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〔研究論文〕 芝草研究 J. Jpn. Soc. Turfgrass Sci. 48（2），142～ 148

Salt Gland Characteristics and Activity of matrella Merr. in Environments with Different Levels of Salinity*1, *2

Souichirou Sugiura*3

Summary: To clarify the salt stress response of Zoysia matrella from the perspective of salt gland activity, four different concentrations of NaCl solution were used to treat the when the pot soil surface appeared to be dry. After 35 days of treatment, the Na+ amount in the and excreted Na+ increased with increasing NaCl treatment concentrations. The amounts of Na+ and Cl− accumulated in the were higher than the amounts excreted. Overall, the adaxial side of the leaves showed a higher salt gland density with larger sizes than those on the abaxial side. No significant differences in salt gland density or size were observed among the four NaCl treatments. Previous studies conducted in a high-moisture environment such as in hydroponic culture showed that Na+ excretion was higher than the accumulation in the leaf. In contrast, the present study showed Na+ excretion from the leaf was lower than the accumulated amount. These results indicate that salinity in the soil does not affect the leaf salt gland density or size, and salt excretion from Z. matrella may be highly affected by soil moisture rather than by salt gland density or size on the leaf surface. Furthermore, these results suggest that Z. matrella can adjust the amount of salt excretion according to soil moisture.

摘要：耐塩性を有する植物の特徴として，葉身部表面に存在する塩類腺が多いほど多くの塩分を排出することが 可能であり，塩類腺の密度と耐塩性の関係が報告されている。そこで本研究では，高い耐塩性を有するコウライ シバ（Zoysia Matrella Merr.）の塩ストレス対応の一端を明らかにするため，本種に 4 段階［0 g/L（対照区），7.5 g/L，15 g/L および 30 g/L］の塩分濃度の NaCl 溶液を 35 日間与えた。NaCl 溶液の施用は，土壌表面に乾きが見 られた時に行った。35 日後，葉身部の乾燥重量，葉身部の枯死率，葉身部表面の塩類腺の密度および大きさを測 定し，さらに，各イオン（Na+，Cl− および K+）について，葉身内部のイオン量（蓄積イオン），葉身外部のイオ ン量（排出イオン）を測定した。その結果，施用 NaCl 溶液の濃度間の比較では，葉身部の枯死率に有意な違い が見られず，コウライシバの高い耐塩性が示された。葉身部の蓄積 Na+ 量および排出 Na+ 量は施用塩分濃度が高 くなるにつれて高い値を示した。葉身部の Na+ および Cl− 量は，4 段階の NaCl 溶液濃度全てで，排出イオン量よ りも蓄積イオン量で高い値を示した。さらに，施用 NaCl 溶液の濃度間の比較では，塩類腺の密度や大きさには 有意な差が見られなかった。水耕栽培等の高水分環境における類似研究では，葉身部から排出された Na+ 量が葉 身内部の Na+ 量よりも高く，本研究とは逆の結果が報告されている。本研究の結果より，施用 NaCl 溶液の濃度 の違いが，塩類腺の密度や大きさに影響しないことから，コウライシバの塩分排出特性は，塩類腺の密度や大き さよりも，生育する土壌の水分状況に大きく影響されると考えられた。また，本種は，土壌の水分状況に応じて， 塩分の排出量や蓄積量を調整していると推察された。土壌水分量と塩類腺からの塩分排出に焦点を当てた研究は 見当たらず，今後研究が必要であろう。

Gramineae is considered as a salt-tolerant family Introduction compared to other families, and many studies have been Zoysia matrella Merr. is a salt-tolerant turfgrass and conducted to evaluate the salt glands and salt excretion was previously shown to accumulate more NaCl in the in its members including Bermudagrass2,12,13), Rhodes leaf blade than in the and roots after NaCl grass7,19), seashore paspalum2,12), Centipede grass12), St. uptake from the soil22). However, NaCl excretion from Augustine grass12), and Sporobolus virginicus21). Various the salt glands on the leaf blade has not been evaluated studies of the salt glands and salt excretion have also in detail. Salt-tolerant species possess salt glands on the been conducted to evaluate the genus Zoysia. The trait leaf surface to excrete excessive salt from the plant8,26). of salt excretion differs among Zoysia species. High salt In Limonium bicolor (Bag.) Kuntze and Aeluropus litto- gland density on the leaf is related to the salt excretion ralis (Wild) Parl, salt gland densities on the leaf surface amount and salt tolerance14). Compared to Z. japonica, and salt excretions increased with increasing salinity in Z. matrella has more salt glands on the leaf surface and the growing environment1,24). excretes more salt from its salt glands11).

