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Meloidogyne incognita Resistance in Soybean under Midwest Conditions

^a Dep. of Botany and Plant Pathology, Purdue Univ., West Lafayette, IN 47907-2054
^b Dep. of Agronomy, Purdue Univ., West Lafayette, IN 47907-2054
^c Dep. of Botany and Plant Pathology, Purdue Univ., West Lafayette, IN 47907-2054. This manuscript is published with the Purdue University, Agricultural Research Program number 2006-17974

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

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Soybean cultivars of maturity groups II to IV were tested in the greenhouse for resistance to Meloidogyne incognita (Kofoid and White) Chitwood. Selected cultivars were tested in a field of sandy loam soil naturally infested with M. incognita and Heterodera glycines Ichinohe (2004) or in a silt loam soil artificially infested with M. incognita (2005). In 2004, H444NRR was resistant to M. incognita, but not to H. glycines; LS94-3207 and LNX97164-35-5 were resistant to both nematodes; Gateway 427, H444NRR, LNX97164-35-5, and SB4399CT were moderately resistant to M. incognita in greenhouse tests; HF9665-2-15 was resistant to M. incognita but highly susceptible to H. glycines. In 2005, LS94-3207, H444NRR, LNX97164-35-5, and Manokin were resistant to M. incognita. In microplots with two sandy loam soils, HF9665-2-15 exhibited tolerance to increasing inoculum levels of M. incognita. High-yielding soybean cultivars in maturity groups II to IV with resistance and tolerance to M. incognita were identified. Under field conditions, resistance to the more widespread nematode H. glycines, combined with resistance to M. incognita, is highly desirable to reduce the risk of yield reduction and to improve cropping sequences that include soybean.

Abbreviations: GH1–GH6, greenhouse experiments • MG, maturity group • OM, organic matter

	INTRODUCTION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
SOYBEAN [Glycine max (L.) Merr.] is a major agricultural commodity in the United States. In 2004, 85 million tonnes were harvested nationally (USDA-National Agricultural Statistics Service, 2008). Sedentary plant-parasitic nematodes are important pests of soybean. For example, the soybean cyst nematode (Heterodera glycines Ichinohe) was the most damaging pest of soybean between 1999 and 2002 in the United States and Ontario, Canada, and remained the most important in the United States thereafter (Wrather et al., 2003; Wrather and Koenning, 2006). Root-knot nematodes (Meloidogyne spp.) occurred on soybean but to a lesser extent than H. glycines (Wrather et al., 2003).

Over 93,000 tonnes of soybean production is lost annually to Meloidogyne spp. and other minor plant-parasitic nematodes in the United States (Wrather et al., 2003). The four major species of M. incognita (Kofoid and White) Chitwood, M. hapla Chitwood, M. arenaria (Neal) Chitwood, and M. javanica (Treub) Chitwood (>95% of all Meloidogyne infestations in agricultural production) all damage soybean (Hussey and Janssen, 2002). In the Midwest, M. incognita has been reported in fields in Missouri (Wrather et al., 1992), Illinois (Allen et al., 2005), Kansas (Walters and Barker, 1994), and Indiana (Brust et al., 2003; Kruger et al., 2007). Because Meloidogyne spp. and H. glycines can damage soybean singly or in an additive way (Niblack et al., 1986a, 1986b), studies have included the effects of crop rotation on both nematode genera in soybean production (Weaver et al., 1989, 1995).

In the southern United States, soybean cultivars of the appropriate maturity groups (MGs) with high levels of resistance to Meloidogyne spp. have been identified for the management of these plant-parasitic nematodes (Davis et al., 1998; Harris et al., 2003; Herman et al., 1990; Hussey et al., 1991; Luzzi et al., 1996; Riggs et al., 1988). As one example of the genetics, partial resistance to M. incognita is conferred by the single Rmi1 gene in the cultivar Forrest (Luzzi et al., 1987). In soybean, resistance to M. incognita is more common than resistance to M. javanica and M. arenaria (Hussey and Janssen, 2002). Marker-assisted selection for genes conferring resistance to M. incognita in the soybean plant introduction PI96354 has facilitated the process of breeding resistance into commercially available soybean cultivars (Li et al., 2001; Ha et al., 2004).

The objectives of this study were to identify resistance to M. incognita among soybean cultivars in maturity groups II to IV and to determine the response of these cultivars under nematode-infested field conditions. Soybean cultivars with H. glycines resistance, M. incognita resistance, and unknown disease reaction were tested for resistance to M. incognita in the greenhouse and under naturally or artificially infested field conditions.

