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. 2024 Mar 8;14(4):103. doi: 10.1007/s13205-024-03943-6

Mechanism of salt tolerance in the endangered semi-mangrove plant Barringtonia racemosa: anatomical structure and photosynthetic and fluorescence characteristics

Ju Hu 1,2,#, Xu Deng 1,#, Caihong Bai 1,2,#, Lin Li 1, Xiuling Yang 1,2, Chunxiao Lan 1, Haiyan Zhong 1, Xiaohui Tan 3,4,✉, Fang Liang 1,2,✉
PMCID: PMC10923768  PMID: 38464614

Abstract

To elucidate the mechanisms governing the salt tolerance of the endangered semi-mangrove plant Barringtonia racemosa, the biomass, photosynthetic and fluorescent characteristics, and anatomical structure of B. racemosa were studied under low, medium and high salt stress. The results showed that the stem dry weight, net photosynthetic rate, intercellular CO2 concentration, Fv/Fm, and ΦPSI of B. racemosa decreased under high salt stress, which led to a significant reduction in total dry weight. Stem dry weight was significantly positively correlated with the thickness of palisade tissue and significantly negatively correlated with the thickness of the epidermis of roots and xylem of stems. Therefore, a stable net photosynthetic rate and intercellular CO2 concentration, an increase in Fv/Fm and ΦPSI, an increase in or stable palisade tissue and spongy mesophyll of leaves and an increase in xylem thickness of the stem and epidermis, outer cortex, and stele diameter of roots could contribute to the salt tolerance of B. racemosa.

Keywords: Photosynthesis, Fluorescence, Anatomical structure, Barringtonia racemosa, Salt stress

Introduction

Salt stress, the most prevalent type of abiotic stress, affects physiological, biochemical, and molecular properties in plants and reduces their productivity (Van Zelm et al. 2020; Zhao et al. 2021; Fu et al. 2023). Salt stress can cause ion imbalance, osmotic stress, oxidative stress, water and nutrient deficiency, and growth retardation, damage biological macromolecules and even lead to death (Munns and Tester 2008; Liu et al. 2021, 2022; Van Zelm et al. 2020). Salt-tolerant plants play an important role in saline soil remediation and utilization; they can improve the soil structure and fertility by saving energy, exhibiting stable and lasting effects, and causing almost no pollution to the environment (Munns and Tester 2008; Zahra et al. 2022). Salt-tolerant plants are tolerant to osmotic stress and exhibit sodium (Na) exclusion from leaf blades and tissue tolerance (Munns and Tester 2008). They can also improve their photosynthetic capacity by modifying and redistributing electron transport between photosystems and changing root, stem, and leaf subcellular structures to improve the stability of the photosystem to improve salt stress tolerance in field conditions (Zahra et al. 2022).

The sea level is rising from year to year due to global warming, and the salt concentration has reached approximately 30–40‰ in the South China Sea, which has resulted in an increase in the coastal saline soil area in China (Huang, et al. 2018). However, only a few plant species, such as Tamarix chinensis (Chen et al. 2022) and Rhizophora stylosa (Qiu et al. 2021), are suitable for coastal mudflats (Long et al. 2016; Meena et al. 2019; Zhao et al. 2022). Semi-mangrove plants grow in the intertidal zone of tropical and subtropical coastlines and provide a natural barrier to the coast in China (Fan and Wang 2017; Zhen et al. 2018). Barringtonia racemosa, an evergreen tree belonging to the Lecythidaceae genus Barringtonia, is an endangered semi-mangrove ornamental plant (Lin 1998), and it is a typical tropical and subtropical coastal plant that is widely distributed in Guangxi, Guangzhou, Hainan, and Taiwan provinces in China (Nong and Li 2006).

Photosynthesis, chlorophyll fluorescence characteristics and anatomical structure changes in plants, which are affected by salt stress, impact biomass (Miyashita et al. 2005; Hu et al. 2014; Ghafoor et al. 2019). Chlorophyll fluorescence is very sensitive to salt stress and plays an important role in the absorption, transmission, distribution, dissipation and conversion of light energy in the light system (Baker 2008). Therefore, studying the photosynthetic and fluorescence characteristics and anatomical structure of B. racemosa is an effective way to determine the mechanisms of salt stress tolerance. Previous studies found that B. racemosa was tolerant to low salt stress (≤ 15‰) (Liang et al. 2019, 2021; Tan et al. 2021); however, the mechanism has not been reported. The main objective of this study was to investigate the mechanism of salt tolerance in 2-year-old B. racemosa seedlings under low, medium and high salt stress by studying the photosynthetic and fluorescence characteristics and anatomical structure of roots, stems and leaves.

