Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions

Piotr Salachna; Rafał Piechocki

doi:10.3390/agronomy11010049

Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions

Salachna, Piotr;Piechocki, Rafał 2020-12-28 00:00:00 agronomy Article Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions Piotr Salachna * and Rafał Piechocki Department of Horticulture, West Pomeranian University of Technology, 3 Papieza ˙ Pawła VI Str., 71-459 Szczecin, Poland; rafal.piechocki@zut.edu.pl * Correspondence: piotr.salachna@zut.edu.pl; Tel.: +48-91-4496-359 Abstract: Hardy ferns form a group of attractive garden perennials with an unknown response to abiotic stresses. The aim of this study was to evaluate the tolerance of three species of ferns of Dryopteris genus (D. affinis, D. atrata and D. filix-mas) and one cultivar (D. filix-mas cv. “Linearis-Polydactylon”) to salinity and light stress. The plants were grown in full sun and shade and watered with 50 and 100 mM dm NaCl solution. All taxa treated with 100 mM NaCl responded with reduced height, leaf greenness index and fresh weight of the above-ground part. In D. affinis and D. atrata salinity caused leaf damage manifested by necrotic spots, which was not observed in the other two taxa. The effect of NaCl depended on light treatments and individual taxon. D. affinis and D. atrata were more tolerant to salinity when growing under shade. Contrary to that, D. filix-mas cv. “Linearis-Polydactylon” seemed to show significantly greater tolerance to this stress under full sun. Salt-treated D. filix-mas cv. “Linearis-Polydactylon” plants accumulated enhanced amounts of K in the leaves, which might be associated with the taxon’s tolerance to salinity. Among the investigated genotypes, D. filix-mas cv. “Linearis-Polydactylon” seemed the most and D. affinis and D. atrata the least tolerant to salinity and light stress. Keywords: hardy ferns; salt stress; NaCl; light stress; shade; multiple stresses; abiotic stresses Citation: Salachna, P.; Piechocki, R. Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris 1. Introduction Adans. Grown under Different Light Conditions. Agronomy 2021, 11, 49. Ornamental plants are constantly exposed to adverse effects of stress factors that https://doi.org/10.3390/agronomy disturb their growth and diminish their decorative value [1]. These factors operate both during production and after planting at the target site. The stress can be caused by an excess or deﬁciency of any abiotic factor [2]. Very often stresses evoked by unfavorable Received: 30 November 2020 environmental conditions overlap with each other [3]. Most studies conducted so far have Accepted: 25 December 2020 focused on the response of ornamental plants to single stress factors [1,4,5], while their Published: 28 December 2020 response to multiple stresses experienced simultaneously is less known. Excessive substrate salinity causing salt stress is one of the most common abiotic Publisher’s Note: MDPI stays neu- stresses that negatively affect the quality of ornamental plants [4]. Exceeding tolerance tral with regard to jurisdictional clai- threshold for salt triggers numerous adverse changes in plant growth and development [6,7]. ms in published maps and institutio- Too high salinity limits water availability, lowers turgor and leads to inhibition of cell nal afﬁliations. elongation growth, tissue necrosis, yellowing, drying and falling of leaves [8]. The negative effects of salinity are due to toxicity of sodium ions that accumulate in plant tissues and disturb plant ionic balance [9]. The assessment of ion content in plants grown under salt Copyright: © 2020 by the authors. Li- stress is important from a cognitive and practical perspective, as the ion level might be censee MDPI, Basel, Switzerland. a marker for selecting species and cultivars tolerant to elevated salinity [10,11]. This article is an open access article Global climatic changes increase the intensity of extreme weather phenomena, includ- distributed under the terms and con- ing heat waves and ensuing intense solar radiation that causes light stress in plants [12,13]. ditions of the Creative Commons At- Excessive solar radiation results in photoinhibition and photodestruction of pigments, tribution (CC BY) license (https:// and further consequences include reduced photosynthesis efﬁciency and extensive tissue creativecommons.org/licenses/by/ damage [14]. Ornamental plants exposed to adverse light conditions respond with growth 4.0/). Agronomy 2021, 11, 49. https://doi.org/10.3390/agronomy11010049 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, 49 2 of 13 disturbances and diminished decorative value [15]. There are many reports on the reaction of photophilic ornamental plants to light deﬁciency [16–18]. However, the effects of light stress on the quality of shade tolerant ornamental plants have not been extensively studied. Pteridophytes (ferns) are a highly diverse plant group including at least 10,000 species growing in all climatic zones except for extremely dry or cold areas [19]. Many fern species have high decorative value and are grown in pots, gardens and as cut plants [20]. Some of them are also edible and medicinal plants [21]. In general, ferns are sensitive to salinity, excessive sunlight and water shortage. Nevertheless, a few studies reported on fern genotypes tolerant to abiotic stresses and capable of adapting to adverse habitat conditions [22–24]. Different species and cultivars collectively named hardy ferns, and comprising garden ferns with attractive foliage and habit and tolerant to frost, are gaining popularity [20]. The group includes e.g., many ornamental species of Dryopteris Adans genus (Dryopteridaceae family) [25]. A typical species, Dryopteris filix-mas L., forms loose tufts and is deemed to be one of the easiest fern species to cultivate. Of numerous morphotypes and cultivars of D. filix-mas, the one particularly original is cv. “Linearis-Polydactylon” forming dense tufts of upright and extremely delicate, lacy leaves. Dryopteris atrata has decorative, evergreen, dark- green blades sitting on petioles densely covered with dark scales. The ornamental feature of Dryopteris affinis are dark-green, evergreen leaves of slightly shiny, leathery texture [20,25]. Apart from their decorative qualities, D. affinis, D. atrata and D. filix-mas are also sources of valuable metabolites for phytomedicine [26]. Wider dissemination of Dryopteris species and cultivars is prevented by a lack of detailed data on the methods of their cultivation. Moreover, there is little information on Dryopteris resistance to environmental stresses. The stress response of ornamental seed plants is relatively well researched [1,14] but the effects of stress factors on growth and ornamental value of spore plants are much less known. To ﬁll in the gaps in our knowledge, this study investigated the response of selected hardy ferns to salt stress, light stress and a combination of both. We assessed the effects of two salinity levels (50 and 100 mM NaCl) and two light treatments (sun and shade) on morphological traits, visual score, leaf greenness index and leaf content of Na , + 2+ K and Ca in four taxa of Dryopteris genus. We hypothesized that the tested hardy ferns may include taxa tolerant to environmental stresses. 2. Materials and Methods 2.1. Plant Material The study involved three species of hardy ferns belonging to Dryopteris genus (D. affinis, D. atrata and D. filix-mas) and one cultivar of this genus (D. filix-mas “Linearis-Polydactylon”). The plants were propagated in vitro and acclimatized in pots (0.5 dm capacity) in a green- house at a horticultural farm (Rzgów, Poland). Each plant had 5–7 leaves and a very well developed rhizome clump. 2.2. Culture Conditions The plants were planted on 15 July 2019. Each round, a black PVC pot of 1.7 dm capacity harbored a single plant and was ﬁlled with peat substrate (pH 6.0) supplemented with PG Mix fertilizer (Yara, Poland) at a dose of 1.0 kg m . The fertilizer contained: 5.5% N-NO , 8.5% N-NH , 16% P O , 18% K O, 0.8% MgO, 19% SO , 0.03% B, 0.12% 3 4 2 5 2 3 Cu, 0.09% Fe, 0.16% Mn, 0.20% Mo, and 0.04% Zn. The pots were placed on white nursery mats in an unheated plastic tunnel of the area of 225 m , and covered with 0 0 a double layer of inﬂated poly ﬁlm (lat. 53 25 N, long. 14 32 E; elevation, 25 m). The plants were watered every three days with tap water of pH 6.4, electrolytic conductivity 1 3 + 2+ + 0.64 mS cm containing (mg dm ) 6.2 K , 98 Ca and 25 Na . The tunnel’s roof ventilation opened when the temperature inside exceeded 18 C. Air temperature and relative humidity were recorded with a portable USB data logger. The average monthly maximum/minimum air temperature and average maximum/minimum relative humidity (RH) in the plastic house were, respectively: July 28.6 C/15.1 C, RH 93.3%/44.9%; Agronomy 2021, 11, 49 3 of 13 August 29.5 C/15.2 C, RH 94.5%/44.8%; September 22.8 C/11.3 C, RH 96.5%/56.1%; and October 21.9 C/9.2 C, RH 91.6%/67.0%. 