Effect of Salt Stress on the Growth, Physiology, and Mineral Nutrients of Two Penstemon Species

Authors:
Asmita Paudel Department of Plants, Soils, and Climate, Utah State University, 4820 Old Main Hill, Logan, UT 84322, USA

Search for other papers by Asmita Paudel in
This Site
Google Scholar
Close
and
Youping Sun Department of Plants, Soils, and Climate, Utah State University, 4820 Old Main Hill, Logan, UT 84322, USA

Search for other papers by Youping Sun in
This Site
Google Scholar
Close

Click on author name to view affiliation information

Abstract

Penstemons are a diverse group of flowering plants valued for their ability to enhance the visual appearance of urban landscapes. Penstemon barbatus (Cav.) Roth ‘Novapenblu’ (rock candy blue® penstemon) and Penstemon strictus Benth ‘Rocky Mountain’ (rocky mountain beardtongue) are widely used in landscapes, but their tolerance to soil salinity remains poorly understood. This study aimed to investigate the effects of salinity levels at electrical conductivities (ECs) of 1.0 (nutrient solution), 2.5, 5.0, 7.5, and 10.0 dS⋅m−1 on two penstemons (P. barbatus and P. strictus). Penstemons were irrigated with nutrient or saline solution for 8 weeks and various growth and physiological data were recorded before harvest. Salinity stress degraded the visual quality of penstemon species and led to a reduction in the growth rate and biomass production. Leaf burn and necrosis were observed in penstemons because of salinity stress. The visual score of P. barbatus and P. strictus decreased with increasing EC levels in the saline solution. When irrigated with saline solution at an EC of 7.5 dS⋅m−1, Penstemon barbatus and P. strictus had severe-to-moderate foliar salt damage with average visual scores of 1.7 and 2.5, respectively (0 = dead plant; 5 = excellent plant without any foliar damage). The two penstemon species had severe foliar salt damage or were dead when irrigated with saline solution at an EC of 10.0 dS⋅m−1. There were 87% and 92% decreases in the leaf area of P. barbatus and P. strictus, respectively, when irrigated with saline solution at an EC of 10.0 dS⋅m−1 compared with those in the control. Although not statistically significant, there were 7% to 18% decreases in shoot dry weight of P. barbatus when irrigated with saline solutions at ECs of 2.5 to 10.0 dS⋅m−1 compared with control. However, P. strictus displayed declines of 13% to 31% in shoot dry weight as the salinity levels of the irrigation solution increased. As the salinity levels increased, the net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration (E) rates decreased. Furthermore, sodium (Na+) and chloride (Cl) contents of P. barbatus and P. strictus increased with the increase in salinity levels of the treatment solution. Consequently, P. barbatus and P. strictus demonstrated sensitivity to salinity stress at ECs of 7.5 and 10.0 dS⋅m−1. This study provides important insights for their effective utilization in landscaping practices within saline-prone areas.

Ornamental plants play a significant role in the horticultural industry because they are widely used in landscaping to create visually appealing outdoor environments. Traditionally, homeowners have used good-quality water to irrigate landscape plants because of the primary importance of their external appearance. However, landscape plants consume a substantial amount of water. The water requirement for producing 1 kg of dry matter in ornamental plants ranges from 100 kg to 350 kg, depending on the plant species, cultivation system, and growing environment (Fornes et al. 2007).

As the population and agricultural production increase, there is a growing competition for good-quality water. Although recycled water can be used to irrigate landscape plants, it often contains a higher salt content, which can lead to soil salinity (Carter and Grieve 2008). Recycled or reclaimed water is being used to irrigate landscape plants in many parts of the world, which can be a significant factor contributing to soil salinity in urban landscapes (Gorji et al. 2015). Ornamental plants are sold in potted containers filled with substrates such as peatmoss and grown under field conditions (Reid and Jiang 2012). Whether grown in pots or in landscapes, ornamental plants are influenced by soil salinity and irrigation water quality (Gracia-Caparros and Lao 2018).

The presence of excessive salts reduces the availability of water to plants by decreasing the soil water potential. As a result, plants experience limited access to water, hindering essential physiological processes such as nutrient uptake, photosynthesis, and cellular expansion (Munns 2002; Zhang et al. 2013). Excessive salt levels disrupt the ionic balance and impose osmotic stress on plants, resulting in severe damage to their morphology, biomass, and biochemical processes (Rahneshan et al. 2018; Zhang et al. 2013). Soil salinity leads to increased sodium (Na+) and chloride (Cl) contents in plants, which affect the normal ionic activities in plants (Singh et al. 2014).

Plants have developed various strategies to combat these challenges, including osmotic adjustment, compartmentalization, which helps store excess Na+ in the vacuole, and the synthesis of osmolytes (Queiros et al. 2009; Rahneshan et al. 2018; Silva et al. 2015). Osmolytes, such as proline, protect plant cells, aiding in osmotic adjustment and increasing salinity tolerance (Rahneshan et al. 2018). Additionally, high salt levels can affect the metabolism of sensitive plants and cause the accumulation of toxic ions, disrupting normal cellular processes (Munns and Tester 2008). The effects of salinity in various ornamental plants have been previously studied. For example, Sedum telephium (autumn joy) and Sedum reflexum (blue spruce) were considered relatively salt-tolerant, whereas Sedum rupestre (angelina) and Evolvulus glomeratus (blue daze) were found to be less tolerant (Hooks and Niu 2019). Similarly, Tetraneuris acaulis cultivar arizonica (arizona four-nerve daisy) was reported as a salt-tolerant species (Paudel et al. 2019).

Among the diverse array of ornamental plants, penstemons stand out as one of the most attractive native flowers of North America, with high aesthetic importance in urban landscape, leading to their increasing popularity. Penstemon represents America’s largest endemic genus within the Plantaginaceae family, encompassing more than 270 species (Kramer 2009). These plants are commonly used in gardens because of their showy flowers during spring and summer (Lattier 2016) and have been used in ecological restoration efforts (Howe et al. 2006). Most penstemon species are drought-tolerant and thrive in well-drained soils (Kratsch 2011). In the United States, the annual sales of potted penstemon for garden and landscape uses are estimated at $3.2 million (US Department of Agriculture 2020).

Penstemon species are listed as herbaceous plants that have medium tolerance to saline soil (Jull 2009). Previous research of the salinity tolerance of penstemons is limited. Niu and Rodriguez (2006) investigated the salt tolerance of Penstemon eatonii A. Gray (firecracker penstemon), Penstemon pseudospectabilis M.E. Jones (desert beardtongue), and Penstemon strictus Benth. up to an electrical conductivity (EC) of 12.0 dS⋅m−1 and found that these plants exhibited low salt tolerance. Niu and Rodriguez (2006) studied the effect of salinity stress on plant growth, osmotic potential, and mineral nutrient content. However, they did not investigate the gas exchange rate of penstemons, which has been recorded in this present study. Similarly, Zollinger et al. (2007) reported that Penstemon palmeri A. Gray (palmer penstemon) showed intermediate levels of salt tolerance, whereas Penstemon ×mexicali ‘Red Rocks’ (red rocks penstemon) was relatively intolerant to salinity stress at 3000 mg⋅L−1 (∼4.7 dS⋅m−1). Zollinger et al. (2007) tested penstemons up to 5000 mg⋅L−1 (∼6.3 dS⋅m−1). However, during the present study, penstemons were tested for salinity levels up to an EC of 10.0 dS⋅m−1. The present study aimed to access the morphological and physiological responses of two penstemon species, namely Penstemon barbatus (Cav.) Roth ‘Novapenblu’ (rock candy blue® penstemon) and Penstemon strictus ‘Rocky Mountain’ (rocky mountain beardtongue), under salt stress. By examining their response to elevated salt levels, this research contributes to our understanding of the salt tolerance of penstemon species and inform their potential use in landscape and gardening practices. We hypothesized that P. barbatus and P. strictus irrigated with higher salinity levels exhibit foliar salt damage, decreased plant growth, and altered plant physiological status.

Materials and Methods

To assess the salinity tolerance of penstemons across varying salinity levels, a greenhouse study was conducted. The experiment was focused on investigating the morphological, physiological, and biochemical attributes of the penstemons under controlled conditions.

Plant materials and culture conditions.

The experiment was conducted at the Utah State University Research Greenhouse in Logan, UT, USA. Penstemon barbatus (Cav.) Roth ‘Novapenblu’ (rock candy blue® penstemon) and Penstemon strictus ‘Rocky Mountain’ (rocky mountain beardtongue) in 2.8-L injection molded polypropylene containers (Pro-CalTM; South Gate, CA, USA) were purchased from Perennial Favorites (Layton, UT, USA). The plants were transplanted into 7.6-L injection molded polypropylene containers (No. 2B; Nursery Supplies, Orange, CA, USA) filled with a soilless growing medium (Metro-Mix® 820; Canadian sphagnum peatmoss, 35% to 45% composted pine bark, coir, coarse perlite, and dolomitic limestone; SunGro Horticulture, Agawam, MA, USA) on 2 May 2022. Logan City potable water (EC = 0.35 ± 0.01 dS⋅m−1; pH = 7.7 ± 0.2, mean ± SD) was applied to plants when needed. Penstemons were pruned to 12 cm tall, and flowers were removed. Uniform plants that were free from any visible signs of stress or disease were then selected for the salinity study. A shadecloth (60%) was placed at the top of the greenhouse during the research period. The experiment started on 16 Jun 2022 and ended on 12 Aug 2022. Plants were grown in the greenhouse with day temperatures of 26.2 ± 0.5 °C, night temperatures of 22.8 ± 0.6 °C, and a daily light integral of 13.0 ± 2.9 mol⋅m−2⋅d−1.

Treatments.

This study exposed penstemons to either a nutrient or a saline solution at ECs of 1.0, 2.5, 5.0, 7.5, or 10.0 dS⋅m−1. The nutrient (control) solution was prepared in a 100-L tank by adding 0.8 g⋅L−1 15N–2.2P–12.5K water-soluble fertilizer (Peters Excel 15–5–15 Cal-Mag Special; ICL Specialty Fertilizers, Dublin, OH, USA) to reverse osmosis water. The saline solutions were prepared by adding sodium chloride (NaCl; Fisher Scientific, Waltham, MA, USA) and dihydrate calcium chloride (CaCl2⋅2H2O; Hi Valley Chemical, Centerville, UT, USA) to the nutrient solution at a molar ratio of 2:1 (Table 1). The initial pH of the treatment solutions was adjusted to 6.0 to 6.5 using 88% potassium hydroxide pellets (Sigma-Aldrich, St. Louis, MO, USA) or 1 M nitric acid (Fisher Chemical, Fair Lawn, NJ, USA) as needed. The EC, sodium adsorption ratio (SAR), adjusted SAR (Lesch and Suarez 2009), and elemental analysis results were confirmed by the Utah State University Analytical Laboratory (Logan, UT, USA) (Table 1). Treatment solutions of 1200 mL per pot were manually applied weekly, and 30% of the leachate volume was maintained. The treatment solutions were applied using a beaker through the top of the pot in the morning of each week. Plants were irrigated with 500 to 600 mL of reverse osmosis water when the top (∼1 cm) soilless medium was dry to avoid the confounding effects of drought.

