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. 2022 Mar 31;28(3):625–635. doi: 10.1007/s12298-022-01169-5

Salicylic acid alleviates selenium stress and promotes selenium uptake of grapevine

Zhiyu Li 1, Rong Fan 2, Xuemei Peng 3, Junjiang Shu 3, Lei Liu 4, Jin Wang 1, Lijin Lin 1,✉
PMCID: PMC8986911  PMID: 35465205

Abstract

To determine suitable cultivation measures to enrich selenium (Se) and alleviate the Se stress in fruit trees, the effects of different exogenous salicylic acid (SA) concentrations (0, 50, 100, 150 and 200 mg/L) on the growth and Se uptake of grapevine under Se stress were studied. Under Se stress, SA increased the biomass of grapevine to some extent and had a linear relationship with both root and shoot biomass. The chlorophyll content, net photosynthetic rate, transpiration rate, stomatal conductance, and intercellular CO2 concentration of grapevine tended to increase when the concentration of SA was < 150 mg/L and decrease when the concentration of SA was > 150 mg/L. Different concentrations of SA enhanced the activity of superoxide dismutase, while reducing that of peroxidase. It had no significant effect on the catalase activity of grapevine. SA decreased the content of osmotically active substances in grapevine to some extent. SA also increased the contents of total Se, inorganic Se and organic Se in grapevine to some extent, and had a linear or quadratic polynomial relationship with the total Se contents in both roots and shoots. When the SA concentration was 250 mg/L, the total Se contents in the roots and shoots were the highest and increased by 10.41% and 58.46%, respectively, compared with the control. Therefore, exogenous SA could promote the growth and Se uptake of grapevine under Se stress, with 250 mg/L serving as the most effective concentration.

Keywords: Salicylic acid, Grapevine, Selenium stress, Growth, Physiological characteristics

Introduction

Selenium (Se) is a nutrient that is beneficial to plants (Yin et al. 2019). However, excessive Se can also negatively affect the growth of plants (Chen et al. 2016a). Plants can assimilate inorganic Se into selenocysteine and selenomethionine, and selenocysteine can replace the cysteine in proteins. Formation of this non-specific selenoprotein can lead to Se poisoning in plants (Li et al. 2008; Van Hoewyk 2013). Selenite stress inhibits the development of Arabidopsis thaliana taproots, and the concentrations of auxin, cytokinin and ethylene in the plant are also affected (Lehotai et al. 2012). High Se stress causes the excessive accumulation of reactive oxygen species (ROS), which lead to oxidative damage in plants, causing leaves to turn yellow and wilt and inhibiting photosynthesis (Wang 2019; Mostofa et al. 2017). Thus, Se stress has a serious impact on the growth and development of plants, and finding appropriate methods to alleviate the negative effects of Se stress on plant growth has gradually become an intensive focus of research.

Many agronomic measures, such as intercropping (Ma et al. 2020), grafting (Fu and Yang 2021), straw return (Wang 2016) and applying plant growth regulators (Feng et al. 2021), can affect the absorption of mineral elements by plants. The most widely used plant growth regulators are a class of signal molecules that can produce obvious physiological effects at lower concentrations (Li and Li 2019) and are widely used to regulate plant growth and improve plant resistance (Rademacher 2015). As a plant growth regulator, salicylic acid (SA) is a phenolic compound that is synthesized by the iso-branched acid synthase and phenylalanine ammonia lyase pathways in plants. It not only participates in various physiological activities of plants, but also plays an important role in plant stress resistance (Lefevere et al. 2020; Osama et al. 2019). Many studies have proven that SA can protect plants from stress, such as drought (Tayeb and Ahmed 2010), salt (Rajabi Dehnavi et al. 2019), high temperature (Kousar et al. 2018) and heavy metals (Zanganeh et al. 2019). SA can quickly activate the non-enzymatic defense system of safflower (Carthamus tinctorius) under drought conditions, regulate its content of osmotically active substances, and play a role in maintaining the balance of ROS, thereby reducing their damage to cells (Chavoushi et al. 2019). Similarly, under heavy metal stress conditions, SA can regulate the activity of plant antioxidant systems through H2O2-mediated signal pathways, stimulate plants to remove active oxygen free radicals, and thereby reduce the oxidative damage caused by heavy metal stress to plants (Chen et al. 2007). Under low temperature stress, the combined application of SA and Se is beneficial to increase the chlorophyll content, proline content, and antioxidant enzyme activity in Dendrobium candidumin, which alleviates the damage caused by low temperature stress to plants (Ding et al. 2021). Under Se stress, SA changes the transcriptional expression of sulfur-related genes in Brassica juncea seedlings, such as by upregulating the expression levels of LAST, MT-2 and APS genes and downregulating the expression level of OASL gene (Gupta and Gupta 2016). In addition, the mechanism of detoxification that SA uses on Se is to maintain the homeostasis of Se in rice tissues by limiting the excessive accumulation of Se in rice, and SA induces the activity of glyoxylase to protect rice plants from the toxic effect of methylglyoxal (Mostofa et al. 2020). These studies indicate that SA can improve the resistance of plants to Se stress, and there are few studies on the fruit trees.

