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TURFGRASS SCIENCE

Response of Creeping Bentgrass Carotenoid Composition to High and Low Irradiance

Plant Sciences Dep., Univ. of Tennessee, 2431 Joe Johnson Dr., 252 Plant Science Bldg., Knoxville, TN 37996

^* Corresponding author (mcelroy{at}utk.edu)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Carotenoids are important photoprotectant and light-harvesting pigments within the photosynthetic apparatus. Little information is available regarding carotenoid physiology in creeping bentgrass (Agrostis stolonifera L.). Research was conducted to investigate relative high and low irradiance adaptation of creeping bentgrass with respect to ß-carotene and xanthophyll composition. ‘Crenshaw’ creeping bentgrass plants were acclimated for 7 d to relative high [47.9 mol m^–2 d^–1 photosynthetically active radation (PAR)] or low irradiance (4.7 mol m^–2 d^–1 PAR). After the acclimation period, plants were transferred from high to low (low irradiance treatment) and low to high (high irradiance treatment) irradiance. Clippings were harvested at 0, 24, 72, and 168 h after the acclimation period. Zeaxanthin and antheraxanthin decreased from 5.1 and 3.4 to 0.9 and 0.6 mg 100 g^–1 fresh weight (FW), respectively, over 168 h in low irradiance. As the turf adapted to low irradiance, violaxanthin, lutein, and lutein-5,6-epoxide (epoxylutein) increased at 24 h, but levels decreased from 24 to 168 h. Zeaxanthin and antheraxanthin increased in high irradiance, while violaxanthin and ß-carotene decreased. Lutein was the predominant carotenoid quantified regardless of irradiance treatment. Cumulative zeaxanthin, antheraxanthin, and violaxanthin increased as a percentage of the total carotenoids as the turfgrass adapted to high irradiance, but decreased in low irradiance. Conversely, neoxanthin and ß-carotene decreased in high irradiance and increased in low irradiance. Creeping bentgrass produces carotenoid amounts comparable to other plant species potentially attributable to selection efforts of more stress-tolerant varieties.

Abbreviations: ELU/LU ratio, epoxylutein to lutein ratio • FW, fresh weight • HPLC, high performance liquid chromatography • LHC, light harvesting complex • NPQ, nonphotochemical quenching • PAR, photosythetically active radiation • ZA/ZAV ratio, zeaxanthin + antheraxanthin to zeaxanthin + antheraxanthin + violaxanthin ratio

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
CAROTENOIDS are lipid-soluble yellow, orange, and red pigments that are uniquely synthesized in plants, algae, fungi, and bacteria (Sandmann, 2001). They are secondary plant compounds which are divided into two groups: the oxygenated xanthophylls such as lutein, zeaxanthin, and violaxanthin, and the hydrocarbon carotenes such as -carotene, ß-carotene, and lycopene (Zaripheh and Erdman, 2002). Carotenoids are integrated into light-harvesting complexes (LHC) along with chlorophyll and perform physiological roles of photoprotection and light harvesting (Croce et al., 1999a, 1999b). Photoprotection is the prevention of oxidative damage, or photoinhibition, to the LHC allowing plants to maintain efficient rates of photosynthesis (Niyogi, 1999). Carotenoids function as photoprotectants by quenching free radical triplet-state chlorophyll and singlet oxygen before oxidative damage can occur or by active nonphotochemical quenching (NPQ), or heat dissipation, of excess light energy (Niyogi, 1999; Croce et al., 1999b; Frank and Cogdell, 1996; Demmig-Adams et al., 1996). Carotenoids function as light-harvesting pigments by channeling photons unabsorbed by the chlorophyll molecule to the reaction center for photosynthesis (Niyogi, 1999; Goodwin, 1980).

Carotenoid formation is highly conserved throughout all plant species with six primary functioning carotenoids: zeaxanthin, antheraxanthin, violaxanthin, lutein, ß-carotene, and neoxanthin (Table 1; Sandmann, 2001). The carotenoid pathway begins with dimerization of the C₂₀ compound geranyl-geranyl pyrophosphate to produce phytoene, the first C₄₀ carotenoid (Fig. 1 ). Phytoene is desaturated to form lycopene. Branching of the pathway occurs when lycopene is cyclized into -carotene or ß-carotene. -Carotene forms lutein and lutein-5,6-epoxide (epoxylutein), while ß-carotene forms neoxanthin and the xanthophyll cycle pigments, zeaxanthin, antheraxanthin, and violaxanthin.

