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CROP PHYSIOLOGY & METABOLISM

Interaction between Waterlogging Injury and Irradiance Level in Alfalfa

Hortic. and Crop Sci. Dep., Ohio Agric. Res. and Development Center and The Ohio State Univ., 1680 Madison Ave., Wooster, OH 44691-4096

* Corresponding author (barta.2{at}osu.edu)

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
This study investigates the interaction between irradiance and waterlogging injury in alfalfa (Medicago sativa L.) at various plant developmental stages. Alfalfa was subjected to flooding for 8 to10 d under high or low irradiance levels in controlled environmental chambers. Treatments were imposed on alfalfa 8 and 21 d after planting (DAP) and during regrowth following clipping at 31 DAP. Flooding significantly reduced dry matter accumulation regardless of growth stage, although damage was most severe when flooding was imposed on plants during regrowth after clipping. Irradiance levels primarily affected shoot and root dry matter in 21- and 31-DAP treatments. Much greater shoot dry matter accumulation in nonflooded high irradiance plants was observed relative to low irradiance plants. A flooding x irradiance interaction was found at every growth stage except for root dry weight in the regrowth stage after clipping. The flooding interaction was due to greater injury of flooded high-irradiance plants relative to flooded low-irradiance plants when injury was expressed as a percentage of the unflooded control. Results indicate that the irradiance level during flooding can influence damage rating when expressed as a percentage of control. Assimilate supply to roots was sharply reduced by low irradiance as evidenced by reduced root growth and carbohydrate concentration in unflooded controls. Flooding damage, however, was not enhanced under low irradiance, lending support to the hypothesis that carbohydrate (i.e., energy supply) is not a limiting factor in survival of alfalfa roots during short-duration flooding stress.

Abbreviations: DAP, days after planting • PPFD, photosynthetic photon flux density • TNC, total nonstructural carbohydrates

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
ALFALFA is one of the most widely grown perennial forage crops in the USA and worldwide because of its yield potential and high nutritive value. It has a very wide range of adaptation in part due to its extensive tap root system that allows it to extract water from deep in the soil profile. However, alfalfa does not tolerate wet, poorly drained soils, or extended periods of soil saturation. This susceptibility to root waterlogging and soil hypoxia limits the areas where alfalfa can be reliably grown and contributes to loss of stand where soil moisture excess is chronic.

Flooding injury in alfalfa has been well characterized and is influenced by factors that include cultivar, plant age, clipping management, duration of stress, interaction with pathogens, and temperature (Erwin et al., 1959; Rai et al., 1971; Cameron, 1973; Faris and Sabo, 1981; Teutsch and Sulc, 1997; Barta, 1988). There have been few reports on the effects of irradiance level on flooding injury even though light is a major environmental factor impacting plant growth and response in the field. Wagner and Dreyer (1997) reported limited interactions between long-term waterlogging and irradiance on three species of Quercus (oak) seedlings. Results of one experiment (out of two conducted) suggested that shading Quercus rubra L. seedlings (the most waterlogging sensitive species of the three examined) might limit the extent of waterlogging injury. In studies on Veronica chamaedrys L., V. montana L., and V. officinalis L., Dale and Causton (1992) indicated that growth rate reductions caused by waterlogging were much greater than those caused by low levels of irradiance. When 21- to 28-d-old alfalfa roots grown in nutrient solution were submitted to short term (1- or 3-d) hypoxia in full irradiance or shading, shoot and root fresh weight were sharply reduced in response to hypoxia and no interaction between irradiance and hypoxia response was found (Barta, 1987). In a field flooding study, waterlogging injury was enhanced in one field experiment where flooding coincided with cloudy weather (Barta, 1988). It was suggested that cloudy weather at time of flooding may have increased alfalfa injury through reduced photosynthate supply to roots.