	MATERIALS AND METHODS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Greenhouse Experiments
Soybean cultivars were tested for resistance to M. incognita by standard procedures (Hussey and Boerma, 1981). The cultivars were chosen because of their current popularity, yield potential, or their known disease response to H. glycines. Sand, autoclaved twice for 2 h with 24 h between autoclavings, was placed in plastic cones (4-cm diameter, 20.8-cm deep, Stuewe & Sons, Corvallis, OR). Two seeds of the test soybean cultivars (surface-sterilized for 2 min in 1% NaOCl solution), rinsed with tap water, were inoculated with commercial rhizobium inoculum (Cell-Tech Soybean, Nitragin, Inc., Milwaukee, WI), before planting at 1-cm depth. The cones were watered and their tops individually covered with parafilm. The cones were arranged in randomized complete block designs with six replications in commercial support trays and incubated in a 12/12 h day/night cycle at 25/21°C. When the seeds had germinated, parafilm was removed, plants were thinned to one plant per cone, and the seedlings were watered twice daily and fertilized weekly with approximately 9 mL per cone of standard rate (2.6 g L^–1) solution of Miracle Gro (Scott Miracle Gro Products, Inc., Marysville, OH; 15.0% N, 13.1% P, 12.5% K). Six greenhouse experiments (GH1–GH6) were conducted, including one experiment in which inoculum level was tested (GH1).

In the first experiment (GH1), soybean seedlings of six cultivars were inoculated with a series of egg densities of 1000, 2000, or 3000 eggs cone^–1 to determine the effective inoculum amount for distinguishing resistant and susceptible cultivars. In all other tests, the soybean seedlings were inoculated with 2000 eggs of M. incognita in 5 mL of water per cone 2 wk after planting. Nematode egg inoculum of a single–egg mass culture originating from southern Indiana, maintained in the greenhouse on tomato (Lycopersicon esculentum Miller cv. Rutgers), was extracted by standard procedures (Hussey and Barker, 1973).

Four weeks after inoculation, soybean tops were excised, weighed, and oven dried at 38°C to a constant weight, and dry plant tops were weighed. The root systems were washed free of soil and weighed; M. incognita-induced galls were counted. In each experiment (GH2–GH6; Table 1 , 2 , 3 ), PI96354 and G93-9009 were used as resistant controls, and Spencer and Williams 82 were used as susceptible controls.

View this table: [in this window] [in a new window]   Table 4. Top and root weights of soybean at midseason and late-season samplings of the eight cultivars and two fumigated treatments in Meloidogyne incognita- and Heterodera glycines-infested soil in a planting date trial near Vincennes, IN, in 2004.

Twice during the growing season for each planting date, fresh plant tops were sampled and weighed, plant heights measured, and roots removed with spades 30 cm deep from 1 m of each of the outside rows of the four-row plots. After washing, M. incognita-induced galls were counted. On 31 Oct. 2004, the center two rows were harvested with a small plot combine to determine seed yields and grain moisture. Yields were converted to kilograms per hectare at 13% moisture.

Field Experiment in Soil Artificially Infested with Meloidogyne incognita in 2005
The trial was conducted in a silt loam soil (18% sand, 60% silt, 22% clay, 2.9% OM, pH 6.9) in a field artificially infested with M. incognita on the Purdue University Meigs farm near Romney, IN (Xing and Westphal, 2005). At initiation of the previous experiment with cowpea (Vigna unguiculata L.), the field was fumigated with methyl bromide (98% methyl bromide and 2% chloropicrin) at 450 kg ha^–1 on 9 June 2004 to reduce random error from other soil-borne pathogens, especially H. glycines. After a fall cover crop of canola (Brassica napus L.) and before planting in spring 2005, the field was cultivated to mix the soil horizontally and to obtain uniform population densities of M. incognita. In 2005, inoculations with M. incognita were done as described previously (Xing and Westphal, 2005) by delivering suspensions of M. incognita eggs at 450 eggs mL^–1 in sloppy water agar at 7.3 mL m^–1 of row. A sample of the egg suspension was collected to determine the nematode hatch rate of the eggs in the suspension.

Eight cultivars (Table 5 ), selected for their disease response to H. glycines and M. incognita as reported in published information or based on our greenhouse tests, were planted in a randomized complete block design with four replications. The cultivars were JGL934014XRJ, JGL937014XRJ, H444NRR, LNX97164-35-5, LS94-3207, Manokin, Gateway 427, and Williams 82. In addition, Gateway 427 and Williams 82 were also planted into noninoculated plots.