View larger version (22K): [in this window] [in a new window]   Fig. 1. Schematic of conversion pathway of primary plant carotenoids responsible for photoprotection and light harvesting (Demmig-Adams et al., 1996; Garcia-Plazaola et al., 2002).

Limited information is available regarding carotenoid composition in turfgrass species. Previous research has primarily quantified carotenoids for their potential phytonutrient availability to grazing animals and is limited to forage-type grasses. Further, those reports evaluating turfgrass carotenoids do not separate different carotenoids and limit reporting to total carotenoids and xanthophylls (Lee et al., 1996; Bailey and Chen, 1988). Bell and Danneberger (1999) reported the most extensive results on carotenoids in turfgrass species. These researchers separated neoxanthin, violaxanthin, and lutein in creeping bentgrass (Agrostis stolonifera L.) under different shade regimes. However, the lack of internal standards prevented the quantification of these carotenoids and only carotenoid chromatographic peak heights were reported.

Creeping bentgrass is an important turfgrass species throughout the world and specifically in the golf course industry of the United States. Like many turfgrass species, it is often grown in environmentally challenging conditions, such as shaded, low-irradiance environments. Under low irradiance or shade conditions, creeping bentgrass decreases in turf density and eventual stand failure can occur (Bell and Danneberger, 1999; Goss et al., 2002). The objective of this research is to quantify the major carotenoids present in creeping bentgrass under changes from high to low (low irradiance treatment) and from low to high (high irradiance treatment) irradiance, thus improving our understanding of the response of creeping bentgrass to changing irradiance stress conditions. Improved knowledge of irradiance adaptability of carotenoids could aid researchers in evaluating new creeping bentgrass cultivars or potential manipulation of beneficial carotenoid levels through xenobiotic applications.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Cores (10-cm diameter, 20-cm depth) of ‘Crenshaw’ creeping bentgrass were collected from Cherokee Country Club, Knoxville, TN. Plugs were transplanted into 15-cm-diam pots and back filled with an 80:20 v/v mixture of sand and potting mix (Berger Tourbieres Peat Moss Growing Mix, Saint Modeste, QC) and maintained in a greenhouse environment for 3 wk to allow for acclimation. Plants were fertilized weekly with a complete fertilizer (Howard Johnson's Triple Twenty Plus Minors, Milwaukee, WI) at 5.2 kg N ha^–1 and watered daily with overhead irrigation to maintain adequate soil moisture. Plants were clipped with hand shears two times per week to 2-cm height.

After acclimation, plants were placed in an environmental growth room (Environmental Growth Chambers, Chagrin Falls, OH) at 23/16°C day/night temperature under a 16-h photoperiod. Plants were clipped and fertilized for the final time 24 h before transferring to the environmental growth room. Irradiance was provided by a mixture of metal halide and high pressure sodium lamps. Relative high irradiance conditions (47.9 mol m^–2 d^–1 PAR) were achieved by raising the vertical position of the plants within the growth chamber. Relative low irradiance conditions (4.7 mol m^–2 d^–1 PAR) were achieved by placing the plants on the floor of the growth chamber and surrounding the plants with a shade cloth (A.M. Leonard, Inc., Piqua, OH). Variation in pertinent environmental conditions within the irradiance regimes were also documented (Table 2). Temperature was measured during the middle of the photoperiod three times throughout the experiments on four random plants using an infrared thermometer (Cole-Parmer Instrument Company, Vernon Hills, IL). Variation in temperature is known to affect plant pigment concentrations (Ruter and Ingram, 1992). While this information is provided as potential confounding variables, we emphasize that carotenoids are photoprotective pigments associated with the photosystem and quantities are primarily influenced by irradiance conditions (Demmig-Adams et al., 1999). All efforts were taken to control all confounding variables, however, maintaining consistent temperature over the two irradiance regimes was not achieved.