Table 1.

Calcium (Ca2+), magnesium (Mg2+), sodium (Na+), sulphate (SO42-), chloride (Cl), and boron (B) contents, sodium adsorption ratio (SAR), adjusted SAR, and electrical conductivity (EC) of nutrient and saline solutions used to irrigate penstemon plants.

Table 1.

Leachate and substrate EC.

The EC of the leachate was measured by the pour-through method as described by Cavins et al. (2008) using an EC meter (LAQUA Twin; Horiba, Kyoto, Japan) after applying the treatment solution. When the leachate EC was greater than that of the treatment solution, the substrate was washed with reverse osmosis water to maintain similar EC levels in the substrate over time. A single plant was chosen for the measurement of leachate EC in each treatment for each species. After harvest, the substrate EC was determined using the saturated paste extraction method with some changes (Gavlak et al. 2005) after the substrate was left to dry for 2 weeks. Five plants were chosen for measurement in each treatment. The leachate and substrate EC data were pooled across the species because there were no differences observed between species.

Visual quality.

A visual score of 0 to 5 was assigned to each plant biweekly based on the percentage of leaves with burnt leaves or necrosis (Sun et al. 2015) (Table 2). A score of 0 indicated that the plant was dead. A score of 1 indicated severe foliar damage (>90%). A score of 2 indicated moderate foliar damage (51%–90%). A score of 3 indicated slight foliar damage (10%–50%). A score of 4 indicated good quality with minimal foliar damage (<10%). A score of 5 indicated excellent quality without any foliar damage. The plant growth was not considered while determining the visual score.

Table 2.

Visual score of penstemon plants in response to salinity stress.

Table 2.

Growth parameters and plant harvest.

Plant heights (centimeters) were recorded at the beginning and end of the experiment. At harvest, the area (square centimeters) of all leaves was measured for all the surviving plants using a leaf area meter (LI-3100; LI-COR® Biosciences, Lincoln, NE, USA). Additionally, the shoot dry weight (DW) (stem DW + leaf DW) and the root DW of plants were determined by drying the plants for 1 week at 60 °C.

Chlorophyll content, chlorophyll fluorescence, and leaf gas exchange.

Relative chlorophyll content (or leaf greenness) of all plants was determined using a chlorophyll meter [Soil Plant Analysis Development (SPAD)-502; Minolta Camera, Osaka, Japan] before harvest. Eight mature leaves from each plant were measured, and the average value was recorded.

The maximum photochemical quantum yield of photosystem II (PSII) [Fv/Fm = (Fm−Fo)/Fm] was measured on dark-adapted leaves using a chlorophyll fluorometer (PEA version 12.1; Hansatech Instrument Ltd., Norfolk, UK), where Fo denotes the minimum fluorescence at low-modulated light and Fm denotes the maximum fluorescence signal at saturating light. Six plants for each species and treatment were used for measurement. First, leaves were adapted in the dark for at least 30 min using leaf clips (diameter, 4 mm) (Hansatech Instrument Ltd.). Measurements were performed in the middle of fully developed leaves on both species. Additionally, the performance index (PIabs) for energy conservation from photons absorbed by PSII was recorded.

Leaf gas exchange of five plants for each species and treatment was measured using a portable photosynthesis system (CIRAS-3; PP Systems, Amesbury, MA, USA) with an automatic universal leaf cuvette (PLC3; PP Systems). The leaf net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of plants in each treatment were recorded based on the measured carbon dioxide (CO2) and water vapor (H2O) exchange on the youngest fully emerged leaves. All plants were watered 1 d before measurements to avoid water stress condition.

Mineral analyses.

Dried penstemon leaves were ground with a stainless-steel Wiley mill (Thomas Scientific, Swedesboro, NJ, USA) and allowed to pass through a 1-mm mesh screen. The powder samples were analyzed at the Utah State University Analytical Laboratories for mineral contents. In brief, the concentrations of Na+, calcium (Ca2+), potassium (K+), boron (B), magnesium (Mg2+), phosphorus (P), zinc (Zn2+), and manganese (Mn2+) were determined using nitric/hydrogen peroxide following the protocol described by Gavlak et al. (2005). The concentration of Cl was measured using a Flow Injection Analysis and Ion Chromatograph System (QuikChem 8000; Lachat Instrument, Loveland, CO, USA) and expressed on a dry plant basis (mg⋅g−1). To determine the levels of Na+, Ca2+, K+, B, Mg2+, P, Zn2+, and Mn2+, 0.5 g of powdered samples were mixed with 6 mL of nitric acid (HNO3) in a digestion tube, which was then subjected to a digestion block for 10 min at 80 °C, followed by cooling for 2 min. A total of 2 mL of 30% hydrogen peroxide (H2O2) was added into the digestion tube that was again placed in the digestion block at 130 °C for 1 h. The digestion tubes were mixed using a vortex stirrer. Then, the digestion tube was cooled at room temperature, and the contents of the digestion tube were transferred into a 25-mL volumetric flask. The digest was analyzed using inductively coupled plasma-optical emission spectrometry (iCAP 6300 ICP-AES; Thermo Scientific, Waltham, MA, USA) and reported based on DW (mg·g−1).

Proline estimation.

The acid-ninhydrin method was used for the quantification of proline in penstemons (Bates et al. 1973; Claussen 2005; Rakesh et al. 2021). In brief, leaf samples collected after the sixth irrigation event were frozen in liquid nitrogen and subsequently stored at −80 °C until use. Leaf samples (0.2 g) were ground in 5 mL of 3% sulfosalicylic acid (Spectrum Chemical, Gardena, CA, USA) and centrifuged for 5 min at room temperature using a benchtop centrifuge (SpectrafugeTM Labnet 6C Centrifuge; The Laboratory Depot, Dawsonville, GA, USA) with 5000 gn. After centrifugation, 200 μL of supernatant, 200 µL of glacial acetic acid (Fisher Chemical, Fair Lawn, NJ, USA), and 200 μL of acid ninhydrin (Sigma-Aldrich, St. Louis, MO, USA) were combined in a tube and incubated in a boiling water bath at 95 °C for 1 h. After 1 h, tubes were immediately placed in an ice bath to arrest the reaction. Thereafter, 400 μL of toluene (Fisher Chemical, Colonnade Road, Ottawa, ON, USA) was added to each tube, and the mixture was vortexed and left to settle for 10 min. The upper layer of 200 μL of the resulting solution was pipetted to a microplate reader (Greiner bio-one; Cellstar, F-bottom, Monroe, NC, USA). Absorbance was recorded using a spectrophotometer (Spectra max M2; Molecular Devices, CA, USA) at 520 nm. Proline (L-Proline, St. Louis, MO, USA) was taken as standard, and a graph was plotted to estimate the proline content in the samples. The concentration of proline was calculated as follows:
µmol·g1 tissue = µg proline·mL1* mL toluene/115.5 * 25·g1 sample

Experimental design and statistical analysis.

The experiment was conducted using a randomized complete block design with 10 replications encompassing five treatments and two species. Each experimental unit consisted of one pot containing a single plant. Statistical analyses were conducted using SAS (version 14.1; SAS Institute, Cary, NC, USA) with PROC MIXED procedure. An analysis of variance (ANOVA) was performed to evaluate the effects of saline solution irrigation and species on various plant characteristics, including growth, gas exchange, and mineral nutrients. To normalize the data, logarithmic transformation was applied for all response variables to improve model performance. Dead plants were excluded from the data analysis of all parameters except for the visual score. Because of the diverse growth habits of each species, means separation among treatments was adjusted using Tukey’s method for multiplicity at α = 0.05. Furthermore, means separation between species was conducted for proline content. To explore relationships, correlation analyses were performed between visual scores, Na+ and Cl contents, and K+/Na+ and Ca2+/Na+ ratios. Correlation analyses of gas exchange parameters, Na+ and Cl contents, and K+/Na+ and Ca2+/Na+ ratios were performed. Additionally, linear and quadratic trend analyses of the plant growth data were performed.

Results

During this study, we delve into the effects of salinity stress on P. barbatus and P. strictus, with a focus on visual quality, plant growth, and physiological parameters. Understanding these responses is critical to formulating strategies to mitigate the adverse effects of salinity stress on urban landscapes.

Visual score and plant growth parameters.

Salt damage was observed on penstemon species at higher salinity levels, mainly in the form of burnt leaves and necrosis (Fig. 1). After the second irrigation event, visual scores were affected by salinity (P < 0.0001) (Table 3), and an interaction was observed between species × salinity (P = 0.004). The average visual score of P. barbatus at an EC of 10.0 dS⋅m−1 was 4.3, which was lower than that of other treatments (Fig. 2). After the fourth irrigation event, visual scores were affected by salinity (P < 0.0001), and an interaction was observed between species × salinity (P = 0.002) (Table 3). Penstemon barbatus had an average visual score of 3.7 when irrigated with saline solution at an EC of 7.5 dS⋅m−1 (Fig. 2). However, minimal to no foliar salt damage was observed in P. strictus for up to 4 weeks. When irrigated with saline solution at an EC of 10.0 dS⋅m−1, the visual scores were 3.0 and 3.7 for P. barbatus and P. strictus, respectively. After the sixth irrigation event, visual scores were affected by salinity (P < 0.0001), and an interaction was observed between species × salinity (P < 0.0001) (Table 3). Penstemon barbatus and P. strictus had average visual scores of 1.6 and 3.4, respectively, when irrigated with saline solution at an EC of 7.5 dS⋅m−1 (Fig. 2). Visual scores were 1.2 and 1.6, respectively, when P. barbatus and P. strictus were irrigated with saline solution at an EC of 10.0 dS⋅m−1. When irrigated with saline solution at ECs of 7.5 and 10.0 dS⋅m−1, one P. barbatus plant in each treatment died. Finally, after the eighth irrigation event, salinity affected the visual score (P < 0.0001), and the interaction between species × salinity was insignificant (Table 3). Visual scores were 3.2 and 4.0 for P. barbatus and P. strictus, respectively, when irrigated with saline solution at an EC of 5.0 dS⋅m−1 (Fig. 2). Penstemon barbatus and P. strictus had average visual scores of 1.7 and 2.5, respectively, when irrigated with saline solution at an EC of 7.5 dS⋅m−1. Similarly, visual scores were 1.4 and 1.3, respectively, when P. barbatus and P. strictus were irrigated with saline solution at an EC of 10.0 dS⋅m−1. Furthermore, two P. barbatus died when irrigated with saline solution at an EC of 7.5 dS⋅m−1. At an EC of 10.0 dS⋅m−1, three P. barbatus and five P. strictus plants were dead.

Fig. 1.
Fig. 1.

Photos of representative penstemons after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

Table 3.