View this table: [in this window] [in a new window]   Table 5. Population densities of Heterodera glycines cysts and eggs in soil at harvest of eight cultivars and two fumigated treatments in a Meloidogyne incognita- and Heterodera glycines-infested soil in a planting date study near Vincennes, IN, in 2004.

On 5 Sept. 2005 at midseason sampling, fresh top weights, plant heights, and plant populations were determined, and roots were excavated 30 cm deep from a total of 1 m of row from the two outside rows of the plots. Root systems were washed and M. incognita galls counted. On 27 Oct. 2005, the center two rows were harvested with a plot combine except the plots of the immature cultivar Manokin, where plant tops were excised at the soil line and air dried in a barn for threshing at a later date.

Microplot Experiment in 2004
In microplots at the Southwest Purdue Agricultural Center at Vincennes, IN, the soybean cultivar HF9665-2-15 was exposed to four inoculum levels of M. incognita in two sandy loam soils (67% sand, 22% silt, 11% clay, 1.2% OM, pH 7.3; 68% sand, 19% silt, 13% clay, 1.5% OM, pH 7.4) in a two-factor factorial design with four replications. The 45-cm-diam. polyethylene tubes were inserted perpendicularly into the ground to a depth of 55 cm. On 15 Apr. 2004, plots were fumigated with methyl bromide (98% methyl bromide, 2% chloropicrin) at 392 kg ha^–1. On 5 May 2004, plots were inoculated at 10 depressions per microplot with a total of 50 mL egg suspensions of a single–egg mass culture of M. incognita to establish 0, 100, 1000, and 10,000 eggs per 100 mL of soil, at 0- to 15-cm depth. Soils were mixed horizontally in each plot. On 14 May 2004, 50 soybean seeds per plot were planted in three parallel rows (outside two rows, 25 cm long; center row, 38 cm long; 13 cm between rows).

Population densities of J2 of M. incognita were determined for soil samples at planting and harvest by Baermann funnel extraction. At midseason, plant heights and fresh top weights were determined, roots were removed from soil from one random outside row, and galls on the entire root systems were counted. Grain yields were determined on 31 Oct. 2004 for the remaining two rows.

Data Analysis
The Box–Cox procedure was used to test for homogeneity of error variances (Box et al., 1978). All zero standard deviations were excluded in Box–Cox [log₁₀(x + 1)]. Arcsine transformations were used on root ratings [arcsine (x/10)]. Log-transformations [log₁₀(x + 1)] were used on all nematode-related counts. All root ratings and nematode counts were presented as transformed data. In the analysis of variance (ANOVA), observations with zero means and zero standard deviations were excluded from the analysis of variance. Mean separation tests were conducted at P = 0.05 (SAS Institute, Cary, NC). For the greenhouse experiments, nematode-induced galling was indexed in relation to standard resistant cultivar G93-9009 by generating the log-transformed ratio of the gall counts of the test cultivar and the control cultivar {log₁₀[(each individual cultivar + 1)/(resistant control cultivar G93-9009 + 1) + 1]} within each experimental replication, similar to the index used for Rotylenchulus reniformis Linford and Oliveira (Robbins et al., 2000). The test cultivars were compared to the susceptible and resistant standard cultivars by t tests. Cultivars with zero means and zero standard deviations were included in the t tests. Regression analysis was conducted on the microplot data.

	RESULTS

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Greenhouse Experiments
In the inoculum level experiment (GH1), inoculum x soybean cultivar interactions were negligible (P = 0.39). At the three inoculum levels, the two resistant soybean cultivars G93-9009 and PI96354 had no root galls; the highly susceptible cultivars Spencer and Lee 74 had many; while Cyst-X20-18, known to be highly resistant to H. glycines (Faghihi et al., 1995), and Gateway 427 had significantly fewer galls than the susceptible controls but significantly more than the resistant controls (Fig. 1 ).

View larger version (31K): [in this window] [in a new window]   Figure 1. Meloidogyne incognita-induced gall numbers on roots of soybean in an inoculum level greenhouse experiment with various soybean cultivars (GH1). Means with standard error are presented.

In GH5, the gall indices of neither of the two resistant nor the two susceptible controls were significantly different from one another, but those of the two susceptible controls were significantly higher than those of the resistant ones (Table 2). In this experiment, many of the cultivars were highly susceptible, but none was highly resistant. Fifteen cultivars (RC4332–RC4233) in this experiment were neither in the susceptible nor the resistant group (Table 2).

