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Published in Crop Sci. 43:1848-1851 (2003).
© 2003 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA

PLANT GENETIC RESOURCES

Additional Sources of Soybean Germplasm Resistant to Two Species of Root-Knot Nematode

Donna K. Harrisa, H. Roger Boerma*,b, Richard S. Husseyc and Steven L. Finnertyc

a Pioneer Hi-Bred International, Crop Genetics Res. and Development, 19456 St. Hwy 22, Mankato, MN 56001
b Dep. of Crop and Soil Sci., Center for Applied Genetic Technologies, 111 Riverbend Road, Athens, GA 30602
c Dep. of Plant Pathology, Univ. of Georgia, Athens, GA 30602

* Corresponding author (rboerma{at}uga.edu).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Root-knot nematodes (Meloidogyne spp.) can significantly reduce seed yield in soybean [Glycine max (L.) Merr.]. Identification of soybean germplasm with unique genes for resistance to root-knot nematodes would allow development of cultivars with high levels of resistance. The objective of this study was to identify additional sources of resistance to root-knot nematodes. We evaluated 608 recently imported soybean PIs from the southern provinces of the People's Republic of China for resistance to M. incognita (MI) and M. arenaria (MA). After three sequential levels of greenhouse screening, seven resistant PIs were identified for MI and seven for MA. In a fourth screening level to determine their level of resistance, PI 594753A and PI 594775A had MI gall resistance equal to the highly resistant check PI 96354. Three other PIs had more galls than PI 96354, but produced fewer galls than ‘Haskell’, the resistant check. However, the numbers of MI eggs produced on PI 594753A and PI 594775A were equal to the highly susceptible ‘Bossier’. The MA screening identified PI 594427C and PI 594403 with the same number of galls as the resistant check Haskell, but they had more galls than the highly resistant PI 200538. The number of MA eggs produced by PI 594427C was equal to the highly resistant check PI 200538, and PI 594403 produced fewer eggs per plant than PI 200538. These new sources of MA resistance may possess previously unidentified genes.

Abbreviations: MA, Meloidogyne arenaria • MI, Meloidogyne incognita • PI, plant introduction • QTLs, quantitative trait loci


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
ROOT-KNOT NEMATODES, Meloidogyne species, are parasites of almost every crop species. Two of the most common root-knot nematode species, MA and MI, are found throughout the southeastern USA. In 1996, the average soybean yield loss across 16 southern states because of root-knot nematodes was 1.02% and ranged from a trace amount to 5.0% (Pratt and Wrather, 1998).

Crop management to prevent losses from these nematodes can be difficult. Because of the cancellation of important fumigant nematicides including DBCP (1,2-dibromo3-chloropropane) and EDB (ethylene dibromide) in past years, plant resistance has become an increasingly important component in root-knot nematode management in the Southeast as well as other areas of the USA (Boerma and Hussey, 1992).

Luzzi et al. (1987) conducted an experiment where 2370 soybean accessions in the USDA-ARS Germplasm Collection from Maturity Groups V, VI, VII, and VIII were screened for resistance to both MI and MA. The screening was done in the greenhouse and resistance was characterized based on root galling and nematode reproduction. Five levels of screening were conducted using progressively increasing levels of inoculum (ranging from 3 000 to 10 000 eggs per plant) and number of replications (1 to 10). Plant Introduction 96354 was found to possess a high level of resistance to MI and PI 200538 to MA. Plant Introduction 96354 showed lower MI gall indices, fewer MI eggs per gram of root and per root system than ‘Forrest’, the resistant check. The MA-resistant PI 200538 showed these same characteristics compared with the resistant check ‘Jackson’ (Luzzi et al., 1987).

Currently, elite soybean cultivars do not possess the PI 96354 level of resistance to MI or the PI 200538 resistance to MA. Hussey et al. (1991) evaluated the level of MI and MA resistance in 139 soybean cultivars from Maturity Groups V to VIII. None of the 139 cultivars were considered to be highly resistant to MI (PI 96354 level) or MA (PI 200538 level). Twenty-eight and three percent of cultivars tested were identified as having a high level of resistance to MI and MA, respectively, based on a gall index of <=1.5. Twenty-four percent of the cultivars tested were found to be moderately resistant to MA and 23% to MI.