Summary of the analysis of variance of the effects of species, treatments, and their interactions on visual score (VS) of Penstemon barbatus and P. strictus after irrigating with a nutrient solution [electrical conductivity (EC) = 1.0 dS⋅m−1] or saline solution (EC = 2.5, 5.0, 7.5, or 10.0 dS⋅m−1) for a period of 2, 4, 6, and 8 weeks, as well as on the increase in plant height (Ht), leaf area (LA), shoot dry weight (DW), root DW, chlorophyll content [Soil Plant Analysis Development (SPAD)], chlorophyll fluorescence parameters (Fv/Fm and PIabs), net photosynthetic rate (Pn), stomatal conductance (gs), transpiration rate (E), and proline content after irrigating for a period of 8 weeks in a greenhouse.

Table 3.
Fig. 2.
Fig. 2.

Visual scores of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period 2 (A), 4 (B), 6 (C), and 8 (D) weeks in a greenhouse. Vertical bars represent SEs of 10 plants. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Visual scores: 0 = dead plant caused by salinity stress; 1 = severe foliar damage (burnt leaves and necrosis, >90%); 2 = moderate foliar damage (51%–90%); 3 = slight foliar damage (10%–50%); 4 = good quality with minimal foliar damage (<10%); and 5 = excellent without foliar damage (Sun et al. 2015).

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

After 8 weeks of growing under different saline solutions, the two penstemon species exhibited differences in terms of growth measurements. Saline solution irrigation significantly impacted the height of penstemon plants (P < 0.0001) (Table 3), leading to an 84% to 94% reduction in the height of P. barbatus at ECs of 7.5 and 10.0 dS⋅m−1 compared with the control (Table 4). However, there was no notable difference in the plant height of P. strictus among treatments. Furthermore, leaf area varied significantly with species and salinity (P < 0.0001) (Table 3). The leaf area of P. barbatus and P. strictus decreased linearly with increasing EC levels in the saline solution (P < 0.0001) (Table 4). In addition, the leaf area of P. strictus decreased quadratically (P < 0.0001). Compared with the control, there was an 87% reduction in the leaf area of P. barbatus when irrigated with saline solutions at ECs of 7.5 and 10.0 dS⋅m−1. Similarly, a 69% to 92% reduction in the leaf area of P. strictus was observed when irrigated with saline solutions at ECs of 7.5 and 10.0 dS⋅m−1. Furthermore, although it is not statistically significant, there was a 12% to 39% reduction in the leaf area of P. barbatus and P. strictus when irrigated with saline solutions at ECs of 2.5 and 5.0 dS⋅m−1.

Table 4.

Increase in the plant height (ht) and leaf area of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 or saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

Table 4.

Shoot dry weight was impacted by salinity (P = 0.003) (Table 3). The shoot dry weight of P. strictus decreased linearly with increasing EC levels in the saline solution (P = 0.02) (Table 5). Compared with the control, although not significant, there were 7%, 18%, 7%, and 12% decreases in shoot DW of P. barbatus when irrigated with saline solutions at ECs of 2.5, 5.0, 7.5, and 10.0 dS⋅m−1, respectively. Similarly, shoot DW of P. strictus decreased by 13%, 13%, 30%, and 31%, respectively, when irrigated with saline solutions at ECs of 2.5, 5.0, 7.5, and 10.0 dS⋅m−1. Furthermore, root DW was significantly impacted by salinity (P = 0.004) (Table 3). Root DW of P. strictus decreased linearly (P = 0.01) and quadratically (P = 0.047) with increasing EC levels in the saline solution (Table 5). There were 45% to 50% decreases in root DW of P. barbatus when irrigated with saline solution at ECs of 5.0 to 10.0 dS⋅m−1 compared with the control. Similarly, when irrigated with saline solution at an EC of 10.0 dS⋅m−1, there was a 50% reduction in root DW of P. strictus.

Table 5.

Dry weights (DWs) of shoots and roots of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 or saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

Table 5.

The visual quality and growth data suggest that the penstemons underwent salinity stresses, which can be attributed to the accumulation of salts in the substrate. The EC of the leachate solution remained consistent throughout the experiment (Fig. 3). In addition, the pH of the leachate solution during the experiment was 6.6 ± 0.4. However, the EC of the substrate increased with increasing EC level of saline solution (Fig. 4). The average ECs of the substrate were 11.5, 13.4, and 15.2 dS⋅m−1 when irrigated with saline solution at ECs of 5.0, 7.5, and 10.0 dS⋅m−1, respectively.

Fig. 3.
Fig. 3.

Electrical conductivity (EC) of leachate solution over the course of the experiment collected after Penstemon barbatus and P. strictus were irrigated with a nutrient solution at an EC of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of two measurements.

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

Fig. 4.
Fig. 4.

Electrical conductivity (EC) of soil extraction from Penstemon barbatus and P. strictus irrigated with a nutrient solution at an EC of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of five measurements.

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

Relative chlorophyll content, chlorophyll fluorescence, and gas exchange.

The relative chlorophyll content (SPAD reading) of two penstemon species varied with species and salinity (P < 0.0001) (Table 3). There were 28% and 26% reductions in the SPAD readings of P. barbatus and P. strictus, respectively, at an EC of 5.0 dS⋅m−1 compared with those of the control (Fig. 5). Likewise, 71% and 40% reductions in the SPAD readings were observed in P. barbatus and P. strictus, respectively, when irrigated with saline solution at an EC of 7.5 dS⋅m−1. In addition, Fv/Fm and PIabs readings varied with salinity levels (P < 0.0001) (Table 3). Penstemon barbatus had significant reductions in both Fv/Fm and PIabs when irrigated with saline solution at an EC of 7.5 dS⋅m−1, but readings were similar for P. strictus among treatments.

Fig. 5.
Fig. 5.

Chlorophyll content [Soil Plant Analysis Development (SPAD)], chlorophyll fluorescence parameters (Fv/Fm, and PIabs) of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent standard errors of 10 measurements for SPAD and six measurements for Fv/Fm, and PIabs. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Penstemons were dead or had severe foliar salt damage when treated with saline solution at an EC of 10.0 dS⋅m−1; therefore, the chlorophyll content and fluorescence data were not taken.

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

The net photosynthetic rate (Pn) of two penstemon species decreased with increasing salinity levels of the solution (P < 0.0001) (Table 3). In addition, Pn varied with species (P = 0.0024) and showed interactive effects between species and salinity levels (P = 0.0477). Penstemon barbatus had a Pn of 13.1 μmol⋅m−2⋅s−1 when irrigated with saline solution at an EC of 2.5 dS⋅m−1 (Fig. 6). The net photosynthetic rate of P. barbatus decreased from 18.6 μmol⋅m−2⋅s−1 to 7.9 μmol⋅m−2⋅s−1 when irrigated with saline solution at an EC of 5.0 dS⋅m−1. Similarly, Pn of P. strictus decreased from 20.1 μmol⋅m−2⋅s−1 to 12.6 and 9.5 μmol⋅m−2⋅s−1 when irrigated with saline solutions at ECs of 5.0 and 7.5 μmol⋅m−2⋅s−1, respectively.

Fig. 6.
Fig. 6.

Net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of five measurements. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Gas exchange data of P. barbatus at ECs of 7.5 and 10.0 dS⋅m−1 and P. strictus at an EC of 10.0 dS⋅m−1 were not measured as plants had severe foliar salt damage or were dead.

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

The stomatal conductance (gs) also decreased with increasing salinity levels (P < 0.0001) (Table 3). The gs of P. barbatus decreased from 731.3 to 252.3 mmol⋅m−2⋅s−1 when irrigated with saline solution at an EC of 5.0 dS⋅m−1 (Fig. 6). Similarly, gs decreased from 783.7 to 174.9 mmol⋅m−2⋅s−1 for P. strictus when irrigated with saline solution at an EC of 7.5 dS⋅m−1. The transpiration rate (E) decreased as salinity levels in the solution increased for two penstemon species (P < 0.0001) (Table 3). The E of P. barbatus decreased from 10.3 to 5.4 mmol⋅m−2⋅s−1 when irrigated with saline solution at an EC of 5.0 dS⋅m−1 compared with the control (Fig. 6). Similarly, E decreased from 10.4 to 4.8 mmol⋅m−2⋅s−1 for P. strictus when irrigated with saline solution at an EC of 7.5 dS⋅m−1.

Mineral nutrients.

Leaves accumulated significant number of anions and cations, particularly Na+ and Cl (P < 0.0001) (Table 6). There was a significant effect of species on Na+ accumulation in leaves (P < 0.0001), but not on Cl. After 8 weeks of irrigation, the Na+ content of control plants was 0.05 mg⋅g−1 for P. barbatus and 0.03 mg⋅g−1 for P. strictus. However, the Na+ content increased to 5.02 mg⋅g−1 for P. barbatus and 2.80 mg⋅g−1 for P. strictus when irrigated with saline solution at an EC of 10.0 dS⋅m−1, which were 99-times and 92-times greater than that of their respective controls. Similarly, control plants had Cl contents of 2.3 and 3.0 mg⋅g−1 for P. barbatus and P. strictus, respectively. However, the Cl content increased to 51.1 and 53.5 mg⋅g−1 for P. barbatus and P. strictus, respectively, when irrigated with saline solution at an EC of 10.0 dS⋅m−1; these were 21-times and 17-times greater than that of their respective controls.

Table 6.

Contents of sodium (Na+), chloride (Cl), calcium (Ca2+), potassium (K+), K+/Na+ ratio, and Ca2+/Na+ ratio in leaves of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 or saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

Table 6.

A low increment was observed in the Ca2+ content with increasing salinity levels in the solution, but the content varied with both species and salinity (P < 0.0001) (Table 6). After 8 weeks of irrigation, the Ca2+ content increased from 20.6 to 32.5 mg⋅g−1 for P. barbatus and from 11.7 to 25.5 mg⋅g−1 for P. strictus when irrigated with saline solution at an EC of 10.0 dS⋅m−1 compared with control plants.

The reduction in the K+ content was observed in leaves with increasing salinity levels in the solution (P = 0.04) (Table 6). Penstemon strictus had 10.9%, 18.4%, 8.8%, and 23.4% reductions in the K+ content when irrigated with saline solutions at ECs of 2.5, 5.0, 7.5, and 10.0 dS⋅m−1, respectively, compared with the control. Similarly, there were 15.3%, 9.7%, 2.7%, and 10.8% reductions in the K+ content of P. barbatus leaves when irrigated with saline solutions at ECs of 2.5, 5.0, 7.5, and 10.0 dS⋅m−1, respectively, compared with the control. However, these reductions were not statistically significant. Furthermore, the K+/Na+ and Ca2+/Na+ ratios in penstemon leaves also varied with species and salinity (P < 0.0001) (Table 6). As salinity levels increased in the solutions, a decrease in both ratios was observed. The K+/Na+ ratio was 112-times and 138-times greater in control for P. barbatus and P. strictus, respectively, than that in those irrigated with saline solution at an EC of 10.0 dS⋅m−1. Similarly, the Ca2+/Na+ ratio was 63-times and 48-times greater in control for P. barbatus and P. strictus than that in those irrigated with saline solution at an EC of 10.0 dS⋅m−1, respectively.

