J. Agr. Sci. Tech. (2014) Vol. 16: 137-149

Growth, Leaf Gas Exchange, and Chlorophyll Fluorescence Responses of Two Cultivars of Salix integra Thunb. to Waterlogging Stress

H. F. Zhao 1 , Y. Zhao 1, C. Zhang 1, X. Tao 1, and X. N. Xu 1*

ABSTRACT

Salix integra Thunb. is a shrub distributed in China along the Huai River riparian zone, and plays an important role in water and soil conservation. S. integra shrub land is easily submerged during July to October due to the flooding of Huai River. In order to characterize the physiological mechanisms of waterlogging tolerance of S. integra and to help rationally select waterlogging-tolerant species to alleviate the flood damage to agricultural production, we studied the effects of flooding on the growth, leaf gas exchange, and chlorophyll fluorescence of S. integra cuttings during a growth season (from August to October 2011). The biomass production and photosynthesis of S. integra cv. qingpi were promoted under moderate waterlogging stress, whereas its growth, chlorophyll content, net photosynthetic rate, and stomatal conductance were all significantly lower than those of the control group. A significant increase in non- photochemical quenching (NPQ) and a reduction in PSII maximal quantum photochemistry efficiency (F v/F m) were observed in flooded seedlings of S. integra cv. hongpi . In the case of S. integra cv. qingpi , however, there were no significant differences in NPQ and Fv/F m between the treatment and the controls. Our results demonstrated that S. integra cv. hongpi exhibited slight damage to its photosynthetic apparatus under flooding. In contrast, a moderate flooding stress promoted the leaf and root production of S. integra cv. qingpi , indicating that S. integra cv. qingpi can tolerate prolonged soil flooding better than S. integra cv. hongpi. Thus, S. integra cv. qingpi is more suitable for afforestation in the riparian zone.

Keywords: Biomass, Flooding, Photosynthetic rate, Shrub, Tolerate.

INTRODUCTION also shown that waterlogging stress does not significantly influence the growth of Japanese Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 Waterlogging is one of the primary forms of cedar and Taxodium distichum (L.) Rich. and abiotic stress confronting many plants. The promotes biomass accumulation in Salix trees problem develops when the water content in and Fraxinus velutina (Hou , 2003; Tang et the soil surpasses the field moisture capacity, al ., 1998). The photosynthetic rate, stomatal inducing waterlogging stress on plants conductance, and photochemical quantum growing in the soil. Waterlogging affects trees efficiency of plants under flooding stress growing in coastal and riverside areas that are typically decrease over short term (in frequently flooded. Waterlogging stress waterlogging-tolerant plants) or in the long generally inhibits plant root and shoot growth, term (in waterlogging-susceptible plants) leading to reduced biomass production and (Carvalho and Amancio, 2002; Schwanz et al ., premature falling of fruit (Vartapetian and 1996). Waterlogging also induces degradation Jackson, 1997). However, several studies have of chlorophylls, an increase in membrane ______1 Department of Forestry, College of Forestry and Landscape Architecture, Anhui Agricultural University, No. 130, West Changjiang Road, Hefei 230036, Anhui, People’s Republic of China. * corresponding author; e-mail: [email protected]

