Published in Agron J 99:88-98 (2007)
DOI: 10.2134/agronj2006.0128
© 2007 American Society of Agronomy
677 S. Segoe Rd., Madison, WI 53711 USA
Wheat
Hard Red Winter Wheat Cultivar Responses to a pH and Aluminum Concentration Gradient
S. K. Kariukia,
H. Zhanga,*,
J. L. Schrodera,
J. Edwardsa,
M. Paytonb,
B. F. Carvera,
W. R. Rauna and
E. G. Krenzera
a Dep. of Plant and Soil Sciences, Oklahoma State Univ., Stillwater, OK 74078
b Dep. of Statistics, Oklahoma State Univ., Stillwater, OK 74078
* Corresponding author (hailin.zhang{at}okstate.edu)
Received for publication April 24, 2006.
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ABSTRACT
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Aluminum (Al) toxicity is a major yield-limiting factor in winter wheat production in many parts of the world. The use of Al-tolerant cultivars reduces the impact of this problem and is common to the southern Great Plains where wheat is managed as a dual-purpose crop. However, no quantitative data exist on the Al tolerance ranking of winter wheat cultivars often grown in a dual-purpose management system. This study was established to classify on a field scale the Al tolerance of common winter wheat cultivars (Ok101, Ok102, 2137, 2174, Jagger, Jagalene, Custer, and AP502CL). Fall forage yield of each cultivar was harvested by hand clipping. Soil samples were collected at the same time and analyzed for pH and Al saturation (Alsat). Grain was hand-harvested in June of each year from the same rows harvested for forage. Cultivar differences (P < 0.1) were found in forage and grain yields for the Alsat > 30% range. Al tolerance based on grain yield ranked as follows: 2137 > Jagalene = Ok101 > Jagger = 2174 
Ok102 > Custer = AP502CL. Al tolerance based on forage yield ranking was similar to that of grain: 2137 > Ok101 = Jagalene = Jagger > 2174 = Ok102 > Custer = AP502CL. Grain yield seemed to be less affected by Alsat than forage yields. The use of Al-tolerant winter wheat cultivars may minimize producers' risk of crop loss; therefore, this ranking of Al tolerance should help winter wheat producers make informed decisions if they have acid soils with high Al content and no other remedies available.
Abbreviations: AlKCl, KCl extractable aluminum • Alsat, aluminum saturation • ECEC, effective cation exchange capacity
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INTRODUCTION
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WHEAT is a major commodity in Oklahoma, where 49% of the total acreage is produced with dual-purpose intentions (Hossain et al., 2004), whereby forage is grazed in fall and winter, cattle are removed at or near first hollow stem, and the grain is harvested in the summer. This practice has been successful in diversifying producers' income in spite of significant amount of wheat acreage having been planted in strongly acidic (pH < 5.0) to moderately acidic (pH 5.0–6.0) soils.
Soil acidity, with a resultant elevation in available soil Al concentration, has been a major cause of crop failure in central and western Oklahoma (Zhang and Raun, 2006). There are several causes of soil acidity: The nitrification process, organic matter decomposition, and acid rain contribute to increased soil acidity (Prasad and Power, 1997; Sparks, 2003). Intensive and continuous crop production accelerates the acidification of soil because the conversion of ammonium-based N fertilizer sources to nitrate causes a net H+ release, which lowers the soil pH in the plant rooting zone (Tang, 2004; Garvin and Carver, 2003; Prasad and Power, 1997). A survey conducted in 1996 revealed that over 35% of the total wheat production acreage in Oklahoma was planted in soils with a pH less than 5.5 (Zhang et al., 1998). There is no evidence that this level of soil acidity has changed since.
