Sci. 2018;19(10). pmid:30297682
16. He H, Li Y, He LF. Aluminum toxicity and tolerance in Solanaceae plants. S Afr J Bot. 2019;123:23–29.
17. Vasconcelos CV, Costa AC, Muller C, Castoldi G, Costa AM, de Paula Barbosa K, et al. Potential of calcium nitrate to mitigate the aluminum toxicity in Phaseolus vulgaris: effects on morphoanatomical traits, mineral nutrition and photosynthesis. Ecotoxicology. 2020;29(2):203–16. pmid:32006192
18. Li Z, Xing F, Xing D. Characterization of target site of aluminum phytotoxicity in photosynthetic electron transport by fluorescence techniques in tobacco leaves. Plant Cell Physiol. 2012;53(7):1295–1309. pmid:22611177
19. Dawood M, Cao F, Jahangir MM, Zhang G, Wu F. Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater. 2012;209–210:121–128. pmid:22281027
20. Zhao X, Chen Q, Wang Y, Shen Z, Shen W, Xu X. Hydrogen-rich water induces aluminum tolerance in maize seedlings by enhancing antioxidant capacities and nutrient homeostasis. Ecotoxicol Environ Saf. 2017;144:369–379. pmid:28647604
21. Zhang XB, Liu P, Yang YS, Xu GD. Effect of Al in soil on photosynthesis and related morphological and physiological characteristics of two soybean genotypes. Botanical Studies. 2007; 48: 435–444.
22. Guo P, Qi YP, Cai YT, Yang TY, Yang LT, Huang ZR, et al. Aluminum effects on photosynthesis, reactive oxygen species and methylglyoxal detoxification in two Citrus species differing in aluminum tolerance. Tree Physiol. 2018;38(10):1548–1565. pmid:29718474
23. Yang M, Tan L, Xu Y, Zhao Y, Cheng F, Ye S, et al. Effect of low pH and aluminum toxicity on the photosynthetic characteristics of different fast-growing Eucalyptus vegetatively propagated clones. PLoS One. 2015;10(6):e0130963. pmid:26090998
24. Mukhopadyay M, Bantawa P, Das A, Sarkar B, Bera B, Ghosh P, et al. Changes of growth, photosynthesis and alteration of leaf antioxidative defence system of tea [Camellia sinensis (L.) O. Kuntze] seedlings under aluminum stress. Biometals. 2012;25(6):1141–1154. pmid:22850809
25. Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PB. Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol. 2004;161(1):63–68. pmid:15002665
26. Gao J, Li P, Ma F, Goltsev V. Photosynthetic performance during leaf expansion in Malus micromalus probed by chlorophyll a fluorescence and modulated 820nm reflection. J Photochem Photobiol B. 2014;137:144–150. pmid:24373888
27. Kar S, Montague DT, Villanueva-Morales A. Measurement of photosynthesis in excised leaves of ornamental trees: a novel method to estimate leaf level drought tolerance and increase experimental sample size. Trees. 2021;35(3):889–905.
28. Zhou R, Kan X, Chen J, Hua H, Li Y, Ren J, et al. Drought-induced changes in photosynthetic electron transport in maize probed by prompt fluorescence, delayed fluorescence, P700 and cyclic electron flow signals. Exp. Bot. 2019;158:51–62.
29. Schansker G, Srivastava A, Strasser RJ. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol. 2003;30(7):785–796. pmid:32689062
30. Duan Y, Zhang M, Gao J, Li P, Goltsev V, Ma F. Thermotolerance of apple tree leaves probed by chlorophyll a fluorescence and modulated 820nm reflection during seasonal shift. J Photochem Photobiol. B, Biol. 2015;152. pmid:26298695
31. Yang XQ, Zhang QS, Zhang D, Sheng ZT. Light intensity dependent photosynthetic electron transport in eelgrass (Zostera marina L.). Plant Physiol Biochem. 2017;113:168–176. pmid:28236752
32. Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, et al. Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol. 2016;63(6):869–893.
33. Shen J, Li X, Zhu X, Ding Z, Huang X, Chen X, et al. Molecular and photosynthetic performance in the yellow leaf mutant of Torreya grandis according to transcriptome sequencing, chlorophyll a fluorescence, and modulated 820 nm reflection. Cells. 2022;11(3). pmid:35159241
34. Chen W, Jia B, Chen J, Feng Y, Li Y, Chen M, et al. Effects of different planting densities on photosynthesis in maize determined via prompt fluorescence, delayed fluorescence and p700 signals. Plants (Basel). 2021;10(2). pmid:33572625
35. Dabrowski P, Baczewska-Dabrowska AH, Kalaji HM, Goltsev V, Paunov M, Rapacz M, et al. Exploration of chlorophyll a fluorescence and plant gas exchange parameters as indicators of drought tolerance in perennial ryegrass. Sensors (Basel). 2019;19(12). pmid:31216685
36. Guo Y, Lu Y, Goltsev V, Strasser RJ, Kalaji HM, Wang H, et al. Comparative effect of tenuazonic acid, diuron, bentazone, dibromothymoquinone and methyl viologen on the kinetics of Chl a fluorescence rise OJIP and the MR(820) signal. Plant Physiol Biochem. 2020;156:39–48. pmid:32906020
37. Zhu CY. The resources and landscaping applications in Rhododendron (Thesis). Zhejiang University; 2008.
38. Ma QH, Zhang KL. Progresses and prospects of the research on soil erosion in Karst area of Southwest China. Advances in Earth Science. 2018;33(11):1130–1141.
