Soil Science Society of America Journal 65:1448-1454 (2001)
© 2001 Soil Science Society of America
DIVISION S-4 - SOIL FERTILITY & PLANT NUTRITION
A Chloride Deficient Leaf Spot of Durum Wheat
R. E. Engel*,
L. Bruebaker and
T. J. Emborg
Dep. Land Resources and Environmental Sci., Montana State Univ., Bozeman, MT 59717-3120
* Corresponding author (engel{at}montana.edu)
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ABSTRACT
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A leaf spot complex of ‘WB881’ durum (Triticum turgidum L. var. durum), similar to symptoms observed in winter wheat (Triticum aestivum L), was greatly suppressed by Cl at a field site in Montana. The objectives were to determine: (i) if this leaf spot phenomenon could be reproduced under hydroponics; (ii) the effect of Cl on leaf spot severity, water use, and plant growth; (iii) whether Br could substitute for Cl; and (iv) whether other durum cultivars were susceptible to leaf spotting under Cl deficiency. WB881 durum was grown at four halide (Cl and Br) levels of 1.5, 3.0, 6.0, and 30.0 mmole pot-1, plus a control. Three cultivars (WB881, Kyle, and Monroe) were grown at Cl levels of 0, 1.2, and 24.0 mmole pot-1. Withholding Cl from starter and refill solutions reproduced leaf spotting in WB881 similar to symptoms observed in the field. Leaf spotting was suppressed by Cl up to the 30.0 mmole pot-1 dose, but was aggravated by Br. Plant water use increased with Cl up to the 30.0 mmole pot-1 dose and was related to the beneficial effect of Cl in suppressing tissue necrosis. Leaf spot severity was closely related to shoot Cl concentration. Tissue necrosis was minor if Cl concentration was 
1.0 g kg-1, but increased exponentially below this level. Withholding Cl from the hydroponic cultures reduced shoot and grain yield 58.2 and 98.9%, respectively. Bromide did not substitute for Cl by improving shoot and grain yield. Monroe was less susceptible to this Cl-deficient leaf spot than was WB881 or Kyle. Cultivar susceptibility or tolerance to leaf spotting could not be explained by differences in Cl partitioning within the plant (e.g., roots, shoots, leaves).
Abbreviations: df, degrees of freedom • FGS, Feekes growth stage
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INTRODUCTION
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A PECULIAR LEAF SPOT COMPLEX that results in tissue necrosis and yield losses has been present in wheat fields of the Pacific Northwest and Great Plains for decades (Chester, 1944; Atkinson and Grant, 1967; Smiley et al., 1993a,b). Smiley et al. (1993a) have described leaf spot appearance and symptom progression. Until recently, the cause of this leaf spot complex has been unknown. Historically, plant pathologists and breeders have referred to this phenomenon as a physiological leaf spot of wheat (Wiese, 1977, p. 93) because it was presumed to result from an unknown metabolic process, or genetic dysfunction, rather than an infectious pathogen. Recent investigations in Montana (Engel et al., 1994; Engel et al., 1997) have revealed this nonpathogenic leaf spot complex results from inadequate Cl nutrition. The name Cl-deficient leaf spot syndrome of wheat has been proposed to describe this phenomenon. This proposal was based on the following considerations: (i) the leaf spot problem was associated with soils testing <1 mg kg-1 Cl (0–60 cm); (ii) Cl fertilization prevented or eliminated leaf spot symptoms in cultivars which were susceptible to this phenomenon; and (iii) the strong relationship between leaf spot severity (portion of leaves affected by chlorotic and necrotic lesions) and plant Cl concentration. Leaf spot damage in susceptible winter wheat cultivars was minimal at or above 1.0 g kg-1 plant Cl. Leaf spot damage increased exponentially as plant Cl levels dropped below a 1.0 g kg-1 threshold level.