Several studies have documented that root tissue survival under hypoxia is dependent upon fermentation rate and sufficient sugar supply to maintain cell energy charge and membrane function (Vartapetian et al., 1977; Saglio and Pradet, 1980). High levels of soluble sugars and starch are found in flooded alfalfa roots (Barta, 1987; Castonguay et al., 1993), suggesting that carbohydrate supply was not limiting to hypoxia stress tolerance. However, Drew (1997) suggested even though high concentrations of sugars can be found in hypoxic root tissue, the movement of these carbohydrates to the apical zone under anoxia might be inhibited. This could lead to energy shortage and tissue damage. If this intercellular carbohydrate transport hypothesis is true, then photo-assimilate supply to flooded root apical zones might be important to plant survival. The fact that clipped alfalfa is more sensitive to root waterlogging than plants with shoots present (Erwin et al., 1959; Cameron, 1973; Barta, 1988) suggests a possible role for assimilate supply to roots although other clipping-related factors such as changes in hormonal balance and transpiration-related processes (Castonguay, 1993) could be involved.

The objective of this research was to describe the interaction between irradiance level and long-term waterlogging injury in alfalfa, and to determine if photo-assimilate supply impacts root flooding response. Flooding treatments were imposed at three widely divergent plant growth stages in order to characterize the irradiance-flooding interaction under potentially different photo-assimilation and assimilate partitioning patterns.

	MATERIALS AND METHODS

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Plant Growth
Alfalfa cv. WL323 was grown in a sterilized sand:soil (2:1, v:v) mixture. Seeds were sown in 15-cm diam. pots and thinned to 10 plants per pot. Plants were watered as needed with nutrient solution at pH 6.5. The composition of the nutrient solution (formulated using tap water) was 0.5 M Ca(NO₃)₂ · 4H₂O, 0.3 M KH₂PO₄, 0.5 M KNO₃, 0.3 M NH₄NO₃, 0.25 M MgSO₄ · 7H₂O and 5µM Fe supplied as Fe-N-hydroxyethylenediaminetriacetate. Plants were grown in environmental chambers at constant 23°C with a 15-hr photoperiod, 80% relative humidity, and a light irradiance of 950 to 1000 µmol m^-2 s^-1 photosynthetic photon flux density (PPFD).

Protocol for Flooding and Light Intensity Treatments, Recovery Periods
Waterlogging and irradiance level treatments were imposed simultaneously in the same environmental chamber. The waterlogging and irradiance level treatments were initiated on plants at three widely divergent developmental stages of growth (each a separate run of the experiment): (i) 8 DAP when the first trifoliolate leaf was exposed, (ii) 21 DAP when four to five branches were present on the main stem, and (iii) 31 DAP immediately after the flowering shoots were clipped to a 3- to 4-cm stubble height with minimal basal residual leaf area remaining. The 8-DAP stage represents plants where most photo-assimilate is utilized for rapid shoot growth while 21-DAP plants exhibit rapid dry matter accumulation in both shoots and roots. Clipped plants (31 DAP) have low levels of photo-assimilate production and exhibit loss of root dry matter due to remobilization of root reserves for shoot regrowth. Because only one environmental chamber was available, separate runs of the experiment were conducted for each developmental stage of growth. The experiment was repeated for each stage of growth, for a total of six runs (two runs for each of three growth stages).

For each stage of growth (each run), plants were subjected to one of two irradiance levels: high irradiance at 950 to 1000 µmol m^-2 s^-1 PPFD and low irradiance at 150 to 200 µmol m^-2 s^-1 PPFD. In comparison, the irradiance level under field conditions at Wooster, OH, (40°47' N) can exceed 1800 µmol m^-2 s^-1 PPFD at full sun in midsummer. Under dense cloud cover, irradiance levels as low as 300 µmol m^-2 s^-1 PPFD may occur. Low irradiance was accomplished by suspending multiple layers of cheese cloth between the light source and the plants in one half of the growth chamber. There were 16 pots under each light regime. Within each irradiance level, flooded and unflooded treatments were imposed (8 pots per treatment). Root waterlogging was initiated by placing the pot in a larger container and adding de-oxygenated water (cooled hot water) until the water level was 1 cm above the media surface. Additional water was added as needed to maintain this level during the course of the experiment. The pots were rotated regularly within each light regime during the course of the experiment. Four pots per treatment combination were harvested for each recovery period.