In GH6, Adler362RRN, HF9665-2-15, SB2665R, and SB3955 were highly resistant, and the cultivar Pioneer 93M90 was highly susceptible (Table 3), confirming the results in GH3 (Table 2). A group of eight cultivars (gall indices: 0.526–0.588) was not significantly different from G93-9009, PI96354, or from Spencer, suggesting that they were partially resistant. All other cultivars were susceptible.

Field Experiment in Naturally Infested Soil in 2004
In the field trial at Vincennes, IN, HF9665-2-15 was shortest in both fumigated and nonfumigated treatments at both plantings dates (data not shown). Plant height of Gateway 427 was not increased for either planting date (data not shown). LS94-3207 had the highest yields at the early planting date. At the late planting date, LS94-3207, JGL934014XRJ, JGL937014XRJ, and both treatments with Gateway 427 had similar yields (Fig. 2 ). HF9665-2-15 had the lowest yields for both planting dates, and this cultivar and Gateway 427 had no yield benefit from soil fumigation. The planting date x treatment effect was significant (P = 0.0237). Yields were higher at the late planting date for JGL934014XRJ and at the early planting date for SB4399CT compared to the alternative planting date (Fig. 2).

View larger version (24K): [in this window] [in a new window]   Figure 2. Grain yields of soybean in a trial at Vincennes, IN, in a Meloidogyne incognita and Heterodera glycines-infested soil with 10 treatments and two planting dates, harvested on 31 Oct. 2004. Bars indexed with the same letter were not significantly different at P = 0.05. Lowercase letters: early planting date on 5 May 2004; uppercase letters: late planting date on 11 June 2004. Planting date x treatment effects were significant (P = 0.0237); *, significant difference of early and late planting date for within one treatment using the LSD for planting date x treatment. Fum.: plots were preseason fumigated with 1,3-dichloropropene as Telone II at 132 kg a.i. ha–1 before planting.

JGL937014XRJ had the most galls at both planting dates, whereas galling, though high, was more variable on JGL934014XRJ (Fig. 3 ). H444NRR, LNX97164-35-5, LS94-3207, SB4399CT, Gateway 427, and HF9665-2-15 all had somewhat less galling (Fig. 3). At harvest of both planting dates, egg population densities of H. glycines were higher under HF9665-2-15 (both treatments), SB4399CT, and H444NRR than under JGL934014XRJ, LS94-3207, LNX97164-35-5, and both treatments of Gateway 427; cyst population densities followed a similar pattern (Table 5). For the early planting, LS94-3207 had fewer eggs in the soil at harvest than all nine other entries. For the late planting, LS94-3207 had fewer H. glycines eggs in the soil than seven of the other treatments but was not significantly different from the fumigated Gateway 427 treatment or the LNX97164-35-5 treatment (Table 5). Planting date and planting date x treatment effects were nonsignificant for cysts (P = 0.5282; P = 0.7574, respectively) or eggs (P = 0.78; P = 0.73, respectively).

View larger version (23K): [in this window] [in a new window]   Figure 3. Root knot nematode-induced galls on roots of soybean in Meloidogyne incognita and Heterodera glycines-infested soil at Vincennes, IN. Plants were collected on 17 Aug. 2004 (early planting) and 6 Sept. 2004 (late planting). Means and standard errors are presented. Bars indexed with the same letter were not significantly different at P = 0.05; lowercase letters: early planting date; uppercase letters: late planting date. Fum.: fumigated with 1,3-dichloropropene as Telone II at 132 kg a.i. ha–1 before planting. Planting date effects were nonsignificant (P = 0.9820).

View larger version (35K): [in this window] [in a new window]   Figure 4. Reproductive factors of eggs of Heterodera glycines in a Meloidogyne incognita and H. glycines-infested soil with 10 treatments at two planting dates in a trial at Vincennes, IN, in 2004. Means and standard errors are presented. Bars indexed with the same letter were not significantly different at P = 0.05; lowercase letters: early planting date; uppercase letters: late planting date. Fum.: plots were preseason-fumigated with 1,3-dichloropropene as Telone II at 132 kg a.i. ha–1 before planting. Planting date effects were nonsignificant (P = 0.5050).

View this table: [in this window] [in a new window]   Table 6. Plant populations, yield, and second stage juveniles (J2) of Meloidogyne incognita in an artificially Meloidogyne incognita infestation trial near Romney, IN, in 2005.