Recent investigations of Cl-deficient leaf spot syndrome have dealt solely with winter wheat (Engel et al., 1994; Engel et al., 1997; Smiley et al., 1993a,b). Other species of cereal grains may be affected. In a 1994 field investigation, we observed a leaf spot phenomenon in WB881 durum that resembled the complex described for winter wheat (Engel et al., 1997). Lesion numbers and percentage of tissue damage were greatly suppressed by Cl fertilization at this site. For these reasons, experiments under controlled growth room conditions were initiated to learn more about the origin of the leaf spotting in this durum cultivar. The objectives were to determine: (i) if the lesion symptoms observed at this field site could be reproduced under hydroponics culture by depriving plants of Cl; (ii) the effect of Cl nutrition on leaf spot severity, water use, and plant growth; (iii) whether Br could substitute for Cl by suppressing lesions and increasing plant growth; and (iv) whether other cultivars of durum might be affected by leaf spotting under Cl deficient conditions. This article summarizes the results from our initial field experiment and reports on the outcome of studies conducted in a plant growth room (objective i–iv).
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MATERIALS AND METHODS
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Field Experiment
Durum wheat (cv. WB881) was seeded on 13 Apr. 1994 at a field site 
35 km north of Poplar, MT. The soil, William silt, fine-loamy mixed (Typic Agriboroll) contained 0.63, 0.71, and 0.58 mg kg-1 Cl in the 0- to 30-, 30- to 60-, and 60- to 90-cm depth layers and was located adjacent to a spring wheat study described earlier (Exp. 23, 24: Engel et al., 1998). Treatments consisted of a 0 (control) and 45 kg ha-1 Cl fertilizer rate replicated five times in a randomized complete block. Fertilizer KCl was used as the Cl source. Fertilizer K2SO4 was applied to the control treatment to maintain a constant rate of K. Variable S rates that resulted from using K2SO4 were not deemed important because of high levels of indigenous soil SO4. Durum was seeded in rows spaced 15-cm apart and at a rate of 250 pure-live seeds m-2. Individual plots were 180-cm wide and 9 m long. Whole plant samples (aboveground tissue including stems, leaves, and heads) or plant shoots were collected (60 cm of row) at head emergence or Feekes growth stage (FGS) 10 to 10.3 (Large, 1954). Plant samples were oven dried at 70°C before grinding for chemical analyses. Leaf spot severity (percentage of tissue affected by chlorotic and necrotic lesions) was estimated in the flag and flag-1 leaf blades at the watery-ripe stage (FGS 10.5.4). A small-plot combine was used to harvest the eight-center rows of each plot. (9–10 m2 area) for grain yield estimates. Mature kernel weights were based on counts of 500 kernels from subsamples of grain collected at harvest.
Growth Room Experiments
Experiment I—Halide Dose Study with WB881 Durum
Durum plants were grown in nutrient solution in a controlled environmental growth room (2.7 by 3.7 m). Seeds were germinated in small flats containing a perlite and vermiculite mix. Seedlings were transplanted to 15-L pots at the one-leaf stage. The experimental treatments consisted of a control (no halide salts applied), plus a factorial combination of two halide ions (Cl and Br) and four halide levels (1.5, 3.0, 6.0, and 30.0 mmol total pot-1). All treatments were replicated three times. Treatments were arranged as a randomized complete block design. Each block of treatments was placed under a separate bank of lights that contained a 3:1 ratio of Cool White and Gro-Lux fluorescent lamps(GTE Products Corp., Dancers, MA). A photosynthetic flux of 360 µmol m-1 s-1 was measured at the tops of pots with a LI-COR model LI-185 quantum meter (Apogee Instruments, Logan, UT). The photoperiod was 16 h with a temperature of 24°C during the day and 17°C during the night. Initially each pot contained four plants. The pots were thinned to the three most uniform plants at late tillering (FGS 5). One plant was removed at early head emergence (FGS 10–10.1) and separated into stems and leaves for plant tissue analyses. The remaining two plants were allowed to grow to physiologic maturity (FGS 11.3).