Materials and methods

Plant materials

The seeds of B. racemosa used in the following experiments were collected from the natural forest in Qili village, Zhonghe town, Danzhou city, Hainan Province, China (N19°45′, E109°22′). The formal identification of B. racemosa was undertaken by Taiping He, who is a professor in plant taxonomy at Guangxi University. The plant materials were compared with the specimens (AU058561) of B. racemosa in the plant herbarium of the School of Life Science, Xiamen University. Voucher specimens (YLSY-BR001) of B. racemosa were deposited in the Southeast Guangxi Distinctive Medicinal Plant Herbarium, Yulin Normal University (N22°41′, E110°12′). The seeds were sown in a nursery shed in a greenhouse at Yulin Normal University, Guangxi Province, China (N22°64′, E110°14′). Upon reaching a height of approximately 20 cm, the seedlings were transplanted into pots (one plant in each pot) with orchard soil and coconut bran (1:1, volume ratio) for growth. Finally, 2-year-old seedlings with uniform growth (80 cm height) were selected for further study.

Experimental design

According to Cheng et al. (2020), there were seven sea salt treatments, which included control (0‰), 15‰, 20‰, 25‰, 30‰, 35‰, and 40‰ sea salt, 15‰ was a low salt treatment, 20‰ and 25‰ were medium salt treatments, and 30‰, 35‰, and 40‰ were high salt treatments. The solutions with different sea salt concentrations were prepared by dissolving sea salt in tap water (w/w). Then, the solution was put in the tank of an automatic tide device, which was used to mimic tides. This device had a plant cultivation tank, a timer, a water pump, a filtering system, a fill light system and a shading system. The pumping time was automatically controlled by the timer. The seedlings in the pots were submerged (just above the pot) for 6 h from 9:00 am to 15:00 pm every day. After 9 days of salt treatments, when more than 50% of the leaves of the plants under 40‰ salt treatment turned brown and wilted or were shed, salt stress was stopped, and three plants were selected from each treatment for all measurements.

Determination of photosynthetic and fluorescence characteristics

After 9 days of salt treatments, during the period of 9:00–11:00 am, three leaves were randomly selected from each seedling to obtain the net photosynthetic rate (Pn), intercellular CO2 concentration (Ci), stomatal conductance (Gs) and transpiration rate (Tr) with a portable photosynthetic analyser (TPS-2, PP Systems, New York, USA); the quantumyield (Fv/Fm), nonphotochemical quenching (NPQ), PSII actual photochemical quantum yield (ΦPSII) and PSI actual photochemical quantum yield (ΦPSI) under steady-state conditions were measured by a CF Imager chlorophyll fluorescence imaging system (Technologica, Ltd., UK) (Rao et al. 2021), and each leaf was measured three times.

Anatomical analysis

The root, stem and leaf of each seedling were fixed in FAA (formalin: 70% ethanol: glacial acetic acid = 1: 18: 1, v/v/v) solution, embedded in paraffin and sectioned (3 μm), sequentially placed in xylene for 20 min twice, absolute ethanol for 5 min twice, and 75% alcohol for 5 min. Then, the slices were stained with 5 g L–1 safranin solution for 1 to 2 h and Fast Green for 30 to 60 s. The slices were mounted with neutral gum and dried at 40 °C for 12 h in an electric constant temperature drying oven (Jinghong, DHG-9077A, Shanghai, China). Root, stem and leaf sections were examined under a light microscope (Olympus, BH2 REC, Tokyo, Japan), and cellSens Standard software was used for photography and analysis. The anatomical structure was analysed by Image-Pro Plus Software 6.0 (Media Cybemetics, Silver Spring, USA).