Grape (Vitis vinifera) is a perennial woody vine that does not accumulate Se (Liu et al. 2019). In recent years, some progress has been made in the research and application of SA in improving the quality of fruit trees (Huang 2007; Lin 2016). The external application of SA during the ripening period of grape can increase the total content of phenolics in grape berries, and it gradually increases in parallel with the concentration of Se (Blanch et al. 2020). However, the relationship between external application of SA and the absorption of Se by fruit trees is still unclear. In the previous study, the effects of different concentrations of Se on growth of grape seedlings were studied, and the concentration of  ≥ 0.1 mg/L Se in culture medium inhibits the growth of grape seedlings (Liu et al., 2019). In this study, effects of SA on the growth and uptake of Se by grapevine were studied under Se stress (0.1 mg/L). The purpose of this study was to select the most effective concentration of SA that could alleviate Se stress and promote the Se uptake of grapevine and provide a reference to produce Se-enriched grapes.

Materials and methods

Materials

Stem cuttings of ‘Summer Black’ grapes (triploid seedless grape, a hybrid from Japan, with female parent of ‘Kyoho’ and male parent of ‘Bushu’) that were 10 cm long and had one bud, were collected from the Chengdu Campus Farm of Sichuan Agricultural University (30°42′N, 103°51′E) in December 2019. The stem cuttings were placed in perlite in February 2020 to develop  root and sprout, and the plants were placed in a greenhouse for 30 days. The conditions of greenhouse for the 14 h day were 25ºC, relative humidity 70%, and 4000 Lux; and for the 10 h night were 20 °C, relative humidity 90%, and 0 Lux (Liu et al. 2021). The perlite was irrigated with 1/2 Hoagland solution every 3 days.

Experimental design

When the grape seedlings grew to approximately 15 cm (March 2020), two plants were transplanted into each plastic pot. The pots contained perlite [15 cm (height) × 18 cm (diameter)]. The transplanted grape seedlings were placed in a greenhouse as described in the Materials section (Liu et al. 2021). After transplanting, SA solutions at concentrations of 0, 50, 100, 150 and 200 mg/L were fully sprayed on the leaves of grape seedlings using approximately 10 mL per pot. Each treatment was completed with four replicates (two pots for one replicate) with 40 pots in total. The plants were sprayed again with a solution of SA after 15 days. During seedling growth, the plants were irrigated with 100 mL Hoagland solution that contained 0.1 mg/L Se (Liu et al. 2019) every 3 days, and the Se was added in the form of analytically pure Na2SeO3.

After 1 month of planting (April 2020), the net photosynthetic rate (Pn), transpiration rate (Tr), stomatal conductance (Gs), intercellular CO2 concentration (Ci) and vapor pressure deficit of leaves (VpdL) were measured using Li-6400 photosynthetic system (LI-COR, Lincoln, NE, USA). The conditions during the measurements with Li-6400 photosynthetic system were 400 μmol CO2/mol CO2 concentration, 25 °C, and 1200 μmol/m2/s light intensity, and the plants were measured during 9:00–11:00 AM. After that, the fifth mature leaf from the top of grapevine was selected to determine the contents of photosynthetic pigments, including chlorophyll a, chlorophyll b, and total chlorophyll, by extracting with a 1:1 mixture of acetone and ethanol (Hao et al. 2004). The fourth mature leaf from the top of grapevine was selected to determine the antioxidant enzymes [superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT)] activity, soluble protein content, malondialdehyde (MDA) content, and relative conductivity by the nitroblue tetrazole method, guaiacol colorimetric method and potassium permanganate titration method, Coomassie bright blue staining method, thiobarbituric acid method, and electric conductometer, respectively, as described by Hao et al. (2004). After that, the entire grapevine were harvested and divided into roots, stems and leaves. They were washed repeatedly with tap water and then three times with deionized water. They were dried in an oven at 110 °C for 15 min and then at 80 °C to determine the constant dry weight, and the shoot biomass (stem biomass + leaf biomass) was calculated. The dry tissue samples were finely ground. The proline content was determined using the sulfosalicylic acid method (Hao et al. 2004). To determine the total content of Se, nitrate: perchloric acid (4:1 by volume) was added to the finely dried tissue sample and incubated for 12 h before digestion until the solution was transparent. After hydrochloric acid reduction, the total Se content was determined by hydride generation-atomic fluorescence spectrometry (Bao 2000). The final tissue sample was extracted with 6 mol/L hydrochloric acid, and the extracted solution was added to nitrate: perchloric acid (4:1 by volume) solution to digest until the solution was transparent. After hydrochloric acid reduction, the inorganic Se content was determined by hydride generation-atomic fluorescence spectrometry (Bao 2000). The following measurements were done: organic Se content = total Se content–inorganic Se content; and Se content in shoots = (Se content in stems × stem biomass + Se content in leaves × leaf biomass)/ shoot biomass (Rastmanesh et al. 2010).