Table 1 outlines the experimental variables including plant stage, treatment, and harvest variables. A shorter flood duration was necessary for the 31-DAP growth stage since flooding injury was more severe on clipped plants and flooding for 10 d would have likely killed most of the plants. For the 21-DAP growth stage, both flooded and control plants were in late bud or early flower stage of development at the end of the 10-d treatment. Two recovery intervals were utilized after termination of flooding or irradiance treatments: (i) 0-d recovery, with the objective of determining the immediate response to irradiance level and flooding treatments, and (ii) 10-d recovery, with the objective of examining the recovery response after termination of the irradiance and flooding treatments. At the termination of the irradiance and flooding treatments, residual water and nutrient solution was removed from flooded pots using vacuum applied to the bottom of the pot in order to reestablish an aerobic root environment.

Redox Measurement of Flooding Media
A preliminary test was conducted to characterize the hypoxic status of the rooting media at the start of flooding and to verify that the redox of the flooding media declined with time as occurs under field flooding conditions (Gambrell et al., 1991). A single pot with 10 16-d-old plants was flooded in the growth chambers at 23°C and high irradiance. Redox status of the flooding medium was monitored using a platinum electrode referenced to a Ag/AgCl electrode and standardized using a ferrous-ferric solution with potential of +475 mV (Light, 1973). Use of a Ag/AgCl reference electrode yields a somewhat higher standardized potential, +475 mV, relative to a platinum:saturated calomel reference electrode (+435 mV) that has been reported for soil redox measurements (Patrick and Delaune, 1977). Subtracting 40 mV from platinum:Ag/AgCl electrode readings approximates readings with a platinum:saturated calomel sensor. The platinum:Ag/AgCl electrode was placed in the center of the pot 3 cm below the soil surface after which the pot was flooded with deoxygenated tap water. Redox potential (mV) was recorded daily for 7 d with a pH meter. The experiment was repeated twice.

Harvest and Growth Measurement
All harvests were made with plants that were 3 to 4 hr into the light cycle. Shoots were severed from the root at the crown. Roots were gently separated from the growth media by manipulating the roots in water to remove as much media as possible. A stream of water was then directed through the root mass placed on a fine screen. All tissue was quickly frozen and freeze-dried. Dry weight of root and shoot tissue was determined. Root tissue was ground to pass a 30-mesh (openings per 2.54 cm) screen.

Carbohydrate Analysis
Changes in root TNC, along with root dry matter, served to characterize the net effects of flooding and irradiance on tissue energy accumulation and assimilate partitioning. Previous studies by Barta (1987) and Castonguay et al. (1993), have shown that neither concentration of starch nor soluble sugar concentration are related to flooding stress.

Carbohydrate analyses were conducted only on 0-d recovery treatments. Total nonstructural carbohydrates, consisting of soluble sugars plus starch, were extracted from 25 mg of root tissue in 1.5-mL microfuge tubes following the procedure of Li et al. (1996). Starch was gelatinized by adding 0.5 mL water and heating the mixture for 10 min in a boiling water bath. The pH was adjusted to 4.5 by addition of 0.6 mL of 0.1 M Na-acetate buffer. Starch was digested by adding 0.1 mL of a solution containing 0.2 units of amyloglucosidase (Sigma product A3514; Sigma Chemical Co., St. Louis, MO). Tubes were incubated in a shaking incubator at 55°C for 24 h. Tubes were placed in a boiling water bath for 10 min, centrifuged, and the supernatant decanted. Sucrose and residual polysaccharides were hydrolyzed by adding 0.2 mL of 0.2 M sulfuric acid to 0.1 mL of tissue extract and heating in a boiling water bath for 10 min. After neutralization with 0.2 mL 0.4 M sodium hydroxide, samples were analyzed for reducing sugar concentration using the potassium ferricyanide method as described previously (Barta 1979).

Statistical Analysis
Each run of the experiment consisted of a factorial combination of light and flooding treatments with a split-plot restriction on randomization and four replications. Light treatments were considered as whole plots. Flooding and recovery period treatment combinations were assigned as subplots within each run of the experiment. Treatment effects (light level, flooding, recovery period) and their interactions were assessed using ANOVA, with each plant developmental stage (8, 21, and 31 DAP) being analyzed separately. Two runs of the experiment were conducted for each plant stage, resulting in eight observations for each treatment combination. The two runs of the experiment were used as the replication factor for the light treatments since they could not be replicated and randomized within each run (the environmental chamber was divided in half for each light treatment). Thus, experiment x light served as the error term for the main effect of light treatment in the ANOVA. Root and shoot dry weight data were log-transformed to conform with assumptions of normality for ANOVA; however, nontransformed means and standard errors were computed and presented herein. There was no need to log-transform the TNC data prior to ANOVA.