Determination of biomass and root-shoot ratio

The root, stem and leaf of each seedling were separated, and the fresh weight was measured. Then, the seedlings were dried at 105 °C for 30 min and dried at 70 °C to a constant weight (approximately 48 h) in an electric constant temperature drying oven (Jinghong, DHG-9077A, Shanghai, China). The dry weights of the roots (RDW), stems (SDW) and leaves (LDW) were measured. Total dry weight (TDW) and root/shoot (R/S) ratios were calculated using the following formulae (Shen et al. 2019):

TDW=RDW+SDW+LDW
R/S=RDWSDW+LDW

Statistics and analysis

All statistical analyses were performed with SPSS Statistics 22 (SPSS Inc., Chicago, USA), and the data were analysed by one-way analysis of variance (ANOVA) and the least significant difference test (Duncan, P < 0.05). OriginPro 2021b 9.8.5.201 (OriginLab, Inc., Massachusetts, USA) was used to draw the figures.

Results

Biomass and root-shoot ratio

Compared with the control, 30‰-40‰ salt stress significantly reduced SDW and TDW (Table 1), while 15‰ salt stress significantly increased TDW. No significant differences were found among RDW, LDW or RSR across all salt treatments and the control.

Table 1.

Root, stem, leaf and total dry weight (RDW, SDW, LDW and TDW) and root shoot ratio (RSR) of B. racemosa under salt stress

Treatments RDW (g) SDW (g) LDW (g) TDW (g) RSR
0 (Control) 1.26 ± 0.05ab 1.21 ± 0.02ab 1.12 ± 0.08a 3.59 ± 0.11bc 0.54 ± 0.01a
15‰ 1.36 ± 0.02a 1.32 ± 0.06a 1.19 ± 0.14a 3.86 ± 0.19a 0.55 ± 0.04a
20‰ 1.33 ± 0.10ab 1.30 ± 0.08a 1.16 ± 0.02a 3.79 ± 0.19ab 0.54 ± 0.02a
25‰ 1.34 ± 0.01ab 1.13 ± 0.11bc 1.18 ± 0.05a 3.65 ± 0.13abc 0.58 ± 0.04a
30‰ 1.25 ± 0.04b 1.09 ± 0.02c 1.10 ± 0.00a 3.40 ± 0.06c 0.57 ± 0.01a
35‰ 1.28 ± 0.08ab 1.09 ± 0.04c 1.14 ± 0.03a 3.50 ± 0.09c 0.58 ± 0.04a
40‰ 1.27 ± 0.05ab 1.06 ± 0.04c 1.14 ± 0.05a 3.47 ± 0.07c 0.58 ± 0.02a
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All data in the table are presented as the means with standard deviations (means ± SDs; n = 3). Different lowercase letters indicate that the mean values are significantly different among the treatments at P < 0.05 according to Duncan′s test

Photosynthetic and fluorescence characteristics

Photosynthetic parameters (Pn, Tr, Gs and Ci) of B. racemosa under different salt treatments are shown in Table 2. Under 35‰ and 40‰ salt treatments, Pn significantly decreased by 63.38% and 65.10%, respectively, and Ci decreased by 17.42% and 18.22%, respectively, compared with the control. There were no significant differences in the Tr and Gs of B. racemosa between all salt treatments and the control.

Table 2.

Net photosynthetic rate (Pn), transpiration rate (Tr), stomatal conductance (Gs), and intercellular CO2 concentration (Ci) of B. racemosa under salt stress

Treatment Pn (µmol CO2 m−2 s−1) Tr (mmol m−2 s−1) Gs (mmol m−2 s−1) Ci (µmol CO2 mol−1)
0 (Control) 4.67 ± 1.16a 0.50 ± 0.37a 7.33 ± 4.16a 601.83 ± 45.73a
15‰ 3.87 ± 1.33a 0.45 ± 0.16a 5.33 ± 1.16a 567.84 ± 0.91a
20‰ 3.71 ± 1.40ab 0.37 ± 0.07a 4.67 ± 4.62a 564.81 ± 12.77a
25‰ 3.45 ± 1.59ab 0.34 ± 0.17a 4.67 ± 2.31a 556.35 ± 67.90ab
30‰ 3.25 ± 0.51ab 0.29 ± 0.15a 4.00 ± 2.00a 544.21 ± 3.53abc
35‰ 1.71 ± 0.72a 0.24 ± 0.17a 3.33 ± 1.16a 496.97 ± 23.62bc
40‰ 1.63 ± 0.46a 0.17 ± 0.06a 2.67 ± 1.16a 492.20 ± 15.98c
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All data in the table are presented as the means with standard deviations (means ± SDs; n = 3). Different lowercase letters indicate that the mean values are significantly different among the treatments at P < 0.05 according to Duncan′s test

Significantly lower Fv/Fm values were observed only after treatment with 40‰ salt compared with the control (Table 3). The seedlings treated with 35‰ and 40‰ salt had significantly lower ΦPSI values than the control, and ΦPSI reached the lowest value under the 40‰ salt treatment. The 20‰, 30‰, 35‰ and 40‰ salt treatments significantly decreased NPQ. No significant differences were observed in ΦPSII across all salt treatments and the control.