2.3. Experimental Design and Treatments Form 5 August 2019 until the end of the trial (23 October 2019), half plants of each fern taxon were grown in a tunnel in full sun, and the other half of the plants were grown in a tunnel under shading screens (a highly reflective aluminized shade fabric). Measurements with a Radiometer-Fotometr RF-100 (Sonopan, Białystok, Poland) determined the photosyn- 2 1 thetic photon flux density (PPFD) on a cloudless day of 4 August 2019 at 609.1 mol m s 2 1 for full sun and 151 mol m s , i.e., 24% of this value, in shade. Starting on 5 August 2019, plants at the two sites (full sun and shade) were watered four times, i.e., every ﬁve days with a solution of sodium chloride (NaCl) pure p.a. 99.9% (Chempur, Poland). NaCl concentration was either 50 or 100 mM, and each plant was provided with 100 mL of the solution per watering. The control plants were irrigated with tap water. NaCl concentrations were selected based on a study by Bogdanovic et al. [24]. After the last dose of NaCl was applied, all plants were watered with tap water until the end of the experiment. The experimental design was a sub-block one, with three repetitions per combination and nine plants per repetition. 2.4. Assessment of Greenness Index, Ornamental Value and Morphological Features On the last day of the experiment we measured leaf greenness index in Soil Plant Analysis Development (SPAD) units with a Chlorophyll Meter SPAD-502 (Minolta, Japan). The measurements were conducted between 10.00 a.m. and noon and included three fully developed leaves without any signs of necrosis, located in the middle of the plant. Three readings were taken per each leaf. Nine plants were assessed per each combination. To determine the decorative value of the plants, ﬁve researchers conducted a bonitation assessment (visual score) by rating all plants according to a ﬁve-point scale, where 1 meant low attractiveness, expressed as insufﬁcient foliage, poor growth and unattractive habit, and 5 meant the maximum decorative value manifested in vigorous growth, attractive habit and healthy foliage. All plants in all combinations were also assessed for their height (from the soil surface to the tip of the tallest leaf) and fresh weight of the above-ground part cut at the substrate level in the pots. + + 2+ 2.5. Analysis of Na , K and Ca Content + + 2+ To determine the content of Na , K and Ca , the collected leaves were rinsed twice with deionized water, blotted dry, placed into brown paper bags and left in an oven at 65 C for 72 h. Dried material was pulverized into particles of diameter below 1 mm, and wet mineralized in 17 mL of 96–97% H SO per 2.0 g of the material. The ion content was 2 4 determined by the flame photometry on a flame photometer AFP-100 (Biotech Engineering Management, Nicosia, Cyprus, as described by Ostrowska [27]. Each mineral was determined in three analytical replicates per treatment. 2.6. Statistical Analysis The experimental data were statistically analyzed by means of a variance analysis for two-factor (salinity and light) experiments in Statistica Professional 13.3 package (TIBCO Software, Palo Alto, CA, USA). Date were analyzed separately for each taxon. The multiple comparison procedure based on the Tukey’s HSD post-hoc test with the signiﬁcance level p 0.05 was used to identify differences between the means. Agronomy 2021, 11, x FOR PEER REVIEW 4 of 13 Software, Palo Alto, CA, USA). Date were analyzed separately for each taxon. The multi- ple comparison procedure based on the Tukey’s HSD post-hoc test with the significance level p ≤ 0.05 was used to identify differences between the means. Agronomy 2021, 11, 49 4 of 13 3. Results 3.1. Overall Effects of Salinity Treatments 3. Results Salinity stress strongly affected plant height, leaf greenness index (SPAD), fresh 3.1. Overall Effects of Salinity Treatments weight of the above-ground parts (Figure 1a–c) and visual score (Table 1) of all investi- Salinity stress strongly affected plant height, leaf greenness index (SPAD), fresh weight gated fern taxa. Plants of all combinations survived the salt stress. NaCl at 50 and 100 mM of the above-ground parts (Figure 1a–c) and visual score (Table 1) of all investigated fern caused a clear plant height reduction in D. atrata, D. affinis, and D. filix-mas whereas D. taxa. Plants of all combinations survived the salt stress. NaCl at 50 and 100 mM caused filix-mas cv. “Linearis-Polydactylon” responded this way only to 100 mM NaCl. SPAD a clear plant height reduction in D. atrata, D. afﬁnis, and D. ﬁlix-mas whereas D. ﬁlix-mas index in D. atrata, D. affinis and D. filix mas dropped with growing salt concentration, and cv. “Linearis-Polydactylon” responded this way only to 100 mM NaCl. SPAD index in it was also reduced in D. filix-mas cv. “Linearis-Polydactylon” but did not depend on NaCl D. atrata, D. afﬁnis and D. ﬁlix mas dropped with growing salt concentration, and it was levels. In A. atrata and A. affinis the drop in fresh weight of the above-ground parts was also reduced in D. ﬁlix-mas cv. “Linearis-Polydactylon” but did not depend on NaCl levels. more intense at higher NaCl concentration. Fresh weight of D. filix-mas plants was also In A. atrata and A. afﬁnis the drop in fresh weight of the above-ground parts was more intense at higher NaCl concentration. Fresh weight of D. ﬁlix-mas plants was also lower lower under salt stress but no significant differences were spotted for 50 and 100 mM under salt stress but no signiﬁcant differences were spotted for 50 and 100 mM NaCl. In NaCl. In D. filix-mas cv. “Linearis-Polydactylon” plants the decrease in fresh weight was D. ﬁlix-mas cv. “Linearis-Polydactylon” plants the decrease in fresh weight was only visible only visible at 100 mM NaCl. Salinity considerably affected the visual score of A. atrata at 100 mM NaCl. Salinity considerably affected the visual score of A. atrata and D. afﬁnis in and D. affinis in a concentration dependent way. In D. filix species and its cultivar “Line- a concentration dependent way. In D. ﬁlix species and its cultivar “Linearis-Polydactylon” aris-Polydactylon” the visual score was also lower in the presence of salt but there was no the visual score was also lower in the presence of salt but there was no difference between difference between NaCl concentrations. NaCl concentrations. (a) (b) Figure 1. Cont. Agronomy 2021, 11, x FOR PEER REVIEW 5 of 13 Agronomy 2021, 11, 49 5 of 13 (c) Figure 1. Effect of salinity on plant height (a), leaf greenness index (Soil Plant Analysis Development Figure 1. Effect of salinity on plant height (a), leaf greenness index (Soil Plant Analysis Develop- (SPAD)) (b) and fresh weight of the above-ground part (c) of D. afﬁnis, D. atrata, D. ﬁlix-mas and ment (SPAD)) (b) and fresh weight of the above-ground part (c) of D. affinis, D. atrata, D. filix-mas D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Different letters indicate and D. filix-mas cv. Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. Different letters signiﬁcant differences for p 0.05. indicate significant differences for p ≤ 0.05. Table 1. Effect of salinity on visual score of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Table 1. Effect of salinity on visual score of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. Line- Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are expressed as mean and standard deviation (SD). aris-Polydactylon (D. filix-mas cv.). Data are expressed as mean and standard deviation (±SD). Salinity Species/Cultivar Salinity Species/Cultivar (mM NaCl) D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. (mM NaCl) D. filix-mas cv. D. atrata D. affinis D. filix-mas 0 4.9 0.1a 4.5 0.6a 4.7 0.4a 4.5 0.6a 0 4.5 ± 0.6a 4.9 ± 0.1a 4.5 ± 0.6a 4.7 ± 0.4a 50 2.6 0.6b 3.8 1.2b 3.7 0.5b 4.3 0.3b 50 2.6 ± 0.6b 3.8 ± 1.2b 3.7 ± 0.5b 4.3 ± 0.3b 100 2.0 1.1c 3.2 0.6c 3.5 0.5b 4.4 0.5b Means not marked with the same letter are signiﬁcantly different at p 0.05. 100 2.0 ± 1.1c 3.2 ± 0.6c 3.5 ± 0.5b 4.4 ± 0.5b Means not marked with the same letter are significantly different at p ≤ 0.05. In all fern taxa, salinity signiﬁcantly increased the leaf content of Na with increasing rates of NaCl (Table 2). Salt treatment resulted in a drop of K levels in D. atrata and its In all fern taxa, salinity significantly increased the leaf content of Na with increasing surge in D. ﬁlix-mas cv. “Linearis-Polydactylon” at both NaCl levels. + Plants of both taxa rates of NaCl (Table 2). Salt treatment resulted in a drop of K levels in D. atrata and its 2+ exposed to the higher NaCl dose (100 mM) accumulated lower content of Ca . surge in D. filix-mas cv. “Linearis-Polydactylon” at both NaCl levels. Plants of both taxa 2+ exposed to the higher NaCl dose (100 mM) accumulated lower content of Ca . + + 2+ Table 2. Effect of salinity on Na , K and Ca content (expressed in % dry weight) in leaves of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are + + 2+ Table 2. Effect of salinity on Na , K and Ca content (expressed in % dry weight) in leaves of D. affinis, D. atrata, D. filix- expressed as mean and standard deviation (SD). mas and D. filix-mas cv. Linearis-Polydactylon (D. filix-mas cv.). Data are expressed as mean and standard deviation (±SD). Species/Cultivar Ion Content Salinity Ion Content Salinity Species/Cultivar D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. (% DW) (mM NaCl) (% DW) (mM NaCl) D. filix-mas cv. D. atrata D. affinis D. filix-mas 0 0.24 0.03c 0.19 0.07c 0.24 0.06c 0.27 0.06c 0 0.24 ± 0.03c 50 0.41 0.19 ± 0.06b 0.07c 0.73 0.09b 0.24 ±0.67 0.06 c 0.10b 0.46 0.2 70.10b ± 0.06c Na 100 1.53 0.13a 0.86 0.06a 0.89 0.15a 1.12 0.06a Na 50 0.41 ± 0.06b 0.73 ± 0.09b 0.67 ± 0.10b 0.46 ± 0.10b 0 1.62 0.03a 1.25 0.16 1.28 0.12 1.08 0.09b 100 1.53 ± 0.13a 0.86 ± 0.06a 0.89 ± 0.15a 1.12 ± 0.06a 50 1.22 0.15b 1.23 0.09 1.35 0.11 1.46 0.24a 0 1.62 ± 0.03a 1.25 ± 0.16 1.28 ± 0.12 1.08 ± 0.09b 100 1.26 0.07b 1.41 0.16 1.38 0.06 1.38 0.17a + 0 0.97 0.06a 0.88 0.16 0.72 0.04 0.74 0.14a K 50 1.22 ± 0.15b 1.23 ± 0.09 1.35 ± 0.11 1.46 ± 0.24a 2+ 50 0.93 0.10a 0.91 0.07 0.80 0.07 0.69 0.14ab Ca 100 1.26 ± 0.07b 1.41 ± 0.16 1.38 ± 0.06 1.38 ± 0.17a 100 0.76 0.04b 0.93 0.08 0.75 0.11 0.56 0.11b 0 0.97 ± 0.06a 0.88 ± 0.16 0.72 ± 0.04 0.74 ± 0.14a Means not marked with the same letter are signiﬁcantly different at p 0.05. 