At harvest, clippings were immediately frozen in liquid N and placed on ice for transfer to storage at –80°C. Carotenoid compounds were extracted and quantified according to previously published methods (Emenhiser et al., 1996; Kopsell et al., 2003). All clippings were first homogenized in liquid N using a mortar and pestle. An approximately 0.50-g subsample was placed into a Potter-Elvehjem tissue grinder tube (Kontes, Vineland, NJ) with 0.8 mL of ethyl-ß-apo-8'-carotenoate (Sigma Chemical Co., St. Louis, MO), as an external standard, and 2.5 mL of tetrahydrofuran (THF) stabilized with 2,6-di-tert-butyl-4-methoxyphenol (BHT). The sample was vortexed and homogenized in the tube using approximately 25 insertions with a Potter-Elvehjem tissue grinder pestle attached to a drill press (Craftsman 15-inch drill press; Sears, Roebuck, and Co., Hoffman Estates, IL) set at 540 rpm while the tube was immersed in ice to dissipate heat. The tube was then placed into a centrifuge for 3 min at 500 g. Precautions were taken to keep the tissue samples on ice during extraction to decrease degradation and increase percentage of recovery (Kimura and Rodriguez-Amaya, 1999). The supernatant was removed with a pasteur pipette, placed into a conical 15-mL test tube, capped, and held on ice during the remainder of the extraction. The sample pellet was resuspended in 2 mL THF stabilized with BHT and the extraction procedure was repeated. By the fourth or fifth extraction, the supernatant was colorless and one additional extraction was conducted. The remaining sample pellet was discarded and the combined supernatants were placed in a water bath at 40°C and reduced to 0.5 mL under N stream (N-EVAP 111; Organomation Inc., Berlin, MA). To each 0.5-mL sample, 4.5 mL MeOH was added and vortexed. Samples were then filtered through a 0.20-µm polytetrafluoroethylene filter (Econofilter PTFE 25/20; Agilent Technologies, Wilmington, DE) before high performance liquid chromatography (HPLC) analysis.

An Agilent 1100 series HPLC unit with a photodiode array detector (Agilent Technologies, Palo Alto, CA) was used for sample separation. All samples were analyzed for carotenoid compounds using a ProntoSIL C₃₀ RP column (4.6 by 250 mm; MAC-MOD Analytical Inc., Chadds Ford, PA) with a 5.0-µm particle size and 200-Å pore size fitted with a guard column (4 by 23 mm, 7.0 µm; S-5, Nesterenko and Sink, 2003). The column was maintained at 30°C using a thermostatted column compartment. Pigment separation was performed using an isocratic mixture of methanol/methyl-tert-butyl-ether 89:10.9% (v/v) plus 0.1% triethylamine. Eluted carotenoid compounds from a 20-µL injection were detected at 453 nm and data were collected, recorded, and integrated using 1100 HPLC ChemStation Software (Agilent Technologies, Palo Alto, CA). Carotenoids evaluated include ß-carotene, antheraxanthin, lutein, epoxylutein, neoxanthin, violaxanthin, and zeaxanthin. These carotenoids were selected based on their active roles in photoprotection and light harvesting. Peak assignment was performed by comparing retention times to internal standards and line spectra (250–650 nm) obtained from photodiode array detection with authentic standards purchased from commercial venders (CaroteNature GmbH, Lupsingen, Switzerland, http://www.carotenature.com). Concentrations of the authentic standards were determined spectrophotometrically using quantitative spectroscopic data (Table 1; Davies and Köst, 1988). HPLC recovery rates of ethyl-ß-apo-8'-carotenoate (64–91%) were used to estimate carotenoid losses during extraction. All carotenoids were calculated on a 100 g FW of creeping bentgrass leaf tissue basis. -Carotene was undetectable and therefore not quantified. Percentage of carotenoid composition was also calculated for ß-carotene, epoxylutein, lutein, neoxanthin, and cumulative zeaxanthin, antheraxanthin, and violaxanthin. Ratios of zeaxanthin + anteraxanthin to zeaxanthin + antheraxanthin + violaxanthin (ZA/ZAV ratio), and epoxylutein to lutein (ELU/LU ratio) were also calculated for comparison (Demmig-Adams et al., 1999; Latowski et al., 2004).