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permeability, and an insufficient oxygen cultivars, S. integra cv. hongpi (SIh) and cv. supply for the root system. Waterlogging- qingpi (SIq), were selected for the tolerant plants neutralize the stress by forming experiment. Cuttings were collected from 1- hypertrophied lenticels and aerenchymas and year-old shoots of two cultivars of S. integra developing adventitious roots to adapt to the from Huanggang, Funan County Anhui waterlogging (Kozlowski, 1997). Province (32°24'19"N and 115°16'30"E). The Salix integra Thunb. is a multipurpose 1-year-old shoots were cut to lengths of 15 shrub that is predominantly distributed in the cm. The diameters at the centers of the riparian zone of the Huai River basin in China, cuttings ranged from 8.1 to 10.0 mm. where it plays key roles in soil and water Cuttings were planted in the experimental conservation. The S. integra shrub frequently field of Anhui Agricultural University on 2 nd suffers widespread waterlogging stress during of March 2011. In the middle of May 2011, the season from July to October as a result of uniformly growing seedlings were selected the often-overflowing Huai River. There have and transplanted to pots (23 cm in diameter been studies on the growth, physiological, and 28 cm in height), with three seedlings per ecological, and photosynthetic properties pot. The pots were filled with a 3:1 nursery under drought and waterlogging stress soil-to-merchandised peat substrate mixture. conditions for Populus deltoides and S. To guarantee a uniform growing matsudana (Tang et al. , 1998), Populus alba environment, all of the seedlings were var. pyramidalis Bunge and Populus nigra L. exposed to natural sunlight and rainfall, with var. thevestina (Li and Kakubari, 2001), and S. well-watered conditions to promote growth. gracilistyla and S. subfragilis (Nakai et al ., To determine the response of S. integra 2010, 2011). However, the effects of cuttings to waterlogging stress, on 3rd of waterlogging stress on the growth and August, 2011, a total of 72 uniformly sized photosynthetic eco-physiology of S. integra pots of each cultivar were selected and have not been reported. randomly distributed into three groups, each In the present study, we investigated the group receiving one treatment and each pot eco-physiological responses of S. integra to representing one replicate. The average base the simulated waterlogging stress for a 75-day diameter of cuttings and average fresh weight period from August to October. The objectives were not significantly different among of this study were to (1) characterize the treatments at the outset. impacts of waterlogging on the morphology, The pots were placed into larger growth, leaf gas exchange, and chlorophyll containers, the experimental design involved fluorescence response of the two types of Salix two waterlogging treatments (moderate and Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 trees, and (2) help rationally select severe) and a control group with no waterlogging-tolerant species to alleviate the flooding/no drought. Treatment duration was waterlogging damage to plants while 75 days for waterlogging treatments from 3rd investigating the physiological mechanisms of of August to 17 th of October, 2011 to waterlogging tolerance of S. integra. correspond to the typical duration of a flooding season in Funan. In the moderate MATERIALS AND METHODS waterlogging treatment, cuttings were watered to keep water-level 10 cm below the pot soil surface to simulate a shallow Materials groundwater level. In the severe waterlogging treatment, water level was kept at 4-5 cm Salix integra Thunb. belongs to the above the soil surface throughout the duration Salicaceae family and Salix genus and is a of the experiment. In the control, cuttings perennial deciduous shrub that is were watered with about 1500 ml daily and predominantly distributed in the riparian zone left to drain freely. of the Huai River basin in China. Two

138 Salix integra Cultivars and Waterlogging Stress ______

Measurements Leaves that were in the same position and of the same maturity level as those measured The occurrence of leaf color changes, the using the Li-6400 system were sampled, and leaf abscission, and the formation of 0.1 g of the leaves was extracted with 80% adventitious roots and hypertrophied lenticels acetone. The extractions were analyzed using were regularly monitored and recorded. The UV- visible spectrophotometry to determine cutting height was measured with a measuring the concentrations of chlorophyll a (Chla), tape with an accuracy of 0.1 cm. The base chlorophyll b (Chlb), and total chlorophyll diameter at 5 cm above the ground was (Chl (a+b)), which were calculated using the measured twice using a Vernier caliper with an Aron revised method (Li, 2000). The chlorophyll content per gram of dry leaf (mg g - accuracy of 0.01 cm, and the average value 1 was recorded. ) was determined based on the chlorophyll The biomass measurements were performed concentration in the extract and the water twice: once before the waterlogging and once content of the leaf. after. The cuttings from 6 pots from each treatment group were analyzed prior to the Statistical Analysis waterlogging, and the remaining 18 pots in each treatment group were analyzed after the All statistical analyses were performed whole waterlogging experiment. At the end with Data Processing System for Windows. of the experiment, the cuttings were carefully Repeated measurement analysis of variance removed from the pots and divided into above- (ANOVA) was used, and differences were ground and below-ground biomass. The considered significant at P= 0.05. weights of the roots, shoots, and leaves were measured separately, then, they were dried in an oven at 60°C for 48 hours. Finally, the RESULTS biomass and its distribution were determined (Farquhar and Sharkey, 1982). Morphological Features On the sunny day between 9:00 and 13:00, under a natural light level of 1000-1500 µmol m-2 s-1, the net photosynthetic rate and stomatal Throughout the 75-day waterlogging period, conductance of the cuttings in the different the survival rates of the two cultivars i.e. SIh treatment groups were measured in a 20×30 and SIq, were 100%; however, the mm transparent leaf chamber with a Li-6400 morphological characteristics of the cuttings exhibited remarkable differences. Under the Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 portable photosynthesis system (LI-COR Inc., Lincoln, NE, USA). The leaves measured moderate waterlogging treatment, the were fully expanded and were the fourth to morphology of the leaves was almost identical seventh leaves from the top of the plant. The to that of the control. Late in the severe air temperature and humidity of the leaf waterlogging treatment period (55 days), about chamber were maintained at 30°C and 40- 11% (6-7 leaves) of the total number of leaves 60%, respectively, during the measurements. per cutting on the lower portion turned yellow and 9% (5 leaves) fell off for SIq. In the case Chlorophyll fluorescence parameters (F v/F m) and non-photochemical quenching (NPQ) of SIh, 13% (5-9 leaves) of leaves turned were measured in a standard fluorescence leaf yellow on day 40, under the moderate chamber with a Li-6400 portable waterlogging, and 10% (5-7 leaves) of the total photosynthesis system. Prior to the number of leaves per cutting developed measurement in the early morning, a clip was necrosis spots on day 33 under severe placed on each leaf for 30-40 min for dark waterlogging condition, when 17% of the total adaptation (Yi et al., 2006). leaves fell off and the tree growth slowed considerably.