In addition, the B content decreased with increasing salinity levels in the solutions for P. barbatus and P. strictus (P < 0.0001) (Table 7). The Mg2+ content remained similar among treatments but varied with species. Furthermore, saline solutions had a significant impact on the P, Zn2+, and Mn2+ contents of penstemons.

Table 7.

Contents of boron (B), magnesium (Mg2+), phosphorus (P), zinc (Zn2+), and manganese (Mn2+) in leaves of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 or saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

Table 7.

Proline content.

The leaf proline content observed in the experiment was mostly species-dependent (P < 0.0001) (Table 3). There was no difference among salinity levels in the proline content of P. barbatus and P. strictus (Table 8). However, a greater proline content was observed in P. strictus when compared with that in P. barbatus. Penstemon strictus had the highest proline content of 1.2 μmol⋅g−1 when irrigated with saline solution at an EC of 7.5 dS⋅m−1.

Table 8.

Proline contents in leaves of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) or saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 in a greenhouse.i

Table 8.

Discussion

Salinity stress can severely impact the overall appearance of plants, making visual quality assessments crucial when evaluating the aesthetic appeal and market value of ornamental plants in landscaping projects and horticultural industries. Visual quality considers factors such as flowers, foliage color, texture, shape, and form. The present data revealed the detrimental effects of salinity on the visual quality of P. barbatus and P. strictus caused by leaf burn and necrosis. The results indicated that P. barbatus experienced more foliar salt damage and was more susceptible to saline water irrigation than P. strictus. Similarly, P. eatonii, P. pseudospectabilis, and P. strictus had salt injury with leaf necrosis and browning when they were irrigated with saline solutions prepared using NaCl, magnesium sulfate (MgSO4), and CaCl2 for 12 weeks (Niu and Rodriguez 2006). In addition, P. ×mexicali exhibited sharp declines in visual quality as salinity levels increased from 3000 to 5000 mg⋅L−1 (∼4.7 to 6.3 dS⋅m−1) (Zollinger et al. 2007). Likewise, severe leaf burns and wilting were observed in P. palmeri when exposed to saline solution greater than 3000 mg⋅L−1 (∼4.7 dS⋅m−1) (Zollinger et al. 2007). In this study, Zollinger et al. (2007) irrigated P. ×mexicali and P. palmeri with a saline solution containing CaCl2 and NaCl at a molar ratio of 2:1.

During this study, we observed salt injury on the leaves of P. barbatus and P. strictus as the salinity levels in the solution increased, but no mortality was observed at less than 7.5 dS⋅m−1. However, Niu and Rodriguez (2006) reported that P. strictus did not survive when irrigated with saline solution at an EC of 3.2 dS⋅m−1 or greater. This difference in observations could be attributed to variations in climate, saline solutions, growing substrates, and irrigation procedures. Saline solutions with various compositions can lead to different responses in plants, influencing nutrient uptake, osmotic regulation, and plant health (Nebauer et al. 2013). Niu and Rodriguez (2006) used saline solutions prepared with NaCl, MgSO4, and CaCl2, whereas the present study only used NaCl and CaCl2. Moreover, local climate conditions and growing substrate properties have been found to influence the response to salinity stress in previous studies (Costello et al. 2003; Fox et al. 2005). Microclimate conditions like temperature and humidity in a greenhouse play an important role in plant physiology and growth patterns.

In addition to its visual effects, salinity stress can significantly impede plant growth. In this study, the plant heights of both P. barbatus and P. strictus were affected by salinity stress. Exposure of ornamental plants to saline conditions can lead to decreased plant growth, which may have the benefit of achieving more compact plant sizes. However, it is essential to consider that maintaining compact plant size may require continued irrigation with saline water, potentially posing harm to other plants in the landscape. Additionally, salinity stress impacts the expansion of cells in young leaves, resulting in a decrease in leaf area (Munns and Tester 2008). Reduced leaf growth is the earliest response of glycophytes when exposed to salinity stress (Munns and Termaat 1986). Plants reduce leaf size to minimize water loss by transpiration, which allows conservation of soil moisture and prevents an increase in salt concentration in the soil (Munns and Tester 2008). In the case of P. barbatus and P. strictus, an increase in EC levels in the saline solution corresponded to a reduction in leaf area. Likewise, the decrease in leaf area was noted in numerous plants as the concentration of saline water increased (Paudel et al. 2019; Sun et al. 2020; Wu et al. 2016).

Plant biomass is one of the most direct indicators of salinity tolerance. Acosta-Motos et al. (2017) reported that the decrease in shoot DW of plants exposed to salinity stress is primarily attributed to the development of smaller and fewer leaves and stunted plant growth. In this study, there was a significant reduction in shoot DW of P. strictus. Similarly, shoot DW of P. ×mexicali and P. palmeri decreased with increasing salinity levels in the solution (Zollinger et al. 2007). Additionally, Niu et al. (2010) found that Angelonia angustifolia (angelonia) cultivars in the Plantaginaceae family exhibited 25% and 50% reductions in shoot DW when irrigated with saline solution at ECs of 5.1 and 7.4 dS⋅m−1, respectively, compared with those at an EC of 2.8 dS⋅m−1. Plant roots are highly susceptible to salinity because they are in direct contact with salts, impacting their ability to absorb water, their water use efficiency, and other physiological processes (Sanchez-Blanco et al. 2014). In this study, there was a decreasing trend in the root DW of penstemons, reflecting the inhibition of root growth caused by osmotic and toxic effects of high salinity (Banon et al. 2012). Inhibition of root growth may have been caused by the reduced capacity of the shoot to deliver nutrients to the roots, which can affect plant development and survival (Munns and Termaat 1986).

The negative effects on the visual quality and stunted growth of P. barbatus and P. strictus may be attributed to the salts accumulated in the growing substrate, which can directly affect plant health. This accumulation of salts in the substrate can be evaluated through the pour-through method as described by Cavins et al. (2008) or the saturated paste extraction method described by Gavlak et al. (2005). During the experiment, although leachate ECs from the substrate remained similar throughout the duration of each treatment, there was a significant difference among the treatments. The EC of the substrate was greater than that of the corresponding saline solution, indicating the presence of salt accumulation in the growing substrate.

The results of the study revealed significant variations in the SPAD readings of P. barbatus and P. strictus under different salinity levels. These findings align with those of previous research that found that increasing levels of salinity in the solution caused reductions in the SPAD readings of several landscape plants (Liu et al. 2017; Niu et al. 2007). Interestingly, the present study also demonstrated species-specific responses to salinity stress. The SPAD readings of P. barbatus exhibited greater sensitivity to salinity compared with P. strictus. This was evident from the larger reductions in SPAD readings for P. barbatus at an EC of 7.5 dS⋅m−1. Furthermore, the measurements of chlorophyll fluorescence parameters (Fv/Fm and PIabs) provided insights into the photosynthetic efficiency of the penstemon species. The significant reduction in Fv/Fm and PIabs for P. barbatus with increasing salinity levels in the solution indicated compromised photosynthetic activity. The Fv/Fm parameter is of crucial importance because it signifies the effectiveness of the light reaction and is extensively used for studying the effects of stress on plants. Salinity stress obstructs the process of electron transfer from the primary acceptor to the secondary acceptor in the PSII, which may have led to a reduction in Fv/Fm (Shu et al. 2012).

Salinity stress can have significant effects on plant growth because it disrupts several essential physiological processes. These processes may encompass interference with photosynthesis, osmoregulation, and mineral supply to the aerial part (Negrao et al. 2017). The photosynthetic apparatus of plants may be harmed, and plant photosynthesis can be inhibited under salinity stress (Taiz et al. 2015). Exposing plants to high levels of soil salinity can disrupt their water balance, resulting in water moving out of plant cells and into the surrounding soil (Munns and Tester 2008). This, in turn, can lead to dehydration and reduction in Pn. Additionally, high levels of salt can also cause damage to chloroplasts, which are responsible for Pn, and interfere with the process of photosynthesis itself. Furthermore, the buildup of excessive amounts of Na+ and Cl- ions can impede Pn, as noted by Zhang et al. (2014). Moreover, salinity stress can also impact gs, which refers to the opening and closing of the stomata. When plants are exposed to high levels of salinity, the stomata may close to conserve water, reducing the uptake of carbon dioxide (CO2) for Pn and the release of oxygen (O2). In the present study, Pn and gs of the penstemons were reduced in response to salinity stress. Similarly, there were decreases in the Pn and gs rates in P. palmeri with increasing salinity levels in the solution (Zollinger et al. 2007). To mitigate the negative impacts of salinity stress on Pn and gs, several strategies can be used. For instance, the application of silicon (Si) can improve the shoot growth and net photosynthetic rates. Research indicated that Si may play a crucial role in sustaining high photosynthetic rates in plants under salt stress conditions (Coskun et al. 2019; Zargar et al. 2019). Furthermore, applying arbuscular mycorrhizal fungi has been found to help maintain osmotic balance, exhibit a greater gs, and improve the overall photosynthetic efficiency of plants (Evelin et al. 2009). In addition, saline conditions may create a water deficit in plants, leading to stomatal closure and, ultimately, a decrease in E (Wang et al. 2019). Likewise, two penstemon species in this study exhibited reductions in E in response to salinity stress.

The nutritional status of a plant is influenced by salinity stress through a complicated network of interactions, which may involve a reduction in the uptake and/or transportation of nutrients from roots to shoots (Munns and Tester 2008). Although low Na+ levels can be beneficial to plants in some situations, moderate and high levels are harmful to most plants (Maathuis 2014). Furthermore, plants take-up Cl ions, which are important for stabilizing membrane potential and regulating pH and turgor (Marschner 2012). Although plants generally require only small amounts of Cl, deficiencies are rare. However, excessive Na+ and Cl ions in plants can lead to toxicity. Under the salinity treatments in this study, the Na+ and Cl contents of penstemon leaves in both species were dramatically increased. This suggests an accumulation of these ions in the plant tissues caused by salinity stress. Importantly, a negative correlation between the visual score and Na+ and Cl contents was observed (P < 0.0001) (Fig. 7). The visual score provides an indication of the foliar salt damage, and the negative correlation suggests that higher Na+ and Cl contents are associated with greater visual damage. In addition to the visual damage, the reduction in Pn observed in the penstemons under salinity stress was also negatively correlated with the Na+ and Cl contents in the leaf tissue (P ≤ 0.009) (Fig. 8). Similarly, leaf Na+ and Cl concentrations in A. angustifolia increased as salinity levels of irrigation water increased (Niu et al. 2010). The increasing ion concentration in the leaves of penstemons could have caused foliar salt damage.

Fig. 7.
Fig. 7.