Statistical analyses

Statistical analyses were performed using SPSS 20.0.0. Data were analyzed with a one-way analysis of variance (ANOVA) with the least significant difference at the 95% confidence level. A regression analysis was used to analyze the relationship between SA and biomass or total Se content. The relationships among indicators were analyzed by Pearson correlation.

Results

Biomass

When the concentration of SA was up to 150 mg/L, the various types of tissue biomass of grapevine gradually increased, whereas they gradually decreased when the concentration of SA was > 150 mg/L under Se stress (Table 1). Compared with the control, concentrations of 150, 200 and 250 mg/L SA increased the root, stem, leaf and shoot biomass of grapevine, respectively. When the SA concentration was 150 mg/L, the root, stem, leaf and shoot biomass of grapevine significantly increased (p < 0.05) by 38.89%, 47.24%, 40.00% and 41.48%, respectively, compared with the control. In addition, the regression analysis showed that SA had a linear relationship with the root biomass (y = 0.0002x + 0.128, R2 = 0.570, p = 0.001) and had a liner relationship with the shoot biomass (y = 0.001x + 0.713, R2 = 0.689, p = 0.000). SA had no significant effects on the root/shoot ratio of grapevine compared with the control (p > 0.05).

Table 1.

Biomass

SA (mg/L) Root (g/plant DW) Stem (g/plant DW) Leaf (g/plant DW) Shoot (g/plant DW) Root/shoot ratio
0 0.126 ± 0.005c 0.127 ± 0.007c 0.590 ± 0.005d 0.716 ± 0.003c 0.176 ± 0.007a
100 0.133 ± 0.009c 0.131 ± 0.005c 0.616 ± 0.014c 0.746 ± 0.018c 0.178 ± 0.016a
150 0.175 ± 0.007a 0.187 ± 0.009a 0.826 ± 0.012a 1.013 ± 0.003a 0.173 ± 0.007a
200 0.170 ± 0.004ab 0.182 ± 0.006ab 0.820 ± .015a 1.002 ± 0.021a 0.169 ± 0.002a
250 0.160 ± 0.005b 0.173 ± 0.008b 0.795 ± 0.013b 0.968 ± 0.019b 0.166 ± 0.003a
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05)

DW dry weight, Shoot biomass = stem biomass + leaf biomass

Photosynthetic pigment content

When the SA concentration was up to 150 mg/L, the contents of chlorophyll a, chlorophyll b and total chlorophyll in grapevine tended to increase; however, they decreased when the SA concentration was > 150 mg/L under Se stress (Table 2). When the concentration of SA was 150 mg/L, the contents of chlorophyll a, chlorophyll b, and total chlorophyll were at their highest, which was 13.41% (p < 0.05), 11.48% (p < 0.05), and 12.88% higher (p < 0.05), respectively, compared with the control. Only a concentration of 200 mg/L SA enhanced the chlorophyll a/b ratio of grapevine compared with the control, while the other concentrations of SA had no significant (p > 0.05) effects.

Table 2.