Table 3.

Quantum yield (Fv/Fm), nonphotochemical quenching (NPQ), PSII actual photochemical quantum yield (ΦPSII), and PSI actual photochemical quantum yield (ΦPSI) of B. racemosa under salt stress

Treatment Fv/Fm NPQ ΦPSII ΦPSI
0 (Control) 0.78 ± 0.02a 3.09 ± 0.75a 0.11 ± 0.02a 2.63 ± 0.42a
15‰ 0.75 ± 0.04ab 2.66 ± 0.19ab 0.12 ± 0.04a 2.02 ± 1.00ab
20‰ 0.75 ± 0.04ab 1.58 ± 0.47c 0.13 ± 0.04a 1.62 ± 0.90ab
25‰ 0.75 ± 0.06ab 2.36 ± 0.46abc 0.13 ± 0.06a 2.00 ± 1.43ab
30‰ 0.75 ± 0.01ab 1.83 ± 0.23c 0.12 ± 0.01a 1.69 ± 0.28ab
35‰ 0.68 ± 0.03ab 2.18 ± 0.26bc 0.11 ± 0.04a 0.74 ± 0.12b
40‰ 0.67 ± 0.10b 1.72 ± 0.37c 0.10 ± 0.01a 0.76 ± 0.56b
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All data in the table are presented as the means with standard deviations (means ± SDs; n = 3). Different lowercase letters indicate that the mean values are significantly different among the treatments at P < 0.05 according to Duncan′s test

Anatomical analysis of roots, stems and leaves of B. racemosa

The roots shrank under salt stress, especially under 35‰ and 40‰ salt stress (Fig. 1). Compared with the control, the thickness of the epidermis (Ep) significantly increased under the 25‰ and 40‰ salt treatments (Table 4), and the outer cortex (Ex) significantly decreased under the salt treatments, except for the 30‰ salt treatment. Under the 15‰ and 25‰ salt treatments, the stele (St) diameters significantly increased, while under the 30‰, 35‰ and 40‰ salt treatments, they significantly decreased compared with those of the control. For stems, under salt stress, xylem (Xy) and phloem (Ph) under salt treatments were significantly thicker than those under the control, except for Xy under 20‰ salt treatment and Ph under 40‰ salt treatment (Fig. 2, Table 5). The highest values of Xy (3368.06 μm) and Ph (782.95 μm) were observed in the 25‰ and 30‰ salt treatments, respectively. The cambium (Ca) and cortex (Co) under salt treatments were significantly thinner than those under the control (Table 6, Fig. 3). The lowest values of Ca (48.22 μm) and Ph (268.81 μm) were observed in the 20‰ and 30‰ salt treatments, respectively.

Fig. 1.

Fig. 1

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Cross-sections of B. racemosa root tips under 0‰ (control) (A), 15‰ (B), 20‰ (C), 25‰ (D), 30‰ (E), 35‰ (F) and 40‰ (G) salt treatments. Ep epidermis, Ex outer cortex, St stele. Scale bars = 200 μm

Table 4.

The thickness of the epidermis (Ep), outer cortex (Ex), and stele (St) diameter of B. racemosa roots under salt stress

Treatment Thickness of Ep (μm) Thickness of Ex (μm) St diameter (μm)
0 (Control) 17.26 ± 0.67cd 330.88 ± 4.59a 298.39 ± 10.44c
15‰ 15.18 ± 10.58d 283.21 ± 22.43bc 349.99 ± 30.83b
20‰ 17.14 ± 1.06cd 259.21 ± 49.81c 183.28 ± 10.57e
25‰ 25.71 ± 3.47a 123.24 ± 11.42e 524.65 ± 21.52a
30‰ 19.16 ± 1.68bc 307.26 ± 27.24ab 248.43 ± 22.2d
35‰ 16.78 ± 1.70cd 255.66 ± 16.07c 212.75 ± 23.13de
40‰ 20.69 ± 2.37b 201.42 ± 51.13d 201.76 ± 82.84de
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All data in the table are presented as the means with standard deviations (means ± SDs; n = 5). Different lowercase letters indicate that the mean values are significantly different among the treatments at P < 0.05 according to Duncan′s test

Fig. 2.