Correlation analyses between the sodium (Na+), chloride (Cl), potassium-to-sodium ratio (K+/Na+), calcium-to-sodium ratio (Ca2+/Na+), and visual score of Penstemon barbatus and P. strictus. Visual scores: 0 = dead plant caused by salinity stress; 1 = severe foliar damage (burnt leaves and necrosis, >90%); 2 = moderate foliar damage (51%–90%); 3 = slight foliar damage (10%–50%); 4 = good quality with minimal foliar damage (<10%); and 5 = excellent quality without foliar damage (Sun et al. 2015).

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

Fig. 8.
Fig. 8.

Correlation analyses between the sodium (Na+), chloride (Cl), potassium-to-sodium ratio (K+/Na+), calcium-to-sodium ratio (Ca2+/Na+), net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of Penstemon barbatus and P. strictus.

Citation: HortScience 59, 2; 10.21273/HORTSCI17409-23

Calcium plays a crucial role in maintaining the integrity of cell plasma membranes in roots and restricting the toxic effect of Na+ (Gucci and Tattini 1997; Rengel 1992). It also serves as a secondary messenger in regulating signal transduction pathways for abiotic stress response and in promoting K+/Na+ selectivity (Rengel 1992). Similarly, the leaf Ca+ concentration has been reported to increase with increasing salinity in many ornamental plant species (Paudel et al. 2019; Sun et al. 2015; Wu et al. 2016). Consistent with these findings, the present study also observed an increase in leaf Ca+ concentration, likely caused by the use of CaCl2 in the preparation of the saline solution (Table 1). A positive correlation was observed between visual score and K+/Na+ and Ca2+/Na+ ratios (P ≤ 0.05) (Fig. 7). The increment in Ca2+ content was low in penstemons when compared with the Na+ and Cl increments. These findings highlight the role of Ca2+ in mitigating the toxic effects of Na+ and its involvement in maintaining ion selectivity and osmotic adjustment in response to salinity stress (Rengel 1992). The positive correlation between the visual score and Ca2+/Na+ ratio further supports the significance of Ca2+ in minimizing the harmful effects of salinity. Enhancing Ca2+ availability to plants under salinity stress is crucial for maintaining normal physiological processes in plants. In our case, calcium chloride was added to the solution so that plants could presumably access more Ca2+. To increase calcium uptake in plants, boosting water flow to the roots is an option, but it is not ideal because of limited freshwater availability (Yang et al. 2012). Increasing the cation exchange capacity of soil can be another strategy to make more Ca+ available to plants (Mengel 2023).

In plants, K+ serves as the primary cation that counterbalances anions and activates enzymes for metabolic processes, protein and carbohydrate synthesis, and the regulation of stomatal movement (Rahneshan et al. 2018). In the present study, the K+ contents remained similar for P. barbatus and slightly reduced for P. strictus under salinity stress. However, the K+/Na+ and Ca2+/Na+ ratios decreased with increasing salinity levels for both penstemon species. This suggests that the high concentration of Na+ present in saline soils may have replaced the essential K+ and Ca2+ ions in the penstemons, which are crucial for proper growth and development. Furthermore, Pn of the penstemons was reduced in response to salinity and positively correlated with K+/Na+ and Ca2+/Na+ ratios (P ≤ 0.02) (Fig. 8). Similarly, gs and E of P. strictus were also influenced by K+/Na+ and Ca2+/Na+ ratios (P ≤ 0.01) (Fig. 8). These findings suggest that the imbalance caused by the replacement of K+ and Ca2+ with Na+ in the penstemons negatively affected their physiological processes.

Boron plays an important role in several physiological processes in plants, including cell wall structure, root elongation, shoot growth, membrane integrity, and reproduction (Broadley et al. 2012). Boron deficiency can lead to the inhibition of root elongation and shoot meristematic growth (Broadley et al. 2012). In this study, it was observed that the B content was reduced in two penstemons species in response to salinity stress, which also may have contributed to the reduction in the growth of shoots and roots.

Magnesium is a component of chlorophyll and is required for photosynthesis and protein synthesis, whereas P is crucial for nucleic acids and carbohydrate transfer in leaf cells (Hawkesford et al. 2012). Zinc contributes to detoxification of superoxide radicals, membrane integrity, protein synthesis, and phytohormone production (Broadley et al. 2012). Manganese activates enzymes involved in detoxification and lignin synthesis (Broadley et al. 2012). In this study, Mg2+ content remained consistent in both penstemon species, but the P content decreased in P. strictus under higher salinity levels. Plant type and growing conditions play an important role in P accumulation (Grattan and Grieve 1999). Moreover, the Zn2+ content increased in P. strictus and the Mn2+ content increased in both species, suggesting a potential role in detoxification of superoxide radicals (Broadley et al. 2012).

Some plants can tolerate salinity stress through osmotic adjustment, which involves the accumulation of solutes that help reduce cellular solute potential and maintain water uptake (Hasegawa et al. 2000). Proline is one such solute that can assist plants in adjusting the pH in the cytosol, thereby protecting cellular membranes and proteins from damage during salinity stress (Behzadi Rad et al. 2021). However, in this study, the proline content in the leaves varied between the two penstemon species while remaining similar across all treatments. This suggests that proline may not play a significant role in the salinity stress responses for these penstemon species within the context of this study. The variations in proline content observed could be attributed to inherent genetic differences or physiological adaptations between the species.

Conclusions

Two penstemon species tested during this study showed variations in response to salinity stress. Saline solution irrigation reduced the growth and biomass of both penstemon species. The net photosynthetic rate, gs, and E of penstemons were negatively impacted by salinity stress. Furthermore, the Na+ and Cl uptake increased, and the K+ and Ca2+ uptake was also affected. Based on the findings of this study, P. barbatus and P. strictus are sensitive to salinity levels at ECs of 7.5 and 10.0 dS⋅m−1. These results have implications for the cultivation and management of these penstemon species in saline environments, thus highlighting the need for appropriate irrigation strategies to mitigate the negative effects of salinity stress on their growth and physiological processes.

References Cited

  • Acosta-Motos JR, Ortuno MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA. 2017. Plant responses to salt stress: Adaptive mechanisms. Agronomy. 7(1):18. https://doi.org/10.3390/agronomy7010018.

    • Search Google Scholar
    • Export Citation
  • Banon S, Miralles J, Ochoa J, Sanchez-Blanco MJ. 2012. The effect of salinity and high boron on growth, photosynthetic activity and mineral contents of two ornamental shrubs. Hortic Sci. 39:188194. https://doi.org/10.17221/167/2011-HORTSCI.

    • Search Google Scholar
    • Export Citation
  • Bates LS, Waldren RP, Teare ID. 1973. Rapid determination of free proline for water-stress studies. Plant Soil. 39:205207. https://doi.org/10.1007/BF00018060.

    • Search Google Scholar
    • Export Citation
  • Behzadi Rad P, Roozban MR, Karimi S, Ghahremani R, Vahdati K. 2021. Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture. 11(8):708. https://doi.org/10.3390/agriculture11080708.

    • Search Google Scholar
    • Export Citation
  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F. 2012. Function of nutrients: Micronutrients, p 191–248. In: Marschner’s mineral nutrition of higher plants (3rd ed). Elsevier/Academic Press, London, MA. https://doi.org/10.1016/B978-0-12-384905-2.00007-8.

  • Carter CT, Grieve CM. 2008. Mineral nutrition, growth, and germination of Antirrhinum majus L. (snapdragon) when produced under increasingly saline conditions. HortScience. 43(3):710718. https://doi.org/10.21273/HORTSCI.43.3.710.

    • Search Google Scholar
    • Export Citation
  • Cavins TO, Whipker BE, Fonteno WC. 2008. PourThru: A method for monitoring nutrition in the greenhouse. Acta Hortic. 779:289298. https://doi.org/10.17660/ActaHortic.2008.779.35.

    • Search Google Scholar
    • Export Citation
  • Claussen W. 2005. Proline as a measure of stress in tomato plants. Plant Sci. 168(1):241248. https://doi.org/10.1016/j.plantsci.2004.07.039.

    • Search Google Scholar
    • Export Citation
  • Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Belanger RR. 2019. The controversies of silicon’s role in plant biology. New Phytol. 221:6785. https://doi.org/10.1111/nph.15343.

    • Search Google Scholar
    • Export Citation
  • Costello LR, Perry EJ, Matheny NP, Henry JM, Geisel PM. 2003. Abiotic disorders of landscape plants: A diagnostic guide, Publication 3420, University of California Division of Agricultural and Natural Resources.

  • Evelin HR, Kapoor R, Giri B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann Bot. 104:1263–1280. https://doi.org/10.1093/aob/mcp251.

  • Fornes F, Belda RM, Carrion C, Noguera V, Gracia-Agustin P, Abad M. 2007. Pre-conditioning ornamental plants to drought by means of saline water irrigation as related to salinity tolerance. Sci Hortic. 113:5259. https://doi.org/10.1016/j.scienta.2007.01.008.

    • Search Google Scholar
    • Export Citation
  • Fox LJ, Grose N, Appleton BL, Donohue SJ. 2005. Evaluation of treated effluent as an irrigation source for landscape plants. J Environ Hortic. 23:174178. https://doi.org/10.24266/0738-2898-23.4.174.

    • Search Google Scholar
    • Export Citation
  • Gavlak RG, Horneck DA, Miller RO. 2005. Soil, plant, and water reference methods for the western region. Western Regional Extension Publication (WREP) 125. https://www.naptprogram.org/files/napt/western-states-method-manual-2005.pdf. [accessed 12 Oct 2023].

  • Gorji T, Tanik A, Sertel E. 2015. Soil salinity prediction, monitoring and mapping using modern technologies. Procedia Earth and Planetary Science. 15:507512. https://doi.org/10.1016/j.proeps.2015.08.062.

    • Search Google Scholar
    • Export Citation
  • Gracia-Caparros P, Lao MT. 2018. The effects of salt stress on ornamental plants and integrative cultivation practices. Sci Hortic. 240:430439. https://doi.org/10.1016/j.scienta.2018.06.022.

    • Search Google Scholar
    • Export Citation
  • Grattan SR, Grieve CM. 1999. Salinity – mineral nutrient relations in horticultural crops. Sci Hortic. 78:127157. https://doi.org/10.1016/S0304-4238(98)00192-7.

    • Search Google Scholar
    • Export Citation
  • Gucci R, Tattini M. 1997. Salinity tolerance in olive, p 177–214. In: Janik J (ed). Horticultural reviews, Volume 21. https://doi.org/10.1002/9780470650660.ch6.

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. 2000. Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol. 51:463499. https://doi.org/10.1146/annurev.arplant.51.1.463.

    • Search Google Scholar
    • Export Citation
  • Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Moller IS, White P. 2012. Functions of macronutrients, p 135–189. Marschner’s mineral nutrition of higher plants (3rd ed). Elsevier/Academic Press, London, MA, USA. https://doi.org/10.1016/B978-0-12-384905-2.00006-6.