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Under the waterlogging treatment, both of adventitious roots of SIq (2.39 g plant -1) was cultivars behaved similarly with regard to their as high as 227% of the SIh (1.05 g plant -1). root growth compared with the controls. After 15 days of severe waterlogging, white fattened Growth and Biomass lenticels and red adventitious roots were developed at the base of the submerged shoot for SIh, whereas the white attachment In the first 20 days of the waterlogging appeared at the base of the submerged shoot treatment (under both the moderate and for SIq after 20 days, and enlarged lenticels severe waterlogging), the base diameter and and a few adventitious roots appeared after 24 shoot height of the cuttings for SIh and SIq days. The quantity of adventitious roots for were similar and not significantly different SIq under severe waterlogging condition (P> 0.05) from those in the controls. increased with experimental time and was However, after 20 days of severe significantly greater than that for SIh. At the waterlogging, the growth of base diameter end of the waterlogging treatment, the biomass and the shoot height of SIh were remarkably

0.9 (A) 0.9 SIh (B) SIq

* * 0.8 0.8 * * 0.7 * 0.7

0.6diameterBase (cm) Base diameter diameter (cm) Base 0.6

0.5 0.5 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d) 200 200 SIh (C) SIq (D)

180 180 Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 * * * 160 * 160 *

140 140 Height (cm) Height Height (cm) Height

◊ Control 120 120 ■ moderate waterlogging ▲ severe waterlogging 100 100 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d) Figure 1 . Variations in the base diameters and shoot heights of Salix integra cv. hongpi and cv. qingpi under the waterlogging stress (mean ± sd). Asterisks(*) indicate significantly different (P<0.05).

140 Salix integra Cultivars and Waterlogging Stress ______

inhibited and became more severely inhibited as the waterlogging continued (Figures 1-a and -c). At the end of the waterlogging experiment, the base diameters of SIh under both waterlogging conditions decreased by, respectively, 6 and 9%, and its shoot heights decreased by 7 and 10%, respectively, compared with those in the control. During the entire experimental period, the base diameter and shoot height of SIq were not significantly different from those in the controls ( P> 0.05). Under the moderate waterlogging stress, the biomass production of SIh was not significantly different from that of the controls (Table 1). The severe waterlogging stress slowed the biomass accumulation of SIh, which was predominantly manifested by the decrease in leaf biomass. Under the moderate waterlogging, SIq significantly increased in biomass compared with the controls, while in severe waterlogging, no significant difference in biomass production was found compared to the control. The root biomass of SIq under both the moderate and severe waterlogging treatments significantly increased by, respectively, 35 and 23% greater than those of the controls. During the whole moderate waterlogging process, no adventitious root was developed at the base of the submerged shoot for SIq. The biomass of non-adventitous root for SIq under control and severe waterlogging treatment were 6.36 g plant -1 and 5.45 g plant -1, Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 respectively, and there was no significant difference between them, indicating that the root biomass increase was due to adventitious root formation under severe waterlogging stress. Biomass productions increased in both cultivars despite the exposure to waterlogging stress in the end of the experiment.

Physiological Responses

After 19 days of waterlogging stress, the net photosynthetic rate decreased for SIh, compared with that for the control, by 25 and 48% under the moderate and severe

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waterlogging stress, respectively (Figure 2a). severe waterlogging (Figure 2-d). At the end At the end of the experiment, the net of the waterlogging treatment, the stomatal photosynthetic rate of SIh decreased by 34 and conductance of SIh under moderate and severe 46% under the moderate and severe waterlogging decreased by 24 and 51%, waterlogging, respectively. There was no respectively, compared with that of the significant difference in the net photosynthetic control, whereas SIq showed no significant rate of SIq among the three treatment groups difference from the control. (P> 0.05) (Figure 2-b). The Chla and Chl(a+b) contents of SIh Compared with the control, after 19 days of were significantly different among the the waterlogging stress, the stomatal treatments, whereas the Chla, Chlb, and conductance of SIh under the moderate and Chl(a+b) contents of SIq exhibited no severe waterlogging deceased by 35 and 56%, significant difference among the respectively (Figure 2-c). In contrast, the treatments ( P> 0.05; Figures 3-a, -b , -d, - stomatal conductance of SIq was 24% greater e, and -f). The chlorophyll contents of SIh than that of the control in the moderate began to decrease after 19 days and waterlogging, but was not significantly continued to decrease thereafter in different ( P> 0.05) than the control under