*1 Part of this study was presented at the spring meeting of the JSTS (Japanese Society of Turfgrass Science) in 201723). *2 This study was partially supported by a Grant-in-Aid for turf research of the JSTS (Japanese Society of Turfgrass Science). *3 Department of Landscape Architecture, Graduate School of Agriculture, Tokyo University of Agriculture, Tokyo 156-8502, . Souichirou Sugiura: Salt Gland Characteristics and Activity of Zoysia matrella Merr. in Environments with Different Levels of Salinity 143

Zoysia matrella Merr. is a Gramineae appeared to be dry [August 26 and 30, and September member and a popular turf grass in green spaces and 5, 12, and 22 (5 treatments)]. The soil was treated by on golf courses. Further, compared to other Zoysia using a funnel to avoid contact of the salt solution with species, Z. matrella has higher salt tolerance9). Zoysia the Zoysia leaves. During NaCl solution treatment, the species have been examined to determine the relation- average temperature was 28.7°C and average humidity ship between salt gland density and salt excretion11,25) in the glasshouse was 73%. and turf quality and salt excretion amount from salt To evaluate salinity in the pot, the water discharged glands10,15). However, many previous studies were con- from the pot drain hole as gravity water was collected ducted under extremely high moisture conditions, such in a centrifuge tube after treatment with NaCl solu- as studies on Z. matrella growing in hydroponic cul- tion. Electronic conductivity (EC) of the collected grav- ture with NaCl solution10,11). Turf growth under high ity water was measured with an electrical conductivity moisture conditions such as in hydroponic culture may meter (CM-60G, DKK-TOA Corporation, Tokyo, Japan). greatly differ from Z. matrella growth in the actual field Subsequently, the measured EC was converted to an environment. Further, there are no detailed studies on estimated NaCl concentration using the following for- the relationships between salt gland density, salt gland mula9): size, salt accumulation in the leaf, amount of salt excre- Estimated NaCl concentration (mg/L) = 640 × EC tion from the salt gland, and turf quality in environ- (mS/cm) ments with different salt concentrations. Measurement of salt gland density and salt gland size on In this study, NaCl solution at four different con- the leaf surface centrations was used to treat Z. matrella at moderate After 35 days of NaCl treatment, 6 mature leaves treatment intervals, and turf quality, ion accumulation were collected from each , rinsed well with dis- in the leaf, ion excretion from the salt glands, salt gland tilled water, and wiped to remove the water on the density, and salt gland size on the leaf were measured. leaf surface. To prepare replicas of leaf surfaces, nail The aim of this study was to clarify the response of polish was used5). Nail polish was applied to the leaf Z. matrella to salt stress in the context of salt gland surfaces (adaxial side and abaxial side, each 3 leaves) activity. These findings will be valuable for issues such and allowed to dry for 30 min. After the nail polish on as the increasing demand for the use of saline water the leaves was dry, the replica of the leaf surface was for turfgrass worldwide2,9), uptake of NaCl from the removed using adhesive tape. The replica was then soil and mitigating salt accumulation using salt tolerant attached to a slide glass to observe the leaf surface. plants8,22), and determining the requirements for breed- Salt glands on the leaf surface were observed under a ing species with high salt-tolerance14). microscope (BA210EINT, Shimadzu Rika Corp., Kyoto, Japan). Leaf surface observation and salt gland density Materials and Methods and size measurements were performed using image Species and experimental design analysis software (Motic Images Plus, attachment soft- The sod of Zoysia matrella was purchased from the ware of BA210EINT, Motic Microscopy, Hong Kong, Tottori Product Association (Tottori, Japan). Three ). The leaf surface structure was observed at stolons (3 cm each) were planted in a pot (1/5,000 ×100 magnification on the PC monitor display with are Wagner pot, diameter: 174 mm, depth: 197 mm) on a magnified size of 0.5 mm2 (Fig. 1). The salt gland April 14, 2016 and filled with 1.0 kg gravel as a drain- density and size were measured at ×400 magnification age layer and 4.0 kg river sand (maximum particle size: on the PC monitor display with a magnified size of 2 mm) as bed soil. Each pot was irrigated with tap water 0.03 mm2 (Fig. 2). Five points were measured per slide for 132 days until the plant was well-established. Chemi- glass (5 × 3 points on both the adaxial side or abaxial cal fertilizer (6 : 4: 3, N : P : K) was applied twice at 0.3 g side per pot). per pot on April 27 and May 5, 2016. For NaCl treat- Measurement of ion accumulation in leaves and ion ment, four treatments were prepared [0 (as control), excretion from salt glands 7.5, 15, and 30 g/L], with 3 repetitions for each treat- After 35 days of NaCl treatment, 5-6 mature leaves ment. Each pot containing a plant was placed at random were collected from each pot and placed in a 15-mL cen- in a glasshouse at the Tokyo University of Agriculture, trifuge tube with 13 mL of distilled water (distilled water Tokyo, Japan. was weighed before leaves were placed). To measure NaCl solution treatment and gravity water measurement the ion excretion from the leaf surface, the tubes were After supplying tap water to the pots for 132 days, placed in an ultrasonic washer which was run for 30 NaCl solution was added. NaCl (99.5%) was mixed with min16). The washed leaves were then removed from the tap water in a plastic tank and four concentrations [0 tube, and the water in the tube was stored in a refrigera- g/L (control), 7.5 g/L (≒ 12 mS/cm), 15 g/L (≒ 24 mS/ tor until measurement. The washed leaves were dried cm), and 30 g/L (≒ 48 mS/cm)]. Next, 600 mL of NaCl in an oven at 90°C for 24 h, and then the dry weight solution or tap water (control) was used to treat to each (DW) was measured. The dried leaves were milled pot. NaCl solutions were treated from August 25 to Sep- using beads in a centrifuge tube with a homogenizer tember 29, 2016 (35 days) and when the pot soil surface (BMS-A20TP, Bio Medical Science Co., Ltd., Tokyo, 144 芝草研究 第 48 巻 第 2 号 2020 年 3 月