Photosynthetic pigment content

SA (mg/L) Chlorophyll a (mg/g FW) Chlorophyll b (mg/g FW) Total chlorophyll (mg/g FW) Chlorophyll a/b
0 1.469 ± 0.034c 0.549 ± 0.022bc 2.018 ± 0.032c 2.679 ± 0.146b
100 1.487 ± 0.017c 0.527 ± 0.017c 2.014 ± 0.001c 2.824 ± 0.125ab
150 1.666 ± 0.026a 0.612 ± 0.019a 2.278 ± 0.025a 2.724 ± 0.108b
200 1.609 ± 0.036b 0.551 ± 0.020bc 2.160 ± 0.049b 2.924 ± 0.097a
250 1.580 ± 0.035b 0.584 ± 0.016ab 2.164 ± 0.049b 2.708 ± 0.041b
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). FW = fresh weight

Photosynthetic characteristics

Different concentrations of SA increased the Pn, Gs, Ci, and Tr of grapevine compared with the control under Se stress (Table 3). The Pn, Gs, Ci and Tr of grapevine peaked when the concentration of SA was 150 mg/L, which was an increase of 268.44% (p < 0.05), 35.37% (p < 0.05), 34.69% (p < 0.05), and 72.02% (p < 0.05), respectively, compared with the control. At higher SA concentrations (200 and 250 mg/L), Pn, Gs,Ci and Tr decreased. SA reduced the VpdL of grapevine compared with the control.

Table 3.

Photosynthetic characteristic

SA (mg/L) Pn (μmol CO2/m2/s) Gs (mol H2O/m2/s) Ci (µmol CO2/mol) Tr (mmol H2O/m2/s) VpdL (kPa)
0 1.971 ± 0.058e 0.0554 ± 0.0023d 182.2 ± 3.33d 1.523 ± 0.075d 3.667 ± 0.027a
100 2.151 ± 0.022d 0.0597 ± 0.0011c 196.3 ± 3.55c 1.591 ± 0.036 cd 3.356 ± 0.037b
150 7.262 ± 0.075a 0.0750 ± 0.0020a 245.4 ± 6.29a 2.620 ± 0.048a 3.116 ± 0.054d
200 5.354 ± 0.107b 0.0646 ± 0.0025b 227.4 ± 6.97b 1.891 ± 0.093b 3.181 ± 0.080 cd
250 4.152 ± 0.054c 0.0591 ± 0.0021c 221.7 ± 5.14b 1.693 ± 0.047c 3.262 ± 0.090bc
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). Pn = net photosynthetic rate, Tr = transpiration rate, Gs = stomatal conductance, Ci = intercellular CO2 concentration, and VpdL = vapor pressure deficit of leaves

Antioxidant enzyme activities

Compared with the control, different concentrations of SA enhanced the activity of SOD of grapevine, while they reduced the activity of POD of grapevine under Se stress (Table 4). When the concentration of SA was 150 mg/L, the SOD activity reached its highest level, which was an increase of 24.04% (p < 0.05) compared with that of the control. The activity of POD was the lowest when the concentration of SA was 150 mg/L, representing a decrease of 67.87% (p < 0.05) compared with the control. The SA treatments had no significant (p > 0.05) effects on the CAT activity of grapevine compared with the control; a significant difference can be seen only between 150 mg/L (highest CAT activity) and 250 mg/L (lowest CAT activity).

Table 4.

Antioxidant enzyme activity

SA (mg/L) SOD activity (U/g FW) POD activity (U/g/min FW) CAT activity (mg/g/min FW)
0 786.7 ± 844d 981.6 ± 10.36a 1.754 ± 0.097ab
100 815.3 ± 9.74c 562.5 ± 19.64b 1.781 ± 0.028ab
150 975.8 ± 13.11a 315.4 ± 15.88e 1.842 ± 0.069a
200 946.9 ± 19.33b 369.5 ± 17.74d 1.782 ± 0.039ab
250 946.6 ± 20.08b 483.3 ± 14.55c 1.693 ± 0.035b
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). FW = fresh weight

Osmotic regulation substance content, relative conductivity and MDA content

When the concentration of SA was up to 150 mg/L, the contents of proline, soluble protein content, and MDA and the relative conductivity of grapevine gradually decreased, whereas they gradually increased when the concentration of SA was > 150 mg/L (Table 5). When the concentration of SA was 150 mg/L, the contents of proline, soluble protein, MDA, and relative conductivity were the lowest with reductions of 19.17% (p < 0.05), 16.06% (p < 0.05), 22.75% (p < 0.05), and 14.23% (p < 0.05), respectively, compared with the control.

Table 5.