  • Hooks T, Niu G. 2019. Relative salt tolerance of four herbaceous perennial ornamentals. Horticulturae. 5:36. https://doi.org/10.3390/horticulturae5020036.

    • Search Google Scholar
    • Export Citation
  • Howe HF, Zorn-Arnold B, Sullivan A, Brown JS. 2006. Massive and distinctive effects of meadow voles on grassland vegetation. Ecology. 87:30073013. https://doi.org/10.1890/0012-9658(2006)87[3007:MADEOM]2.0.CO;2.

    • Search Google Scholar
    • Export Citation
  • Jull LG. 2009. Winter salt injury and salt-tolerant landscape plants. Univ. Wisconsin Coop. Ext. A3877. https://cdn.shopify.com/s/files/1/0145/8808/4272/files/A3877.pdf. [accessed 12 Oct 2023].

  • Kramer AT. 2009. Ecological genetics of penstemon in the Great Basin, USA (PhD Diss). University of Illinois at Chicago, Chicago, IL, USA. https://www.fs.usda.gov/rm/boise/research/shrub/Links/2009papers/Kramer2009thesis.pdf. [accessed 12 Oct 2023].

  • Kratsch H. 2011. Some good native plants for Great Basin landscapes. Special Publication 11-13, University of Nevada Cooperative Extension, Nevada. https://extension.unr.edu/publication.aspx?PubID=3347. [accessed 12 Oct 2023].

  • Lattier KS. 2016. Inducing and evaluating phenotypic and cytometric variation in landscape plants: Observations from Acer, Ornithogalum, and Penstemon (MS Thesis). Oregon State University, Corvallis, OR, USA.

  • Lesch SM, Suarez DL. 2009. A short note on calculating the adjusted SAR index. Trans ASABE. 52(2):493496.

  • Liu Q, Sun Y, Niu G, Altland J, Chen L, Jiang L. 2017. Morphological and physiological responses of ten ornamental taxa to saline water irrigation. HortScience. 52:18161822. https://doi.org/10.21273/HORTSCI12463-17.

    • Search Google Scholar
    • Export Citation
  • Maathuis FJ. 2014. Sodium in plants: Perception, signalling, and regulation of sodium fluxes. J Expt Bot. 65(3):849858. https://doi.org/10.1093/jxb/ert326.

    • Search Google Scholar
    • Export Citation
  • Marschner H. 2012. Marschner’s mineral nutrition of higher plants (3rd ed). Elsevier/Academic Press, London, MA, USA.

  • Mengel DB. 2023. Fundamentals of soil cation exchange capacity (CEC). Agronomy Guide AY-238 Soils (Fertility). Purdue University Cooperative Extension Service, West Lafayette, IN, USA. https://www.extension.purdue.edu/extmedia/ay/ay-238.html. [accessed 12 Oct 2023].

  • Munns R. 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25:239250. https://doi.org/10.1046/j.0016-8025.2001.00808.x.

    • Search Google Scholar
    • Export Citation
  • Munns R, Termaat A. 1986. Whole plant response to salinity. Aust J Plant Physiol. 13(1):143160. https://doi.org/10.1071/PP9860143.

  • Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 59:651681. https://doi.org/10.1146/annurev.arplant.59.032607.092911.

    • Search Google Scholar
    • Export Citation
  • Nebauer SG, Sanchez M, Martinez L, Llunch Y, Renau-Morata B, Molina RV. 2013. Differences in photosynthetic performance and its correlation with growth among tomato cultivars in response to different salts. Plant Physiol Biochem. 63:6169. https://doi.org/10.1016/j.plaphy.2012.11.006.

    • Search Google Scholar
    • Export Citation
  • Negrao S, Schmockel SM, Tester M. 2017. Evaluating physiological responses of plants to salinity stress. Ann Bot (Lond). 119(1):111. https://doi.org/10.1093/aob/mcw191.

    • Search Google Scholar
    • Export Citation
  • Niu G, Rodriguez DS. 2006. Relative salt tolerance of selected herbaceous perennials and groundcovers. Scientia Hortic. 110:352358. https://doi.org/10.1016/j.scienta.2006.07.020.

    • Search Google Scholar
    • Export Citation
  • Niu G, Rodriguez DS, Aguiniga L. 2007. Growth and landscape performance of ten herbaceous species in response to saline water irrigation. J Environ Hortic. 25:204210. https://doi.org/10.24266/0738-2898-25.4.204.

    • Search Google Scholar
    • Export Citation
  • Niu G, Rodriguez DS, Starman T. 2010. Response of bedding plants to saline water irrigation. HortScience. 45(4):628636. https://doi.org/10.21273/HORTSCI.45.4.628.

    • Search Google Scholar
    • Export Citation
  • Paudel A, Chen JJ, Sun Y, Wang Y, Anderson R. 2019. Salt tolerance of Sego SupremeTM plants. HortScience. 54(1):20562062. https://doi.org/10.21273/HORTSCI14342-19.

    • Search Google Scholar
    • Export Citation
  • Queiros F, Fontes N, Silva P, Almeida D, Maeshima M, Gerós H, Fidalgo F. 2009. Activity of tonoplast proton pumps and Na+/H+ exchange in potato cell cultures is modulated by salt. J Expt Bot. 60(4):13631374. https://doi.org/10.1093/jxb/erp011.

    • Search Google Scholar
    • Export Citation
  • Rahneshan Z, Nasibi F, Moghadam AA. 2018. Effects of salinity stress on some growth, physiological, biochemical parameters, and nutrients in two pistachio (Pistacia vera L.) rootstocks. J Plant Interact. 13:7382. https://doi.org/10.1080/17429145.2018.1424355.

    • Search Google Scholar
    • Export Citation
  • Rakesh B, Bindu KH, Praveen N. 2021. Variations in the L-DOPA content, phytochemical constituents, and antioxidant activity of different germlines of Mucuna pruriens (L.) DC. Asian J Chem. 33(8):18811890. https://doi.org/10.14233/ajchem.2021.23293.

    • Search Google Scholar
    • Export Citation
  • Reid MS, Jiang CZ. 2012. Postharvest biology and technology of cut flowers and potted plants. Hortic Rev. 40:154. https://doi.org/10.1002/9781118351871.ch1.

    • Search Google Scholar
    • Export Citation
  • Rengel Z. 1992. The role of calcium in salt toxicity. Plant Cell Environ. 15:625632. https://doi.org/10.1111/j.1365-3040.1992.tb01004.x.

    • Search Google Scholar
    • Export Citation
  • Sanchez-Blanco MJ, Alvarez S, Ortuno MF, Ruiz-Sanchez M. 2014. Root system response to drought and salinity: Root distribution and water transport. Root Eng. 325352.

    • Search Google Scholar
    • Export Citation
  • Shu S, Guo S, Sun J, Yuan L. 2012. Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol Plant. 146:285296. https://doi.org/10.1111/j.1399-3054.2012.01623.x.

    • Search Google Scholar
    • Export Citation
  • Silva EN, Silveira JAG, Rodrigues CRF, Viégas RA. 2015. Physiological adjustment to salt stress in Jatropha curcas is associated with accumulation of salt ions, transport, and selectivity of K+, osmotic adjustment and K+/Na+ homeostasis. Plant Biol. 17(5):10231029. https://doi.org/10.1111/plb.12337.

    • Search Google Scholar
    • Export Citation
  • Singh M, Kumar J, Singh VP, Prasad SM. 2014. Plant tolerance mechanism against salt stress: The nutrient management approach. Biochem Pharmacol. 3:e165. https://doi.org/10.4172/2167-0501.1000e165.

    • Search Google Scholar
    • Export Citation
  • Sun Y, Chen JJ, Xing H, Paudel A, Niu G, Chappell M. 2020. Growth, visual quality, and morphological responses of 12 viburnum taxa to saline water irrigation. HortScience. 55(8):12331241. https://doi.org/10.21273/HORTSCI14940-20.

    • Search Google Scholar
    • Export Citation
  • Sun Y, Niu G, Perez C. 2015. Relative salt tolerance of seven Texas Superstar® perennials. HortScience. 50(10):15621566. https://doi.org/10.21273/HORTSCI.50.10.1562.

    • Search Google Scholar
    • Export Citation
  • Taiz L, Zeiger E, Møller IM, Murphy A. 2015. Plant physiology and development (6th ed). Sinauer Associates, Sunderland, MA, USA.

  • US Department of Agriculture. 2020. 2014 Census of horticultural specialties, Table 8. Washington, DC. https://www.nass.usda.gov/Publications/AgCensus/2012/Online_Resources/Census_of_Horticulture_Specialties/hortic_1_008_008.pdf. [accessed 20 Apr 2023].

  • Wang Y, Sun Y, Niu G, Deng C, Wang Y, Gardea-Torresdey J. 2019. Growth, gas exchange, and mineral nutrients of ornamental grasses irrigated with saline water. HortScience. 54(10):18401846. https://doi.org/10.21273/HORTSCI13953-19.

    • Search Google Scholar
    • Export Citation
  • Wu S, Sun Y, Niu G, Altland J, Cabrera RI. 2016. Response of ten aster species to saline water irrigation. HortScience. 51:197201. https://doi.org/10.21273/HORTSCI.51.2.197.

    • Search Google Scholar
    • Export Citation
  • Yang J, Punshon T, Guerinot ML, Hirschi KD. 2012. Plant calcium content: Ready to remodel. Nutrients. 4(8):11201136. https://doi.org/10.3390%2Fnu4081120.

    • Search Google Scholar
    • Export Citation
  • Zargar SM, Mahajan R, Bhat JA, Nazir M, Deshmukh R. 2019. Role of silicon in plant stress tolerance: Opportunities to achieve a sustainable cropping system. 3 Biotech. 9:72. https://doi.org/10.1007%2Fs13205-019-1613-z.

  • Zhang L, Ma H, Chen T, Pen J, Yu S, Zhao X. 2014. Morphological and physiological responses of cotton (Gossypium hirsutum L.) plants to salinity. PLoS One. 9(11). https://doi.org/10.1371/journal.pone.0112807.

    • Search Google Scholar
    • Export Citation
  • Zhang M, Fang Y, Ji Y, Jiang Z, Wang L. 2013. Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot. 85:19. https://doi.org/10.1016/j.sajb.2012.11.005.

    • Search Google Scholar
    • Export Citation
  • Zollinger N, Koenig R, Cerny-Koenig T, Kjelgren R. 2007. Relative salinity tolerance of intermountain western united states native herbaceous perennials. HortScience. 42(3):529534. https://doi.org/10.21273/HORTSCI.42.3.529.

    • Search Google Scholar
    • Export Citation
  • Fig. 1.

    Photos of representative penstemons after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

  • Fig. 2.

    Visual scores of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period 2 (A), 4 (B), 6 (C), and 8 (D) weeks in a greenhouse. Vertical bars represent SEs of 10 plants. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Visual scores: 0 = dead plant caused by salinity stress; 1 = severe foliar damage (burnt leaves and necrosis, >90%); 2 = moderate foliar damage (51%–90%); 3 = slight foliar damage (10%–50%); 4 = good quality with minimal foliar damage (<10%); and 5 = excellent without foliar damage (Sun et al. 2015).