Fig. 1 Salt gland on the leaf surface of Zoysia matrella (×100 Fig. 2 Salt glands on the leaf surface of Zoysia matrella (×400 magnification, 0.5 mm2 image area), (a) adaxial side, (b) magnification, 0.03 mm2 image area), (a) adaxial side, abaxial side. SG = Salt gland, ST = Stomata. (b) abaxial side. SG = Salt gland, ST = Stomata.

Japan). To measure the ion accumulation in the leaves, green leaves (healthy leaves) and brown leaves (dead milled dried leaves were placed in a 2-mL centrifuge leaves) to measure the dry weight. The shoot mortality tube with distilled water. The tube was then shaken well ratio (turf quality) was calculated using data from the by hand for 30 s. and the solution was filtered through dry weight of green and brown leaves. The calculation a 0.45- m membrane filter (NY025045, Membrane Solu- formula was as follows: tions Limited).휇 The amount of each ion (Na+, Cl−, and Shoot mortality ratio (%) = brown leaves dry weight K+) in the leaf (ion accumulation) and outside of the (g) ÷ [green leaves dry weight (g) + brown leaves leaf (ion excretion) were measured with an ion analyzer dry weight (g)] × 100 (IA-300, DKK-TOA Corporation, Tokyo, Japan). Statistical analysis All measured data were calculated based on the dry To evaluate significant differences among all data, weight of the leaf (mg/g DW). The ion excretion ratio Student’s t-test and Tukey’s test were used, using the was calculated using the data of ion accumulation and add-in analysis software in Microsoft Excel (BellCurve ion excretion from the leaves. The calculation was per- for Excel, Social Survey Research Information Co, Ltd.). formed according to the following formula: Results and Discussion Ion excretion ratio (%) = ion excretion amount (mg/g DW of leaf tissue) ÷ [ion accumulation amount (mg/ Salinity of gravity water g DW of leaf tissue) + ion excretion amount (mg/g The salinity concentration in gravity water from the DW of leaf tissue)] × 100 pot drain holes are shown in Fig. 3. Gravity water salin- Measurement of shoot biomass and turf quality ity increased in all pots irrigated with NaCl solution Immediately after collecting the leaves to measure the and increased over time (except for September 22). On ion amount, all plant shoots (leaves and erect stems) in September 12 (fourth treatment), the salinities of the the pot were cut from the soil and dried in an oven at gravity water from pots irrigated with 7.5, 15, and 30 90°C for 24 h. The dried shoots were then divided into g/L NaCl solution were 12.6, 22.5, and 38.9 g/L, respec- Souichirou Sugiura: Salt Gland Characteristics and Activity of Zoysia matrella Merr. in Environments with Different Levels of Salinity 145

Fig. 3 Estimated NaCl concentration in gravity water from pots with four NaCl solution treated for 35 days. Data are the means of triplicate analyses. Vertical bars repre- sent ± SD of triplicates analyses.