Osmotic adjustment substance content, relative conductivity and MDA content

SA (mg/L) Proline content (μg/g FW) Soluble protein content
(mg/g FW)		 Relative conductivity (μS/cm) MDA content (μmol/kg FW)
0 16.85 ± 0.60a 53.10 ± 0.88a 162.6 ± 548a 136.65 ± 1.44a
100 16.66 ± 0.91ab 46.93 ± 1.11c 158.6 ± 3.57a 129.34 ± 3.04b
150 13.62 ± 0.58c 41.02 ± 0.94d 140.1 ± 4.24c 117.20 ± 3.41c
200 15.45 ± 0.88b 49.11 ± 1.28b 143.5 ± 2.05bc 120.45 ± 2.21c
250 16.23 ± 0.77ab 49.88 ± 1.19b 150.0 ± 5.37b 125.28 ± 2.05b
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). FW = fresh weight

Total Se content

Compared with the control, only the concentration of 250 mg/L SA increased the total Se content in the roots of grapevine, while the other treatments had no significant (p > 0.05) effects under Se stress (Table 6). The different concentrations of SA increased the total Se contents in the stems, leaves, and shoots of grapevine. With the increase in the concentration of SA, the total contents of Se in the stems, leaves, and shoots increased. When the concentration of SA was 250 mg/L, the contents of Se in the roots, stems, leaves, and shoots of grapevine peaked and increased by 10.41% (p < 0.05), 46.10% (p < 0.05), 62.44% (p < 0.05), and 58.46% (p < 0.05), respectively, compared with the control. The regression analysis showed that SA had a quadratic polynomial relationship with the total Se content in roots (y = 0.0001x2 + 0.021x + 25.917, R2 = 0.714, p = 0.001). In addition, it had a linear relationship with the total Se content in shoots (y = 0.001x + 0.713, R2 = 0.689, p = 0.000).

Table 6.

Total Se content

SA (mg/L) Root (mg/kg DW) Stem (mg/kg DW) Leaf (mg/kg DW) Shoot (mg/kg DW)
0 25.85 ± 0.28b 2.618 ± 0.035d 1.672 ± 0.045d 1.839 ± 0.050e
100 25.22 ± 0.93b 2.877 ± 0.098c 1.949 ± 0.020c 2.111 ± 0.018d
150 25.74 ± 0.70b 3.249 ± 0.050b 2.000 ± 0.055c 2.231 ± 0.050c
200 26.02 ± 0.89b 3.793 ± 0.049a 2.362 ± 0.062b 2.622 ± 0.060b
250 28.54 ± 0.91a 3.825 ± 0.077a 2.716 ± 0.080a 2.914 ± 0.061a
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). DW = dry weight. Se content in shoots = (Se content in stems × stem biomass + Se content in leaves × leaf biomass)/ shoot biomass

Inorganic Se content

When the plants were stressed by Se, an increase in the concentrations of SA resulted in an increase in the contents of inorganic Se in various tissues of grapevine (Table 7). When the concentration of SA was 250 mg/L, the contents of inorganic Se in various tissues of the grapevine reached their maximum. Compared with the control, the contents of inorganic Se in roots, stems, leaves, and shoots of grapevine increased by 131.18% (p < 0.05), 54.50% (p < 0.05), 81.65% (p < 0.05), and 65.69% (p < 0.05), respectively.

Table 7.

Inorganic Se content

SA (mg/L) Root (mg/kg DW) Stem (mg/kg DW) Leaf (mg/kg DW) Shoot (mg/kg DW)
0 0.526 ± 0.011d 0.200 ± 0.007b 0.0278 ± 0.0004e 0.0583 ± 0.0007c
100 0.709 ± 0.010c 0.208 ± 0.011b 0.0299 ± 0.0011d 0.0611 ± 0.0029c
150 0.979 ± 0.025b 0.212 ± 0.004b 0.0369 ± 0.0005c 0.0693 ± 0.0020b
200 0.965 ± 0.033b 0.211 ± 0.008b 0.0407 ± 0.0013b 0.0716 ± 0.0020b
250 1.216 ± 0.027a 0.309 ± 0.010a 0.0505 ± 0.0010a 0.0966 ± 0.0007a
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). DW = dry weight. Se content in shoots = (Se content in stems × stem biomass + Se content in leaves × leaf biomass)/ shoot biomass

Organic Se content

Compared with the control, only the concentration of 250 mg/L SA increased the content of organic Se in the roots of grapevine, while the other treatments had no significant (p > 0.05) effects under Se stress (Table 8). The different concentrations of SA increased the contents of organic Se in the stems, leaves, and shoots of grapevine. With the increase in concentration of SA, the contents of organic Se in the stems, leaves, and shoots increased. When the concentration of SA was 250 mg/L, the contents of organic Se in the roots, stems, leaves, and shoots of grapevine reached their maximum, with increases of 7.94% (p < 0.05), 45.41% (p < 0.05), 62.10% (p < 0.05), and 58.17% (p < 0.05), respectively, compared with the control.