Fig. 2

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Cross-sections of B. racemosa stems under 0‰ (control) (A), 15‰ (B), 20‰ (C), 25‰ (D), 30‰ (E), 35‰ (F) and 40‰ (G) salt treatments. Xy xylem, Ca cambium, Ph phloem, Co cortex. Scale bars = 1000 μm

Table 5.

The thickness of the xylem (Xy), cambium (Ca), phloem (Ph) and cortex (Co) of B. racemosa stems under salt stress

Treatment Xy (μm) Ca (μm) Ph (μm) Co (μm)
0 (Control) 2652.96 ± 122.79c 104.16 ± 18.20a 487.79 ± 115.84c 622.48 ± 63.85a
15‰ 3079.50 ± 45.99b 70.72 ± 7.26b 768.11 ± 59.92a 308.64 ± 48.17c
20‰ 2195.90 ± 137.72d 48.22 ± 6.93c 624.42 ± 29.60b 272.92 ± 63.83c
25‰ 3236.32 ± 58.85a 57.61 ± 4.89bc 782.95 ± 40.31a 270.71 ± 30.04c
30‰ 3368.06 ± 208.50a 55.06 ± 4.81bc 758.39 ± 51.21a 268.81 ± 25.42c
35‰ 3048.83 ± 65.83b 58.53 ± 25.82bc 745.44 ± 157.66a 447.65 ± 107.56b
40‰ 3274.81 ± 81.32a 65.15 ± 6.75b 575.95 ± 22.14bc 488.99 ± 32.06b
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All data in the table are presented as the means with standard deviations (means ± SDs; n = 5). Different lowercase letters indicate that the mean values are significantly different among the treatments at P < 0.05 according to Duncan′s test

Table 6.

The thickness of the upper epidermis (Ue), lower epidermis (Le), palisade tissue (Pt), spongy mesophyll (Sm), midrib bund (Mb), and parenchyma (Pc) of B. racemosa leaves under salt stress

Treatment Ue (μm) Le (μm) Pt (μm) Sm (nm) Mb (μm) Pc(μm)
0 (Control) 23.86 ± 0.81ab 19.30 ± 1.42a 67.49 ± 2.16b 94.37 ± 4.31bc 105.51 ± 34.35b 154.31 ± 29.08a
15‰ 21.94 ± 1.18cd 18.31 ± 1.64a 74.18 ± 1.97a 102.04 ± 4.63a 158.58 ± 20.02a 168.88 ± 25.34a
20‰ 20.74 ± 1.32d 15.44 ± 0.87b 66.57 ± 2.88bc 90.67 ± 3.24cd 144.18 ± 31.59a 162.23 ± 16.55a
25‰ 20.67 ± 0.63d 15.04 ± 1.49b 62.46 ± 4.88c 97.75 ± 5.24ab 97.10 ± 26.57b 162.19 ± 20.72a
30‰ 25.12 ± 2.10a 19.13 ± 1.42a 69.62 ± 3.73b 102.17 ± 2.73a 177.75 ± 49.61a 180.57 ± 15.23a
35‰ 21.06 ± 1.30d 18.69 ± 1.40a 74.48 ± 3.57a 85.67 ± 4.93d 160.14 ± 14.06a 178.68 ± 42.04a
40‰ 23.21 ± 1.43bc 18.38 ± 0.89a 53.02 ± 2.44d 96.61 ± 2.88ab 72.04 ± 10.33b 146.59 ± 32.74a
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All data in the table show are presented as the means with standard deviations (means ± SDs; n = 5). Different lowercase letters indicate that the mean values are significantly different among the treatments at P < 0.05 according to Duncan′s test

Fig. 3.