18 18 SIh (A) SIq (B) 16 16

14 14 ) -1 12 12 •s * ) -2 * -1

* s 10 • -2 10 m * • 8 mol

µ 8 ( (µmol•m N N N 6 P P 6 4 4 2 0 2 0 4 12 19 34 43 55 75 0 Time of waterlogging (d) 0 4 12 19 34 43 55 75 Time of waterlogging (d) 0.30 0.30 SIh SIq

Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 (C) (D) 0.25 * 0.25 * ) )

-1 0.20 -1 s

0.20 s • •

-2 * -2 m m • * 0.15 • 0.15 * * * 0.10 (mmol ◊ Control (mmol s 0.10 s G ■ Moderate waterlogging G 0.05 ▲ Severe waterlogging 0.05 0.00 0 4 12 19 34 43 55 75 0.00 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d) Figure 2 . The effect of waterlogging stress on the photosynthetic rate and stomatal conductance of Salix integra cv. hongpi and cv. qingpi (mean ± sd). Asterisks(*) indicate significantly different (P<0.05).

142 Salix integra Cultivars and Waterlogging Stress ______

3 3 SIh (A) SIq (B)

2.5 2.5 * ** 2 ) 2 ) * -1 -1 * 1.5 1.5 Chla (mg•g Chla (mg•g 1 1

0.5 0.5

0 0 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d)

1.1 1.1 SIh (C) SIq (D) * 1 1 * * 0.9 * 0.9

0.8 )

-1 0.8

0.7 0.7 0.6 Chlb (mg•g-1) 0.6 Chlb (mg•g

0.5 0.5

0.4 0.4

0.3 0.3 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d)

4 4 SIh (E) SIq (F) 3.5 3.5 Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 * 3 3 * * ) -1 ) ** 2.5 -1 2.5 2 2 1.5

1.5 (mg•g Chla+b Chla+b (mg•g 1 1 ◊ Control 0.5 ■ Moderate waterlogging 0.5 ▲ Severe waterlogging 0 0 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d)

Figure 3 . The effect of waterlogging stress on the chlorophyll contents of Salix integra cv. hongpi and cv. qingpi (mean ± sd). Asterisks(*) indicate significantly different (P<0.05).

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waterlogged trees compared to controls. in the chlorophyll content of SIq was The average contents of Chla, Chlb, and relatively small throughout the study period; Chl(a+b) for SIh under the moderate the chlorophyll content decreased only waterlogging were 1.08 mg g -1, 0.59 mg g -1, slightly after 43 days of the waterlogging and 1.67 mg g -1, respectively, at the end of stress (Figures 3-b, -d, and -f). the experiment, and were 0.91 mg g -1, 0.52 Under the two waterlogging stresses, the -1 -1 mg g , and 1.43 mg g , respectively, after maximum photochemical efficiency (F v/F m) the severe waterlogging. Compared with the of SIh began to decrease after 34 days, with control, the decrease in the Chla content of the average values of, respectively, 0.739 SIh was greater than that of the Chlb. The and 0.697 after 75 days, while the maximum Chla and Chlb content of SIh under efficiency of the control was 0.811. The moderate waterlogging decreased by 32% Fv/F m ratio of SIq fluctuated in the range of and 24%, respectively, and the 0.8-0.85 during the waterlogging period, corresponding decrease was 43% and 33% which was statistically similar to the values under severe waterlogging. The fluctuation in the control (Figure 4a, b). The NPQ of

0.9 0.9 SIh (A) SIq (B)

* 0.85 * 0.85 * * * * 0.8 0.8 Fv/Fm Fv/Fm 0.75 0.75

0.7 0.7

0.65 0.65 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d)

0.9 0.9 (C) SIq (D) SI h * * Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 0.8 * 0.8 * * 0.7 0.7

0.6 0.6 NPQ NPQ 0.5 0.5

0.4 0.4 ◊ Control ■ Moderate waterlogging 0.3 0.3 ▲ Severe waterlogging

0.2 0.2 0 4 12 19 34 43 55 75 0 4 12 19 34 43 55 75 Time of waterlogging (d) Time of waterlogging (d)

Figure 4 . Variations in the maximum photochemical efficiency and non-photochemical quenching (NPQ) coefficient of Salix integra cv. hongpi and cv. qingpi under waterlogging stress (mean ± sd). Asterisks(*) indicate significantly different (P<0.05).