  • Fig. 3.

    Electrical conductivity (EC) of leachate solution over the course of the experiment collected after Penstemon barbatus and P. strictus were irrigated with a nutrient solution at an EC of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of two measurements.

  • Fig. 4.

    Electrical conductivity (EC) of soil extraction from Penstemon barbatus and P. strictus irrigated with a nutrient solution at an EC of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of five measurements.

  • Fig. 5.

    Chlorophyll content [Soil Plant Analysis Development (SPAD)], chlorophyll fluorescence parameters (Fv/Fm, and PIabs) of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent standard errors of 10 measurements for SPAD and six measurements for Fv/Fm, and PIabs. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Penstemons were dead or had severe foliar salt damage when treated with saline solution at an EC of 10.0 dS⋅m−1; therefore, the chlorophyll content and fluorescence data were not taken.

  • Fig. 6.

    Net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of five measurements. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Gas exchange data of P. barbatus at ECs of 7.5 and 10.0 dS⋅m−1 and P. strictus at an EC of 10.0 dS⋅m−1 were not measured as plants had severe foliar salt damage or were dead.

  • Fig. 7.

    Correlation analyses between the sodium (Na+), chloride (Cl), potassium-to-sodium ratio (K+/Na+), calcium-to-sodium ratio (Ca2+/Na+), and visual score of Penstemon barbatus and P. strictus. Visual scores: 0 = dead plant caused by salinity stress; 1 = severe foliar damage (burnt leaves and necrosis, >90%); 2 = moderate foliar damage (51%–90%); 3 = slight foliar damage (10%–50%); 4 = good quality with minimal foliar damage (<10%); and 5 = excellent quality without foliar damage (Sun et al. 2015).

  • Fig. 8.

    Correlation analyses between the sodium (Na+), chloride (Cl), potassium-to-sodium ratio (K+/Na+), calcium-to-sodium ratio (Ca2+/Na+), net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of Penstemon barbatus and P. strictus.

  • Acosta-Motos JR, Ortuno MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA. 2017. Plant responses to salt stress: Adaptive mechanisms. Agronomy. 7(1):18. https://doi.org/10.3390/agronomy7010018.

    • Search Google Scholar
    • Export Citation
  • Banon S, Miralles J, Ochoa J, Sanchez-Blanco MJ. 2012. The effect of salinity and high boron on growth, photosynthetic activity and mineral contents of two ornamental shrubs. Hortic Sci. 39:188194. https://doi.org/10.17221/167/2011-HORTSCI.

    • Search Google Scholar
    • Export Citation
  • Bates LS, Waldren RP, Teare ID. 1973. Rapid determination of free proline for water-stress studies. Plant Soil. 39:205207. https://doi.org/10.1007/BF00018060.

    • Search Google Scholar
    • Export Citation
  • Behzadi Rad P, Roozban MR, Karimi S, Ghahremani R, Vahdati K. 2021. Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture. 11(8):708. https://doi.org/10.3390/agriculture11080708.

    • Search Google Scholar
    • Export Citation
  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F. 2012. Function of nutrients: Micronutrients, p 191–248. In: Marschner’s mineral nutrition of higher plants (3rd ed). Elsevier/Academic Press, London, MA. https://doi.org/10.1016/B978-0-12-384905-2.00007-8.

  • Carter CT, Grieve CM. 2008. Mineral nutrition, growth, and germination of Antirrhinum majus L. (snapdragon) when produced under increasingly saline conditions. HortScience. 43(3):710718. https://doi.org/10.21273/HORTSCI.43.3.710.

    • Search Google Scholar
    • Export Citation
  • Cavins TO, Whipker BE, Fonteno WC. 2008. PourThru: A method for monitoring nutrition in the greenhouse. Acta Hortic. 779:289298. https://doi.org/10.17660/ActaHortic.2008.779.35.

    • Search Google Scholar
    • Export Citation
  • Claussen W. 2005. Proline as a measure of stress in tomato plants. Plant Sci. 168(1):241248. https://doi.org/10.1016/j.plantsci.2004.07.039.

    • Search Google Scholar
    • Export Citation
  • Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Belanger RR. 2019. The controversies of silicon’s role in plant biology. New Phytol. 221:6785. https://doi.org/10.1111/nph.15343.

    • Search Google Scholar
    • Export Citation
  • Costello LR, Perry EJ, Matheny NP, Henry JM, Geisel PM. 2003. Abiotic disorders of landscape plants: A diagnostic guide, Publication 3420, University of California Division of Agricultural and Natural Resources.

  • Evelin HR, Kapoor R, Giri B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann Bot. 104:1263–1280. https://doi.org/10.1093/aob/mcp251.

  • Fornes F, Belda RM, Carrion C, Noguera V, Gracia-Agustin P, Abad M. 2007. Pre-conditioning ornamental plants to drought by means of saline water irrigation as related to salinity tolerance. Sci Hortic. 113:5259. https://doi.org/10.1016/j.scienta.2007.01.008.

    • Search Google Scholar
    • Export Citation
  • Fox LJ, Grose N, Appleton BL, Donohue SJ. 2005. Evaluation of treated effluent as an irrigation source for landscape plants. J Environ Hortic. 23:174178. https://doi.org/10.24266/0738-2898-23.4.174.

    • Search Google Scholar
    • Export Citation
  • Gavlak RG, Horneck DA, Miller RO. 2005. Soil, plant, and water reference methods for the western region. Western Regional Extension Publication (WREP) 125. https://www.naptprogram.org/files/napt/western-states-method-manual-2005.pdf. [accessed 12 Oct 2023].

  • Gorji T, Tanik A, Sertel E. 2015. Soil salinity prediction, monitoring and mapping using modern technologies. Procedia Earth and Planetary Science. 15:507512. https://doi.org/10.1016/j.proeps.2015.08.062.

    • Search Google Scholar
    • Export Citation
  • Gracia-Caparros P, Lao MT. 2018. The effects of salt stress on ornamental plants and integrative cultivation practices. Sci Hortic. 240:430439. https://doi.org/10.1016/j.scienta.2018.06.022.

    • Search Google Scholar
    • Export Citation
  • Grattan SR, Grieve CM. 1999. Salinity – mineral nutrient relations in horticultural crops. Sci Hortic. 78:127157. https://doi.org/10.1016/S0304-4238(98)00192-7.

    • Search Google Scholar
    • Export Citation
  • Gucci R, Tattini M. 1997. Salinity tolerance in olive, p 177–214. In: Janik J (ed). Horticultural reviews, Volume 21. https://doi.org/10.1002/9780470650660.ch6.

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. 2000. Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol. 51:463499. https://doi.org/10.1146/annurev.arplant.51.1.463.

    • Search Google Scholar
    • Export Citation
  • Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Moller IS, White P. 2012. Functions of macronutrients, p 135–189. Marschner’s mineral nutrition of higher plants (3rd ed). Elsevier/Academic Press, London, MA, USA. https://doi.org/10.1016/B978-0-12-384905-2.00006-6.

  • Hooks T, Niu G. 2019. Relative salt tolerance of four herbaceous perennial ornamentals. Horticulturae. 5:36. https://doi.org/10.3390/horticulturae5020036.

    • Search Google Scholar
    • Export Citation
  • Howe HF, Zorn-Arnold B, Sullivan A, Brown JS. 2006. Massive and distinctive effects of meadow voles on grassland vegetation. Ecology. 87:30073013. https://doi.org/10.1890/0012-9658(2006)87[3007:MADEOM]2.0.CO;2.

    • Search Google Scholar
    • Export Citation
  • Jull LG. 2009. Winter salt injury and salt-tolerant landscape plants. Univ. Wisconsin Coop. Ext. A3877. https://cdn.shopify.com/s/files/1/0145/8808/4272/files/A3877.pdf. [accessed 12 Oct 2023].

  • Kramer AT. 2009. Ecological genetics of penstemon in the Great Basin, USA (PhD Diss). University of Illinois at Chicago, Chicago, IL, USA. https://www.fs.usda.gov/rm/boise/research/shrub/Links/2009papers/Kramer2009thesis.pdf. [accessed 12 Oct 2023].

  • Kratsch H. 2011. Some good native plants for Great Basin landscapes. Special Publication 11-13, University of Nevada Cooperative Extension, Nevada. https://extension.unr.edu/publication.aspx?PubID=3347. [accessed 12 Oct 2023].

  • Lattier KS. 2016. Inducing and evaluating phenotypic and cytometric variation in landscape plants: Observations from Acer, Ornithogalum, and Penstemon (MS Thesis). Oregon State University, Corvallis, OR, USA.

  • Lesch SM, Suarez DL. 2009. A short note on calculating the adjusted SAR index. Trans ASABE. 52(2):493496.

  • Liu Q, Sun Y, Niu G, Altland J, Chen L, Jiang L. 2017. Morphological and physiological responses of ten ornamental taxa to saline water irrigation. HortScience. 52:18161822. https://doi.org/10.21273/HORTSCI12463-17.

    • Search Google Scholar
    • Export Citation
  • Maathuis FJ. 2014. Sodium in plants: Perception, signalling, and regulation of sodium fluxes. J Expt Bot. 65(3):849858. https://doi.org/10.1093/jxb/ert326.

    • Search Google Scholar
    • Export Citation
  • Marschner H. 2012. Marschner’s mineral nutrition of higher plants (3rd ed). Elsevier/Academic Press, London, MA, USA.

  • Mengel DB. 2023. Fundamentals of soil cation exchange capacity (CEC). Agronomy Guide AY-238 Soils (Fertility). Purdue University Cooperative Extension Service, West Lafayette, IN, USA. https://www.extension.purdue.edu/extmedia/ay/ay-238.html. [accessed 12 Oct 2023].

  • Munns R. 2002. Comparative physiology of salt and water stress. Plant Cell Environ. 25:239250. https://doi.org/10.1046/j.0016-8025.2001.00808.x.

    • Search Google Scholar
    • Export Citation
  • Munns R, Termaat A. 1986. Whole plant response to salinity. Aust J Plant Physiol. 13(1):143160. https://doi.org/10.1071/PP9860143.

  • Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 59:651681. https://doi.org/10.1146/annurev.arplant.59.032607.092911.

    • Search Google Scholar
    • Export Citation
  • Nebauer SG, Sanchez M, Martinez L, Llunch Y, Renau-Morata B, Molina RV. 2013. Differences in photosynthetic performance and its correlation with growth among tomato cultivars in response to different salts. Plant Physiol Biochem. 63:6169. https://doi.org/10.1016/j.plaphy.2012.11.006.

    • Search Google Scholar
    • Export Citation
  • Negrao S, Schmockel SM, Tester M. 2017. Evaluating physiological responses of plants to salinity stress. Ann Bot (Lond). 119(1):111. https://doi.org/10.1093/aob/mcw191.