Fig. 3

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Cross-sections of whole leaf (A1—G1), leaf-bade (A2—G2) and midrib (A3—G3) of B. racemosa leaves under 0‰ (control), 15‰, 20‰, 25‰, 30‰, 35‰ and 40‰ salt treatments. P palisade cell, Ue upper epidermis, Sm spongy mesophyll, Le lower epidermis, Mb midrib bund, Pc parenchymal. Scale bars = 1000, 100, and 200 μm

In terms of leaves, a significantly thinner upper epidermis (Ue) was observed after treatment with 15‰, 20‰, 25‰ and 35‰ salt compared with the control, and a significantly thinner lower epidermis (Le) was observed after treatment with 20‰ and 25‰ salt compared with the control (Fig. 3, Table 6). Significantly thicker midrib bunds (Mb) were observed after treatment with 15‰, 20‰, 25‰ and 35‰ salt compared with the control. For palisade tissue (Pt) and spongy mesophyll (Sm), compared with the control, the 15‰ and 35‰ salt treatments significantly increased the thickness of Pt, while the 25‰ and 40‰ salt treatments significantly decreased the thickness of Pt; the 15‰ and 30‰ salt treatments significantly increased the thickness of Sm, while the 35‰ salt treatment significantly decreased the thickness of Sm. No significant differences were observed in the width of Pc across all salt treatments and the control.

Correlation between photosynthesis and fluorescence parameters and biomass and root-shoot ratio

As shown in Fig. 4, SDW had a significant positive correlation with Tr, Ci and ΦPSI, and SDW had a significant positive correlation with ΦPSII. RSR had a significant negative correlation with Tr, Ci, ΦPSII and ΦPSI. No significant correlations were observed between photosynthesis or fluorescence parameters and RDW or TDW.

Fig. 4.

Fig. 4

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Pearson correlation matrix between photosynthetic and fluorescence parameters and dry weight and root-to-shoot ratio. Significant values are marked with * (P ≤ 0.05), ** (P ≤ 0.01) and *** (P ≤ 0.001). Colours indicate the level of correlation (r) from positive correlation (red) to negative (blue). Variations in the colour of blue and red indicate the level of significance. RDW root dry weight, SDW stem dry weight, LDW leaf dry weight, TDW total dry weight, RSR root shoot ratio, Pn net photosynthetic rate, Tr transpiration rate, Gs stomatal conductance, Ci intercellular CO2 concentration, Fv/Fm quantum yield, NPQ nonphotochemical quenching, ΦPSII actual photochemical quantum yield, ΦPSI actual photochemical quantum yield, Ep epidermis, Ex outer cortex, St stele, Xy xylem, Ca cambium, Ph phloem, Co cortex, Ue upper epidermis, Le lower epidermis, Pt palisade cell, Sm spongy mesophyll, Mb midrib bund, Pc parenchymal

Discussion

The biomass (dry weight) of plants is a comprehensive response to salt stress (Chen et al. 2017). In this study, the SDW decreased significantly under the 30–40‰ salt treatment, which was the main reason for the significantly lower TDW compared with the control. This is consistent with the results in Suaeda salsa (Zhang et al. 2016), Avena sativa (Mu et al. 2015) and Gossypium hirsutum (Qi et al. 2016). No significant differences were found in root and leaf dry weight and RSR under all salt treatments and the control. The results indicated that the biomass of B. racemosa in response to high-concentration salt stress was reflected by a greatly reduced SDW.

Photosynthesis in plants is highly sensitive to salt stress (Loreto et al. 2003) and plays an important role in biomass production. In this study, Ci was significantly positively correlated with SDW. The Pn and Ci of B. racemosa significantly decreased under 35‰ and 40‰ salt treatments, Pn decreased 2.96 µmol CO2 m−2 s−1 and 3.04 µmol CO2 m−2 s−1 under 35‰ and 40‰ salt treatments, respectively, and Ci decreased 104.86 µmol CO2 mol−1 and 109.63 µmol CO2 mol−1 under 35–40‰ salt treatments, respectively. Tr and Gs did not change significantly under any of the salt treatments compared with the control. Ci was significantly correlated with SDW. Therefore, the reduction in Ci and Pn of B. racemosa was one of the reasons that SDW was reduced under high salt stress.