Table 8.

Organic Se content

SA (mg/L) Root (mg/kg DW) Stem (mg/kg DW) Leaf (mg/kg DW) Shoot (mg/kg DW)
0 25.32 ± 0.291b 2.418 ± 0.040d 1.644 ± 0.045d 1.781 ± 0.050e
100 24.51 ± 0.938b 2.669 ± 0.100c 1.919 ± 0.021c 2.050 ± 0.021d
150 24.77 ± 0.672b 3.037 ± 0.049b 1.963 ± 0.055c 2.161 ± 0.050c
200 25.05 ± 0.892b 3.582 ± 0.053a 2.321 ± 0.063b 2.550 ± 0.061b
250 27.33 ± 0.933a 3.516 ± 0.075a 2.665 ± 0.079a 2.817 ± 0.061a
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Values are means (± SE) of four replicates. Significant differences (indicated by different lowercase letters) within a column are based on a one-way analysis of variance with least significant difference (p < 0.05). DW = dry weight. Se content in shoots = (Se content in stems × stem biomass + Se content in leaves × leaf biomass)/ shoot biomass

Correlation between biomass and Se content

There was no correlation between the root total Se content, root organic Se content, and stem inorganic Se content (p > 0.05) with the biomass of various tissues (Table 9). The root biomass was highly significantly positively correlated (p < 0.01) with the contents of total Se in the stem, organic Se in the stem, inorganic Se in the roots, and inorganic Se in the leaves, respectively, and significantly positively correlated (0.01 ≤ p < 0.05) with the leaf total Se content, shoot total Se content, leaf organic Se content, and shoot organic Se content, respectively. The stem biomass was highly significantly positively correlated (p < 0.01) with the stem total Se content, shoot total Se content, stem organic Se content, shoot organic Se content, root inorganic Se content, and leaf inorganic Se content, respectively, and significantly (0.01 ≤ p < 0.05) positively correlated with the leaf total Se content, leaf organic Se content, and shoot inorganic Se content, respectively. The leaf or shoot biomass was highly significantly positively correlated with the stem total Se content, leaf total Se content, shoot total Se content, stem organic Se content, leaf organic Se content, shoot organic Se content, root inorganic Se content, and leaf inorganic Se content (p < 0.01), respectively, and significantly positively correlated with the shoot inorganic Se content (0.01 ≤ p < 0.05).

Table 9.

Correlation between biomass and Se content

Items Root biomass Stem biomass Leaf biomass Shoot biomass Root total Se Stem total Se Leaf total Se Shoot total Se Root organic Se Stem organic Se Leaf organic Se Shoot organic Se Root inorganic Se Stem inorganic Se Leaf inorganic Se Shoot inorganic Se
Root biomass
Stem biomass 0.946**
Leaf biomass 0.951** 0.971**
Shoot biomass 0.954** 0.981** 0.999**
Root total Se 0.227 0.309 0.385 0.372
Stem total Se 0.778** 0.797** 0.855** 0.848** 0.564*
Leaf total Se 0.560* 0.624* 0.687** 0.678** 0.704** 0.926**
Shoot total Se 0.624* 0.682** 0.741** 0.733** 0.678** 0.957** 0.996**
Root organic Se 0.096 0.180 0.255 0.242 0.988** 0.447 0.602* 0.571*
Stem organic Se 0.795** 0.811** 0.865** 0.859** 0.519* 0.998** 0.903** 0.938** 0.401
Leaf organic Se 0.558* 0.622* 0.685** 0.676** 0.702** 0.926** 1.000** 0.995** 0.601* 0.902**
Shoot organic Se 0.627* 0.683** 0.742** 0.734** 0.670** 0.959** 0.995** 1.000** 0.563* 0.941** 0.995**
Root inorganic Se 0.784** 0.816** 0.868** 0.862** 0.635* 0.906** 0.909** 0.922** 0.508 0.886** 0.907** 0.920**
Stem inorganic Se 0.272 0.324 0.393 0.381 0.842** 0.622* 0.812** 0.776** 0.787** 0.566* 0.811** 0.767** 0.760**
Leaf inorganic Se 0.647** 0.713** 0.774** 0.766** 0.742** 0.913** 0.956** 0.959** 0.636* 0.886** 0.954** 0.955** 0.955** 0.850**
Shoot inorganic Se 0.504 0.579* 0.627* 0.620* 0.811** 0.804** 0.920** 0.905** 0.724** 0.762** 0.918** 0.899** 0.901** 0.951** 0.965**
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The correlation was based on the Pearson correlation analysis function of SPSS 20.0.0. **: Correlation is significant at the 0.01 level (2-tailed test). *: Correlation is significant at the 0.05 level (2-tailed test). N = 20