Table 1 Shoot mortality ratio of Zoysia matrella with four con- centrations of treated NaCl solution. Treated NaCl Shoot dry weight (g/200cm2) Shoot solution mortality ratio concentration Green leaves Brown leaves (%) (g/L) Control 3.40 ± 1.25 a 0.82 ± 0.27 a 19.4 ± 7.6 a 7.5 2.37 ± 0.58 a 0.52 ± 0.10 a 18.0 ± 6.9 a 15 2.65 ± 0.07 a 0.65 ± 0.24 a 19.7 ± 6.0 a 30 2.67 ± 0.19 a 0.68 ± 0.14 a 20.3 ± 4.5 a Data are the means±SD of triplicates analyses. Values shar- ing the same letters are not significantly different (p = 0.05) using Tukey’s test.

Fig. 4 Ion accumulation and ion excretion of Zoysia matrella tively (Fig. 3). This was higher than the concentration leaves with four concentrations of treated NaCl solution, of the NaCl solutions used for treatment, suggesting (a) Na+, (b) Cl−, and (c) K+. Data are the means. Verti- that salt accumulation occurred in the pots irrigated cal bars represent ± SD of triplicates analyses. Values with NaCl solution. sharing the same letters are not significantly differ- Shoot dry weight and turf quality ent (p = 0.05) using Tukey’s test. Small letter indicates The shoot (leaves and erect stems) dry weight of Z. accumulation in leaves and large letter indicates excre- matrella and mortality ratio of green and brown leaves tion from the leaves in Tukey’s test results. with each NaCl concentration treatment are shown in Table 1. The dry weight of green leaves was 2.37-3.40 long time. Chen et al. reported that Z. matrella treated g DW/pot (200 cm2) and that of brown leaves was with tap water (control) and 21 g/L NaCl solution for 9 0.52-0.82 g DW/pot (200 cm2) for the four NaCl treat- months showed no significant difference in the percent ments. There was no significant difference in the dry green leaf canopy area2). Further, Sugiura et al. showed weight of green and brown leaves among the NaCl that the biomass (shoot and root) was nearly the same treatment concentrations (Table 1). The mortality ratios between control plants and Z. matrella treated with 7.5 were 18.0-20.3% in four NaCl treatments and there g/L NaCl solution for 175 days22). These reports sug- were no significant differences among the NaCl treat- gest that Z. matrella can survive and maintain good turf ments (Table 1). Compared to the control pot, the 30 quality in high-salinity water irrigation areas. g/L NaCl solution-treated pot showed no significant Ion accumulation and ion excretion of leaves and ion difference in both dry weight or mortality ratio. These excretion ratio results indicate a high salt-tolerance in Z. matrella as The accumulation of each ion (Na+, Cl−, and K+) was described previously9,12), and other studies showed that higher than that excreted at all four concentrations of Z. matrella can survive in a saline environment for a NaCl solutions (Fig. 4). Accumulated Na+ and Cl− and 146 芝草研究 第 48 巻 第 2 号 2020 年 3 月