View larger version (20K): [in this window] [in a new window]   Figure 5. Nematode-induced galls per root averaged for soybean roots of 1 m of row in plots artificially infested with Meloidogyne incognita {log10 [(counts/root) +1]} in 2005. Bars indexed with the same letter were not significantly different at P = 0.05. ni.: noninoculated plots. All other plots were inoculated during planting with 3280 eggs m–1 of row.

Microplot Experiment in 2004
At planting, the log-transformed counts of J2 from soil were significantly different between the two soil types (P = 0.05) and among the inoculum levels (P = 0.01), increasing with increasing inoculum levels (data not shown). Data of all other variables were combined, because there were no significant differences between the soil types. The regression model of plant heights, measured on 11 June 2004, was negatively correlated with the log-transformed inoculum amounts and an R² of 0.79 but was not significant (P = 0.4610, data not shown). At midseason root sampling, the regression model of the log-transformed gall counts of the roots was positively correlated with the log-transformed inoculum amounts and an R² of 1.00 (P = 0.06; Fig. 6 ). The log-transformed counts of M. incognita J2 in the soil at harvest were positively linearly correlated (R² = 0.97, P = 0.02) with the inoculum amounts (Fig. 7 ).

View larger version (7K): [in this window] [in a new window]   Figure 6. Meloidogyne incognita-induced galls on roots of soybean cultivar HF9665-2-15 from varying inoculum levels in a microplot trial in two sandy soils at Vincennes, IN, on 11 Sept. 2004.

View larger version (7K): [in this window] [in a new window]   Figure 7. Populations of second stage juveniles (J2) of Meloidogyne incognita in soil at varying infestation levels in a microplot trial in two sandy loam soils at Vincennes, IN, at soybean harvest on 31 Oct. 2004.

	DISCUSSION

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

The field trial of 2004 showed that cultivars with resistance to M. incognita but without resistance to H. glycines have limited benefit for soybean production in soils with both nematodes. Growers who produce in fields with both H. glycines and M. incognita must consider resistance to both of the nematodes to minimize losses in soybean. Although H. glycines and M. incognita are believed to have no synergistic damage potential, these nematodes infected soybean at similar rates and damaged susceptible cultivars additively in microplot experiments (Niblack et al., 1986a, 1986b). They appear to be competing for similar feeding sites (Melakeberhan and Dey, 2003). In the field studies at Vincennes, H. glycines–resistant cultivars were damaged by M. incognita, and M. incognita–resistant cultivars were damaged by H. glycines. HF9665-2-15, which was resistant and tolerant to M. incognita in the absence of H. glycines in the microplot trial, yielded poorest of all cultivars tested in the presence of H. glycines. This cultivar has a 3.9 relative maturity and was released by the Ohio Agricultural Research and Development Center because of its high yield potential and resistance to Roundup herbicide. It was not previously known to be resistant to M. incognita. HF9665-2-15 appears tolerant to M. incognita because, despite some galling on its roots and some initial growth reduction at high inoculum levels of M. incognita in the microplot trial, it produced similar grain yields at all levels of inoculum. HF9665-2-15 with its high yield potential and the newly demonstrated resistance and tolerance to M. incognita provides a genetic source of resistance to M. incognita to incorporate into cultivars with H. glycines resistance. In another example, the highly resistant PI96354 had a <1% reduction in yield and also suppressed the M. incognita population density in a microplot study in Georgia (Herman et al., 1990). In the greenhouse, levels of resistance of HF9665-2-15 were similar to those described for PI96354 (Luzzi et al., 1987).

We confirmed that resistance to H. glycines cannot be used to predict resistance to M. incognita (Davis et al., 1998). For example, the two cultivars JGL934014XRJ and JGL937014XRJ that were resistant to H. glycines were highly susceptible to M. incognita. Some cultivars were resistant to both H. glycines and M. incognita. We confirmed that LS94-3207 is resistant to H. glycines (Schmidt and Klein, 2004) and M. incognita (Allen et al., 2005).

In the field experiment in 2005, when only M. incognita was present, most cultivars produced comparable yields. Disease reaction as inferred from the field trial in 2004 was confirmed for JGL934014XRJ, JGL937014XRJ, H444NRR, NX97164-35-5, LS94-3207, and Gateway 427. Similarly, the reaction determined by greenhouse experiments was confirmed in the field tests and thus the utility of the greenhouse testing was corroborated. Some cultivars classified as resistant in the greenhouse tests were also resistant in the field (e.g., LS94-3207). Conversely, some cultivars that allowed for minimal reproduction of M. incognita in the greenhouse were resistant in the field (e.g., HF9665-2-15, SB4399CT, Manokin, Gateway 427, H444NRR, and LNX97164-35-5). Such discrepancy of greenhouse and field results is common in soil-borne diseases. In this case, the greenhouse test was conservative in that it unambiguously identified resistant germplasm and it did not predict resistance if the germplasm was not resistant. LS94-3207 yielded poorly in the artificial infestation trial probably because poor seed germination resulted in insufficient plant populations.