Discussion

When plants are subjected to environmental stress, both their growth and metabolic activity are inhibited, and SA plays a key role in regulating plant growth (Hayat et al. 2010). Under salt stress, SA increases the plant height, leaf area and biomass accumulation of Hosta ensata, and reduces the increase in salt damage index (Tan 2021). Under heavy metal stress, SA can induce the increase in activity of H+-ATPase and alleviate the inhibitory effect of this stress on the absorption of mineral elements (Shi and Zhu 2008). Simultaneously, SA also alleviates the inhibition of heavy metal stress on the root elongation and fibrous root growth of Trichosthes kirilowii (Zhou 2012). In this experiment, concentrations of 150–250 mg/L SA increased the biomass of various tissues of grapevine and were most effective at a concentration of 150 mg/L SA. In addition, the concentration of SA had a linear response with the root and shoot biomass of grapevine. These results are consistent with those of previous studies on the same plant species (Liu et al. 2021). The primary reason is that SA can not only promote the growth of plant roots, enhance root vitality, and promote the absorption of nutrients by roots, but also affect cell division by regulating the content of some hormones in plants (Chavoushi et al. 2020). Thus, exogenous SA can promote the growth of grapevine under Se stress.

In previous studies, SA increased the chlorophyll content of mustard seedlings under Se stress and relieved the toxicity of Se stress on mustard seedlings (Gupta and Gupta 2016). Similarly, under Se stress, SA alleviates the chlorosis and inhibition of rice growth caused by excessive Se (Mostofa et al. 2020). In this study, SA increased the contents of photosynthetic pigments (chlorophyll a, chlorophyll b, and total chlorophyll), Pn, Gs, Ci, and Tr of grapevine, and reduced the VpdL of grapevine. These results are consistent with those of previous studies (Gupta and Gupta 2016; Mostofa et al. 2020), which found that that SA maintains the stability of photosynthetic pigment content and stimulates the activity of Rubisco (Li et al. 2014). Thus, treatment with exogenous SA helps grape plants to limit the degradation of chlorophyll and improve photosynthesis when subjected to Se stress.

Antioxidant enzymes can alleviate the negative effects on cells caused by the increase in the numbers of active oxygen free radicals in plants that is a result of external environmental stress (Hu et al. 2020). In this experiment, SA enhanced the activity of SOD activity of grapevine. This result is consistent with previous studies in corn (Li 2015), strawberry (Jamali et al. 2016) and wheat (Chen et al. 2016b), which because that SA can regulate the expression of genes related to SOD activity (Zawoznik et al. 2007). One of the mechanisms of SA improving plant resistance is to inhibit the activity of POD, resulting in an increase in the level of H2O2 in plants, which in turn activates related defense genes (Srivastava and Dwivedi 1998). In this experiment, SA reduced the POD activity of grapevine, which may be the method of SA improving plant resistance (Srivastava and Dwivedi 1998), and result the increase of SOD activity. In addition, as a signaling molecule, SA can regulate the expression of genes related to CAT activity (Zawoznik et al. 2007), but also can bind to CAT and inhibit the activity of CAT (Conrath et al. al. 1995). In this study, the insignificant changes in CAT activity of grapevine may be due to the antagonism between the stimulation of CAT activity by Se stress and the inhibition of CAT activity by SA, which need further study. So, SA can alleviate the inhibitory effect of Se stress on grapevine growth by inhibiting the severe peroxidation in plants under Se stress.