Nutrient solutions (starter and refill) were similar to the system described by Bugbee (1995), except as noted below. Starter solutions and refill solutions up to jointing received N (100% NO3) as CaNO3 · 2H2O and KNO3. Thereafter, NH4SO4 was added with CaNO3 · 2H2O and KNO3 in sufficient quantity to the refill solutions such that 25 and 75% of the N equivalents added were NH4 and NO3, respectively. Manganese sulfate was substituted for MnCl2. Silicon was added to all nutrient mediums as suggested by Epstein (1994). Growth mediums were buffered with 1 mM 2-(N-morpholino) ethanesufonic acid (MES) to stabilize pH (Bugbee and Salisbury, 1985). Solution pHs were adjusted to 5.7 with 1 M HNO3 or 1 M KOH immediately after refills solutions were added. Stock solutions of 1 M KCl and 1 M KBr were used to produce the appropriate halide level. Halide salts were added in five equal increments spaced over an 8-wk period. Applications were made at the two-leaf stage, tiller (FGS 3), late tillering to joint (FGS 5–6), flag leaf to boot (FGS 9–10), and flowering (FGS 10.5.1), or 4, 20, 33, 48, and 61 d posttransplanting, respectively. All starter and refill solutions were prepared using deionized water (<0.6 µS cm-1). Refill solutions were weighed with a platform scale to estimate plant water use.
The fraction of flag and flag-1 leaves affected by chlorotic and necrotic lesions was estimated for each pot. The estimates for the two leaves were averaged to give the leaf spot severity score for a treatment. Severity estimates were made at boot-head emergence (FGS 10–10.1), flowering (FGS 10.5.1–10.5.4), watery-ripe (FGS 11.1), and milk-soft dough (FGS 11.2) stages; or 53, 61, 68, and 89 d posttransplanting, respectively. All plant tissue samples collected were dried in an oven (70°C) prior to weighing and grinding. Plants harvested at physiologic maturity (2 pot-1) were separated into root and shoot material. Root material was rinsed with deionized water prior to placing in the oven. After drying, heads were clipped from the shoots and hand-threshed to determine grain yield and kernel weights.
Experiment II—Durum Cultivar Comparison
Durum plants were started in flats and transplanted to hydroponics pots as described under Exp. I. The growth room characteristics (temperature, day length, light, and dimensions) and starter and refill formulas were similar to Exp. I, except that starter solutions and all refill solutions additions received 25 and 75% of the N equivalents as NH4 (NH4SO4) and NO3. The experimental treatments consisted of three durum cultivars (Kyle, Monroe, and WB881) grown at three Cl-dose levels (0, 1.2, and 24.0 mmol pot-1). All treatments were replicated three times. Treatments were arranged as a randomized complete block design with a split-plot arrangement with cultivar main-plot and Cl-dose subplots. Pots were thinned to three plants at the late tillering to joint stage. One plant was removed for plant tissue analyses at the boot stage. The remaining two plants were harvested at the kernel watery-ripe stage (FGS 10.5.4) or 10 d postflower initiation. All harvested plant material was processed in a manner consistent with Exp. I prior to weighing and grinding. Leaf spot severity readings were estimated at the final harvest. Severity scores were based on the fraction of the upper two leaf blades (flag and flag-1) affected by chlorotic and necrotic lesions in the two plants harvested at FGS 10.5.4.
Plant Chemical and Statistical Analyses
All plant tissue and grain samples collected in the field and growth room experiments were ground to pass a 5-mm screen prior to chemical analyses. Plant Cl analysis in the field and growth room Exp. II was performed by potentiometric titration (LaCroix et al., 1970). Plant Cl and Br analyses on tissue collected at head emergence in growth room Exp. I were performed by dry ashing 1 g of plant material in a muffle furnace at 550°C for 4 h. The cooled ash was wetted with deionized water then transferred to a 50-ml volumetric flask. An aliquot was then removed, filtered (0.45 µm), and analyzed for Cl and Br using ion-exchange chromatography (Dionex 4000i, AS4A-SC column, Dionex Corp., Sunnyvale, CA; eluant concentration equaled 1.8 mM Na2CO3/1.7 mM NaHCO3). This approach was chosen because it allowed the simultaneous analyses of Cl and Br on the same tissue subsample. Also, analysis with ion-selective electrodes was not possible, because of the interference problems associated with measuring Cl in a high Br solution (and Br in a high Cl medium). Piper (1950) in a review of dry ashing procedures expressed a need to dry ash plant material with CaO to prevent Cl volatilization. We conducted a number of tests during the course of this study and found this step was not necessary. Analysis of variance and regression analysis were performed using the SAS (SAS Inst., 1985) PROC ANOVA and GLM programs. Single degree of freedom (df) contrasts were performed using MSUSTAT (Lund, 1988).