39. Xu YX, Lei YS, Huang SX, Zhang J, Wan ZY, Zhu XT, et al. Combined de novo transcriptomic and physiological analyses reveal RyALS3-mediated aluminum tolerance in Rhododendron yunnanense Franch. Front Plant Sci. 2022;13. pmid:36035662
40. Liu XJ, Su HG, Peng XR, Bi HC, Qiu MH. An updated review of the genus Rhododendron since 2010: Traditional uses, phytochemistry, and pharmacology. Phytochemistry. 2024;217:113899. pmid:37866447
41. Sex-specific physiological and growth responses to elevated atmospheric CO2 in Silene latifolia Poiret. Glob Chang Biol. 2003;9(4):612–618.
42. Stirbet A, Govindjee . Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res. 2012;113(1–3):15–61. pmid:22810945
43. Qi Y, Zhang Q, Hu SJ, Wang RY, Yang Y, Lei J, et al. Response of photosynthetic parameters to leaf temperature of spring maize under drought stress. J Arid Environ. 2023;41(2):215–222.
44. Zhang Z, Li G, Gao H, Zhang L, Yang C, Liu P, et al. Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence Zea mays L. inbred lines. PLoS One. 2012;7(8):e42936. pmid:22900069
45. Li P, Cheng L, Gao H, Jiang C, Peng T. Heterogeneous behavior of PSII in soybean (Glycine max) leaves with identical PSII photochemistry efficiency under different high temperature treatments. J Plant Physiol. 2009;166(15):1607–1615. pmid:19473728
46. Kalaji H, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska I, et al. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum. 2016;2016:102. pmid:38288405
47. Konôpková A, Kurjak D, Kmeť J, Klumpp R, Longauer R, Ditmarová Ľ, et al. Differences in photochemistry and response to heat stress between silver fir (Abies alba Mill.) provenances. Trees. 2017;32(1):73–86.
48. Tsimilli-Michael M, Strasser R. In vivo assessment of stress impact on plant’s vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. Mycorrhiza. 2008;p679–703.
49. Zhang B, Zhang H, Lu D, Cheng L, Li J. Effects of biofertilizers on the growth, leaf physiological indices and chlorophyll fluorescence response of spinach seedlings. PloS one. 2023;18(12):e0294349. pmid:38096260
50. Kumar D, Singh H, Raj S, Soni V. Chlorophyll a fluorescence kinetics of mung bean (Vigna radiata L.) grown under artificial continuous light. Biochem Biophys Rep. 2020;24:100813. pmid:32984559
51. Pan XD, Wang JW, Hu Y, Chi Y, Jin SH. Physiological and biochemical responses of leaves of four Rhododendron cultivars under heat stress. Molecular Plant Breeding. 2022;20(20):6877–6884.
52. Huang JL, Wang Y. Effects of soil water stress on fast chlorophyll fluorescence induction of pistacia weinmannif olia. Acta Bot Boreal-Occident Sin. 2015;35(12):2505–2512.
53. Zhang K, Chen BH, Hao Y, Yang R, Wang YA. Effects of short-term heat stress on PSII and subsequent recovery for senescent leaves of Vitis vinifera L. cv. Red Globe. J Integr Agric. 2018;17(12):2683–2693.
54. Strehler BL, Arnold W. Light production by green plants. J Gen Physiol. 1951;34(6): 809–820. pmid:14850702
55. Banks JM. Continuous excitation chlorophyll fluorescence parameters: a review for practitioners. Tree Physiol. 2017;37(8):1128–1136. pmid:28575512
56. Chow WS, Fan DY, Oguchi R, Jia H, Losciale P, Park YI, et al. Quantifying and monitoring functional photosystem II and the stoichiometry of the two photosystems in leaf segments: approaches and approximations. Photosynth Res. 2012;113(1–3):63–74. pmid:22638914
57. Shu P, Gong X, Du Y, Han Y, Jin S, Wang Z, et al. Effects of simulated acid rain on photosynthesis in Pinus massoniana and Cunninghamia lanceolata in terms of prompt fluorescence, delayed fluorescence, and modulated reflection at 820 nm. Plants (Basel). 2024;13(5):622. pmid:38475467
58. Zhang D, Zhang QS, Yang XQ, Sheng ZT, Nan GN. The alternation between PSII and PSI in ivy (Hedera nepalensis) demonstrated by in vivo chlorophyll a fluorescence and modulated 820 nm reflection. Plant Physiol Biochem. 2016;108:499–506. pmid:27592174
59. Joliot P, Johnson GN. Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci U S A. 2011;108(32):13317–13322. pmid:21784980
60. Joliot P, Joliot A, Johnson G. Cyclic electron transfer around photosystem I, In: Photosystem I. Springer Netherlands. 2006;639–656.