Soluble protein and proline are important osmotically active substances in plants, which can regulate the osmotic pressure of cells by activating some adaptive responses in plants and play protective roles (Teixeira and Pereira 2007). The application of SA can increase the content of soluble proteins by inducing the synthesis of protein kinase and increasing the activity of nitrate reductase (Faried et al. 2017). In addition, it induces the expression of dehydrin gene and promotes the accumulation of proline (Hayat and Ahmad 2007). Under low temperature stress, SA increases the contents of soluble protein and proline in muskmelon and reduces the relative conductivity and MDA content (Diao et al. 2018). In this experiment, SA decreased the contents of soluble protein and proline in grapevine to some extent, which differs from the results of previous studies (Faried et al. 2017; Hayat and Ahmad 2007; Diao et al. 2018). The high Se stress can disrupt the antioxidant system of plants by increasing the contents of proline and free amino acids (Ulhassan et al. 2019). Therefore, with the increase of SA concentration in this experiment, the proline and soluble protein contents of grapevine showed a trend of first decreasing and then increasing may because the appropriate concentration of SA (150 mg/L) could inhibit the interferes with the antioxidant system of plants by increasing the content of proline and free amino acids under Se stress (Ulhassan et al. 2019). Similarly, when the SA concentration was 150 mg/L, the relative conductivity and MDA content of grapevine got the lowest level, and the relative conductivity and MDA content of grapevine increased when the SA concentration was higher than 150 mg/L. This further explained that the concentration of 150 mg/L SA could effectively regulate the of osmotic adjustment substance content in grapevine, reduce the degree of membrane lipid peroxidation in plant cells, and alleviate the damage to plants caused by Se stress. However, the mechanism for this merits further exploration.

When Se is supplied to plants in the form of selenate, most of the Se absorbed by plants is transported to the shoots, while selenite causes the Se absorbed by plants to be primarily concentrated in the roots (Terry et al. 2000). Thus, the distribution of Se with different valence states in plants also differs greatly. In this experiment, the content of Se in the roots of grapevine was much higher than that in the shoots under Se stress caused by sodium selenite, which was consistent with the results of previous studies (Liu et al. 2021). Under Se stress, the absorption of mineral nutrients in plants is inhibited (Dai et al. 2017). However, SA changes the absorption and transport of mineral elements in plants (Wang 2014; Xia et al. 2020). For example, SA promotes the absorption of phosphorus and potassium nutrients and micronutrient elements, such as zinc and iron, in Malus hupehensis (Cao et al. 2021). Similarly, under copper stress, SA alleviates the inhibitory effect of copper stress on the absorption of elements, such as calcium, iron, and manganese, in tobacco (Xu et al. 2015). In this study, SA increased the total uptake of Se, inorganic Se, and organic Se of grapevine to some extent, and it was most effective at a concentration of 200 mg/L SA. Thus, SA could promote the uptake of Se by grapevine in a manner similar to that of other nutrients in plants (Cao et al. 2021; Xu et al. 2015), but the mechanism merits further study. In addition, in this experiment, SA had a linear or quadratic polynomial relationship with the total Se of the roots and shoots in grapevine. This could be related to the fact that SA can affect the absorption and transport of mineral elements by plants, and the interaction between ions could affect the absorption and accumulation of certain elements by plants (Xia et al. 2020). In this experiment, a correlation analysis showed that, except for the root total Se content, root organic Se content, and stem inorganic Se content did not correlate with the various biomass of different tissues, and the shoot inorganic Se content did not correlate with the root biomass, whereas the other various Se contents had highly significant or significantly positive correlations with the various biomass tissues. In addition, the shoot biomass had highly significant positive correlation with the shoot organic Se content, and significant positive correlation with the shoot inorganic Se content. The root biomass had no correlation with root organic Se content, but had highly significant positive correlation with root inorganic Se content. These result indicated that organic Se had a better effect on promoting the growth of shoot, while the inorganic Se mainly promoted the growth of root. This may be because the mostly form of Se directly absorbed by plant roots from soil is inorganic Se, while the Se in plant roots is mostly transported to the shoot in the form of organic Se such as selenomethionine and selenocysteine (Deng 2015). Thus, the appropriate concentration of SA could not only promote the growth of grapevine but was also leading to the accumulation of Se in grapevine.

Conclusions

Under Se stress, SA promoted the growth of grapevine by increasing their biomass, chlorophyll content, and amount of photosynthesis. It also improved stress resistance by changing the activity of antioxidant enzymes, the contents of osmotic regulation substances, relative conductivity and MDA content. SA also promoted the uptake of Se by grapevine to some extent. The SA had a linear or quadratic polynomial relationship with root biomass, shoot biomass, root total Se content, and shoot total Se content. Therefore, SA could promote the growth and uptake of Se by grapevine. Future study should focus on the effects of SA on the mechanisms of Se uptake and partitioning among organs of grapevine.

Acknowledgements

This work was financially supported by Sichuan Science and Technology Program (2019JDJQ0043).

Declarations

Conflict of interest

The authors declare no conflict and competing interest.

Footnotes

Publisher's Note

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