Potassium chloride–extracted Al and Al saturation (Alsat) have an inverse relationship with pH (Chartres et al., 1990; Evans and Kamprath, 1970). Increased soil acidity causes solubilization of Al, which is the primary source of toxicity to plants at pH below 5.5 (Bohn et al., 2001; Ernani et al., 2002; Parker et al., 1989). Aluminum chemistry varies with soil pH, but only the soluble ions such as Al3+, which exists between pH 4.7 and 6.5, are toxic to plants. When Al3+ concentration is high relative to the basic cations, Alsat percentage increases. If the soil is not corrected for acidity and remains at high concentrations of toxic Al ions, then poor stand establishment and growth for vulnerable crop species and/or cultivars may result, a condition referred to as Al toxicity.
Crops grown in soils with acceptable levels of basic cations may not show Al toxicity symptoms even when the levels of KCl-extractable Al are considered high. Therefore, the mere presence of Al in the soil is not an indicator of Al toxicity (Johnson et al., 1997). A more reliable measure of the potential for Al toxicity is Alsat, which is the Al concentration (commonly measured in 1.0 M KCl extraction) expressed as a percentage of exchangeable cations (i.e., Ca, Mg, K, and Na) (Sumner and Miller, 1996).
Liming is the most widely used long-term method of soil acidity amelioration, and its success is well documented (Haynes, 1982; Conyers et al., 1991; Scott et al., 2001; Zhang et al., 2004; Kaitibie et al., 2002). In Oklahoma, lime is recommended for continuous wheat producers in low-pH soils (Zhang and Raun, 2006). However, the use of lime is not without limitations. Among these are that liming does not always increase yields. For instance, Boman et al. (1993) found no difference between limed and nonlimed plots even when compared in the same low-pH soil. Other reasons why some producers are reluctant to use lime in ameliorating soil acidity are the economics of lime application (Ruiz-Torres et al., 1992) and disease pressure in heavily limed soils (Garvin and Carver, 2003).
The use of Al-tolerant cultivars to ameliorate the effects of Al toxicity has been a successful alternative to liming in winter wheat production (Johnson et al., 1997; Delhaize et al., 2004). Plant Al tolerance has been associated with the ability to exude organic anions such as citrate and malate, which may complex Al and reduce its negative effects on the plant (Yang et al., 2004; Blamey et al., 1997; Tang et al., 2002; Zheng et al., 2004). Plant uptake of P, K, N, Ca, Mg, and other essential nutrients decreases with increased Al levels in a plant (Lidon et al., 2000) due to inhibition of root elongation in low-pH soils (Kochian 1995). Although an Al-tolerant plant is capable of taking up these nutrients in the presence of elevated levels of Al in the root zone, Al-tolerant cultivars grow best at Alsat levels less than 12% (Johnson et al., 1997). Aluminum saturation ranging from 15 to 30% was found to cause a 98% loss in winter wheat forage yield and a grain-crop failure (Wise, 2002).
One method of assessing wheat tolerance to elevated levels of Al is to measure root development of plants grown in different concentrations of Al (Bolt, 1996). The degree of Al tolerance varies not only from crop to crop but also from cultivar to cultivar within a crop. Plant breeders have developed and recommended several Al-tolerant wheat cultivars (Tang et al., 2002) based on their degree of tolerance, primarily in nutrient-solution culture. There are, however, insufficient quantitative data on how these cultivars compare for Al tolerance under actual field conditions.
Carver et al. (2003) used an experimental site with a uniform low pH of 4.2 and a limed control site in their study to compare and rank winter wheat cultivar tolerance to Al toxicity. However, the use of a site with only extreme pH levels may limit the possibility of optimizing pH for a given genotype because it restricts the range of the pH necessary to obtain a threshold. Testing in a site with a pH gradient, varying from very strongly acidic to slightly acidic soil, would provide information useful to quantitatively rank cultivars across a pH range. Such information is vital in guiding wheat producers in choosing appropriate cultivars suitable for acid conditions. Johnson et al. (1997) found cultivar differences in grain and forage yield under low pH soil conditions; however, this conclusion was not consistent across environments. The objective of this study was to examine and quantitatively rank the acid-soil Al tolerance of common winter wheat cultivars grown in the Southern Great Plains of the United States based on forage and/or grain production potential.