The experimental design was completely random with two treatment schemes, high and low irradiance adaptability. Within each treatment scheme, harvest intervals (0, 24, 72, and 168 h after acclimation) were analyzed as subsamples. The experiment was conducted twice with three replicates. All data were subjected to ANOVA (P = 0.05; Statistical Analysis Software, Inc., Cary, N.C.). Treatment schemes were analyzed as main effects. Nonsignificant treatment scheme by run interaction allowed for the data pooling over experimental runs. Means were separated using Fisher's Protected LSD (P = 0.05) where appropriate.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Carotenoid Quantification
When evaluating creeping bentgrass carotenoid changes in low irradiance over 168 h, changes occurred in zeaxanthin, antheraxanthin, violaxanthin, lutein, and epoxylutein levels, but not in neoxanthin or ß-carotene (Table 3). Zeaxanthin decreased from 5.1 to 1.7 mg 100 g^–1 FW in 24 h with an eventual decrease to 0.9 mg 100 g^–1 FW. Antheraxanthin trended similarly from 3.4 to 2.2 mg 100 g^–1 FW in 24 h and 0.6 mg 100 g^–1 FW after 168 h. Violaxanthin increased after 24 h from 3.2 to 5.9 mg 100 g^–1 FW. Increased violaxanthin levels were not maintained and levels moderated to 2.7 mg 100 g^–1 FW after 168 h. Decreases in zeaxanthin and antheraxanthin resulted in a decrease in ZA/ZAV ratio from 0.73 to 0.39 in 24 h after movement of creeping bentgrass from high to low irradiance with similar conditions observed at 72 and 168 h. Within the xanthophyll cycle pool, violaxanthin is known to accumulate under low irradiance conditions and zeaxanthin in high irradiance (Demmig-Adams et al., 1996; Thayer and Björkman, 1990). While epoxidation of zeaxanthin to violaxanthin normally functions slower than de-epoxidation (Demmig-Adams et al., 1996), maximal observed violaxanthin concentration was reached by 24 h; however, violaxanthin decreased over the 168-h period.

Changes in the xanthophyll cycle pigments followed an expected accumulation pattern of zeaxanthin and antheraxanthin in high irradiance (Table 3). Zeaxanthin increased from 0.6 mg to 4.0 mg 100 g^–1 FW at 24 h, with levels increasing to 9.2 and 7.9 mg 100 g^–1 FW at 72 and 168 h, respectively. Antheraxanthin trended similarly, increasing from 1.0 to 2.7 mg 100 g^–1 FW after 24 h, and 3.6 and 3.5 mg 100 g^–1 FW at 72 and 168 h, respectively. Violaxanthin decreased gradually from 4.5 and 3.8 mg 100 g^–1 FW at 0 and 24 h, respectively, to 2.7 and 1.4 mg 100 g^–1 FW at 72 and 168 h, respectively. ß-Carotene also decreased following high irradiance treatment from 9.8 to 5.4 mg 100 g^–1 FW from 0 to 168 h. Changes in the xanthophyll cycle pigments increased the ZA/ZAV ratio from 0.26 to 0.89 at 0 and 168 h, respectively. Zeaxanthin is viewed as the primary carotenoid responsible for photoinhibition prevention through NPQ, with antheraxanthin functioning as a transition state molecule in the xanthophyll cycle (Demmig-Adams et al., 1999). In investigating the photoprotective mechanisms of zeaxanthin, NPQ was reduced in Arabidopsis thaliana (L.) Heynh. mutants unable to convert violaxanthin to zeaxanthin and sensitivity to photoinhibition was increased (Niyogi et al., 1998). Similar mutants of the green algae Chlamydomonas reinhardtii Dangeard that accumulate zeaxanthin with little formation of violaxanthin, or lutein, retain adequate photoprotective capabilities, but have decreased light-harvesting abilities (Baroli et al., 2003). In the absence of zeaxanthin, antheraxanthin functions in photoprotection through NPQ (Goss et al., 1998) suggesting that this molecule is of greater importance than a transition carotenoid to zeaxanthin.