2+ Ca 50 0.93 ± 0.10a 0.91 ± 0.07 0.80 ± 0.07 0.69 ± 0.14ab 100 0.76 ± 0.04b 0.93 ± 0.08 0.75 ± 0.11 0.56 ± 0.11b Means not marked with the same letter are significantly different at p ≤ 0.05. Agronomy 2021, 11, x FOR PEER REVIEW 6 of 13 3.2. Overall Effects of Light Treatments The effects of light conditions on plant height, leaf greenness index (SPAD), fresh weight of the above-ground parts (Figure 2a–c) and visual score (Table 3) was variable and taxon-dependent. D. atrata plants growing in full sun were lower, had smaller fresh weight of the above-ground parts and a lower SPAD index and visual score than shaded plants. Similarly, D. affinis plants grown under full sun had lower fresh weight and re- duced SPAD index and visual score. In D. filix-mas, light conditions did not affect fresh weight or SPAD index but resulted in differences in plant height and visual score. D. filix- mas plants growing in full sun were higher but those growing in the shade had higher Agronomy 2021, 11, 49 6 of 13 visual score. D. filix-mas cv. “Linearis-Polydactylon” plants in high light reached greater SPAD index and higher height than their shaded counterparts. We detected no effects of + + 2+ light availability on the content of Na , K or Ca in all tested ferns (p > 0.05, results not 3.2. Overall Effects of Light Treatments shown). The effects of light conditions on plant height, leaf greenness index (SPAD), fresh weight of the above-ground parts (Figure 2a–c) and visual score (Table 3) was variable Table 3. Effect of light conditions on visual score of D. affinis, D. atrata, D. filix-mas and D. filix-mas and taxon-dependent. D. atrata plants growing in full sun were lower, had smaller fresh cv. Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. weight of the above-ground parts and a lower SPAD index and visual score than shaded plants. Similarly, D. afﬁnis plants grown under full sun had lower fresh weight and reduced Species/Cultivar SPAD index and visual score. In D. ﬁlix-mas, light conditions did not affect fresh weight or Light Conditions D. filix-mas cv. SPAD index but Dr.esulted atrata in differences D. in afplant finis height and D. visual filix-scor mas e. D. ﬁlix-mas plants growing in full sun were higher but those growing in the shade had higher visual score. Full sun 2.3 ± 1.3b 3.4 ± 1.0b 3.4 ± 0.5b 4.5 ± 0.5 D. ﬁlix-mas cv. “Linearis-Polydactylon” plants in high light reached greater SPAD index and Shade 3.7 ± 1.0a 4.6 ± 0.6a 4.3 ± 0.5a 4.4 ± 0.4 higher height than their shaded counterparts. We detected no effects of light availability + + 2+ Means not marked with the same letter are significantly different at p ≤ 0.05. on the content of Na , K or Ca in all tested ferns (p > 0.05, results not shown). (a) (b) Figure 2. Cont. Agronomy 2021, 11, x FOR PEER REVIEW 7 of 13 Agronomy 2021, 11, 49 7 of 13 (c) Figure 2. Effect of light conditions on plant height (a), leaf greenness index (SPAD) (b) and fresh Figure 2. Eff weight ect of of lig the htabove-gr conditiound ons opart n pl(a cn ) of t h D. eig afﬁnis ht (a , D. ), latrata eaf g,rD. een ﬁlix-mas ness in and dex D. (S ﬁlix-mas PAD) ( cv b.) Linearis- and fresh Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Asterisks mark indicate signiﬁcant differences weight of the above-ground part (c) of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. Linearis- for p 0.05. Polydactylon (D. filix-mas cv.). Data are mean ± SD. Asterisks mark indicate significant differences for p ≤ 0.05. Table 3. Effect of light conditions on visual score of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. 3.3. Combined Effects of Salinity and Light Treatment Species/Cultivar The effects of salt stress on plant height, leaf greenness index (SPAD), fresh weight Light Conditions D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. of the above-ground parts (Figure 3a–c) and visual score (Table 4) depended on light con- Full sun 3.4 1.0b 3.4 0.5b 4.5 0.5 2.3 1.3b dition and taxon. In D. atrata and D. affinis salinity reduced plant height considerably Shade 3.7 1.0a 4.6 0.6a 4.3 0.5a 4.4 0.4 stronger in plants growing in full-sun than in shade. In D. filix-mas and cv. “Linearis-Pol- Means not marked with the same letter are signiﬁcantly different at p 0.05. ydactylon” NaCl only slightly diminished plant height under both light conditions. Ex- 3.3. Combined Effects of Salinity and Light Treatment posure to both concentrations of salt resulted in a decrease of fresh weight of D. atrata, D. The effects of salt stress on plant height, leaf greenness index (SPAD), fresh weight of affinis and D. filix-mas in both light treatments, whereas D. filix-mas cv. “Linearis-Polydac- the above-ground parts (Figure 3a–c) and visual score (Table 4) depended on light condition tylon” responded with a drop in fresh weight, both in the sun and in the shade, only to and taxon. In D. atrata and D. afﬁnis salinity reduced plant height considerably stronger in 100 mM NaCl. SPAD greenness index decreased in D. atrata and D. affinis with increasing plants growing in full-sun than in shade. In D. ﬁlix-mas and cv. “Linearis-Polydactylon” concentrati NaCl on o only f Na slightly Cl both diminished under ful plant l sun height andunder shadboth e tre light atmconditions. ents. In DExposur . filix-m eato s, both its salin- concentrations of salt resulted in a decrease of fresh weight of D. atrata, D. afﬁnis and D. ﬁlix- ity-triggered reduction was only perceived in low light intensity. In salt-exposed D. filix- mas in both light treatments, whereas D. ﬁlix-mas cv. “Linearis-Polydactylon” responded mas cv. “Linearis-Polydactylon” plants SPAD value declined in the shade but grew in the with a drop in fresh weight, both in the sun and in the shade, only to 100 mM NaCl. SPAD sun. Control (no salt) and shaded plants of D. atrata, D. affinis and D. filix achieved the greenness index decreased in D. atrata and D. afﬁnis with increasing concentration of NaCl highest visual score. In D. filix-mas cv. “Linearis-Polydactylon” the most decorative plants both under full sun and shade treatments. In D. ﬁlix-mas, its salinity-triggered reduction was only perceived in low light intensity. In salt-exposed D. ﬁlix-mas cv. “Linearis-Polydactylon” were those growing without NaCl pressure in the full sun. Interestingly, we found no leaf plants SPAD value declined in the shade but grew in the sun. Control (no salt) and shaded discoloration or necrosis in D. filix and D. filix-mas cv. “Linearis-Polydactylon” exposed to plants of D. atrata, D. afﬁnis and D. ﬁlix achieved the highest visual score. In D. ﬁlix-mas salt under both light conditions. Salt-exposed plants of D. atrata and D. affinis responded cv. “Linearis-Polydactylon” the most decorative plants were those growing without NaCl with leaf margin chlorosis and necrosis, particularly at 100 NaCl mM and under full sun pressure in the full sun. Interestingly, we found no leaf discoloration or necrosis in D. ﬁlix and D. ﬁlix-mas cv. “Linearis-Polydactylon” exposed to salt under both light conditions. (Figure 4). Salt-exposed plants of D. atrata and D. afﬁnis responded with leaf margin chlorosis and necrosis, particularly at 100 NaCl mM and under full sun (Figure 4). Table 4. Effect of light conditions and salinity on visual score of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. Species/Cultivar Light Salinity Conditions (mM NaCl) D. atrata D. affinis D. filix-mas D. filix-mas cv. 0 3.9 ± 0.1b 4.8 ± 0.1a 3.9 ± 0.1b 5.00 ± 0.00a Full sun 50 2.0 ± 0.0d 2.8 ± 0.1c 3.3 ± 0.6bc 4.55 ± 0.19bc 100 1.0 ± 0.0e 2.6 ± 0.2c 3.1 ± 0.1c 3.96 ± 0.07d 0 5.0 ± 0.0a 5.0 ± 0.0a 5.0 ± 0.0a 4.29 ± 0.25cd Shade 50 3.1 ± 0.2c 4.9 ± 0.1a 4.0 ± 0.0b 4.07 ± 0.13d 100 3.1 ± 0.1c 3.8 ± 0.1b 3.9 ± 0.1b 4.85 ± 0.13ab Means not marked with the same letter are significantly different at p ≤ 0.05. Agronomy 2021, 11, x FOR PEER REVIEW 8 of 13 Agronomy 2021, 11, 49 8 of 13 (a) (b) (c) Figure 3. Effect of light conditions and salinity on plant height (a), leaf greenness index (SPAD) Figure 3. Effect of light conditions and salinity on plant height (a), leaf greenness index (SPAD) (b) (b) and fresh weight of the above-ground part (c) of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas and fresh weight of the above-ground part (c) of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Different letters indicate signiﬁcant Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. Different letters indicate significant differences for p 0.05. differences for p ≤ 0.05. Agronomy 2021, 11, 49 9 of 13 Table 4. Effect of light conditions and salinity on visual score of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Species/Cultivar Light Salinity (mM NaCl) D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. Conditions 0 3.9 0.1b 4.8 0.1a 3.9 0.1b 5.00 0.00a 50 2.0 0.0d 2.8 0.1c 3.3 0.6bc 4.55 0.19bc Full sun 100 1.0 0.0e 2.6 0.2c 3.1 0.1c 3.96 0.07d 0 5.0 0.0a 5.0 0.0a 5.0 0.0a 4.29 0.25cd 50 3.1 0.2c 4.9 0.1a 4.0 0.0b 4.07 0.13d Shade 100 3.1 0.1c 3.8 0.1b 3.9 0.1b 4.85 0.13ab Means not marked with the same letter are signiﬁcantly different at p 0.05. Figure 4. Effect of light conditions and salinity on growth of Dryopteris afﬁnis, Dryopteris atrata, Dryopteris ﬁlix-mas and Dryopteris ﬁlix-mas cv. Linearis-Polydactylon. Left to right: full sun; full sun + 50 mM NaCl; full sun + 100 mM NaCl; shade; shade + 50 