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TURFGRASS SCIENCE

Growth, Physiological, and Anatomical Responses of Creeping Bentgrass Cultivars to Different Depths of Waterlogging

Dep. of Agronomy, Purdue Univ., West Lafayette, IN 47907

^* Corresponding author (yjiang{at}purdue.edu)

	ABSTRACT

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Oxygen deficiency is one of the primary root stresses in waterlogged or flooded soils. The objective of this experiment was to identify growth, physiological, and anatomical traits of creeping bentgrass (Agrostis stolonifera L.) associated with tolerance to different depths of waterlogging (WL). Five cultivars (L-93, A-4, G-6, Penncross, and Pennlinks) were subjected to the four WL treatments for 21 d: (i) drained control; (ii) water level at 15 cm (WL-15); (iii) water at 5 cm (WL-5); and (iv) water at 1 cm (WL-1) below the soil surface, respectively. Waterlogging reduced turf quality (TQ), root dry weight (RDW), root water soluble carbohydrate content (RWSC), and root soluble protein content (RPRO), while no significant reductions in RWSC, RDW, or RPRO were observed among three depths of WL. Turf quality and chlorophyll content (Chl) decreased with increasing water level from 15 to 1 cm. At WL-1, Chl, RDW, RWSC, and RPRO were reduced 27, 20, 44, and 22%, respectively, compared to the control. Cultivar differences in TQ, RDW, shoot water soluble carbohydrate content (SWSC), and RPRO were observed under WL. G-6 and L-93 had better quality than A-4, Penncross, and Pennlinks under WL conditions. The formation of aerenchyma was enhanced at WL-15 and WL-5. Mitochondrial swelling occurred under WL, particularly at WL-1. The results suggest that even partial WL (WL-15 and WL-5) could substantially affect turfgrass growth and physiological activities and cultivar variation in WL tolerance could potentially be used for enhancing breeding programs.

Abbreviations: Chl, chlorophyll content • RDW, root dry weight • RPRO, root soluble protein content • RWSC, root water soluble carbohydrate content • SWSC, shoot water soluble carbohydrate content • TQ, turf quality • WL, waterlogging • WL-1, water level at 1 cm • WL-5, water level at 5 cm • WL-15, water level at 15 cm

	INTRODUCTION

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TRANSIENT FLOODING or heavy irrigation followed by slow drainage can reduce soil oxygen availability and thus affect root respiration. Waterlogging and poor soil aeration lead to hypoxic condition in the soil, and oxygen deficiency is one of the primary root stresses in waterlogged or flooded soils (Kozlowski, 1984). Soil can be too wet to provide sufficient oxygen for optimum growth of turfgrass after flooding or over-irrigation. Creeping bentgrass is a widely used cool-season turfgrass on golf greens and fairways in northern regions and transitional zones. Little is known about effects of WL on growth of creeping bentgrass and potential variation in WL tolerance among cultivars.

Waterlogging reduces shoot and root growth of wheat (Triticum aestivum L.) (Huang et al., 1994), causes yield reduction in soybean [Glycine max (L.) Merr.] (Linkemer et al., 1998), and decreases root length and shoot dry weight of winter oats (Avena sativa L.) (Cannell et al., 1985). Waterlogging also enhances the formation of aerenchyma and increases root porosity in wheat (Huang et al., 1994) and in rice (Oryza sativa L.) (Colmer, 2003). Limited research in turfgrass indicates that growth is negatively affected by poor soil aeration. Root growth of Kentucky bluegrass (Poa pratensis L.) is greatly reduced when oxygen diffusion rate is less than 5 x 10^–8 to 9 x 10^–8 g cm^–2 min^–1 (Waddington and Baker, 1965). Low oxygen caused by short-term soil compaction decreases root weight of Kentucky bluegrass at 15- to 20-cm soil depths (Agnew and Carrow, 1985). A reduction in root growth is also observed in creeping bentgrass (Huang et al., 1998). Mechanisms of tolerance to WL may be associated with plant traits associated with oxygen limitation, including changes in anatomy, morphology, nutrition, and metabolism (Setter and Waters, 2003). However, data to support WL tolerance are limited in turfgrass species.

The responses of plants to WL have often been examined using fully waterlogged soils. However, saturation may not always appear at or above the soil surface in the field. Survival of plants may depend on depths of WL and duration of stress. Depths of WL can also provide a useful indication as to whether the soil is aerobic or anaerobic, and how these conditions affect plant growth. Malik et al. (2001) reported that growth rate of wheat was less affected by WL at a 20-cm depth compared to WL at 10 cm or at soil surface. They also found that photosynthesis was reduced by 70 to 80% for the most severe WL treatment, but photosynthesis was little affected when WL occurred at 20 cm below the soil surface. Their results suggested that different depths of WL had a large impact on plant growth.