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MATERIALS AND METHODS
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Experimental Site Establishment and Treatment Application
The experiment was established in the spring of 2003 at a low and variable pH site at Perkins, Oklahoma (35.99°N, 97.04°W), in Konawa (fine-loamy, mixed, thermic ultic haplustalfs) soil series. Initial soil samples indicated a preexisting pH gradient of 4.2 to 5.3 distributed in several parts of the field. To help us understand the spatial pH variability of the site, "Custer," a winter wheat cultivar known for its susceptibility to low-pH soils, was planted as a test crop. At Feekes 5 (Nelson et al., 1988) growth stage, a vegetation-greenness map derived from normalized difference vegetation index data was used to delineate growth variability and was verified with soil pH tests. With this information, the experiment was established across the pH gradient in a complete randomized design with three replications measuring 12 by 6 m. In each replication, the soil-pH gradient was identified and augmented by liming at 2500 kg ha–1 effective calcium carbonate equivalent 6 mo before planting at the high pH end of the gradient to extend the preexisting pH range. Lime was incorporated by rotor tilling. Each replication was tested for pH immediately before planting to assess the range of the new pH gradient (Fig. 1
), which was found to vary from 4.2 to 6.5. The gradient for the second year of the study was confirmed by soil testing.
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Fig. 1. Field configuration illustrating cultivar growth differences (left to right) along the pH gradient (bottom to top). The smaller arrows points to eight different cultivars; the big arrow points to the direction of soil pH increase.
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Eight commonly grown hard red wheat cultivars in the Southern Plains (Ok101, Ok102, 2137, 2174, Jagger, Jagalene, Custer, and AP502CL) were seeded in rows 15 cm apart side-by-side along the 4.2 to 6.5 pH gradient path (Fig. 1). Planting occurred in early September 2003 and 2004 at a rate of 110 kg ha–1, using an eight-row drill. Four rows per cultivar of two different randomly selected cultivars were created in one drill strip during the initial planting. For 2004, cultivars were not randomized but were planted into the same plot area. This is typical of land management practices in Oklahoma where winter wheat is often grown continuously (Kaitibie et al., 2002; Stone et al., 2006).
Plant Harvest
Wheat forage was harvested in mid-December 2003 and 2004. For each cultivar and within each block, plants were sampled by hand-clipping the two center rows to the ground along the pH gradient at a spacing of 2.0 m (Fig. 1). Thus, six plant samples per cultivar per replicate per year for a total of 288 forage samples were collected. The unclipped forage was mowed to homogenize the experimental site. Forage was oven-dried for 3 d at 105°C before measuring dry weight.
Grain was hand harvested in June 2004 and June 2005 from the same rows where forage was hand clipped at the same spacing as described for forage (Fig. 1). Each sample was bagged and stored to air dry and manually threshed after 14 d. Weight measurements were determined, and data were analyzed.
Soil Sampling and Analysis
Soil samples were collected in 2003 and 2004 at the same spacing as described for plant samples. Six soil samples per cultivar per replicate per year for a total of 288 samples were taken at a depth of 15 cm for every cultivar along the same pH gradient where forage was sampled (Fig. 1). Each sample was a composite of 10 cores that were taken in the area of the two center rows that were harvested for forage and grain. Soil samples were oven-dried at 65°C for 24 h and ground to pass a 2-mm sieve (SERA-IEG-6, 2001).