144 Salix integra Cultivars and Waterlogging Stress ______

SIh began to increase after 34 days and hongpi , whereas the base diameter decreased continued to increase thereafter in slightly. A previous study showed that waterlogged compared to the control. In the waterlogging stress inhibited the growth of end of the experiment, the NPQ increased leaves and induced the abscission of leaves remarkably for SIh compared with that for by hindering differentiation of leaf the control, by 11 and 17%, respectively, primordia and internode growth of plant under the moderate and severe waterlogging (Cao et al. , 1993). The slight decrease in the stress. There was no significant difference in base diameter may result from the formation NPQ of SIq among the three treatment of hypertrophied lenticels and aerenchymas groups (P> 0.05) (Figure 4-c and -d). at the base of the stem. The biomass of S. integra cv. qingpi was significantly different DISCUSSION between moderate waterlogging and the control. However, the abovementioned growth parameters were not significantly Effect of Waterlogging on the different between the control and the severe Morphology and Growth of Salix integra waterlogging treatment. This finding is consistent with the results obtained in Throughout the entire waterlogging studies on Taxodium distichum (Hou, 2003), experiment, the cuttings of both cultivars of indicating that moderate waterlogging could Salix integra produced adventitious roots promote the growth of S. integra cv. qingpi . and hypertrophied lenticels, which are characteristic responses of tolerant wood Effect of Waterlogging on species to waterlogging stress (Close and Photosynthesis of Salix integra Davidson, 2003; Jing et al ., 2001; Yamamoto et al ., 1995). In a continuous waterlogging environment, the occurrence of The net photosynthetic rate and stomatal adventitious roots is advantageous to the conductance of S. integra cv. hongpi under supply and regulation of water, nutrients, severe waterlogging decreased significantly and growth regulators in plants (Emam and in 19 days and, subsequently, decreased at a Bijanzadeh, 2012; Islam and Macdonald, slower rate. The net photosynthetic rate and 2004; Tsukahara and Kozlowski, 1995). The stomatal conductance of S. integra cv. lenticel is the critical pathway of air qingpi under severe waterlogging recovered exchange between the stem and root systems to the levels close to those of the control by the end of the experiment, which was similar

Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 of a plant and the atmosphere (Kozlowski and Pallardy, 2002). Enlarged lenticels and to the observations in studies of aerenchymas increase gaseous diffusion, the Liriodendron chinense , Cleistocalyx total leaf area exposed to the oxygen in the operculatus (Jing et al ., 2000), and Spartina air, and the amount of oxygen transported to patens (Pezeshki et al ., 1993) . The decrease the roots (Kozlowsk, 1997; Yamamoto et in the net photosynthetic rate in the early al ., 1995). Salix integra cv. qingpi stage of waterlogging was related to the developed hypertrophied lenticels and closure of stomata and decreased stomatal adventitious roots earlier than S. integra cv. conductance. The lowered CO 2 intake hongpi did and with more and longer capability of the leaves leads to a smaller adventitious roots. intercellular CO 2 concentration, and the The waterlogging stress had an obvious substrate deficiency for photosynthetic impact on the growth of base diameter, enzymes directly leads to the lowering of the shoot height, and biomass accumulation of net photosynthetic rate (Farquhar and both cultivars. Severe waterlogging stress Sharkey, 1982; Malik et al ., 2001; Pezeshki significantly reduced the shoot height and et al ., 1996; Zoubeir et al , 2012). The biomass accumulation for S. integra cv. decrease in stomatal conductance may be