mM NaCl and shade + 100 mM NaCl. Agronomy 2021, 11, 49 10 of 13 The greatest content of Na was found in all ferns treated with 100 mM NaCl, irre- spective of light conditions. In D. atrata plants cultivated under full sun and shade, salinity at 50 and 100 mM NaCl resulted in lowering K content. In D. ﬁlix-mas cv. “Linearis- Polydactylon” NaCl at 50 and 100 mM boosted K levels irrespective of light intensity. D. atrata treated with 100 mM NaCl and D. ﬁlix-mas cv. “Linearis-Polydactylon” treated 2+ with 50 mM NaCl exposed to the shade accumulated smaller amounts of Ca (Table 5). + + 2+ Table 5. Effect of light conditions and salinity (50 and 100 mM NaCl) on Na , K and Ca content (expressed in % dry weight) in leaves of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis- Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Species/Cultivar Light Salinity D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. Conditions (mM NaCl) Na 0 0.22 0.02b 0.21 0.09b 0.24 0.04b 0.27 0.07bc 50 0.38 0.07b 0.69 0.09a 0.62 0.10a 0.43 0.13bc Full sun 100 1.60 0.15a 0.84 0.04a 0.88 0.09a 1.08 0.08a 0 0.27 0.02b 0.17 0.06b 0.23 0.09b 0.26 0.06c 50 0.43 0.06b 0.77 0.08a 0.72 0.08a 0.49 0.08b Shade 100 1.45 0.07a 0.88 0.08a 0.91 0.22a 1.15 0.02a 0 1.64 0.04a 1.30 0.10 1.33 0.15 1.09 0.15b 50 1.12 0.13c 1.26 0.12 1.33 0.15 1.49 0.29a Full sun 100 1.32 0.02b 1.38 0.08 1.37 0.08 1.29 0.14ab 0 1.61 0.02a 1.19 0.21 1.23 0.06 1.08 0.03b 50 1.33 0.06b 1.20 0.04 1.37 0.08 1.43 0.24a Shade 100 1.20 0.03bc 1.44 0.24 1.39 0.05 1.46 0.17a 2+ Ca 0 0.94 0.05ab 0.99 0.16 0.72 0.03 0.65 0.08ab 0.88 Full sun 50 0.93 0.04 0.75 0.05 0.65 0.06ab 0.08a–c 100 0.78 0.03bc 0.92 0.11 0.76 0.08 0.65 0.14ab 0 0.99 0.06a 0.76 0.07 0.73 0.06 0.83 0.14a 50 0.98 0.10a 0.89 0.09 0.86 0.05 0.47 0.06b Shade 100 0.75 0.05c 0.95 0.05 0.73 0.15 0.74 0.15ab Means not marked with the same letter are signiﬁcantly different at p 0.05. 4. Discussion During their growth and development plants are exposed to different environmental stresses, the effects of which are often synergistic, and their combined outcome is con- siderably more powerful than that of individual stress factors [28,29]. Understanding the response of individual genotypes to adverse environmental conditions allows for proper selection of tolerant and resistant plants [7,10,30]. Most studies on the effects of stressful conditions have been carried out on ﬂower ornamentals, while the group of leaf ornamental plants has so far received very little attention. The aim of this work was to investigate the response of four ferns of Dryopteris genus, generally considered as shade plants, to multi-stress in the form of salinity and high light intensity. Most plants exposed to excessive salinity limit the elongation growth of cells, which results in reduced growth and biomass production [31,32]. Salt stress often diminishes visual quality of plants by evoking brownish necrosis of leaves [4,8]. In our study, salinity also inhibited growth, reduced fresh weight of the above-ground part and lowered the bonitation score of the investigated ferns, and intensity of these effects depended on the taxon and light conditions (Figure 3, Table 4). The species of D. afﬁnis and D. atrata turned out the most sensitive to salt and they demonstrated leaf margin browning and drying (Figure 4). Negative effects of salinity on the growth and quality of D. afﬁnis and D. atrata were particularly visible under full sun. In the shade, the stress affected growth and Agronomy 2021, 11, 49 11 of 13 ornamental value of D. afﬁnis and D. atrata to a lesser degree. Our results conﬁrmed shade afﬁnity of D. afﬁnis and D. atrata, and what is more, shade mitigated negative effects of salt in these species. Similarly, Medina et al. [33] showed that a halophytic fern Acrostichum aureum was much more tolerant to salt stress when growing in the shade than in the sun. In Hibiscus tiliaceus Hau, cultivated under different light conditions, salinity caused stronger total biomass reduction in plants growing in 90% shade than in full sun and 50% shade [34]. In a heliophilous species Vicia faba, the toxic effects of salinity were more considerably alleviated by higher than lower light intensity [35]. In our study, the same relationship was demonstrated in D. ﬁlix-mas cv. “Linearis-Polydactylon”, as salinity experienced by plants growing under full sun did not reduce fresh weight of their above-ground parts. D. ﬁlix-mas cv. “Linearis-Polydactylon” plants cultivated in shade were the smallest and had the lowest fresh weight. We noticed no clear effects of light conditions on fresh weight of D. ﬁlix-mas but plants growing under full sun demonstrated lower ornamental value than those under low light intensities. As shown by Ure [36], D. ﬁlix-mas tolerates a wide range of light/shade levels. In sensitive species salt stress reduces chlorophyll content, while in tolerant ones the pigment level remains unchanged or may even rise [37,38]. Our study assessed leaf greenness index that correlates with chlorophyll content [39]. We found a negative effect of salt stress on leaf greenness in all shaded ferns (Figure 3b). In full sun SPAD index was clearly lowered in all ferns exposed to salinity, except for D. ﬁlix-mas cv. “Linearis- Polydactylon”, where NaCl slightly enhanced SPAD value. Bogdanovic et al. [24] tested the response of Asplenium viride Britton, Ceterach ofﬁcinarum DC and Phyllitis scolopendrium (L.) Newmann to salt stress (0–500 mM NaCl) in vitro and found that high concentrations of NaCl (250 mM and above) drastically lowered total chlorophyll content in all species, while low concentrations (50 and 100 mM NaCl) enhanced the pigment content in A. viride and C. ofﬁcinarum. Experimentally demonstrated stimulating effect of salinity on the greenness index of D. ﬁlix-mas cv. “Linearis-Polydactylon” may indicate that this cultivar grown under full sun is tolerant to increased salinity. NaCl evoked salinity may disturb ion homeostasis and, consequently, disrupt the physiological processes [40]. Usually, excessive content of Na results in deﬁciency of + + K and Ca [37,41]. There are, however, also contradictory data suggesting that salinity + 2+ causes increased accumulation of K [31] and Ca [42]. Potassium and calcium ions regulate activity of numerous enzymes [43,44], and their deﬁciency decreases plant stress tolerance [45]. In our experiment, the content of Na rose in all taxa exposed to salinity (Table 2) due to using NaCl solution as a stress factor. Enhanced content of Na , as a major solute responsible for increased osmotic pressure of the cell sap, was also observed in salt- treated fern A. aureum [33]. A particularly interesting outcome of this study was a boost in K content in D. ﬁlix-mas cv. “Linearis-Polydactylon”. Similarly, Vogelien et al. [46] showed that a mutant of Ceratopteris richardii stl2, relatively tolerant to NaCl, accumulated greater amounts of K when grown on NaCl-supplemented medium than other fern genotypes. As mentioned earlier, despite NaCl treatment D. ﬁlix-mas cv. “Linearis-Polydactylon” maintained its high bonitation score and greenness index, which may indicate its tolerance to the applied NaCl doses. Furthermore, an increased content of K may suggest a role of these ions in plant adaptation to salt stress. A precise marker of salt stress in A. aureum was the content of cyclitol d-1-O-methyl-muco-inositol, a cytoplasmic compatible solute [33], while other ferns, i.e., A. viride, C. ofﬁcinarum and P. scolopendrium responded to NaCl with a shift in total leaf phenolic content [24]. The mechanisms of plant tolerance to stress are highly complex and multidirectional. Therefore, to better understand fern tolerance to salinity, we need further studies, particularly on the level of oxidative stress and compatible solutes that protect protein structure and biological membranes against negative effects of excessive salt concentrations. Agronomy 2021, 11, 49 12 of 13 5. Conclusions From among four investigated fern taxa, D. filix-mas cv. “Linearis-Polydactylon” showed the greatest tolerance to salt stress. Despite salinity, plants of this cultivar main- tained intense, green coloration of leaves assessed by SPAD greenness index, high visual score and demonstrated increased accumulation of K in the leaves. D. affinis and D. atrata turned out sensitive to salinity, as manifested in leaf necrosis. The effects of salt stress on plant growth depended on light condition and taxon; D. filix-mas cv. “Linearis-Polydactylon” plants were more tolerant to salinity when growing under full sun, and D. affinis and D. atrata showed better tolerance to NaCl under shade. Our knowledge on the impact of abiotic stresses on the growth of ornamental garden plants from the fern group is scarce, which is why these findings seem important and may serve as practical recommendations for the selection of fern species intended for areas exposed to environmental stresses. Author Contributions: Conceptualization, methodology, formal analysis, writing and visualization, P.S.; investigation and data curation, R.P.; All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Data sharing not applicable. 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[CrossRef] http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Agronomy Multidisciplinary Digital Publishing Institute http://www.deepdyve.com/lp/multidisciplinary-digital-publishing-institute/salinity-tolerance-of-four-hardy-ferns-from-the-genus-dryopteris-adans-jB0FdV1xok

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DOI: 10.3390/agronomy11010049