Table 2 Ion excretion ratio of Zoysia matrella at four concen- trations of treated NaCl solution. Treated NaCl Ion excretion ratio (%) solution concentration Na+ Cl− K+ (g/L) Control 28.2 ± 4.7 a 16.4 ± 3.3 ab 1.6 ± 1.0 a 7.5 26.5 ± 5.9 a 18.7 ± 4.6 a 3.7 ± 2.3 a 15 22.1 ± 2.1 a 12.3 ± 3.0 ab 1.8 ± 1.4 a 30 22.5 ± 2.5 a 7.6 ± 2.0 b 1.2 ± 0.8 a Data are the means ± SD of triplicates analyses. Values sharing the same letters are not significantly different (p = 0.05) using Tukey’s test. Ion excretion ratio (%) = ion excretion amount (mg/g DW of leaf tissue) ÷ [ion accumulation amount (mg/g DW of leaf tissue) + ion excretion amount (mg/g DW of leaf tissue)] × 100. excreted Na+ of the leaves were increased according with increasing NaCl concentrations used for treatment [Fig. 4 (a), (b)]. However, for excreted Cl−, there was no significant difference among the NaCl treatments [Fig. 4 (b)]. For K+, excretion was considerably low (0.16, 0.31, 0.16, and 0.12 mg/g DW respectively) and there was no significant difference among the four NaCl treatments in both accumulation and excretion Fig. 5 Salt gland density (a) and salt gland size (b) in leaves [Fig. 4 (c)]. of Zoysia matrella with four concentrations of treated The ion excretion ratios of Na+, Cl−, and K+ showed NaCl solution. Data are the means. Vertical bars rep- no significant differences among the NaCl treatments resent ± SD of triplicates analyses. Values sharing the except for Cl− at 30 g/L of NaCl treatment (Table 2). same letters are not significantly different (p = 0.05) using Tukey’s test. Small letter indicates adaxial side For the ion excretion ratio for each ion (Na+, Cl−, and and large letter indicates abaxial side in Tukey’s test K+) among the four NaCl concentrations, Na+ showed results. Significant differences between the adaxial side the highest value, followed by Cl−, and K+ was the and abaxial side are indicated: * p < 0.05; ** p < 0.01, lowest. Especially K+ showed a considerably low ion no mark indicates no significant difference according excretion ratio. Following 30 g/L NaCl treatment, the to Student’s t-test. K+ excretion ratio was 19-fold lower than that of Na+. It is considered that plant leaves with salt glands can selectively excrete specific ions6). Gramineae, Rhodes It was reported that salt gland density does not change grass, and Aeluropus littoralis (Wild) Parl were shown based on the salinity factor but is fixed genetically15). to selectively excrete ions. Na+ excretion was higher For the Rhodes grass (Chloris gayana Kunth) showed than that of K+ in both plants1,7). Marcum et al. reported no difference in the salt gland density on the leaves that Z. matrella under salinity stress showed nearly no between the control and experimental plants irrigated K+ excretion11). Based on these reports and the pres- with 100 mM (5.85 g/L) NaCl solution19). In the pres- ent study, Z. matrella in a salt stress environment can ent study, there were no significant differences in the selectively excrete specific ions, particularly Na+ from leaf salt gland density and salt gland size among the salt glands while retaining K+ in the leaves. four different NaCl treatments, but Na+ excretion was Salt gland density and size on leaf surface increased with increasing NaCl treatment concentra- Overall, the adaxial side of the leaf showed a higher tions (Fig. 4, 5). These results indicate that the salinity salt gland density and larger size than on the abaxial of the soil did not affect the salt gland density or size side (Fig. 5). The NaCl concentration did not signifi- on the Zoysia leaf. Furthermore, Z. matrella showed cantly affect salt gland density or size. Previous studies increased ion excretion from salt glands on the leaf with reported that the number of salt glands is higher on the increasing soil salinity. adaxial side than on the abaxial side of Zoysia leaves18,25). Relationship between experimental conditions and Na+ The results of the present study agreed with those excretion ratio of Zoysia matrella of previous reports. Furthermore, the present study To evaluate the relationship between the experimen- discovered that the size of the salt glands is larger on tal conditions and Na+ excretion ratio of Z. matrella, the the adaxial side than that on the abaxial side. To our data from two previous studies and the present study knowledge, this is the first report on the salt gland size were compiled as shown in Table 3. Previous studies difference between on the adaxial and abaxial sides. of Na+ excretion and Na+ accumulation of Z. matrella Souichirou Sugiura: Salt Gland Characteristics and Activity of Zoysia matrella Merr. in Environments with Different Levels of Salinity 147