A routine soil analysis for N, P, and K was made to determine fertility needs for the crop. Soil pH was measured in a 1:1 soil/water ratio using a combination pH electrode (Thomas, 1996). Levels of extractable cations (Ca, Mg, K, and Na) were determined according to the method of Sumner and Miller (1996). Soil (2.5 g) was mixed with 25 mL of 1 M NH4OAc at pH 7.0. Extractable Al was measured using the Bertsch and Bloom (1996) method, whereby 5.0 g of soil was mixed with 25 mL of 1.0 M KCl. Aluminum, Na, K, Mg, and Ca in the extracts were analyzed by inductively coupled plasma–atomic emission spectroscopy. Effective cation exchange capacity (ECEC) was determined using the equation by Sumner and Miller (1996):
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Alsat was calculated using the following equation:
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Data Analysis
Soil and plant data were analyzed using PC SAS Version 9.2 (SAS Institute, 2001). The Levene's test was performed for each cultivar to determine homogeneity of variance for the 2 yr of data. Because the variances within each cultivar were homogeneous, the data from the 2 yr were combined for statistical analysis. To discriminate the cultivar soil-acidity tolerance, ANOVA procedures were used with PROC MIXED. To separate the means, a DIFF option in an LSMEANS statement was used. Regression analyses were performed using PROC REG to determine cultivar sensitivity to soil acidity, and slopes associated with the cultivars were compared using indicator variables (Eq. [3]).
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where X = Al saturation or pH and DV = indicator or dummy variable for pairwise comparison of cultivars.
Linear-plateau models, performed with PROC NLIN, were used to obtain the threshold pH for each cultivar (Eq. [4]).
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where 
= plateau (level of pH in which yield fails to increase).
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RESULTS AND DISCUSSION
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Relationships between Soil pH and Extractable Aluminum and Aluminum Saturation
Soil pH varied from 4.2 to 6.5, whereas 1 M KCl extractable Al (AlKCl) and Alsat varied from 0 to 159 mg kg–1 and from 0 to 70%, respectively (Fig. 2
and 3
). A significant inverse exponential relationship (P < 0.001; r2 = 0.92) existed between AlKCl and soil pH (Fig. 2). At pH below 5.5, a slight change in pH resulted in a dramatic change in Al. For example, a pH increase from 5.0 to 5.5 decreased AlKCl from 60 to 20 mg kg–1. In contrast, a pH increase from 5.5 to 6.0 caused relatively small decrease in AlKCl from 20 to 4.5 mg kg–1.
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Fig. 2. Relationship between Al concentration (1.0 M KCl extraction) and pH for a Konawa soil at Perkins, OK. *** P < 0.001.
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Fig. 3. Relationship between percent Al saturation (Alsat%) and soil pH for a Konawa soil at Perkins, OK. *** P < 0.001.
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Similarly, a significant inverse exponential relationship (P < 0.001; r2 = 0.89) existed between Alsat and pH (Fig. 3). Comparable to the Al–pH relationship, changes in Alsat were more pronounced at lower than higher pH. An increase in pH from 5.5 to 6.0 resulted in an estimated decrease in Alsat from only 7.3 to 2.2%, compared with a pH increase from 5.0 to 5.5, which caused an estimated decrease in Alsat from 23.5 to 7.3%. Al solubilizes in low pH conditions and is precipitated at high pH by OH–. The higher the soil acidity, the higher the level of Al solubilization, giving rise to increased Alsat. These findings were in agreement with previous studies by Chartres et al. (1990) and Evans and Kamprath (1970).
A relationship was found between threshold pH, a point beyond which further pH increase resulted in no increase in yield, and the level of Al tolerance. This supports the strong correlation between Alsat and pH (Fig. 3). In general, cultivars with higher Al tolerance exhibited tolerance to lower threshold pH than those less tolerant to high Al concentrations (Table 1) and were more vulnerable to Alsat > 30% (Table 2). This means that in comparison to the less Al tolerant cultivars, more tolerant cultivars can maximize their yields in soils otherwise considered too acidic for winter wheat production (Zhang and Raun, 2006).
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Table 1. Slopes and coefficients of determination (r2) for the relationship between grain or forage yield and aluminum saturation (Alsat) (combined data for 2 yr).