Changes in growth, physiological, and anatomical traits of creeping bentgrass cultivars in response to different depths of WL are not well understood. It is important to examine shoot and root adaptive traits under a range of waterlogged soil conditions. Knowledge of how soil anaerobic conditions influence growth of creeping bentgrass and cultivar variation in WL tolerance could provide valuable information for management of creeping bentgrass under excess water and low soil oxygen conditions. Therefore, the objective of this experiment was to identify growth, physiological, and anatomical traits of creeping bentgrass cultivars associated with tolerance to different depths of WL.

	MATERIALS AND METHODS

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Plant Materials and Growing Conditions
Mature, healthy creeping bentgrass (A-4, G-6, L-93, Pennlinks, and Penncross) sod plugs were collected from USGA sand mix at 8 cm deep at the William H. Daniel Research and Diagnostic Center at Purdue University in West Lafayette, IN. The plugs were cut to 2.5 cm thick and were then grown in a greenhouse for 60 d in polyvinylchloride (PVC) tubes (10-cm diam. by 40 cm deep). Holes were drilled in the bottom of tube for drainage. Tubes were filled with gravel 2.0 cm above the bottom and then the remaining tube was filled with medium sand (0.25- to 0.5-mm diam.). Grasses were irrigated daily to field capacity, mowed daily at 0.4 cm with an electric handheld clippers, and fertilized weekly with 40 mL full-strength Hoagland's solution (Hoagland and Arnon, 1950) to supply 290 kg N ha^–1. Grasses were moved to Conviron E15 growth chambers (Controlled Environments Inc., Pembina, ND) for 15 d under temperature of 20 ± 0.1°C/15 ± 0.1°C (day/night), a 14-h photoperiod, and a photosynthetically active radiation of 600 µmol m^–2 s^–1 before WL treatments.

Waterlogging Treatments
Waterlogging was imposed by plugging the drainage holes of PVC tubes. A 1-cm-diam. hole was drilled in the side, 2.5 cm above the bottom, and connected to an open-end transparent tubing with height of other end adjusted to 15, 5, and 1 cm below the soil surface. This transparent tubing was not installed for control PVC tubes. Water was added daily from canopy to maintain different WL levels. A diagram of WL tube is shown on Fig. 1. The WL treatments included:

(i)Control, drained to field capacity

(ii)Water level at 1 cm below the soil surface (WL-1)

(iii)Water level at 5 cm below the soil surface (WL-5)

(iv)Water level at 15 cm below the soil surface (WL-15)

View larger version (29K): [in this window] [in a new window]   Fig. 1. Diagram of waterlogging (WL) tubes. Additional transparent tubing indicates water level.

Sampling and Measurements
Turf quality was visually rated as an integral of color, uniformity, and density on the scale of 1 (brown leaves) to 9 (turgid, green leaves) at 7, 14, and 21 d of WL treatment. At the end of experiment (21 d), shoots were collected and roots were washed free from soil. Leaf Chl was measured according to the methods of Inskeep and Bloom (1985). Leaf Chl was extracted by soaking 50-mg samples in 10 mL dimethyl sulfoxide (DMSO) in the dark for 48 h. The absorbance was read at 662 and 645 nm. Root dry weight was determined after samples were dried in an oven at 80°C for 3 d. A single new root (originating from crown) with maximum length in each tube was chosen to indicate new root growth. Soil Eh was measured using Combination Redox Probe (TPS Pty. Ltd., Brisbane, QLD).

Shoot water soluble carbohydrate content and RWSC were determined using the methods of Dubois et al. (1956), modified by Buysse and Merckx (1993), and the detailed procedure of extraction and assay was described by Jiang and Huang (2001). For soluble protein extraction, a 0.5-g fresh root sample from the entire root profile was ground with liquid N₂ to a fine power, then extracted in 4 mL of extraction buffer (50 mM potassium phosphate, 1 mM ethylenediaminetetraacetic acid [EDTA], 0.1% triton X-100 [v/v], 1% polyvinylpyrrolidone [PVP], 1 mM dithiothreitol [DTT], and 1 mM phenylmethylsulfonyl [PMSF], pH 7.8). Samples then were centrifuged at 15000 g for 30 min, and supernatant was collected for protein assay. Protein content was determined by the method of Bradford (1976).

Root aerenchyma and mitochondria were examined in L-93 and Penncross using electron microscopy at Purdue Life Science Microscope Facility. For aerenchyma, root segments (3 cm in length) at 5 cm from the root tip were processed by fixation and dehydration, and then imaged in a JEOL JSM-840 Scanning Electron Microscopy at 500x to 700x. The samples were also embedded in resin for examination of root mitochondria in FEI/Philips CM-10 Transmission Electron Microscope at 15000x to 20000x.