‘Crenshaw’ creeping bentgrass produced carotenoid levels comparable to many green leafy vegetable and herbal crops. Khachik et al. (1992) reported levels of neoxanthin, violaxanthin, epoxylutein, lutein, and ß-carotene in raw unprocessed spinach (Spinacia oleracea L.) as 2.4, 7.4, 0.5, 9.5, and 8.9 mg 100 g^–1 FW, respectively. Various kale (Brassica oleracea L. var. acephala) cultivars accumulated 4.8 to 13.4 mg lutein 100 g^–1 FW and 3.5 to 10.0 mg ß-carotene 100 g^–1 FW (Kopsell et al., 2004). Creeping bentgrass in the current study produced comparable levels of neoxanthin, epoxylutien, and ß-carotene, lower levels of violaxanthin, and higher levels of lutein than those previously reported for spinach and kale. Parsley (Petroselinum crispum Nym.) accumulated 7.9 mg ß-carotene 100 g^–1 FW and 8.6 mg lutein + zeaxanthin 100 g^–1 FW (Chenard et al., 2005). These values represent similar quantities of ß-carotene and lower amounts of lutein + zeaxanthin than those measured for creeping bentgrass in the current study. Creeping bentgrass in the current study also accumulated much higher levels of zeaxanthin than those reported for sweet basil (Ocimum basilicum L.) (0.37 to 0.62 mg 100 g^–1 FW; Kopsell et al., 2005).

Percentage of Total Carotenoids
Low and high irradiance treatments induced changes in bentgrass percent carotenoid composition (Fig. 2 ). High irradiance treated plants decreased in lutein, ß-carotene, and neoxanthin, but total xanthophyll cycle pigments (zeaxanthin, antheraxanthin, and violaxanthin) increased. Conversely, low irradiance treated plants increased in lutein, ß-carotene, and neoxanthin, but total xanthophyll cycle pigments decreased. Under low irradiance treatments, lutein (53%) was the major carotenoid. Under high irradiance, lutein remained the major carotenoid; however, amounts decreased to 46% of all carotenoids quantified. ß-Carotene and neoxanthin changed similarly accounting for 20 and 12%, respectively, of total carotenoids under low irradiance and 12 and 9%, respectively, of total carotenoids under high irradiance after 168 h. Total xanthophyll cycle pigments accounted for 13% under low irradiance, but 30% under high irradiance after 168 h. Plants growing under high irradiance accumulate more total xanthophyll cycle pigments as a photoprotective measure with decreases observed under low irradiance conditions due to decreases in zeaxanthin and antheraxanthin (Demmig-Adams et al., 1996). In creeping bentgrass, increases in the proportion of xanthophyll cycle pigments are attributed to decreases in ß-carotene, neoxanthin, and lutein and to increases in zeaxanthin and antheraxanthin. Decreases in violaxanthin, potentially decreasing the xanthophyll cycle pool, was compensated for by increases in zeaxanthin and antheraxanthin. Zeaxanthin and antheraxanthin accumulation under high irradiance conditions to the sacrifice of other carotenoids underscores the importance of these pigments as photoprotectants in creeping bentgrass.

View larger version (28K): [in this window] [in a new window]   Fig. 2. Distribution of quantified carotenoids expressed on a total percentage basis as influenced by low and high irradiance adaptability conditions.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
There is limited information on the physiological roles of carotenoids in photoprotection and light harvesting in turfgrass species. Creeping bentgrass has a robust functioning xanthophyll cycle and accumulates high amounts of ß-carotene and lutein under high and low irradiance conditions. Due to the high correlation between chlorophyll and carotenoid pigments (Kopsell et al., 2004), breeding creeping bentgrass for dark green color and stress tolerance has likely created cultivars such as ‘Crenshaw’ with high carotenoid content unbeknownst to the breeders themselves. Carotenoids are beneficial components in creeping bentgrass, potentially contributing to increased performance in stressful conditions. Further evaluations of creeping bentgrass carotenoid physiology under managed conditions will provide added insight into the potential physiological role of carotenoids in turf management.

Received for publication February 22, 2006.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

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