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RESULTS AND DISCUSSION
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Field Experiment
Leaf spotting was apparent during the late-vegetative growth period, or by the time plant tissue samples were collected at head emergence in the plots not receiving Cl. Most of the lesions exhibited abrupt boundary between dead and live tissue, and symptoms were generally more severe on the leaves immediately below the flag. Chloride fertilization greatly suppressed, but did not eliminate leaf spotting. Although foliar fungicide treatments were not incorporated into this study, the majority of the leaf spotting at this site was believed to be physiological and not microbial in origin. This opinion was based on the visually obvious response to applied Cl and similarity in symptoms to the Cl-deficient leaf spot syndrome described for winter wheat (Engel et al., 1997). One difference between this study and earlier investigations was the magnitude of tissue damage. Leaf spot severity for this durum cultivar exceeded by two fold, the most severe damage we had ever observed in a cultivar of winter wheat susceptible to this phenomenon (e.g., CDC Kestrel). Indigenous soil Cl (6.0 kg ha-1 in upper 60 cm) and control plant Cl were extremely low at this site. However, they were no more Cl deficient than sites where we had observed leaf spotting in winter wheat. Chloride fertilization increased grain yield 740 kg ha-1 (22%) over the control (Table 1). Chloride also increased mature kernel weight, but other yield components (kernels spike-1 and spike density) accounted for most of the yield response to applied Cl.
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Table 1. Effect of Cl fertilization on physiological leaf spot severity, yield, mature kernel weight, and shoot Cl concentration at head emergence in WB881 durum wheat (Poplar, MT., 1994).
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Growth Room—Experiment I
Leaf spot symptoms in WB881 durum became apparent by the jointing stage in all pots where Cl was withheld from the nutrient solutions. Symptoms initially appeared on the second or third most recently emerged leaf. Leaf spot severity increased with time until the soft-dough stage or when the top growth began to senescence. Leaf spot appearance in the growth room (Fig. 1A and 1C)
was similar to the lesion symptoms that were observed in the field experiment. Leaf spot severity versus posttransplanting relationships reveals that Cl suppressed leaf spot severity and delayed the appearance of lesions on the plant (Fig. 2)
. The suppression effects increased up to the highest Cl dose (30.0 mmol pot-1) (Fig. 1B). Bromide did not substitute for Cl's role in leaf spot suppression, but enhanced the appearance of lesions at the lower doses (1.5, 3.0, and 6.0 mmol pot-1) (Fig. 1C). At the highest Br dose (30.0 mmol pot-1) plants exhibited toxicity symptoms. No attempt was made to differentiate between chlorosis or necrosis caused by the leaf spot phenomenon versus Br toxicity. Hence, the leaf spot severity ratings for this treatment were biased. Previous investigations under hydroponics have suggested that Br additions to low Cl mediums would prevent or reduce the severity of Cl deficiency in sugarbeet (Beta vulgaris L.) (Ulrich and Ohki, 1956) and tomato (Lycopersicon esculentum L. Mill.) (Ozanne et al., 1957), respectively. There was no evidence of a similar phenomenon in this study with respect to leaf spot suppression in durum. Hence, the physiologic processes responsible for the appearance of Cl-deficient lesions in durum and winter wheat are probably different than processes responsible for the appearance of chlorosis and necrosis in tomatoes and sugarbeets.
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Fig. 1. Comparison of leaf spot symptoms in WB881 durum wheat 1 wk postflowering for plants grown under hydroponics (Growth room Experiment I). A = control, no halide added; B = 30 mmol Cl pot-1; and C =1.5 mmol Br pot-1.