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Table 2. Cultivar comparisons for mean grain and forage yield (kg ha–1) (combined data for 2 yr) at aluminum saturation (Alsat) > 30% and Alsat < 30%.
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Cultivar Sensitivity to Changes in Aluminum Saturation
The linear responses to Alsat differed among cultivars; therefore, the magnitude of the slope was used to explain differences in cultivar sensitivity to Alsat. In grain and forage data, cultivars with greater slope (absolute value) were considered more sensitive to changes in Alsat, an implication of poor Al tolerance. For example, two extreme cultivars in Al sensitivity, AP502CL and 2137, recorded slopes of –38.7 and –10.8 kg ha–1 grain Alsat–1, respectively (Fig. 4
). This was interpreted to mean that 2137 was more Al tolerant than AP502CL because a 1% increase in Alsat caused only a 10.8 kg ha–1 grain yield decrease for 2137 but a 38.7 kg ha–1 yield decrease for AP502CL (Table 1). The Alsat response for forage yields produced a narrower range of slope values than those for grain yield. Jagger, one of the most Al-tolerant cultivars, had a slope of –21.1 kg ha–1 compared with –40.4 kg ha–1 of 2174, a low–Al-tolerant cultivar (Table 1, Fig. 5
).
Ranking Winter Wheat Cultivars for Aluminum Tolerance
All eight wheat cultivars showed an inverse linear relationship between yield (grain or forage) and Alsat (Table 1), an implication that none of them was absolutely tolerant to Al toxicity. A regression analysis between yields and Alsat indicated greater cultivar variability in yields at Alsat > 30% than with the entire Alsat range. Because of the severe toxicity associated with Alsat > 30%, yield differences were driven by cultivar Al tolerance and not by cultivar yield potential in an environment free of Al stress.
There were highly significant differences (P < 0.001) between yields at Alsat > 30% and Alsat < 30% for all cultivars (Table 2). Cultivars with greater tolerance showed smaller differences between yields at Alsat > 30% versus Alsat < 30%. With tolerant cultivars, a large reduction in soil acidity resulted in only a slight increase in yields. For example, the percentage grain yield increase from Alsat > 30% to Alsat < 30% was 34% for Jagalene, one of the most Al-tolerant cultivars, as compared with approximately 3200% for AP502CL, one of the least Al-tolerant cultivars (Table 2). Similar comparison could be made for forage yield. Where there was only a 81% increase in Jagalene forage yield between Alsat > 30% and Alsat < 30%, AP502CL recorded an increase of about 1200% (Table 2). This qualified the use of mean cultivar yields in this Alsat range (>30%) to discriminate (P = 0.1) and further rank cultivars (Table 2). A cultivar producing relatively high yields in the presence of severe Al toxicity was considered Al tolerant. For example, where 2137 yielded an average of 1972 kg ha–1 of grain, AP502CL yield was only 44 kg ha–1. Similarly, 2137 yielded 1236 kg ha–1 forage versus 95 kg ha–1 by AP502CL. Hence, 2137 is much more Al tolerant than AP502CL.
The grain response to Al tolerance cultivar ranking agrees somewhat with the qualitative ranking by Krenzer et al. (2004) (Table 3) in that Ok101, Jagger, Jagalene, and 2137 were the most Al tolerant (Table 2). However, our analysis provided improved discrimination among 2137, Jagalene, Ok101, and Jagger. According to previous ratings, all four cultivars were considered to have the same Al tolerance (Krenzer et al., 2004) (Table 3). The cultivars 2174 and Ok102, and then Custer and AP502CL, exhibited their inferiority in the Al toxic environment as previously documented. The order of grained-based Al tolerance was as follows: 2137 > Jagalene = Ok101 > Jagger = 2174 Ok102 > Custer = AP502CL. The ranking (comparison at Alsat > 30%) corresponded with cultivar sensitivity to Alsat analysis (Table 1), whereby the more sensitive to Alsat a cultivar was, the less Al tolerant it was found to be. The grain yield for 2174 (809 kg ha–1) was not different from that of Ok102 (718 kg ha–1) or from Jagger (1039 kg ha–1) at (P > 0.1), even though Jagger's yield was greater (P < 0.1) than Ok102. This was the basis for using the greater-than-or-equal-to sign between 2174 and Ok102.