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derived from the decrease in hydraulic harvesting chlorophyll a/b protein complex conductivity between soil and plant or from because in photosynthesis, Chla is the shortage in the oxygen supply to the root predominantly bound to the photosynthetic system (Mohd et al ., 2010; Vartapetian and reaction center, whereas Chlb is bound to Jackson, 1997). The emergence of the light-harvesting chlorophyll a/b protein adventitious roots and the formation of complex (Larcher, 2003). enlarged lenticels at the shoot closest to the Changes in the chlorophyll fluorescence water level in the middle and late stages of parameters reflected the degree of damage to the waterlogging period alleviated the low photosystem II. The change in the Fv/F m oxygen status in the root system, thereby ratio revealed the influences on the net leading to the increase in the net photosynthetic rate. A sustainable and stable photosynthetic rate and stomatal Fv/F m ratio indicates an undamaged conductance. The increase in the net photosystem II (Ball et al ., 1994; Jones et photosynthetic rate and stomatal al ., 2006; Lavinsky et al ., 2007). NPQ conductance of S. integra cv. qingpi under reflects the degree of heat dissipation in the the moderate waterlogging stress was similar photochemical reactions, i.e. the quantity of to the reports on Taxodium distichum (Yang, the energy that was not used in the 2007) and Sapium sebiferum (Cao et al ., photochemical reactions (Christiane and 2010), which indicates that S. integra cv. Shabala, 2003; Maxwell and Johnson, qingpi is more tolerant to waterlogging. 2007). The Fv/F m ratio and NPQ of S. Under waterlogging stress, leaves become integra cv. hongpi under severe less green and show signs of abscission, waterlogging continuously decreased and which is related to membrane damage, increased, respectively, in a pattern similar electrolyte leakage, and chlorophyll to that of the net photosynthetic rate, which concentrations decrease (Christiane and is in accordance with previous findings Shabala, 2003; Islam and Macdonald, 2004; (Close and Davidson, 2003; Yi et al. , 2006) Kozlowski, 1997). However, several studies and also revealed the change in the have shown that under waterlogging stress, photochemical properties of S. integra cv. sensitive plants exhibit no change in hongpi under waterlogging stress. The Fv/F m chlorophyll content (Pezeshki et al ., 1996). ratio and NPQ of S. integra cv. qingpi under Early in the waterlogging period, the both moderate and severe waterlogging chlorophyll contents of the two cultivars of stresses were not significantly different from S. integra were similar to those of the the control, which is in accordance with the control. After 12 days of waterlogging, the previous studies (James et al. , 2002; Mielke Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 contents of Chla, Chlb, and Chl (a+b) in S. et al. , 2003; Roohi et al ., 2013; Wu and Bao, integra cv. hongpi began to decrease, and 2011). This observation indicates that S. the leaves gradually became less green. In integra cv. qingpi was highly capable of contrast, the chlorophyll contents in S. adapting to waterlogging stress, with stable integra cv. qingpi changed little and were photosystem II activity and a fluctuating net only slightly lower in the later stages of the photosynthetic rate that likely resulted from waterlogging, with only a limited number of changes in stomatal conductance. leaves on the lower part of the cuttings In general, the potential damage to a plant turning yellow and falling off. Moreover, the due to waterlogging stress increases with the decrease in the Chla content in S. integra cv. duration of the stress. Few plants could only hongpi was greater than that of the Chlb, withstand continuous waterlogging for 1-3 which is similar to a report on Hibiscus months. The fact that both cultivars of S. esculentus (Ashraf and Arfan, 2005). This integra survived 100% after 75 days of result indicated that the degradation of the waterlogging indicates that S. integra has photosynthetic reaction center in the leaves high waterlogging tolerance. The growth was higher than the degradation of the light- and photosynthesis mechanisms of S.