In general, fluorescence characteristic changes can be correlated with inhibition at or close to PSII reaction centres, chlorophyll a fluorescence emitted by green plants reflects photosynthetic activities (Papageorgiou 2011), and Fv/Fm is an important indicator of the efficiency and utilization of excitation energy captured by PSII (Terletskaya et al. 2020). In this study, the Fv/Fm of B. racemosa did not decrease significantly until the salt concentration reached 40‰, which indicated that high-concentration salt stress forced the leaf to have photoinhibition, and the light energy used for photochemical reactions decreased. ΦPSI significantly decreased when the salt concentration reached 35‰ and 40‰, which indicated that the photosynthetic apparatus of ΦPSI was seriously damaged with high salt concentration stress. In addition, ΦPSI was significantly positively correlated with SDW; therefore, Fv/Fm and ΦPSI changes also contributed to SDW reduction. Furthermore, the thickness of Pt and Sm significantly increased or did not change significantly under salt treatments (especially ≤ 30‰), which could lead to these photosynthetic and fluorescence variations under salt stress (Zhi et al. 2020).

The anatomical structures of roots and stems of plants are related to salt tolerance (Hameed et al. 2009; Imada et al. 2015; Zhi et al. 2020; Wang et al. 2021). Changes in anatomical structure help plants improve their water storage, transportation and photosynthetic capacity, alleviate salt damage, and maintain growth, development and physiological functions (Wang et al. 2021). The increase in Ep and Ex of roots under salt stress could block more Na+ out of roots and effectively alleviate salt damage (Zhang et al. 2016; Terletskaya et al. 2019). In this study, the width of Ep and St diameter significantly increased under approximately 25‰, which could contribute to the salt tolerance of B. racemosa. However, under higher salt stress (especially 40‰), the width of Ep, Ex and St diameter decreased, which could impact the water and nutrient uptake and may be another reason for the significant decrease in SDW.

Cortical cells of stems store nutrients and water, and stems with more cortical cells could have larger water storage space and water content (Hameed et al. 2009; Li et al. 2021). The cambium plays a key role in the radial growth of plants and affects the secondary growth stage of plants (Dang et al. 2023). In this study, the thickness of Ca and Co significantly decreased under all salt treatments, which indicated that salt stress could reduce water storage and radial growth of B. racemosa. Xy and Ph are the main tissues for water transportation and photosynthate and assimilation transportation and storage, which are important for tolerance to abiotic stress (Huang et al. 2022; Sun et al. 2022). In this study, Xy and Ph under all salt treatments were significantly thicker than those under the control, except for Xy under 20‰ and Ph under 40‰ salt treatment. B. racemosa could increase the size of Xy and Ph to transport more water, nutrients and assimilating products under salt stress. However, Xy was significantly negatively correlated with SDW, and an increase in Xy could reduce SDW.

Conclusions

The SDW of B. racemosa was significantly reduced under high salt stress (30–40‰), while RDW, SDW and LDW did not vary under low salt stress (≤ 25‰), which could be related to stable Pn and Ci, increases in Fv/Fm and ΦPSI, increases or stable Pt and Sm of leaves, increases in Xy thickness of stems and Ep, Ex, and St diameters of roots.

Acknowledgments

We thank professor Taiping He for formal identification of B. racemosa.

Author contributions

X.T., C.L. and H.Z. performed the experiments and collected the data. J.H., L.L, and X.Y. analyzed, interpreted the data. J.H. and X.D. wrote the manuscript. J.H. and L.F. acquired the funding. C.B. revised the manuscript. All authors contributed to the article and approved the submitted version.

Funding

This research was supported by the Natural Science Foundation of Guangxi Province, China (No. 2022GXNSFBA035540), the National Natural Science Foundation of China (No. 31660226), Guangxi Universities Young and Middle-aged Scientific Research Basic Ability Improvement Project (No. 2022KY0583), the High-level Talent Research Start-up Fund of Yulin Normol University (No. G2019ZK43), and the Special project for basic scientific research of Guangxi Academy of Agricultural Sciences (No. Guinongke 2021YT143).

Data availability

The data supporting this study's findings are available at the request of the corresponding author.

Declarations

Conflicts of interest

The authors declare that they have no competing interests.

Ethical approval

We had obtained permission to collect plants. All experiments were performed in accordance with relevant guidelines/regulations.

Footnotes

Ju Hu, Xu Deng and Caihong Bai contributed equally to this work.

Contributor Information

Xiaohui Tan, Email: xiaohuitan@126.com.

Fang Liang, Email: liangfang360@ylu.edu.cn.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data supporting this study's findings are available at the request of the corresponding author.

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