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Fig. 2. Leaf spot severity for WB881 durum wheat vs. d after transplanting as affected by halide level (0, 1.5, 3.0, 6.0, and 30.0 mmol pot-1) [53, 61, 68, and 89 d posttransplant = boot, flower, watery-ripe, and soft-dough stages, respectively (Growth room Experiment I)].
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Chloride and Br concentrations in the shoot and leaves of WB881 durum increased in response to the higher dose amounts of these ions added to the nutrient medium (Table 2). Shoot Cl concentrations in plants not receiving Cl were <100 mg kg-1. These concentrations are considerably less than the lowest concentrations, 250 to 300 mg kg-1, we had observed previously in field studies (Engel et al., 1997; Engel et al., 1998). Scatter diagrams of leaf spot severity versus shoot Cl concentrations (Fig. 3)
indicates that leaf spot severity in WB881 durum was closely linked to shoot Cl. The relationships were similar to those previously described for winter wheat (Engel et al., 1997). Damage from leaf spotting at the watery-ripe stage was minimal (<10%) where shoot Cl levels exceeded 1.0 g kg-1. Leaf spot damage increased exponentially as shoot Cl dropped below these levels. Shoot and leaf Cl concentrations were similar in the Br treatments compared with the control (Table 2). Hence, the higher leaf spot severity scores for the plants receiving Br could not be attributed to suppression of Cl uptake in the shoot, or a reduction of Cl in the leaves.
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Table 2. Chloride and Br concentrations in leaves and shoots of WB881 durum wheat at head emergence as affected by halide ion and dose (Growth room Experiment I).
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Fig. 3. Leaf spot severity (flag, flag-1) at watery-ripe stage versus shoot plant Cl concentrations for WB881 durum wheat grown under hydroponics (Growth room Experiment I). Observations from 30 mmol pot-1 Br treatment deleted from this analysis.
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Total plant biomass, top growth, and grain yield were improved by increasing the Cl levels in the hydroponic mediums up to 30.0 mmol pot-1 (Table 3). Harvest index values indicate that grain yield was more sensitive than top growth to Cl deficiency. Contrasting the control with the 30.0 mmol Cl pot-1 dose indicates shoot growth and grain yield were retarded 58.3 and 98.8%, respectively. This level of yield loss is much greater than we have previously observed in the field and reflects our ability to starve plants of Cl under hydroponic culture. Although grain yield and harvest index were greater in the Br treatments than the control, the response was nominal. Overall, there was no evidence that Br could compensate appreciably for the top growth and grain yield losses that resulted from withholding Cl. Kernel size increased 20% with the addition of Cl to nutrient medium. The effect of Cl on kernel weight was limited to the first increment (1.5 mmol pot-1) of applied Cl. Hence, other yield components (i.e., spike plant-1 and kernels spike-1) accounted for most of the grain yield response to Cl under hydroponics. This is consistent with the results of the durum field study, but differs from previous winter and spring wheat field experiments (Engel et al., 1998), where kernel size was reported to be the most important yield component affected by Cl. Root biomass was the only yield component not affected by halide level.
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Table 3. Growth, harvest index, and kernel weight of ‘WB881 durum grown under hydroponics and as affected by halide ion and dose level (Growth room Experiment I).
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Consumptive water use for WB881 durum was affected by halide level (Table 3). Plant water use increased with Cl up to the 30 mmol pot-1 dose. Plants receiving Br used less water than the plants receiving Cl. Differences in consumptive water use between the treatments did not become apparent until the flowering stages. Thereafter, these differences grew larger through the grain-fill period and correspond to the changes in plant growth and leaf spot severity over time. Necrosis of leaf tissue from inadequate Cl should result in a reduction in leaf area capable of transpiring water. Hence, the differences in water use would be expected to be, in part, a function of leaf spot severity.