Experimental Design and Statistical Analyses
The experiment was randomized complete block design in a 4 (WL) by 5 (cultivar) factorial arrangement. Four growth chambers representing four replicates were used in this study, and each chamber contained four WL treatments and five cultivars. Waterlogging treatments and grasses were arranged randomly in each chamber. We used the Proc GLM in SAS for statistical analysis (SAS Institute Inc., Cary, NC), with both cultivars and WL being considered as fixed effects. This allowed us to examine trait differences caused by WL effect as well as by cultivar effects. Data from 21 d of WL were used to analyze significance of WL treatment, cultivar, and their interaction by using SAS. The effects of WL treatment and cultivar differences were tested using the Least Significant Difference (LSD) test at 0.05 probability level.

	RESULTS

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The analysis of data determined importance of cultivar, WL, and their interactions (Table 1). No significant cultivar x treatment interactions in all traits were observed at 21 d of treatment.

Cultivar Differences
Overall, G-6 and L-93 exhibited acceptable TQ (>6), while A-4, Penncross, and Pennlinks had unacceptable quality under WL conditions (Table 3). All cultivars had acceptable TQ at 7 d of treatments (Fig. 2). At 14 d of WL-1, G-6, and L-93 maintained desirable TQ while A-4, Penncross, and Pennlinks exhibited unacceptable TQ. At 21 d, G-6 and L-93 had acceptable TQ under WL-5 and WL-15, but TQ dropped to below 6 under all three depths of WL for Penncross and Pennlinks. G-6 had higher Chl than the other four cultivars, and no significant difference in Chl was observed among these four cultivars under WL treatments (Table 3). A-4, Penncross, and Pennlinks had higher SWSC than G-6. Significant differences in RDW were observed among five cultivars with A-4 showing the highest RDW and Pennlinks and Penncross having the lowest (Table 3). Pennlinks had the highest RPRO and Penncross exhibited the lowest RPRO among five cultivars. There were no differences in soil Eh, NRL, and RWSC among cultivars under WL treatments (Table 3).

View larger version (15K): [in this window] [in a new window]   Fig. 2. Turf quality as affected by different depths of waterlogging (WL). Control means drained and non-WL; WL-15, WL-5, and WL-1 represent WL at 15, 5, and 1 cm below the soil surface, respectively.

View larger version (111K): [in this window] [in a new window]   Fig. 3. Aerenchyma formation of creeping bentgrass roots in response to 21 d of waterlogging. WL-15, WL-5, and WL-1 represent waterlogging (WL) at 15, 5, and 1 cm below the soil surface, respectively. A, B, C, D represent the drained control, WL-15, WL-5, and WL-1 of L-93, respectively. E, F, G, H, represent the drained control, WL-15, WL-5, and WL-1 of Penncross, respectively. Images of A to F are at 500x; image of G is at 750x; and image of H is at 600x. Arrow indicates aerenchyma. Bar = 20 µm.

View larger version (189K): [in this window] [in a new window]   Fig. 4. Mitochondrial ultrastructure of creeping bentgrass roots in response to 21 d of treatment. WL-15, WL-5, and WL-1 represent waterlogging (WL) at 15, 5, and 1 cm below the soil surface, respectively. A, B, C, D represent the drained control, WL-15, WL-5 and WL-1 of L-93, respectively. E, F, G, H, represent the drained control, WL-15, WL-5 and WL-1 of Penncross, respectively. All images are at 30 000x. Bar = 0.5 µm.

	DISCUSSION

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Waterlogging promoted development of adventitious roots in all cultivars. The newer roots generated exclusively under WL conditions exhibited white color and larger diameter (visual observation). Although the maximum length of a single new root was not significantly different among cultivars, WL-15 had a longer NRL than WL-5 and WL-1 (Table 2). Chen et al. (2002) reported that number of adventitious root in perennial pepperweed (Lepidium latifolium L.) increased with duration of flooding. These new roots may have a positive role in supporting shoot growth during prolonged flooding (Jackson, 1985; Armstrong et al., 1994). The new root also showed formation of aerenchyma in our study (data not shown), which may enhance plant survival from extended periods of WL conditions.

Depths of WL and duration of stress substantially influenced quality of creeping bentgrass cultivars. G-6 and L-93 had better quality than Penncross and Pennlinks, especially when water levels were 5 and 1 cm below the soil surface. In field conditions, the water table may fluctuate to different levels in the soil after a flooding event or excessive irrigation, depending on soil structure, drainage, and other factors. The depths of WL can provide useful information of aerobic or anaerobic soil conditions, but research on how depths of WL affect plant growth and WL tolerance is limited. Malik et al. (2001) reported that growth rate of wheat was reduced proportionally as the water level increased from 20-cm depth to soil surface, and the decreased growth rate in roots was more than that of shoots. They also found that Chl decreased with increasing water level in the soil after 14 d of WL. Similar results were obtained in our study that Chl decreased with increasing water level in the soil. A decreased Chl is also observed in other plant species in response to WL (Smethurst and Shabala, 2003; Ashraf and Arfan, 2005). In general, WL-1, WL-5, and WL-15 had similar proportions of total root mass (i.e., dry weight) at different depths, indicating water level at 15 cm below the soil surface could also affect root growth.