Forage-based rankings were similar to grain-based rankings and agreed well with Krenzer et al. (2004) in that, except for Jagger, which showed the same Al tolerance as Jagalene, and Ok101, all the cultivars displayed the same tolerance as grain based as follows: 2137 > Ok101 = Jagalene = Jagger > 2174 = Ok102 > Custer = AP502CL. The cultivar 2137 was exclusively the most Al tolerant, with Ok101, Jagalene, and Jagger placing second.
Unlike the grain-based ratings, there was no apparent association for forage yield between Al sensitivity at >30% Alsat and rankings for Al tolerance based on slopes. This was attributed to the fact that forage was affected more by severe Al toxicity (Alsat > 30%) than grain. At Alsat > 30%, forage yield was found to be constantly close to zero in the less tolerant cultivars, such as AP502CL, which decreased the slope, making it appear as if it was not sensitive (Fig. 4).
Impact of Soil Acidity on Grain and Forage Yields
Grain and forage yields responded to changes in soil acidity but at different magnitudes. A mean slope of –25 kg ha–1 Alsat–1 obtained for grain was significantly less (P < 0.1) than –31 kg ha–1 Alsat–1 for forage (Table 1). Likewise, threshold pH was found to be cultivar dependent (Table 1). This was in contrast with a pH of 5.5 previously reported as the ideal pH for wheat production (Bohn et al., 2001; Ernani et al., 2002). At a range of 5.3 to 6.6, threshold pH for grain was more variable among cultivars than for forage, where it ranged between 6.2 and 6.6 (Table 1). Forage yield in most of the cultivars failed to plateau within the pH range of the experimental site (Fig. 6
), which may imply that forage requires a higher pH than is available at the site to generate a plateau response. This was not the case with grain data, where most of the cultivars generated plateaus (Fig. 7
).
The mean percentage grain yield increase (82%) between Alsat < 30% and Alsat > 30% was lower than that for forage yield (159%) (Table 2). Overall, it seems that forage yield in winter wheat is affected more by Al toxicity than grain yield. This could be related to the difference in expected nutrient demand at different stages of growth. Most essential nutrients and water are needed during the vegetative stage, and Al interferes with the uptake of these nutrients; therefore, the younger the plant, the more vulnerable it is to Al toxicity. For example, magnesium, whose uptake decreases in the presence of Al (Lidon et al., 2000), links the ATP molecule to the active site of the enzyme (Hopkins, 1999). However, during flowering and subsequent grain-filling, less mineral nutrients are needed (Stichler and McFarland, 2001) or may be taken up, reducing the impact of Al toxicity. Another possible reason that forage is affected more by Al toxicity than grain is that much of the fall forage growth occurs before the root system is fully developed. Many of theses soils have depressed soil pH near the surface where acid conditions have been induced by fertilizer application, but adequate pH for normal plant growth exists deeper in the soil profile. Because grain yield components are determined later in the season, they may be less affected by Al toxicity due to an expanded and deeper root system.
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CONCLUSIONS
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Overall, the increase in pH resulted in significant increases in forage and grain yields. Differences were found in cultivar response to changes in pH and Al saturation. These differences, which were the basis for ranking the cultivars for Al tolerance, revealed that grain-based ranking was similar to that in the literature, where 2137, Jagalene, Ok101, and Jagger, in that order, were the most Al tolerant. The cultivars 2174 and Ok102 had moderate tolerance, whereas Custer and AP502CL ranked the lowest. Although limited data existed previously on forage-based Al tolerance ranking, our study revealed similarities with grain-based ranking. Forage yield was found to be affected more severely by Al toxicity than grain yield.
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