Growth Room—Experiment II
Growth or biomass production of Kyle, Monroe, and WB881 was affected by Cl dose as in Exp. I (Table 4). Leaf spot symptoms similar to those observed in WB881 were also reproduced in Kyle and Monroe by withholding Cl from the hydroponic medium. Leaf spot susceptibility was affected by cultivar selection. Monroe exhibited less susceptibility to leaf spotting than did WB881 or Kyle. Cultivar susceptibility to leaf spotting under conditions of severe Cl deficiency (i.e., 0 Cl dose level) could not be explained by differences in Cl concentration or uptake (data not shown) in the leaves, shoots, or roots. In general, shoot and leaf blade Cl concentrations were similar for the three cultivars at the equivalent Cl dose levels. Previous field investigations have shown that leaf spot susceptibility in winter wheat can vary greatly with cultivar selection even though Cl concentrations in the plant may be similar (Engel et al., 1997). The results from this growth room study are consistent with these observations. Other mechanisms beyond the ability of plants to absorb and translocate Cl to the shoots or leaves are needed to explain differences in cultivar susceptibility to Cl-deficient leaf spot.
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Table 4. Leaf spot severity, plant biomass, and plant Cl concentration of three durum wheat cultivars (Kyle, Monre, WB881) grown under three Cl dose levels. All parameters measured at the kernel watery ripe stage (Growth room Experiment II).
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Shoot Cl concentration in the controls were somewhat lower in Exp. II (40 mg kg-1) than Exp. I (100 mg kg-1). Reagent grade chemical lots, and our supplier of deionized water differed for the two experiments. Chloride contamination from these sources may have varied sufficiently between the two studies to account for these differences. Early investigators (Broyer et al., 1954; Johnson et al., 1957; Ozanne et al., 1957) used special precautions (e.g., recrystallization of reagent grade salts; and precipitation of halides with AgNO3 and subsequent removal of excess Ag) to minimize Cl contamination for the purposes of producing deficiency symptoms in plants. The lower limits of Cl concentrations reported by Ozanne et al. (1957) and Johnson et al. (1957) were 35 mg kg-1 in tomato and 140 mg kg-1 in barley (Hordeum vulgare L.), respectively. Hence, the special precautions used by early investigators were not needed in our study to achieve similar levels of Cl deficiency.
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SUMMARY AND CONCLUSIONS
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A leaf spot complex of WB881 durum, that was previously (1994) observed in a field experiment (6.0 kg ha-1 soil Cl in 0- to 60-cm depth), was easily reproduced under hydroponics by depriving plants of Cl. The ability to reproduce these symptoms in a disease free environment indicates a physiological or nutritional origin to the leaf spotting. Damage to plant tissue from this Cl-deficient leaf spot was aggravated by addition of Br to the hydroponic culture. Leaf spot severity was related to shoot Cl as in earlier investigations with winter wheat. Chloride-deficient leaf spot is minimal at shoot concentrations 1.0 g kg-1, but increases exponentially as plant Cl falls below this level. Top growth and grain yield were reduced up to 58.2 and 98.9%, respectively, by withholding Cl from the solutions. The reduction in grain yield was much greater than observed in field studies and reflects our ability to deplete shoot Cl to extremely low concentrations under hydroponic culture. Bromide did not compensate for the absence of Cl in the nutrient solutions by reducing leaf spot severity, or improving top growth and grain yield. Early investigators have reported that Br can substitute at least partially for Cl in tomato (Ozanne et al., 1957) and sugarbeet (Ulrich and Ohki, 1956). Hence, the mechanisms responsible for the production of Cl-deficient leaf spot in wheat may be different than the Cl-deficient tissue necrosis reported by earlier investigators in dicots. Leaf spot symptoms similar to those observed in WB881 durum were also reproduced in Kyle and Monroe by withholding Cl from the hydroponic medium. Leaf spot susceptibility was greater in WB881 and Kyle than Monroe. Cultivar susceptibility to Cl-deficient leaf spot symptoms could not be explained by preferential accumulation (e.g., root) or exclusion of Cl from the shoot or leaves. Hence, an explanation for cultivar susceptibility to leaf spot reaction does not appear to involve differences in Cl uptake and partitioning in specific plant parts.
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NOTES
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Contribution from the Montana State Univ. Agric. Exp. Stn.
Received for publication October 30, 2000.
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REFERENCES
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ABSTRACT
INTRODUCTION