Table 3 Experimental conditions and Na+ excretion ratio of Zoysia matrella in two previous studies and the present study. Experimental conditions Leaf Na+ amount (mg/g DW) Na+ Treated NaCl Number of Frequency of Period of excretion Cultivation solution References NaCl solution NaCl solution NaCl solution Accumulation Excretion Total ratio conditions concentration treatment treatment treatment (%) (g/L) Every 4-10 The Sand 30 5 Times days 35 Days 25.2 7.3 32.5 22.5 present culture ＊1 study Sand 17.5-35 5 Times Yamamoto Daily 5 Days 3.9 8.5 12.4 68.5 culture ＊2 ＊2 et al.25) Hydroponic 12 ― ― Marcum culture 7 Days 7.6 16.8 22.4 77.4 ＊3 ＊3 ＊3 et al.11) ＊3 ＊1: NaCl solution was treated only when the pot soil surface was dry. ＊2: A total of five treatments was performed every 24 h for 300, 450, 600, 600, and 600 mmol/L NaCl (600 mmol/L ≒ 35 g/L NaCl). ＊3: The plants were grown in nutrient solutions containing 200 mmol/L NaCl (200 mmol/L ≒ 12 g/L NaCl). leaves were conducted in high-moisture environments and thus studies are needed to determine the relation- such as in hydroponic cultivation conditions or with ship between soil moisture and ion excretion. No stud- daily irrigation11,25). In this study, NaCl solution was ies have focused on the relationship between ion excre- used to treat the plant only when the soil surface was tion and the soil moisture environment. Such studies dry. Previous results for Z. matrella grown in 12 g/L are needed to meet the increasing worldwide demand NaCl for 7 days showed that the Na+ excretion ratio was for the limited water resources and high-salinity recy- 77.4%11). Daily NaCl treatment (35 g/L) of Z. matrella in cled water for turfgrass. sand culture showed that the Na+ excretion ratio from Acknowledgements the leaves was 68.5%25) (Table 3). In contrast, in the present study, Z. matrella in 30 g/L NaCl showed an This study was partially supported by a Grant-in-Aid excretion ratio of 22.5%, which was much lower than for turf research of the JSTS (Japanese Society of Turf- the previous studies. Additionally, salinity did not affect grass Science). the salt gland density or size on the leaves (Fig. 5). References These results suggest that the ion excretion character- istics of Z. matrella are highly affected by soil moisture 1) Barhoumi Z., Djebali W. , Smaoui A., Chaïbi W. and Abdelly C. rather than the salt gland density or size on the leaf (2007): Contribution of NaCl excretion to salt resistance of surface. Aeluropus littoralis (Wild) Parl., Journal of Plant Physiology It has been previously reported that ion excretion 164(7), 842-850 from salt glands is affected by the growth environ- 2) Chen J., Yan J., Qian Y., Jiang Y., Zhang T. , Guo H., Gou A. and Liu J. (2009): Growth responses and ion regulation of four ment of plants6). In the Australian saltgrass (Distichlis spicata Greene), the salt gland is more active during warm season turfgrasses to long-term salinity stress, Scientia Horticulturae 122(4), 620-625 the night than in the day4). Kallar grass (Leptochloa 3) Gorham J. (1987): Photosynthesis, transpiration and salt fluxes fusca L. Kunth) excretes more ions when the air tem- through leaves of Leptochloa fusca L. Kunth, Plant, Cell and 3) perature is high . In Spartina anglica with high soil Environment 10(2), 191-196 20) redox potential, ion excretion is increased . Generally, 4) Hansen D. J., Dayanandan P. , Kaufman P. B. and Brotherson J. plants cannot take up water easily from highly saline D. (1976): Ecological adaptations of salt marsh grass, Distich- soils because of osmotic pressure17). Moreover, ion lis spicata (Gramineae), and environmental factors affecting excretion from the salt gland requires water, as plants its growth and distribution, American Journal of Botany 63(5), excrete ions with water from the salt glands26). Thus, Z. 635-650 matrella may accumulate NaCl ions in the leaf to reduce 5) Hosoya N. and Saito M. (2016): The comparison of replica- the excretion of water from the plant body under low methods to observe stomata, Otsuma Journal of Social Infor- soil moisture conditions. Additionally, Z. matrella may mation Studies 25, 61-70 increase ion excretion from the salt glands when the 6) Kobayashi H. (2008): Ion secretion via salt glands in , soil moisture is high. Therefore, this plant can survive Japanese Journal of Plant Science 2(1), 1-8 in heterogeneous salinity and moisture environments 7) Kobayashi H., Masaoka Y., Takahashi Y., Ide Y. and Sato S. such as coastal habitats possibly by adjusting saline (2007): Ability of salt glands in Rhodes grass (Chloris gayana + + excretion and accumulation. Kunth) to secrete Na and K , Soil Science and Plant Nutri- tion 53(6), 764-771 Soil moisture was not evaluated in the present study, 148 芝草研究 第 48 巻 第 2 号 2020 年 3 月