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Abstract

agronomy Article Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions Piotr Salachna * and Rafał Piechocki Department of Horticulture, West Pomeranian University of Technology, 3 Papieza ˙ Pawła VI Str., 71-459 Szczecin, Poland; rafal.piechocki@zut.edu.pl * Correspondence: piotr.salachna@zut.edu.pl; Tel.: +48-91-4496-359 Abstract: Hardy ferns form a group of attractive garden perennials with an unknown response to abiotic stresses. The aim of this study was to evaluate the tolerance of three species of ferns of Dryopteris genus (D. affinis, D. atrata and D. filix-mas) and one cultivar (D. filix-mas cv. “Linearis-Polydactylon”) to salinity and light stress. The plants were grown in full sun and shade and watered with 50 and 100 mM dm NaCl solution. All taxa treated with 100 mM NaCl responded with reduced height, leaf greenness index and fresh weight of the above-ground part. In D. affinis and D. atrata salinity caused leaf damage manifested by necrotic spots, which was not observed in the other two taxa. The effect of NaCl depended on light treatments and individual taxon. D. affinis and D. atrata were more tolerant to salinity when growing under shade. Contrary to that, D. filix-mas cv. “Linearis-Polydactylon” seemed to show significantly greater tolerance to this stress under full sun. Salt-treated D. filix-mas cv. “Linearis-Polydactylon” plants accumulated enhanced amounts of K in the leaves, which might be associated with the taxon’s tolerance to salinity. Among the investigated genotypes, D. filix-mas cv. “Linearis-Polydactylon” seemed the most and D. affinis and D. atrata the least tolerant to salinity and light stress. Keywords: hardy ferns; salt stress; NaCl; light stress; shade; multiple stresses; abiotic stresses Citation: Salachna, P.; Piechocki, R. Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris 1. Introduction Adans. Grown under Different Light Conditions. Agronomy 2021, 11, 49. Ornamental plants are constantly exposed to adverse effects of stress factors that https://doi.org/10.3390/agronomy disturb their growth and diminish their decorative value [1]. These factors operate both during production and after planting at the target site. The stress can be caused by an excess or deﬁciency of any abiotic factor [2]. Very often stresses evoked by unfavorable Received: 30 November 2020 environmental conditions overlap with each other [3]. Most studies conducted so far have Accepted: 25 December 2020 focused on the response of ornamental plants to single stress factors [1,4,5], while their Published: 28 December 2020 response to multiple stresses experienced simultaneously is less known. Excessive substrate salinity causing salt stress is one of the most common abiotic Publisher’s Note: MDPI stays neu- stresses that negatively affect the quality of ornamental plants [4]. Exceeding tolerance tral with regard to jurisdictional clai- threshold for salt triggers numerous adverse changes in plant growth and development [6,7]. ms in published maps and institutio- Too high salinity limits water availability, lowers turgor and leads to inhibition of cell nal afﬁliations. elongation growth, tissue necrosis, yellowing, drying and falling of leaves [8]. The negative effects of salinity are due to toxicity of sodium ions that accumulate in plant tissues and disturb plant ionic balance [9]. The assessment of ion content in plants grown under salt Copyright: © 2020 by the authors. Li- stress is important from a cognitive and practical perspective, as the ion level might be censee MDPI, Basel, Switzerland. a marker for selecting species and cultivars tolerant to elevated salinity [10,11]. This article is an open access article Global climatic changes increase the intensity of extreme weather phenomena, includ- distributed under the terms and con- ing heat waves and ensuing intense solar radiation that causes light stress in plants [12,13]. ditions of the Creative Commons At- Excessive solar radiation results in photoinhibition and photodestruction of pigments, tribution (CC BY) license (https:// and further consequences include reduced photosynthesis efﬁciency and extensive tissue creativecommons.org/licenses/by/ damage [14]. Ornamental plants exposed to adverse light conditions respond with growth 4.0/). Agronomy 2021, 11, 49. https://doi.org/10.3390/agronomy11010049 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, 49 2 of 13 disturbances and diminished decorative value [15]. There are many reports on the reaction of photophilic ornamental plants to light deﬁciency [16–18]. However, the effects of light stress on the quality of shade tolerant ornamental plants have not been extensively studied. Pteridophytes (ferns) are a highly diverse plant group including at least 10,000 species growing in all climatic zones except for extremely dry or cold areas [19]. Many fern species have high decorative value and are grown in pots, gardens and as cut plants [20]. Some of them are also edible and medicinal plants [21]. In general, ferns are sensitive to salinity, excessive sunlight and water shortage. Nevertheless, a few studies reported on fern genotypes tolerant to abiotic stresses and capable of adapting to adverse habitat conditions [22–24]. Different species and cultivars collectively named hardy ferns, and comprising garden ferns with attractive foliage and habit and tolerant to frost, are gaining popularity [20]. The group includes e.g., many ornamental species of Dryopteris Adans genus (Dryopteridaceae family) [25]. A typical species, Dryopteris filix-mas L., forms loose tufts and is deemed to be one of the easiest fern species to cultivate. Of numerous morphotypes and cultivars of D. filix-mas, the one particularly original is cv. “Linearis-Polydactylon” forming dense tufts of upright and extremely delicate, lacy leaves. Dryopteris atrata has decorative, evergreen, dark- green blades sitting on petioles densely covered with dark scales. The ornamental feature of Dryopteris affinis are dark-green, evergreen leaves of slightly shiny, leathery texture [20,25]. Apart from their decorative qualities, D. affinis, D. atrata and D. filix-mas are also sources of valuable metabolites for phytomedicine [26]. Wider dissemination of Dryopteris species and cultivars is prevented by a lack of detailed data on the methods of their cultivation. Moreover, there is little information on Dryopteris resistance to environmental stresses. The stress response of ornamental seed plants is relatively well researched [1,14] but the effects of stress factors on growth and ornamental value of spore plants are much less known. To ﬁll in the gaps in our knowledge, this study investigated the response of selected hardy ferns to salt stress, light stress and a combination of both. We assessed the effects of two salinity levels (50 and 100 mM NaCl) and two light treatments (sun and shade) on morphological traits, visual score, leaf greenness index and leaf content of Na , + 2+ K and Ca in four taxa of Dryopteris genus. We hypothesized that the tested hardy ferns may include taxa tolerant to environmental stresses. 2. Materials and Methods 2.1. Plant Material The study involved three species of hardy ferns belonging to Dryopteris genus (D. affinis, D. atrata and D. filix-mas) and one cultivar of this genus (D. filix-mas “Linearis-Polydactylon”). The plants were propagated in vitro and acclimatized in pots (0.5 dm capacity) in a green- house at a horticultural farm (Rzgów, Poland). Each plant had 5–7 leaves and a very well developed rhizome clump. 2.2. Culture Conditions The plants were planted on 15 July 2019. Each round, a black PVC pot of 1.7 dm capacity harbored a single plant and was ﬁlled with peat substrate (pH 6.0) supplemented with PG Mix fertilizer (Yara, Poland) at a dose of 1.0 kg m . The fertilizer contained: 5.5% N-NO , 8.5% N-NH , 16% P O , 18% K O, 0.8% MgO, 19% SO , 0.03% B, 0.12% 3 4 2 5 2 3 Cu, 0.09% Fe, 0.16% Mn, 0.20% Mo, and 0.04% Zn. The pots were placed on white nursery mats in an unheated plastic tunnel of the area of 225 m , and covered with 0 0 a double layer of inﬂated poly ﬁlm (lat. 53 25 N, long. 14 32 E; elevation, 25 m). The plants were watered every three days with tap water of pH 6.4, electrolytic conductivity 1 3 + 2+ + 0.64 mS cm containing (mg dm ) 6.2 K , 98 Ca and 25 Na . The tunnel’s roof ventilation opened when the temperature inside exceeded 18 C. Air temperature and relative humidity were recorded with a portable USB data logger. The average monthly maximum/minimum air temperature and average maximum/minimum relative humidity (RH) in the plastic house were, respectively: July 28.6 C/15.1 C, RH 93.3%/44.9%; Agronomy 2021, 11, 49 3 of 13 August 29.5 C/15.2 C, RH 94.5%/44.8%; September 22.8 C/11.3 C, RH 96.5%/56.1%; and October 21.9 C/9.2 C, RH 91.6%/67.0%. 2.3. Experimental Design and Treatments Form 5 August 2019 until the end of the trial (23 October 2019), half plants of each fern taxon were grown in a tunnel in full sun, and the other half of the plants were grown in a tunnel under shading screens (a highly reflective aluminized shade fabric). Measurements with a Radiometer-Fotometr RF-100 (Sonopan, Białystok, Poland) determined the photosyn- 2 1 thetic photon flux density (PPFD) on a cloudless day of 4 August 2019 at 609.1 mol m s 2 1 for full sun and 151 mol m s , i.e., 24% of this value, in shade. Starting on 5 August 2019, plants at the two sites (full sun and shade) were watered four times, i.e., every ﬁve days with a solution of sodium chloride (NaCl) pure p.a. 99.9% (Chempur, Poland). NaCl concentration was either 50 or 100 mM, and each plant was provided with 100 mL of the solution per watering. The control plants were irrigated with tap water. NaCl concentrations were selected based on a study by Bogdanovic et al. [24]. After the last dose of NaCl was applied, all plants were watered with tap water until the end of the experiment. The experimental design was a sub-block one, with three repetitions per combination and nine plants per repetition. 