    • Search Google Scholar
    • Export Citation
  • Niu G, Rodriguez DS. 2006. Relative salt tolerance of selected herbaceous perennials and groundcovers. Scientia Hortic. 110:352358. https://doi.org/10.1016/j.scienta.2006.07.020.

    • Search Google Scholar
    • Export Citation
  • Niu G, Rodriguez DS, Aguiniga L. 2007. Growth and landscape performance of ten herbaceous species in response to saline water irrigation. J Environ Hortic. 25:204210. https://doi.org/10.24266/0738-2898-25.4.204.

    • Search Google Scholar
    • Export Citation
  • Niu G, Rodriguez DS, Starman T. 2010. Response of bedding plants to saline water irrigation. HortScience. 45(4):628636. https://doi.org/10.21273/HORTSCI.45.4.628.

    • Search Google Scholar
    • Export Citation
  • Paudel A, Chen JJ, Sun Y, Wang Y, Anderson R. 2019. Salt tolerance of Sego SupremeTM plants. HortScience. 54(1):20562062. https://doi.org/10.21273/HORTSCI14342-19.

    • Search Google Scholar
    • Export Citation
  • Queiros F, Fontes N, Silva P, Almeida D, Maeshima M, Gerós H, Fidalgo F. 2009. Activity of tonoplast proton pumps and Na+/H+ exchange in potato cell cultures is modulated by salt. J Expt Bot. 60(4):13631374. https://doi.org/10.1093/jxb/erp011.

    • Search Google Scholar
    • Export Citation
  • Rahneshan Z, Nasibi F, Moghadam AA. 2018. Effects of salinity stress on some growth, physiological, biochemical parameters, and nutrients in two pistachio (Pistacia vera L.) rootstocks. J Plant Interact. 13:7382. https://doi.org/10.1080/17429145.2018.1424355.

    • Search Google Scholar
    • Export Citation
  • Rakesh B, Bindu KH, Praveen N. 2021. Variations in the L-DOPA content, phytochemical constituents, and antioxidant activity of different germlines of Mucuna pruriens (L.) DC. Asian J Chem. 33(8):18811890. https://doi.org/10.14233/ajchem.2021.23293.

    • Search Google Scholar
    • Export Citation
  • Reid MS, Jiang CZ. 2012. Postharvest biology and technology of cut flowers and potted plants. Hortic Rev. 40:154. https://doi.org/10.1002/9781118351871.ch1.

    • Search Google Scholar
    • Export Citation
  • Rengel Z. 1992. The role of calcium in salt toxicity. Plant Cell Environ. 15:625632. https://doi.org/10.1111/j.1365-3040.1992.tb01004.x.

    • Search Google Scholar
    • Export Citation
  • Sanchez-Blanco MJ, Alvarez S, Ortuno MF, Ruiz-Sanchez M. 2014. Root system response to drought and salinity: Root distribution and water transport. Root Eng. 325352.

    • Search Google Scholar
    • Export Citation
  • Shu S, Guo S, Sun J, Yuan L. 2012. Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol Plant. 146:285296. https://doi.org/10.1111/j.1399-3054.2012.01623.x.

    • Search Google Scholar
    • Export Citation
  • Silva EN, Silveira JAG, Rodrigues CRF, Viégas RA. 2015. Physiological adjustment to salt stress in Jatropha curcas is associated with accumulation of salt ions, transport, and selectivity of K+, osmotic adjustment and K+/Na+ homeostasis. Plant Biol. 17(5):10231029. https://doi.org/10.1111/plb.12337.

    • Search Google Scholar
    • Export Citation
  • Singh M, Kumar J, Singh VP, Prasad SM. 2014. Plant tolerance mechanism against salt stress: The nutrient management approach. Biochem Pharmacol. 3:e165. https://doi.org/10.4172/2167-0501.1000e165.

    • Search Google Scholar
    • Export Citation
  • Sun Y, Chen JJ, Xing H, Paudel A, Niu G, Chappell M. 2020. Growth, visual quality, and morphological responses of 12 viburnum taxa to saline water irrigation. HortScience. 55(8):12331241. https://doi.org/10.21273/HORTSCI14940-20.

    • Search Google Scholar
    • Export Citation
  • Sun Y, Niu G, Perez C. 2015. Relative salt tolerance of seven Texas Superstar® perennials. HortScience. 50(10):15621566. https://doi.org/10.21273/HORTSCI.50.10.1562.

    • Search Google Scholar
    • Export Citation
  • Taiz L, Zeiger E, Møller IM, Murphy A. 2015. Plant physiology and development (6th ed). Sinauer Associates, Sunderland, MA, USA.

  • US Department of Agriculture. 2020. 2014 Census of horticultural specialties, Table 8. Washington, DC. https://www.nass.usda.gov/Publications/AgCensus/2012/Online_Resources/Census_of_Horticulture_Specialties/hortic_1_008_008.pdf. [accessed 20 Apr 2023].

  • Wang Y, Sun Y, Niu G, Deng C, Wang Y, Gardea-Torresdey J. 2019. Growth, gas exchange, and mineral nutrients of ornamental grasses irrigated with saline water. HortScience. 54(10):18401846. https://doi.org/10.21273/HORTSCI13953-19.

    • Search Google Scholar
    • Export Citation
  • Wu S, Sun Y, Niu G, Altland J, Cabrera RI. 2016. Response of ten aster species to saline water irrigation. HortScience. 51:197201. https://doi.org/10.21273/HORTSCI.51.2.197.

    • Search Google Scholar
    • Export Citation
  • Yang J, Punshon T, Guerinot ML, Hirschi KD. 2012. Plant calcium content: Ready to remodel. Nutrients. 4(8):11201136. https://doi.org/10.3390%2Fnu4081120.

    • Search Google Scholar
    • Export Citation
  • Zargar SM, Mahajan R, Bhat JA, Nazir M, Deshmukh R. 2019. Role of silicon in plant stress tolerance: Opportunities to achieve a sustainable cropping system. 3 Biotech. 9:72. https://doi.org/10.1007%2Fs13205-019-1613-z.

  • Zhang L, Ma H, Chen T, Pen J, Yu S, Zhao X. 2014. Morphological and physiological responses of cotton (Gossypium hirsutum L.) plants to salinity. PLoS One. 9(11). https://doi.org/10.1371/journal.pone.0112807.

    • Search Google Scholar
    • Export Citation
  • Zhang M, Fang Y, Ji Y, Jiang Z, Wang L. 2013. Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot. 85:19. https://doi.org/10.1016/j.sajb.2012.11.005.

    • Search Google Scholar
    • Export Citation
  • Zollinger N, Koenig R, Cerny-Koenig T, Kjelgren R. 2007. Relative salinity tolerance of intermountain western united states native herbaceous perennials. HortScience. 42(3):529534. https://doi.org/10.21273/HORTSCI.42.3.529.

    • Search Google Scholar
    • Export Citation
Asmita Paudel Department of Plants, Soils, and Climate, Utah State University, 4820 Old Main Hill, Logan, UT 84322, USA

Search for other papers by Asmita Paudel in
Google Scholar
Close
and
Youping Sun Department of Plants, Soils, and Climate, Utah State University, 4820 Old Main Hill, Logan, UT 84322, USA

Search for other papers by Youping Sun in
Google Scholar
Close

Contributor Notes

This research was supported in part by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) Hatch project UTA01381 and UTA01666, USDA Agricultural Marketing Service Specialty Crop Block Grant Program, American Penstemon Society Graduate Student Scholarship Grant, Utah State University’s Center for Water-Efficient Landscaping, and Utah Agricultural Experiment Station (UAES). It has been approved as UAES journal paper number 9730. We thank the Open Access Funding at Utah State University Libraries, Hannah Limas, and Atanda Oladejo for technical assistance. We thank Amita Kaundal, Grant Cardon, Shaun Bushman, Shital Poudyal, and anonymous reviewers for valuable comments. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the USDA or the American Society for Horticultural Science and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

Y.S. is the corresponding author. E-mail: youping.sun@usu.edu.

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 280 280 41
PDF Downloads 254 253 41
  • Fig. 1.

    Photos of representative penstemons after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse.

  • Fig. 2.

    Visual scores of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period 2 (A), 4 (B), 6 (C), and 8 (D) weeks in a greenhouse. Vertical bars represent SEs of 10 plants. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Visual scores: 0 = dead plant caused by salinity stress; 1 = severe foliar damage (burnt leaves and necrosis, >90%); 2 = moderate foliar damage (51%–90%); 3 = slight foliar damage (10%–50%); 4 = good quality with minimal foliar damage (<10%); and 5 = excellent without foliar damage (Sun et al. 2015).

  • Fig. 3.

    Electrical conductivity (EC) of leachate solution over the course of the experiment collected after Penstemon barbatus and P. strictus were irrigated with a nutrient solution at an EC of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of two measurements.

  • Fig. 4.

    Electrical conductivity (EC) of soil extraction from Penstemon barbatus and P. strictus irrigated with a nutrient solution at an EC of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 10.0 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of five measurements.

  • Fig. 5.

    Chlorophyll content [Soil Plant Analysis Development (SPAD)], chlorophyll fluorescence parameters (Fv/Fm, and PIabs) of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent standard errors of 10 measurements for SPAD and six measurements for Fv/Fm, and PIabs. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Penstemons were dead or had severe foliar salt damage when treated with saline solution at an EC of 10.0 dS⋅m−1; therefore, the chlorophyll content and fluorescence data were not taken.

  • Fig. 6.

    Net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of Penstemon barbatus and P. strictus after irrigation with a nutrient solution at an electrical conductivity (EC) of 1.0 dS⋅m−1 (control) and saline solutions with varying EC levels ranging from 2.5 to 7.5 dS⋅m−1 for a period of 8 weeks in a greenhouse. Vertical bars represent SEs of five measurements. The same letters above column bars within species represent no significance among treatments as determined by Tukey’s method for multiplicity at α = 0.05. Gas exchange data of P. barbatus at ECs of 7.5 and 10.0 dS⋅m−1 and P. strictus at an EC of 10.0 dS⋅m−1 were not measured as plants had severe foliar salt damage or were dead.

  • Fig. 7.

    Correlation analyses between the sodium (Na+), chloride (Cl), potassium-to-sodium ratio (K+/Na+), calcium-to-sodium ratio (Ca2+/Na+), and visual score of Penstemon barbatus and P. strictus. Visual scores: 0 = dead plant caused by salinity stress; 1 = severe foliar damage (burnt leaves and necrosis, >90%); 2 = moderate foliar damage (51%–90%); 3 = slight foliar damage (10%–50%); 4 = good quality with minimal foliar damage (<10%); and 5 = excellent quality without foliar damage (Sun et al. 2015).

  • Fig. 8.

    Correlation analyses between the sodium (Na+), chloride (Cl), potassium-to-sodium ratio (K+/Na+), calcium-to-sodium ratio (Ca2+/Na+), net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of Penstemon barbatus and P. strictus.

 

Advertisement
Longwood Gardens Fellows Program 2024

 

Advertisement
Save