8) Maeda Y. (2012): Plant salt tolerance and removal of salt in 19) Oi T. , Hirunagi K., Taniguchi M. and Miyake H. (2013): saline soil by plants, Bulletin of the Society of Sea Water Sci- Salt excretion from the salt glands in Rhodes grass (Chloris ence, Japan 66(2), 92-98 gayana Kunth) as evidenced by low-vacuum scanning electron 9) Marcum K. B. (2006): Use of saline and non-potable water in microscopy, Flora 208(1), 52-57 the turfgrass industry: Constraints and developments, Agri- 20) Rozema J., Buys E., Otte M. L., Broekman R. A. and Ernst cultural Water Management 80, 132-146 W. H. O. (1991): Ion content and ion excretion of Spartina 10) Marcum K. B., Anderson S. J. and Engelke M. C. (1998): Salt anglica in relation to salinity and redox potential of salt marsh gland ion secretion: a salinity tolerance mechanism among five soil, Zeitschrift Für Pflanzenernährung Und Bodenkunde Zoysiagrass species, Crop Science 38(3), 806-810 154(4), 307-313 11) Marcum K. B. and Murdoch C. L. (1990): Salt glands in the 21) Shirata K., Takagishi H. and Ichihashi T. (1989): Mechanism , Annals of Botany 66(1), 1-7 of salt tolerance of Gramineae part 1: Salt tolerance and avoid- 12) Marcum K. B. and Murdoch C. L. (1994): Salinity tolerance ance function of wild turf Sporobolus virginicus (L.) Kunth, mechanisms of six C4 turfgrasses, Journal of the American Soil Science and Plant Nutrition 60(3), 220-225 Society of Horticultural Sciences 119(4), 779-784 22) Sugiura S., Tanaka S., Mizuniwa C. and Takahashi S. (2017): 13) Marcum K. B. and Pessarakli M. (2006): Salinity tolerance and Mitigation of salt accumulation in soil by Zoysia matrella salt gland excretion efficiency of bermudagrass turf , Merr., Journal of Japanese Society of Turfgrass Science 45(2), Crop Science 46, 2571-2574 103-107 14) Marcum K. B., Wess G., Ray D. T. and Engelke M. C. (2003): 23) Sugiura S., Tanaka S., Mizuniwa C. and Takahashi S. (2017): Zoysiagrass, salt glands, and salt tolerance: Observing the Salinity transport in leaves of Zoysia matrella Merr. in saline density of salt glands may make selecting for salt-tolerant environment, Journal of Japanese Society of Turfgrass Science grasses a lot easier, USGA Green Section Record 41(6), 20-21 46(extra issue vol.1), 38-39 15) Marcum K. B., Wess G., Ray D. T. and Engelke M. C. (2003): 24) Wang L., Li W. , Yang H., Wu W. , Ma L., Huang T. and Wang X. Zoysiagrasses, salt glands, and salt tolerance, USGA Turfgrass (2016): Physiological and biochemical responses of a medici- and Environmental Research Online 2(14), 1-6 nal halophyte Limonium bicolor (Bag.) Kuntze to salt-stress, 16) Misawa A. (1981): Studies on atmospheric purification as a Pakistan Journal of Botany 48(4), 1371-1377 function of buffer planing belts on roadsides―Experiments 25) Yamamoto A., Hashiguchi M., Akune R., Masumoto T. , on trapping particulates by foliage, Journal of the Japanese Muguerza M., Saeki Y. and Akashi R. (2016): The relationship Institute of Landscape Architects 44(4), 191-202 between salt gland density and sodium accumulation/secretion 17) Munns R. (2002): Comparative physiology of salt and water in a wide selection from three Zoysia species, Australian Jour- stress, Plant, Cell and Environment 25, 239-250 nal of Botany 64(4), 277-284 18) Murata T. (2010): Production of salt tolerant line of Japanese 26) Yuan F. , Leng B. and Wang B. (2016): Progress in studying lawn grass using unused germplasm, Report of the Grant-in- salt secretion from the salt glands in recretohalophytes: How Aid for Scientific Research C (no. 19580007) by Ministry of do plants secrete salt? Frontiers in Plant Science 7, 1-12 Education, Science (Received 10 January 2019, Accepted 12 July 2019)