2.4. Assessment of Greenness Index, Ornamental Value and Morphological Features On the last day of the experiment we measured leaf greenness index in Soil Plant Analysis Development (SPAD) units with a Chlorophyll Meter SPAD-502 (Minolta, Japan). The measurements were conducted between 10.00 a.m. and noon and included three fully developed leaves without any signs of necrosis, located in the middle of the plant. Three readings were taken per each leaf. Nine plants were assessed per each combination. To determine the decorative value of the plants, ﬁve researchers conducted a bonitation assessment (visual score) by rating all plants according to a ﬁve-point scale, where 1 meant low attractiveness, expressed as insufﬁcient foliage, poor growth and unattractive habit, and 5 meant the maximum decorative value manifested in vigorous growth, attractive habit and healthy foliage. All plants in all combinations were also assessed for their height (from the soil surface to the tip of the tallest leaf) and fresh weight of the above-ground part cut at the substrate level in the pots. + + 2+ 2.5. Analysis of Na , K and Ca Content + + 2+ To determine the content of Na , K and Ca , the collected leaves were rinsed twice with deionized water, blotted dry, placed into brown paper bags and left in an oven at 65 C for 72 h. Dried material was pulverized into particles of diameter below 1 mm, and wet mineralized in 17 mL of 96–97% H SO per 2.0 g of the material. The ion content was 2 4 determined by the flame photometry on a flame photometer AFP-100 (Biotech Engineering Management, Nicosia, Cyprus, as described by Ostrowska [27]. Each mineral was determined in three analytical replicates per treatment. 2.6. Statistical Analysis The experimental data were statistically analyzed by means of a variance analysis for two-factor (salinity and light) experiments in Statistica Professional 13.3 package (TIBCO Software, Palo Alto, CA, USA). Date were analyzed separately for each taxon. The multiple comparison procedure based on the Tukey’s HSD post-hoc test with the signiﬁcance level p 0.05 was used to identify differences between the means. Agronomy 2021, 11, x FOR PEER REVIEW 4 of 13 Software, Palo Alto, CA, USA). Date were analyzed separately for each taxon. The multi- ple comparison procedure based on the Tukey’s HSD post-hoc test with the significance level p ≤ 0.05 was used to identify differences between the means. Agronomy 2021, 11, 49 4 of 13 3. Results 3.1. Overall Effects of Salinity Treatments 3. Results Salinity stress strongly affected plant height, leaf greenness index (SPAD), fresh 3.1. Overall Effects of Salinity Treatments weight of the above-ground parts (Figure 1a–c) and visual score (Table 1) of all investi- Salinity stress strongly affected plant height, leaf greenness index (SPAD), fresh weight gated fern taxa. Plants of all combinations survived the salt stress. NaCl at 50 and 100 mM of the above-ground parts (Figure 1a–c) and visual score (Table 1) of all investigated fern caused a clear plant height reduction in D. atrata, D. affinis, and D. filix-mas whereas D. taxa. Plants of all combinations survived the salt stress. NaCl at 50 and 100 mM caused filix-mas cv. “Linearis-Polydactylon” responded this way only to 100 mM NaCl. SPAD a clear plant height reduction in D. atrata, D. afﬁnis, and D. ﬁlix-mas whereas D. ﬁlix-mas index in D. atrata, D. affinis and D. filix mas dropped with growing salt concentration, and cv. “Linearis-Polydactylon” responded this way only to 100 mM NaCl. SPAD index in it was also reduced in D. filix-mas cv. “Linearis-Polydactylon” but did not depend on NaCl D. atrata, D. afﬁnis and D. ﬁlix mas dropped with growing salt concentration, and it was levels. In A. atrata and A. affinis the drop in fresh weight of the above-ground parts was also reduced in D. ﬁlix-mas cv. “Linearis-Polydactylon” but did not depend on NaCl levels. more intense at higher NaCl concentration. Fresh weight of D. filix-mas plants was also In A. atrata and A. afﬁnis the drop in fresh weight of the above-ground parts was more intense at higher NaCl concentration. Fresh weight of D. ﬁlix-mas plants was also lower lower under salt stress but no significant differences were spotted for 50 and 100 mM under salt stress but no signiﬁcant differences were spotted for 50 and 100 mM NaCl. In NaCl. In D. filix-mas cv. “Linearis-Polydactylon” plants the decrease in fresh weight was D. ﬁlix-mas cv. “Linearis-Polydactylon” plants the decrease in fresh weight was only visible only visible at 100 mM NaCl. Salinity considerably affected the visual score of A. atrata at 100 mM NaCl. Salinity considerably affected the visual score of A. atrata and D. afﬁnis in and D. affinis in a concentration dependent way. In D. filix species and its cultivar “Line- a concentration dependent way. In D. ﬁlix species and its cultivar “Linearis-Polydactylon” aris-Polydactylon” the visual score was also lower in the presence of salt but there was no the visual score was also lower in the presence of salt but there was no difference between difference between NaCl concentrations. NaCl concentrations. (a) (b) Figure 1. Cont. Agronomy 2021, 11, x FOR PEER REVIEW 5 of 13 Agronomy 2021, 11, 49 5 of 13 (c) Figure 1. Effect of salinity on plant height (a), leaf greenness index (Soil Plant Analysis Development Figure 1. Effect of salinity on plant height (a), leaf greenness index (Soil Plant Analysis Develop- (SPAD)) (b) and fresh weight of the above-ground part (c) of D. afﬁnis, D. atrata, D. ﬁlix-mas and ment (SPAD)) (b) and fresh weight of the above-ground part (c) of D. affinis, D. atrata, D. filix-mas D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Different letters indicate and D. filix-mas cv. Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. Different letters signiﬁcant differences for p 0.05. indicate significant differences for p ≤ 0.05. Table 1. Effect of salinity on visual score of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Table 1. Effect of salinity on visual score of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. Line- Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are expressed as mean and standard deviation (SD). aris-Polydactylon (D. filix-mas cv.). Data are expressed as mean and standard deviation (±SD). Salinity Species/Cultivar Salinity Species/Cultivar (mM NaCl) D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. (mM NaCl) D. filix-mas cv. D. atrata D. affinis D. filix-mas 0 4.9 0.1a 4.5 0.6a 4.7 0.4a 4.5 0.6a 0 4.5 ± 0.6a 4.9 ± 0.1a 4.5 ± 0.6a 4.7 ± 0.4a 50 2.6 0.6b 3.8 1.2b 3.7 0.5b 4.3 0.3b 50 2.6 ± 0.6b 3.8 ± 1.2b 3.7 ± 0.5b 4.3 ± 0.3b 100 2.0 1.1c 3.2 0.6c 3.5 0.5b 4.4 0.5b Means not marked with the same letter are signiﬁcantly different at p 0.05. 100 2.0 ± 1.1c 3.2 ± 0.6c 3.5 ± 0.5b 4.4 ± 0.5b Means not marked with the same letter are significantly different at p ≤ 0.05. In all fern taxa, salinity signiﬁcantly increased the leaf content of Na with increasing rates of NaCl (Table 2). Salt treatment resulted in a drop of K levels in D. atrata and its In all fern taxa, salinity significantly increased the leaf content of Na with increasing surge in D. ﬁlix-mas cv. “Linearis-Polydactylon” at both NaCl levels. + Plants of both taxa rates of NaCl (Table 2). Salt treatment resulted in a drop of K levels in D. atrata and its 2+ exposed to the higher NaCl dose (100 mM) accumulated lower content of Ca . surge in D. filix-mas cv. “Linearis-Polydactylon” at both NaCl levels. Plants of both taxa 2+ exposed to the higher NaCl dose (100 mM) accumulated lower content of Ca . + + 2+ Table 2. Effect of salinity on Na , K and Ca content (expressed in % dry weight) in leaves of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are + + 2+ Table 2. Effect of salinity on Na , K and Ca content (expressed in % dry weight) in leaves of D. affinis, D. atrata, D. filix- expressed as mean and standard deviation (SD). mas and D. filix-mas cv. Linearis-Polydactylon (D. filix-mas cv.). Data are expressed as mean and standard deviation (±SD). Species/Cultivar Ion Content Salinity Ion Content Salinity Species/Cultivar D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. (% DW) (mM NaCl) (% DW) (mM NaCl) D. filix-mas cv. D. atrata D. affinis D. filix-mas 0 0.24 0.03c 0.19 0.07c 0.24 0.06c 0.27 0.06c 0 0.24 ± 0.03c 50 0.41 0.19 ± 0.06b 0.07c 0.73 0.09b 0.24 ±0.67 0.06 c 0.10b 0.46 0.2 70.10b ± 0.06c Na 100 1.53 0.13a 0.86 0.06a 0.89 0.15a 1.12 0.06a Na 50 0.41 ± 0.06b 0.73 ± 0.09b 0.67 ± 0.10b 0.46 ± 0.10b 0 1.62 0.03a 1.25 0.16 1.28 0.12 1.08 0.09b 100 1.53 ± 0.13a 0.86 ± 0.06a 0.89 ± 0.15a 1.12 ± 0.06a 50 1.22 0.15b 1.23 0.09 1.35 0.11 1.46 0.24a 0 1.62 ± 0.03a 1.25 ± 0.16 1.28 ± 0.12 1.08 ± 0.09b 100 1.26 0.07b 1.41 0.16 1.38 0.06 1.38 0.17a + 0 0.97 0.06a 0.88 0.16 0.72 0.04 0.74 0.14a K 50 1.22 ± 0.15b 1.23 ± 0.09 1.35 ± 0.11 1.46 ± 0.24a 2+ 50 0.93 0.10a 0.91 0.07 0.80 0.07 0.69 0.14ab Ca 100 1.26 ± 0.07b 1.41 ± 0.16 1.38 ± 0.06 1.38 ± 0.17a 100 0.76 0.04b 0.93 0.08 0.75 0.11 0.56 0.11b 0 0.97 ± 0.06a 0.88 ± 0.16 0.72 ± 0.04 0.74 ± 0.14a Means not marked with the same letter are signiﬁcantly different at p 0.05. 