The identified cultivars can potentially improve crop sequences by providing high yield potential in the presence of M. incognita and by reducing soil population densities of this nematode for subsequent crops. Reproduction in one crop can have an impact on subsequent crops as well as the current host (Windham, 1998). Westphal and Scott (2005) demonstrated that the use of soybean cultivars with resistance to R. reniformis benefited the subsequent susceptible crop of cotton (Gossypium hirsutum L.). Implementation of improved cultivar selection in crop sequences is urgently needed for parts of the Midwest where M. incognita–sensitive high value crops (e.g., watermelon), and low value crops (e.g., corn [Zea mays L.] and soybean), are highly susceptible hosts of this nematode. Such an integrated approach with soybean cultivars with resistance to M. incognita is beneficial because other methods have limited effectiveness in maintaining low nematode population densities in the Midwest.

The current soybean greenhouse experiments gave some indication of cultivars with levels of resistance to M. incognita available in northern germplasm similar to those in highly resistant southern cultivars G93-9009 (Luzzi et al., 1996) and PI96354 (Luzzi et al., 1987). The latter cultivars are in MG VI, which prevents their commercial production in many areas of the Midwest. In addition, the extreme lateness in maturation of these lines in the Midwest also precludes their incorporation into a Midwest-based breeding program as donor parent.

Management of plant-parasitic nematodes in soybean in Indiana has focused on H. glycines. But results of a transect study showed that M. incognita can damage soybean under Midwest conditions even when other soil factors confound this observation (Kruger et al., 2007). Thus, producers should be aware of the potential for Meloidogyne spp. damage and manage Meloidogyne spp. infestations properly.

Planting dates had limited effects on yields and nematode reproduction in our study, in contrast to earlier reports, indicating that early planting reduced nematode damage compared to late planting in H. glycines-infested fields (Riggs et al., 2000). In those studies in a southern climate, planting dates varied from April to July in contrast to our studies with only two dates: 5 May and 11 June. Such differences in planting date often do not result in yield differences in the Midwest (Pedersen and Lauer, 2003). The late planting, which was simulating the planting of soybean after winter wheat in a double crop system, was into previously fallow plots. Therefore these soybean yields, which were relatively high, did not relate to a true double-crop situation following wheat. In the late planting date, root weights of most cultivars of the studies were reduced, whereas top masses were increased in some cultivars, a developmental habit that may impact soybean yield negatively when water is limited. Under drier growing conditions, the effect of planting date may be different from our observation because nematode reproduction and damage tend to be more pronounced under drier conditions (Johnson et al., 1994).

In summary, soybean cultivars with high levels of resistance to M. incognita were identified that yielded well under Midwest conditions in M. incognita-infested fields. The M. incognita–resistant cultivars also have potential to reduce the "nematode load" in crop sequences that include other hosts of M. incognita. However, the productivity of M. incognita–resistant cultivars will depend on the presence of other plant-parasitic nematodes, especially H. glycines. If levels of H. glycines are high, concomitant resistance to H. glycines will be necessary for sustainable soybean production.

	ACKNOWLEDGMENTS

 
This research was supported by the Indiana Soybean Board, the Indiana Crop Improvement Association, AgSpectrum, and the Departments of Botany and Plant Pathology, and Agronomy, the College of Agriculture, Purdue University. The authors thank C. Fuhrmann (Hendrix and Dail, Kentucky) for fumigant application, Judy Santini for statistical discussion, B. Banta, H. Gale, A. Marchese, and M. Ngar, the Meigs farm crew, the Southwest Purdue Agricultural Center crew for technical assistance, and Jim Deem for his help. Provision of seed and rhizobium inoculum by R. Dowll, J. Gerard, Nitragin Inc., G. Shanon, and others is acknowledged. Helpful suggestions from E. Davis, L. Dunkle, and R. Hussey are greatly appreciated. The confirmation of the identity of the Meloidogyne incognita populations by E. Davis and J. Eisenback is greatly appreciated.

	NOTES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
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Received for publication April 7, 2007.

	REFERENCES

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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