	RESULTS

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The redox at the start of flooding (Fig. 1) was near 335 mV (approximately equivalent to 300 mV with platinum:calomel electrode). Since free oxygen is undetectable when the redox falls below +350 mV (Patrick and DeLaune, 1977), it is apparent that hypoxia was present at the initiation of waterlogging. The rapidly declining redox of the flooded media indicates that facultative anaerobes in the soil:sand matrix were progressively reducing soil compounds similar to that observed in waterlogged soils (Patrick and DeLaune, 1977). After 4 to 5 d of flooding, the redox potential equilibrated in the range of -300 to -400 mV, which coincided with first observations of flooding injury symptoms (leaf chlorosis). These minimum values are somewhat lower those reported by Patrick and Delaune (1977) in coastal wetlands where minimum potentials of -300 mV were reported.

View larger version (12K): [in this window] [in a new window]   Fig. 1. Redox potential of sand:soil (2:1, v:v) medium flooded with deoxygenated water and using platinum:Ag/AgCl electrode. Values (with SE bars) represent means for two trials.

As expected, the effect of flooding and recovery period on shoot and root dry matter accumulation was highly significant across all plant development stages (Table 2) . Irradiance level affected shoot and root dry matter accumulation primarily at 21 DAP, the growth stage with the greatest leaf area and most rapid growth rate. The flooding x irradiance level interaction was significant for all tissues and treatment stages except roots of 31-DAP plants. These interactions are clearly seen in data presented in Tables 3 and 4 where relative changes in shoot and root dry matter accumulation are much greater for plants flooded under high irradiance than those flooded under low irradiance, with the exception of roots of 8- and 31-DAP plants at 0-d recovery.

The response of roots to flooding under the high and low irradiance regimes (Table 4) is similar to what was observed for shoots; that is, relative differences due to flooding were generally greater for plants under high irradiance. Also, absolute differences in flooded root dry matter were minimal between high and low irradiance level treatments. When 31-DAP flooded roots were harvested, many plants had severely rotted roots. No rotted roots were observed for 8- or 21-DAP treatments. Interpretation of 31-DAP root dry matter response at 0-d recovery is complicated since root dry matter normally declines sharply following cutting and initiation of shoot regrowth. However, mean (of high and low irradiance treatments) 31-DAP root dry matter remained constant in flooded 31-DAP plants from 0-d recovery (2.59 g per pot) to 10-d recovery (2.64 g per pot) while both the 8- and 21-DAP treatments increased root dry weight during the same interval, suggesting greater flooding injury in 31-DAP plants. Table 4 also shows that for 8-DAP plants, roots were greatly impacted by flooding at 0-d recovery while shoot dry matter was not affected (Table 3).

Flooding consistently increased TNC concentration in roots of both high and low irradiance level plants, especially in 8-DAP and 21-DAP roots (Table 5) . Irradiance in general had much less effect on TNC accumulation than did flooding. Although most treatments with low irradiance had numerically lower root TNC levels than the corresponding high irradiance treatments, this effect was only statistically significant for the 31-DAP growth stage. The flooding x irradiance interaction for 8- and 21-DAP was due to greater relative increase in TNC in response to flooding under low irradiance than under high irradiance.

	DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

It is apparent that flooded plants were not able to increase growth by utilizing the additional energy potentially available under high irradiance. This is not unexpected since root waterlogging sharply inhibits root growth and function and results in widespread deleterious effects on physiological functions including reduced photosynthesis rate (Castonguay et al., 1993; Wagner and Dreyer, 1997) and partitioning of assimilates to roots (Barta, 1987), nutrient acquisition including reduced uptake and transport to the shoot (Kozlowski and Pallardy, 1984), and higher levels of shoot abscisic acid which induces stomotal closing (Castonguay et al., 1993).