Waterlogging influences carbohydrate content. An approximate 45% reduction in RWSC content was observed at WL-1 compared to the drained control. Root WSC was not affected by three depths of WL, and a similar pattern was observed in RDW. These results suggested that reduction in WSC under WL is one of the major factors contributing to a decreased root growth, and partial WL had the same effects as fully waterlogged treatment on root growth. Penncross and Pennlinks had lower RDW, consistent with their lower TQ rating under WL treatments. Shoot WSC content generally increased under WL conditions, but significant difference in SWSC was not observed among three depths of WL treatments. Albrecht et al. (1997) found that hypoxia increased both shoot and root carbohydrate content in four species, including flooding-tolerant Senecio aquaticus Hill. and Myosotis palustris (L.) Lehm. Rchb. and flooding-intolerant M. arvensis (L.) Hill. and S. jacobaea (L.). Waterlogging decreases leaf carbohydrate content and enhances partition of carbohydrate to roots in wheat (Huang and Johnson, 1995). The increased SWSC and decreased RSWC in creeping bentgrass could be due to an inhibition of carbohydrate partitioning to roots under WL. However, a further study is needed to demonstrate this pattern. Species variations and WL duration may be a factor influencing shoot and root growth and carbohydrate partitioning.

Waterlogging decreased RPRO, but no differences in reduction in RPRO were observed among three depths of WL. Our result agrees with other studies in beech (Fagus sylvatica L.) (Kreuzwieser et al., 2002) and rice (Mohanty and Ong, 2003), which found that WL or submergence decreased soluble protein content. It has been also reported that protein content remained unchanged in flood tolerant oak (Quercus robur L.) and poplar (Populus tremula x P. alba) (Kreuzwieser et al., 2002) and increased in perennial pepperweed (Chen and Qualls, 2003) in response to flooding.

Waterlogging or flooding enhances the formation of aerenchyma (Huang et al., 1994; Vasellati et al., 2001) and increases root porosity and aerenchyma development in roots of sea barley grass (Critesion marinum Huds.) (McDonald et al., 2001). Aerenchyma can provide a low-resistance internal pathway and enhance transport of oxygen, carbon dioxide, and ethylene between plant parts above water and the submerged tissues (Armstrong 1972; Laan et al., 1990). Formation of aerenchyma may promote root survival under waterlogged or flooded soil, but there is not always a clear relationship between the amount of aerenchyma and WL tolerance (Setter et al., 1999). Under severe reduced soil conditions, root aerenchyma formation may not provide sufficient oxygen to support aerobic respiration completely in one coastal grass, Spartina patens (Burdick and Mendelssohn, 1990).

Mitochondrial swelling and loss of structure became more pronounced as WL depth increased to 1 cm below the soil surface in both L-93 and Penncross. Mitochondria are primary oxygen consumers and they suffer from oxygen deficiency before other cell organelles (Vartapetian et al., 2003). A 6- to 10-h anaerobic incubation can result in irreversible degradation of mitochondria of roots of pumpkin (Cucurbita pepo L.), a flooding-sensitive species (Vartapetian et al., 2003). In our study, the loss of normal structure of mitochondria under WL conditions affected root functions and might contribute to TQ decline.

In conclusion, WL significantly reduced TQ, RWSC, RDW, and RPRO in creeping bentgrass cultivars. Traits of TQ, Chl, and RDW were closely associated with cultivar tolerance to WL. Waterlogging also enhanced the formation of aerenchyma and the damage of mitochondrial ultrastructure in roots. Cultivar of G-6 and L-93 had better TQ than A-4, Penncross, and Pennlinks under WL treatments. The result demonstrated that even partial WL (WL-15 and WL-5) could substantially affect turfgrass growth and physiological activities, particularly to those intolerant cultivars.

	ACKNOWLEDGMENTS

 
The authors would like to thank Chia-Ping Huang and Debra M. Sherman for technical assistance in electron microscopy and Xi Xiong for carbohydrate analysis. The authors also thank Drs. Cale Bigelow and Zac Reicher for critical review for this manuscript.

Received for publication November 3, 2005.

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This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Jiang, Y. Articles by Wang, K. Search for Related Content PubMed Articles by Jiang, Y. Articles by Wang, K. Agricola Articles by Jiang, Y. Articles by Wang, K. Related Collections Water Stress Turfgrass