2+ Ca 50 0.93 ± 0.10a 0.91 ± 0.07 0.80 ± 0.07 0.69 ± 0.14ab 100 0.76 ± 0.04b 0.93 ± 0.08 0.75 ± 0.11 0.56 ± 0.11b Means not marked with the same letter are significantly different at p ≤ 0.05. Agronomy 2021, 11, x FOR PEER REVIEW 6 of 13 3.2. Overall Effects of Light Treatments The effects of light conditions on plant height, leaf greenness index (SPAD), fresh weight of the above-ground parts (Figure 2a–c) and visual score (Table 3) was variable and taxon-dependent. D. atrata plants growing in full sun were lower, had smaller fresh weight of the above-ground parts and a lower SPAD index and visual score than shaded plants. Similarly, D. affinis plants grown under full sun had lower fresh weight and re- duced SPAD index and visual score. In D. filix-mas, light conditions did not affect fresh weight or SPAD index but resulted in differences in plant height and visual score. D. filix- mas plants growing in full sun were higher but those growing in the shade had higher Agronomy 2021, 11, 49 6 of 13 visual score. D. filix-mas cv. “Linearis-Polydactylon” plants in high light reached greater SPAD index and higher height than their shaded counterparts. We detected no effects of + + 2+ light availability on the content of Na , K or Ca in all tested ferns (p > 0.05, results not 3.2. Overall Effects of Light Treatments shown). The effects of light conditions on plant height, leaf greenness index (SPAD), fresh weight of the above-ground parts (Figure 2a–c) and visual score (Table 3) was variable Table 3. Effect of light conditions on visual score of D. affinis, D. atrata, D. filix-mas and D. filix-mas and taxon-dependent. D. atrata plants growing in full sun were lower, had smaller fresh cv. Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. weight of the above-ground parts and a lower SPAD index and visual score than shaded plants. Similarly, D. afﬁnis plants grown under full sun had lower fresh weight and reduced Species/Cultivar SPAD index and visual score. In D. ﬁlix-mas, light conditions did not affect fresh weight or Light Conditions D. filix-mas cv. SPAD index but Dr.esulted atrata in differences D. in afplant finis height and D. visual filix-scor mas e. D. ﬁlix-mas plants growing in full sun were higher but those growing in the shade had higher visual score. Full sun 2.3 ± 1.3b 3.4 ± 1.0b 3.4 ± 0.5b 4.5 ± 0.5 D. ﬁlix-mas cv. “Linearis-Polydactylon” plants in high light reached greater SPAD index and Shade 3.7 ± 1.0a 4.6 ± 0.6a 4.3 ± 0.5a 4.4 ± 0.4 higher height than their shaded counterparts. We detected no effects of light availability + + 2+ Means not marked with the same letter are significantly different at p ≤ 0.05. on the content of Na , K or Ca in all tested ferns (p > 0.05, results not shown). (a) (b) Figure 2. Cont. Agronomy 2021, 11, x FOR PEER REVIEW 7 of 13 Agronomy 2021, 11, 49 7 of 13 (c) Figure 2. Effect of light conditions on plant height (a), leaf greenness index (SPAD) (b) and fresh Figure 2. Eff weight ect of of lig the htabove-gr conditiound ons opart n pl(a cn ) of t h D. eig afﬁnis ht (a , D. ), latrata eaf g,rD. een ﬁlix-mas ness in and dex D. (S ﬁlix-mas PAD) ( cv b.) Linearis- and fresh Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Asterisks mark indicate signiﬁcant differences weight of the above-ground part (c) of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. Linearis- for p 0.05. Polydactylon (D. filix-mas cv.). Data are mean ± SD. Asterisks mark indicate significant differences for p ≤ 0.05. Table 3. Effect of light conditions on visual score of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. 3.3. Combined Effects of Salinity and Light Treatment Species/Cultivar The effects of salt stress on plant height, leaf greenness index (SPAD), fresh weight Light Conditions D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. of the above-ground parts (Figure 3a–c) and visual score (Table 4) depended on light con- Full sun 3.4 1.0b 3.4 0.5b 4.5 0.5 2.3 1.3b dition and taxon. In D. atrata and D. affinis salinity reduced plant height considerably Shade 3.7 1.0a 4.6 0.6a 4.3 0.5a 4.4 0.4 stronger in plants growing in full-sun than in shade. In D. filix-mas and cv. “Linearis-Pol- Means not marked with the same letter are signiﬁcantly different at p 0.05. ydactylon” NaCl only slightly diminished plant height under both light conditions. Ex- 3.3. Combined Effects of Salinity and Light Treatment posure to both concentrations of salt resulted in a decrease of fresh weight of D. atrata, D. The effects of salt stress on plant height, leaf greenness index (SPAD), fresh weight of affinis and D. filix-mas in both light treatments, whereas D. filix-mas cv. “Linearis-Polydac- the above-ground parts (Figure 3a–c) and visual score (Table 4) depended on light condition tylon” responded with a drop in fresh weight, both in the sun and in the shade, only to and taxon. In D. atrata and D. afﬁnis salinity reduced plant height considerably stronger in 100 mM NaCl. SPAD greenness index decreased in D. atrata and D. affinis with increasing plants growing in full-sun than in shade. In D. ﬁlix-mas and cv. “Linearis-Polydactylon” concentrati NaCl on o only f Na slightly Cl both diminished under ful plant l sun height andunder shadboth e tre light atmconditions. ents. In DExposur . filix-m eato s, both its salin- concentrations of salt resulted in a decrease of fresh weight of D. atrata, D. afﬁnis and D. ﬁlix- ity-triggered reduction was only perceived in low light intensity. In salt-exposed D. filix- mas in both light treatments, whereas D. ﬁlix-mas cv. “Linearis-Polydactylon” responded mas cv. “Linearis-Polydactylon” plants SPAD value declined in the shade but grew in the with a drop in fresh weight, both in the sun and in the shade, only to 100 mM NaCl. SPAD sun. Control (no salt) and shaded plants of D. atrata, D. affinis and D. filix achieved the greenness index decreased in D. atrata and D. afﬁnis with increasing concentration of NaCl highest visual score. In D. filix-mas cv. “Linearis-Polydactylon” the most decorative plants both under full sun and shade treatments. In D. ﬁlix-mas, its salinity-triggered reduction was only perceived in low light intensity. In salt-exposed D. ﬁlix-mas cv. “Linearis-Polydactylon” were those growing without NaCl pressure in the full sun. Interestingly, we found no leaf plants SPAD value declined in the shade but grew in the sun. Control (no salt) and shaded discoloration or necrosis in D. filix and D. filix-mas cv. “Linearis-Polydactylon” exposed to plants of D. atrata, D. afﬁnis and D. ﬁlix achieved the highest visual score. In D. ﬁlix-mas salt under both light conditions. Salt-exposed plants of D. atrata and D. affinis responded cv. “Linearis-Polydactylon” the most decorative plants were those growing without NaCl with leaf margin chlorosis and necrosis, particularly at 100 NaCl mM and under full sun pressure in the full sun. Interestingly, we found no leaf discoloration or necrosis in D. ﬁlix and D. ﬁlix-mas cv. “Linearis-Polydactylon” exposed to salt under both light conditions. (Figure 4). Salt-exposed plants of D. atrata and D. afﬁnis responded with leaf margin chlorosis and necrosis, particularly at 100 NaCl mM and under full sun (Figure 4). Table 4. Effect of light conditions and salinity on visual score of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. Species/Cultivar Light Salinity Conditions (mM NaCl) D. atrata D. affinis D. filix-mas D. filix-mas cv. 0 3.9 ± 0.1b 4.8 ± 0.1a 3.9 ± 0.1b 5.00 ± 0.00a Full sun 50 2.0 ± 0.0d 2.8 ± 0.1c 3.3 ± 0.6bc 4.55 ± 0.19bc 100 1.0 ± 0.0e 2.6 ± 0.2c 3.1 ± 0.1c 3.96 ± 0.07d 0 5.0 ± 0.0a 5.0 ± 0.0a 5.0 ± 0.0a 4.29 ± 0.25cd Shade 50 3.1 ± 0.2c 4.9 ± 0.1a 4.0 ± 0.0b 4.07 ± 0.13d 100 3.1 ± 0.1c 3.8 ± 0.1b 3.9 ± 0.1b 4.85 ± 0.13ab Means not marked with the same letter are significantly different at p ≤ 0.05. Agronomy 2021, 11, x FOR PEER REVIEW 8 of 13 Agronomy 2021, 11, 49 8 of 13 (a) (b) (c) Figure 3. Effect of light conditions and salinity on plant height (a), leaf greenness index (SPAD) Figure 3. Effect of light conditions and salinity on plant height (a), leaf greenness index (SPAD) (b) (b) and fresh weight of the above-ground part (c) of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas and fresh weight of the above-ground part (c) of D. affinis, D. atrata, D. filix-mas and D. filix-mas cv. cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Different letters indicate signiﬁcant Linearis-Polydactylon (D. filix-mas cv.). Data are mean ± SD. Different letters indicate significant differences for p 0.05. differences for p ≤ 0.05. Agronomy 2021, 11, 49 9 of 13 Table 4. Effect of light conditions and salinity on visual score of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis-Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Species/Cultivar Light Salinity (mM NaCl) D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. Conditions 0 3.9 0.1b 4.8 0.1a 3.9 0.1b 5.00 0.00a 50 2.0 0.0d 2.8 0.1c 3.3 0.6bc 4.55 0.19bc Full sun 100 1.0 0.0e 2.6 0.2c 3.1 0.1c 3.96 0.07d 0 5.0 0.0a 5.0 0.0a 5.0 0.0a 4.29 0.25cd 50 3.1 0.2c 4.9 0.1a 4.0 0.0b 4.07 0.13d Shade 100 3.1 0.1c 3.8 0.1b 3.9 0.1b 4.85 0.13ab Means not marked with the same letter are signiﬁcantly different at p 0.05. Figure 4. Effect of light conditions and salinity on growth of Dryopteris afﬁnis, Dryopteris atrata, Dryopteris ﬁlix-mas and Dryopteris ﬁlix-mas cv. Linearis-Polydactylon. Left to right: full sun; full sun + 50 mM NaCl; full sun + 100 mM NaCl; shade; shade + 50 mM NaCl and shade + 100 mM NaCl. Agronomy 