146 Salix integra Cultivars and Waterlogging Stress ______

integra cv. hongpi were retarded by the Stress on the Growth and Photosynthesis of waterlogging, whereas moderate Sapium sebiferum . Scientia Silvae Sinicae, waterlogging promoted biomass production 46(10): 57-61. for S. integra cv. qingpi , indicating that it 4. Cao, F. L. and Robert, E. F. 1993. Effect of was more tolerant to waterlogging than S. Artificial Flooding on Physiological Characteristics of Populus Deltoides Clones. integra cv. hongpi and thus more suitable J. Nanjing Forestry Uni., 17(2): 29-44. for the riparian and fluctuating groundwater 5. Carvalho, L. C. and Amancio, S. 2002. level zones. Presently, laboratory Antioxidant Defence System in Plantlets experiments performed predominantly on Transferred From in Vitro to Ex Vitro seedlings provide important insights into the Effects of Increasing Light Intensity and mechanisms of flooding tolerance. However, CO 2 Concentration. Plant Sci. , 162: 33-40. it is difficult to apply these results to adult 6. Christiane, F. S. and Shabala, S. 2003. trees or in situ conditions. To achieve a Screening Methods for Waterlogging better understanding of the flooding Tolerance in Lunceme: Comparative tolerance of this tree species, the findings Analysis of Waterlogging Effects on Chlorophyll Fluorescence, Photosynthesis, from the laboratory experiments must be Biomass and Chlorophyll Content. Funct.l compared and validated with field Plant Biol., 30: 335-343. experiments. The photo-physiological 7. Close, D. C. and Davidson, N. J. 2003. recovery mechanism of S. integra after Long-term Waterlogging: Nutrient, Gas waterlogging also remains to be Exchange, Photochemical, and Pigment investigated, especially with S. integra cv. Characteristics of Eucalyptus nitens hongpi . Saplings. Russ. J. Plant Physiol. , 50: 843- 847. 8. Emam,Y. and Bijanzadeh, E. 2012. Water ACKNOWLEDGEMENTS Uptake and Hydraulic Conductivity of Seminal and Adventitious Roots of Five Wheat Cultivars at Early Growth Stage. J. This study was supported by the National Agr. Sci. Tech. , 14: 1605-1616. Key Support Program of Science and 9. Farquhar, G. and Sharkey, T. D. 1982. Technology for the Eleventh-Five-Year Plan Stomatal Conductance and Photosynthesis. of PR China (No. 2009BADA6B05). We are Annu. Rev. Plant Physiol. Mol. Biol. , grateful to Zhang M.X. and Zhu L.L. for 33: 317-345. skillful technical assistance in the 10. Hou, E. Y. 2003. Effects of Water Stress on laboratory. Ying W.B., Wang L. and Yang J. the One-Year Seedling Growth and assisted in data collection. We would like to Physiology Properties of Pteroceltis Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 thank three anonymous reviewers for their Tatarinowiieroceltis Tatarinowii, Taxodium constructive comments. Distichum, and Fraxinus Velutina. J. Nanjing Forestry Uni., 15(1): 27-42. 11. Islam, M.A. and Macdonald, S. E. 2004. REFERENCES Ecophysiological Adaptations of Black Spruce ( Picea mariana ) and Tamarack (Larix laricina ) Seedlings to Flooding. 1. Ashraf, M. and Arfan, M. 2005. Gas Trees , 18: 35-42. Exchange Characteristics and Water 12. James, R. A., Rivelli, A. R., Munns, R. and Relations in Two Cultivars of Hibiscus Von Caemmerer, S. 2002. Factors Affecting esculentus under Waterlogging. Biol. CO 2 Assimilation, Leaf Injury, and Growth Plantarum, 49: 459- 462. in Salt-stressed Durum Wheat. Funct. Plant 2. Ball, M.C., Butterworth, J.A., Roden, J.S., Biol. , 29: 1393-1403. Christian, R. and Egerton, J. G. 1994. 13. Jing, Y. X., Cheng, Z. P., Cheng, H. Y. and Applications of Chlorophyll Fluorescence to Mo, X. M. 2000. The Relationship between Forest Ecology. Plant Physiol., 22: 311-319. Photosynthetic Character and Adventitious 3. Cao, F. L., Cai, J. F., Wang, G. B. and Roots in Flooded Cleistocalyx Operculatus Zhang, W. X. 2010. Effects of Waterlogging