In these studies, irradiance level served as a physiological tool to modify carbohydrate flux to root apical regions. If adequate and continued supply of carbohydrate to root apical regions is critical to tissue under hypoxia, as postulated by Drew (1997), photo-assimilate deficiency might be expected to have some effect on flooding injury. The data in this study suggests that photo-assimilate supply to flooded roots does not significantly impact flooding injury response. Root dry matter accumulation under 10-d hypoxia was reduced but not halted in this study (data not shown) or in similar studies reported by Castonguay et al. (1993) and Teutsch et al. (1997). This result indicates that assimilates are moving to apical roots under hypoxia and, in this study, at a level related to irradiance level. Low irradiance subjects roots to severe carbon deficiency as evidenced by the lower dry matter accumulation and the sharply reduced TNC found in control roots. The fact that severe carbon deprivation caused by low irradiance did not have a significant effect on flooding injury reinforces previous conclusions by Barta (1987) and Castonguay et al. (1993) that carbohydrate utilization in hypoxic alfalfa roots may be more limiting than available carbohydrate supply.

The significant interaction of irradiance and flooding injury, especially in midvegetative plants (21-DAP), suggests caution when interpreting flooding studies of alfalfa and possibly other species. Plants flooded under low irradiance levels may respond differently when data are expressed relative to the low irradiance control than they would when flooded at higher irradiance levels. For example, in an alfalfa flooding study with mid-vegetative stage plants, Castonguay et al. (1993) reported no reduction in shoot dry matter accumulation after 10-d flooding, which is in contrast to results found in this study. This discrepancy may be due in part to the fact that plants in their study were flooded under 250 µmol m^-2 s^-1 PPFD, which is similar to the low irradiance level used in this study. Possibly the lack of shoot injury after 10-d flooding may have been in part due to low irradiance level used during treatment.

Because higher temperature of flooded soil increases rate of injury (Erwin et al. 1959; Cameron 1973), high irradiance could affect flooding damage by increasing the temperature of the flooding media. Measurements we made in flooded pots at various times of the day cycle (data not shown) indicated that the medium in high irradiance flooded pots was 3°C higher during the light period (3 to 4 cm below the medium surface) than the medium under low irradiance. While this temperature differential was not great, it may have contributed to the greater relative flooding injury under high light treatment.

This study provides additional support for the observation that clipping and flooding stress are synergic and result in severe plant injury (Cameron 1973; Rai et al., 1971; Cameron 1973; Zook et al., 1986). Teutsch and Sulc (1997) reported that vegetatively advanced plants were less susceptible to flooding injury than were younger seedling plants, while Fick et al. (1988) suggested that sensitivity of alfalfa to flooding stress increases up to 6 wk of age. Discerning which of these scenarios is most likely using the flooding response data at the 8- and 21-DAP stages is difficult. While shoot dry matter data at 0-d recovery (Table 2) suggested 21-DAP plants are more susceptible to injury, especially under high irradiance; results for 10-d recovery shoot dry matter indicated no difference between growth stages. Root dry matter response to flooding at the 8- and 21-DAP treatments is also inconsistent. At 0-d recovery, high irradiance resulted in greater injury in 21-DAP plants while under low irradiance, greater injury was observed in 8-DAP plants. In general, differences in flooding sensitivity between 8- and 21-DAP plants were minimal when shoot or root dry matter was measured 10 d after termination of flooding.

Finally, the results show that inducing and quantifying flooding damage is dependent on multiple factors, including irradiance level, the tissue measured, when plants are harvested after treatment, and what controls are used for evaluating treatment effects. Thus, it is important to fully define the experimental protocol when interpreting and expressing flooding injury results, especially in studies using seedling plants. A suggested protocol for evaluating flooding stress might include growth and flooding treatments at high irradiance levels to insure maximum plant dry matter accumulation rates and to utilize a defined recovery period for allowing latent tissue injury to be expressed.

	ACKNOWLEDGMENTS

 
The authors wish to acknowledge the technical assistance of Ms. Melanie Ogle for analysis of root carbohydrate concentration. We also thank Bert Bishop for his assistance with data analysis.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Salaries and research support provided by State and Federal Funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State Univ.

Received for publication October 8, 2001.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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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 Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (1) Citing Articles via Google Scholar Google Scholar Articles by Barta, A. L. Articles by Sulc, R. M. Search for Related Content PubMed Articles by Barta, A. L. Articles by Sulc, R. M. Agricola Articles by Barta, A. L. Articles by Sulc, R. M. Related Collections Crop Growth and Development Crop Physiology & Metabolism