2021, 11, 49 10 of 13 The greatest content of Na was found in all ferns treated with 100 mM NaCl, irre- spective of light conditions. In D. atrata plants cultivated under full sun and shade, salinity at 50 and 100 mM NaCl resulted in lowering K content. In D. ﬁlix-mas cv. “Linearis- Polydactylon” NaCl at 50 and 100 mM boosted K levels irrespective of light intensity. D. atrata treated with 100 mM NaCl and D. ﬁlix-mas cv. “Linearis-Polydactylon” treated 2+ with 50 mM NaCl exposed to the shade accumulated smaller amounts of Ca (Table 5). + + 2+ Table 5. Effect of light conditions and salinity (50 and 100 mM NaCl) on Na , K and Ca content (expressed in % dry weight) in leaves of D. afﬁnis, D. atrata, D. ﬁlix-mas and D. ﬁlix-mas cv. Linearis- Polydactylon (D. ﬁlix-mas cv.). Data are mean SD. Species/Cultivar Light Salinity D. atrata D. afﬁnis D. ﬁlix-mas D. ﬁlix-mas cv. Conditions (mM NaCl) Na 0 0.22 0.02b 0.21 0.09b 0.24 0.04b 0.27 0.07bc 50 0.38 0.07b 0.69 0.09a 0.62 0.10a 0.43 0.13bc Full sun 100 1.60 0.15a 0.84 0.04a 0.88 0.09a 1.08 0.08a 0 0.27 0.02b 0.17 0.06b 0.23 0.09b 0.26 0.06c 50 0.43 0.06b 0.77 0.08a 0.72 0.08a 0.49 0.08b Shade 100 1.45 0.07a 0.88 0.08a 0.91 0.22a 1.15 0.02a 0 1.64 0.04a 1.30 0.10 1.33 0.15 1.09 0.15b 50 1.12 0.13c 1.26 0.12 1.33 0.15 1.49 0.29a Full sun 100 1.32 0.02b 1.38 0.08 1.37 0.08 1.29 0.14ab 0 1.61 0.02a 1.19 0.21 1.23 0.06 1.08 0.03b 50 1.33 0.06b 1.20 0.04 1.37 0.08 1.43 0.24a Shade 100 1.20 0.03bc 1.44 0.24 1.39 0.05 1.46 0.17a 2+ Ca 0 0.94 0.05ab 0.99 0.16 0.72 0.03 0.65 0.08ab 0.88 Full sun 50 0.93 0.04 0.75 0.05 0.65 0.06ab 0.08a–c 100 0.78 0.03bc 0.92 0.11 0.76 0.08 0.65 0.14ab 0 0.99 0.06a 0.76 0.07 0.73 0.06 0.83 0.14a 50 0.98 0.10a 0.89 0.09 0.86 0.05 0.47 0.06b Shade 100 0.75 0.05c 0.95 0.05 0.73 0.15 0.74 0.15ab Means not marked with the same letter are signiﬁcantly different at p 0.05. 4. Discussion During their growth and development plants are exposed to different environmental stresses, the effects of which are often synergistic, and their combined outcome is con- siderably more powerful than that of individual stress factors [28,29]. Understanding the response of individual genotypes to adverse environmental conditions allows for proper selection of tolerant and resistant plants [7,10,30]. Most studies on the effects of stressful conditions have been carried out on ﬂower ornamentals, while the group of leaf ornamental plants has so far received very little attention. The aim of this work was to investigate the response of four ferns of Dryopteris genus, generally considered as shade plants, to multi-stress in the form of salinity and high light intensity. Most plants exposed to excessive salinity limit the elongation growth of cells, which results in reduced growth and biomass production [31,32]. Salt stress often diminishes visual quality of plants by evoking brownish necrosis of leaves [4,8]. In our study, salinity also inhibited growth, reduced fresh weight of the above-ground part and lowered the bonitation score of the investigated ferns, and intensity of these effects depended on the taxon and light conditions (Figure 3, Table 4). The species of D. afﬁnis and D. atrata turned out the most sensitive to salt and they demonstrated leaf margin browning and drying (Figure 4). Negative effects of salinity on the growth and quality of D. afﬁnis and D. atrata were particularly visible under full sun. In the shade, the stress affected growth and Agronomy 2021, 11, 49 11 of 13 ornamental value of D. afﬁnis and D. atrata to a lesser degree. Our results conﬁrmed shade afﬁnity of D. afﬁnis and D. atrata, and what is more, shade mitigated negative effects of salt in these species. Similarly, Medina et al. [33] showed that a halophytic fern Acrostichum aureum was much more tolerant to salt stress when growing in the shade than in the sun. In Hibiscus tiliaceus Hau, cultivated under different light conditions, salinity caused stronger total biomass reduction in plants growing in 90% shade than in full sun and 50% shade [34]. In a heliophilous species Vicia faba, the toxic effects of salinity were more considerably alleviated by higher than lower light intensity [35]. In our study, the same relationship was demonstrated in D. ﬁlix-mas cv. “Linearis-Polydactylon”, as salinity experienced by plants growing under full sun did not reduce fresh weight of their above-ground parts. D. ﬁlix-mas cv. “Linearis-Polydactylon” plants cultivated in shade were the smallest and had the lowest fresh weight. We noticed no clear effects of light conditions on fresh weight of D. ﬁlix-mas but plants growing under full sun demonstrated lower ornamental value than those under low light intensities. As shown by Ure [36], D. ﬁlix-mas tolerates a wide range of light/shade levels. In sensitive species salt stress reduces chlorophyll content, while in tolerant ones the pigment level remains unchanged or may even rise [37,38]. Our study assessed leaf greenness index that correlates with chlorophyll content [39]. We found a negative effect of salt stress on leaf greenness in all shaded ferns (Figure 3b). In full sun SPAD index was clearly lowered in all ferns exposed to salinity, except for D. ﬁlix-mas cv. “Linearis- Polydactylon”, where NaCl slightly enhanced SPAD value. Bogdanovic et al. [24] tested the response of Asplenium viride Britton, Ceterach ofﬁcinarum DC and Phyllitis scolopendrium (L.) Newmann to salt stress (0–500 mM NaCl) in vitro and found that high concentrations of NaCl (250 mM and above) drastically lowered total chlorophyll content in all species, while low concentrations (50 and 100 mM NaCl) enhanced the pigment content in A. viride and C. ofﬁcinarum. Experimentally demonstrated stimulating effect of salinity on the greenness index of D. ﬁlix-mas cv. “Linearis-Polydactylon” may indicate that this cultivar grown under full sun is tolerant to increased salinity. NaCl evoked salinity may disturb ion homeostasis and, consequently, disrupt the physiological processes [40]. Usually, excessive content of Na results in deﬁciency of + + K and Ca [37,41]. There are, however, also contradictory data suggesting that salinity + 2+ causes increased accumulation of K [31] and Ca [42]. Potassium and calcium ions regulate activity of numerous enzymes [43,44], and their deﬁciency decreases plant stress tolerance [45]. In our experiment, the content of Na rose in all taxa exposed to salinity (Table 2) due to using NaCl solution as a stress factor. Enhanced content of Na , as a major solute responsible for increased osmotic pressure of the cell sap, was also observed in salt- treated fern A. aureum [33]. A particularly interesting outcome of this study was a boost in K content in D. ﬁlix-mas cv. “Linearis-Polydactylon”. Similarly, Vogelien et al. [46] showed that a mutant of Ceratopteris richardii stl2, relatively tolerant to NaCl, accumulated greater amounts of K when grown on NaCl-supplemented medium than other fern genotypes. As mentioned earlier, despite NaCl treatment D. ﬁlix-mas cv. “Linearis-Polydactylon” maintained its high bonitation score and greenness index, which may indicate its tolerance to the applied NaCl doses. Furthermore, an increased content of K may suggest a role of these ions in plant adaptation to salt stress. A precise marker of salt stress in A. aureum was the content of cyclitol d-1-O-methyl-muco-inositol, a cytoplasmic compatible solute [33], while other ferns, i.e., A. viride, C. ofﬁcinarum and P. scolopendrium responded to NaCl with a shift in total leaf phenolic content [24]. The mechanisms of plant tolerance to stress are highly complex and multidirectional. Therefore, to better understand fern tolerance to salinity, we need further studies, particularly on the level of oxidative stress and compatible solutes that protect protein structure and biological membranes against negative effects of excessive salt concentrations. Agronomy 2021, 11, 49 12 of 13 5. Conclusions From among four investigated fern taxa, D. filix-mas cv. “Linearis-Polydactylon” showed the greatest tolerance to salt stress. Despite salinity, plants of this cultivar main- tained intense, green coloration of leaves assessed by SPAD greenness index, high visual score and demonstrated increased accumulation of K in the leaves. D. affinis and D. atrata turned out sensitive to salinity, as manifested in leaf necrosis. The effects of salt stress on plant growth depended on light condition and taxon; D. filix-mas cv. “Linearis-Polydactylon” plants were more tolerant to salinity when growing under full sun, and D. affinis and D. atrata showed better tolerance to NaCl under shade. Our knowledge on the impact of abiotic stresses on the growth of ornamental garden plants from the fern group is scarce, which is why these findings seem important and may serve as practical recommendations for the selection of fern species intended for areas exposed to environmental stresses. Author Contributions: Conceptualization, methodology, formal analysis, writing and visualization, P.S.; investigation and data curation, R.P.; All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Data sharing not applicable. 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Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions

Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions

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Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions

Salinity Tolerance of Four Hardy Ferns from the Genus Dryopteris Adans. Grown under Different Light Conditions

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