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رﺷﺪ، ﺗﺒﺎدل ﮔﺎزي ﺑﺮگ، و ﻓﻠﻮﺋﻮرﺳﻨﺲ ﻛﻠﺮوﻓﻴﻞ دو رﻗﻢ ﺑﻴﺪ .Salix integra Thunb در ﭘﺎﺳﺦ ﺑﻪ ﺗﻨﺶ ﻣﺎﻧﺪاﺑﻲ

ح. ف. ژاوو، ي. ژاوو، س. ژاﻧﮓ، ژ. ﺗﺎوو، ژ. ن. ژوو

ﭼﻜﻴﺪه

ﺑﻴﺪ Salix integra درﺧﺘﭽﻪ اي در ﭼﻴﻦ اﺳﺖ ﻛﻪ در ﻛﻨﺎره ﻫﺎي رودﺧﺎﻧﻪ ﻫﻴﻮآي ﭘﺨﺶ اﺳﺖ و ﻧﻘﺶ ﻣﻬﻤﻲ در ﺣﻔﺎﻇﺖ ﺧﺎك وآ ب دارد. زﻣﻴﻦ ﻫﺎي زﻳﺮ اﻳﻦ درﺧﺘﭽﻪ در ﻃﻲ ﻣﺎه ﻫﺎي ژوﺋﻴﻪ ﺗﺎ اﻛﺘﺒﺮ ﺑﻪ آﺳﺎﻧﻲ زﻳﺮ ﺳﻴﻼب رودﺧﺎﻧﻪ ﻫﻴﻮآي ﻣﻲ رود . ﻣﻄﺎﻟﻌﻪ ﺣﺎﺿﺮﺑﻪ ﻣﻨﻈﻮر ﺗﻌﻴﻴﻦ ﺳﺎز وﻛﺎر ﻫﺎي ﻓﻴﺰﻳﻮﻟﻮژﻳﻜﻲ ﺗﺤﻤﻞ ﺷﺮاﻳﻂ ﻣﺎﻧﺪاﺑﻲ در Salix integra و ﻧﻴﺰ ﺑﺮاي اﻧﺘﺨﺎب ﻣﻨﻄﻘﻲ ﮔﻮﻧﻪ ﻫﺎي ﻣﻘﺎوم ﺑﻪ ﻣﺎﻧﺪاﺑﻲ ﺑﺮاي ﻛﺎﺳﺘﻦ از ﺻﺪﻣ ﺎت ﺳﻴﻞ ﺑﻪ ﺗﻮﻟﻴﺪات ﻛﺸﺎورزي اﻧﺠﺎم ﺷﺪ و در آن ﻣﺎ اﺛﺮ ﻫﺎي ﺳﻴﻞ و ﻣﺎﻧﺪاﺑﻲ را روي رﺷﺪ، ﺗﺒﺎدل ﮔﺎزي، و ﻓﻠﻮﺋﻮرﺳﻨﺲ ﻛﻠﺮوﻓﻴﻞ ﻗﻠﻤﻪ ﻫﺎي Salix integra در ﻃﻲ ﻳﻚ دوره رﺷﺪ (اوت ﺗﺎ اﻛﺘﺒﺮ 2011 ) ﺑﺮرﺳﻲ ﻛﺮدﻳﻢ. ﺗﻮﻟﻴﺪ زﻳﺴﺖ ﺗﻮده و ﻓﺘﻮﺳﻨﺘﺰ ﻛﺎﻟﺘﻴﻮار S.integra cv. Qingpi در ﺷﺮاﻳﻂ ﺗﻨﺶ ﻣ ﺘﻮﺳﻂ ﻣﺎﻧﺪاﺑﻲ ﺑﻬﺒﻮد ﻳﺎﻓﺖ در ﺣﺎﻟﻲ ﻛﻪ رﺷﺪ، ﻣﺤﺘﻮي ﻛﻠﺮوﻓﻴﻞ و ﻧﺮخ ﺧﺎﻟﺺ ﻓﺘﻮﺳﻨﺘﺰ و ﻫﺪاﻳﺖ روزﻧﻪ اي اﻳﻦ Downloaded from jast.modares.ac.ir at 18:36 IRST on Thursday September 23rd 2021 ﻛﺎﻟﺘﻴﻮار ﻫﻤﮕﻲ ﺑﻪ ﻃﻮر ﻣﻌﻨﻲ داري ﻛﻤﺘﺮ از ﻗﻠﻤﻪ ﻫﺎي ﮔﺮوه ﺷﺎﻫﺪ ﺑﻮد. ﻫﻤﭽﻨﻴﻦ اﻓﺰاﻳﺶ ﻣﻌﻨﻲ داري در ﺧﺎﺻﺖ ﻏﻴﺮ- ﻓﺘﻮﺷﻴﻤﻴﺎﻳﻲ ﺿﺪ ﻧﻮري ( NPQ) و ﻛﺎﻫﺸﻲ در PSII ﻛﺎر آﻳﻲ ﺑﻴﺸﻴﻨﻪ ﻛﻮاﻧﺘﻮم ﺑﻴﻮ

ﺷﻴﻤﻴﺎﻳﻲ(Fv/F m) در ﻗﻠﻤﻪ ﻫﺎي ﻏﺮﻗﺎب ﺷﺪه ﻛﺎﻟﺘﻴﻮار S.integra cv. hongpi ﻣﺸﺎﻫﺪه ﺷﺪ. اﻣﺎ، در ﻣﻮرد

ﻛﺎﻟﺘﻴﻮار S.integra cv. Qingpi ﺗﻔﺎوت ﻣﻌﻨﻲ داري در ﻣﻘﺪار NPQ و Fv/F m ﺑﻴﻦ ﺗﻴﻤﺎر ﻣﺎﻧﺪاﺑﻲ و ﺷﺎﻫﺪ وﺟﻮد ﻧﺪاﺷﺖ.ﻧﺘﺎﻳﺞ ﭼﻨﻴﻦ ﻧﺸﺎن ﻣﻲ دﻫﺪ ﻛﻪ در ﺷﺮاﻳﻂ ﻏﺮﻗﺎﺑﻲ، دﺳﺘﮕﺎه ﻓﺘﻮﺳﻨﺘﺰ ﻛﺎﻟﺘﻴﻮار .S. integra cv hongpi اﻧﺪﻛﻲ ﺻﺪﻣﻪ دﻳﺪ. ﺑﺮ ﻋﻜﺲ، ﺗﻨﺶ ﻣﺘﻮﺳﻂ ﻣﺎﻧﺪاﺑﻲ ﻣﻨﺠﺮ ﺑﻪ اﻓﺰاﻳﺶ ﺗﻮﻟﻴﺪ ﺑﺮگ ورﻳﺸﻪ S.integra cv. qingpi ﺷﺪ ﻛﻪ ﭼﻨﻴﻦ اﺷﺎره دارد ﻛﻪ S.integra cv. qingpi ﻣﻲ ﺗﻮاﻧﺪ ﺳﻴﻼب ﻃﻮﻻﻧﻲ ﻣﺪت را ﺑﻬﺘﺮ از S. integra cv. hongpi ﺗﺤﻤﻞ ﻧﻤﺎﻳﺪ . ﺑﻨﺎﺑﺮاﻳﻦ، S. integra cv. qingpi ﺑﺮاي درﺧﺘﻜﺎري در ﻛﻨﺎره ﻫﺎي رودﺧﺎﻧﻪ ﻣﻨﺎﺳﺐ ﺗﺮ اﺳﺖ.

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