61. Lambrev P, Goltsev V. PH dependence of the effects of diuron, atrazine and dinoseb on the luminescent properties of thylakoid membranes. Bulg J Plant Physiol. 2001;27:85–100.
62. Lazár D. Chlorophyll a fluorescence induction. Biochim Biophys Acta Bioenerg. 1999;1412(1):1–28. pmid:10354490
63. Mehta P, Kraslavsky V, Bharti S, Allakhverdiev SI, Jajoo A. Analysis of salt stress induced changes in Photosystem II heterogeneity by prompt fluorescence and delayed fluorescence in wheat (Triticum aestivum) leaves. J Photochem Photobiol B. 2011;104(1–2):308–813. pmid:21414797
64. Oukarroum A, Goltsev V, Strasser RJ. Temperature effects on pea plants probed by simultaneous measurements of the kinetics of prompt fluorescence, delayed fluorescence and modulated 820 nm reflection. PLoS One. 2013;8(3):e59433. pmid:23527194
You have requested "on-the-fly" machine translation of selected content from our databases. This functionality is provided solely for your convenience and is in no way intended to replace human translation. Show full disclaimer
Neither ProQuest nor its licensors make any representations or warranties with respect to the translations. The translations are automatically generated "AS IS" and "AS AVAILABLE" and are not retained in our systems. PROQUEST AND ITS LICENSORS SPECIFICALLY DISCLAIM ANY AND ALL EXPRESS OR IMPLIED WARRANTIES, INCLUDING WITHOUT LIMITATION, ANY WARRANTIES FOR AVAILABILITY, ACCURACY, TIMELINESS, COMPLETENESS, NON-INFRINGMENT, MERCHANTABILITY OR FITNESS FOR A PARTICULAR PURPOSE. Your use of the translations is subject to all use restrictions contained in your Electronic Products License Agreement and by using the translation functionality you agree to forgo any and all claims against ProQuest or its licensors for your use of the translation functionality and any output derived there from. Hide full disclaimer
© 2024 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Abstract
Aluminum (Al) toxicity is an important factor restricting the normal growth of plants in acidic soil. Rhododendron (Ericaceae) can grow relatively well in acidic soil. To uncover the adaptive mechanisms of photosynthesis under Al stress, the influence of Al stress on the photosynthetic activities of Al-sensitive (Baijinpao) and Al-resistant (Kangnaixin) rhododendron cultivars was examined by measuring gas exchange, chlorophyll fluorescence, and the modulated reflection of light at 820 nm. Under Al stress conditions, the net photosynthetic rate and stomatal conductance of the rhododendron leaves decreased, whereas the intercellular CO2 concentration increased. The Al stress treatment damaged the oxygen-evolving complex of the rhododendron seedlings, while also inhibiting electron transport on the photosystem II (PSII) donor side. In addition, the exposure to Al stress restricted the oxidation of plastocyanin (PC) and the photosystem I (PSI) reaction center (P700) and led to the re-reduction of PC+ and P700+. The comparison with Kangnaixin revealed an increase in the PSII connectivity in Baijinpao. Additionally, the donor-side electron transport efficiency was more inhibited and the overall activity of PSII, PSI, and the intersystem electron transport chain decreased more extensively in Baijinpao than in Kangnaixin. On the basis of the study findings, we concluded that Al stress adversely affects photosynthesis in rhododendron seedlings by significantly decreasing the activity of PSII and PSI. Under Al stress, Kangnaixin showed stronger tolerance compared with Baijinpao.
You have requested "on-the-fly" machine translation of selected content from our databases. This functionality is provided solely for your convenience and is in no way intended to replace human translation. Show full disclaimer
Neither ProQuest nor its licensors make any representations or warranties with respect to the translations. The translations are automatically generated "AS IS" and "AS AVAILABLE" and are not retained in our systems. PROQUEST AND ITS LICENSORS SPECIFICALLY DISCLAIM ANY AND ALL EXPRESS OR IMPLIED WARRANTIES, INCLUDING WITHOUT LIMITATION, ANY WARRANTIES FOR AVAILABILITY, ACCURACY, TIMELINESS, COMPLETENESS, NON-INFRINGMENT, MERCHANTABILITY OR FITNESS FOR A PARTICULAR PURPOSE. Your use of the translations is subject to all use restrictions contained in your Electronic Products License Agreement and by using the translation functionality you agree to forgo any and all claims against ProQuest or its licensors for your use of the translation functionality and any output derived there from. Hide full disclaimer
Details