Inheritance of soybean resistance to MI was determined in crosses of the susceptible cultivar Bossier with two resistant plant introductions, PI 96354 and PI 417444 (Luzzi et al., 1994a). The entry-mean heritability of gall resistance in these PIs was found to range from 0.91 to 0.92 (based on the mean of three replications, seven plants per plot). In another study, Luzzi et al. (1994b) identified a major gene (Rmi) for resistance to MI. This single additive gene for resistance to galling was identified in the cultivar Forrest. Luzzi et al. (1995) determined inheritance of gall resistance to MA in soybean using crosses of the susceptible ‘CNS’, and the three resistant genotypes Jackson, PI 200538, and PI 230977. The entry-mean heritability for soybean resistance to MA was found to range from 0.74 to 0.83 (based on the mean of three replications, seven plants per plot). Developing soybean cultivars with high levels of MI and MA resistance and multispecies resistance is important for management of these nematodes (Boerma and Hussey, 1992; Boerma and Mian, 1998). The root-knot resistance of PI 96354 and PI 200538 is conditioned by one major and one minor quantitative trait locus (QTL) (Tamulonis et al., 1997a; 1997b; Li et al., 2001). Identification of additional plant introductions with resistance to MI and MA could prove beneficial if these lines possess unique resistance genes from those already found in PI 96354 and PI 200538.

Six hundred and eight germplasm lines from the southern provinces of the People's Republic of China were recently obtained and made available to researchers by Dr. R.L. Nelson (curator of USDA-ARS Soybean Germplasm Collection, Urbana, IL). These lines are the first to become available to U.S. scientists from many of these southern provinces in China. The accessions range from Maturity Group II to Maturity Group IX due to the wide range of planting dates for soybean (spring, summer, fall, and winter) in this region of China. Because these germplasm lines have been selected for adaptation across a wide range of environments, they have the potential to possess diversity not previously available in the USA (R.L. Nelson, 2000, personal communication). The objective of this research was to identify additional sources of MI and MA resistance in these recently obtained Chinese soybean germplasm lines.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
A greenhouse screening assay consisting of four screening levels was used to evaluate the 608 germplasm lines for MI and MA resistance (Luzzi et al., 1987). Each screening level was designed to systematically identify MI and MA lines with low gall numbers. At each progressive level, the number of replications and/or amount of inoculum was increased (Table 1). A randomized complete block experimental design was used for Levels II, III, and IV.


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  		Table 1. Number of replications, inoculum densities, and soybean PIs screened for each Meloidogyne species in each screening level.

 
For all screening levels, three seed of each genotype were individually planted into 206-mm Ray Leach Single Cell Cone-tainers (Model LD-UV SC-10, Stuewe & Sons, Inc., Corvallis, OR) containing {approx}15.6 cm2 of methyl bromide-fumigated Pacolet sandy loam soil (fine, kaolinitic, thermic Typic Kanhapludults), amended with methyl-bromide-fumigated sand to a texture of 80% sand, 12% silt, and 8% clay. Cones were placed in every other row of a 98-cone tray which allowed 45 Chinese PIs and four checks (49 cones per tray) in a 7-by-7 design. Resistant and susceptible checks were planted in each experiment to develop a gall index. The checks for the MI screening were: PI 96354 (highly resistant), Haskell (resistant), ‘GaSoy17’ (susceptible), and Bossier (highly susceptible). The checks for the MA screening included: PI 200538 (highly resistant), Haskell (resistant), GaSoy17 (susceptible), and CNS (highly susceptible) (Table 2).


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  		Table 2. Mean number of Meloidogyne arenaria and M. incognita galls produced on the soybean check lines in the Level I, II, and III greenhouse screening experiments.

 
Approximately 7 to 10 d after planting, the plants were thinned to one plant per cone and then inoculated with the appropriate number of nematode eggs. Meloidogyne incognita and MA were propagated on ‘Marion’ tomato (Lycopersicon esculentum Mill.) and egg inoculum was collected according to the procedure described by Hussey and Barker (1973). The number of eggs per milliliter was adjusted so that the desired inoculum density was applied in a volume of 3 to 5 mL. The inoculum was placed at a soil depth of 20 to 30 mm with a digital dispensing pump. Each plant was fertilized weekly with 6 mg N, 3 mg P, and 5 mg K. Supplemental light was provided by 400-W metal halide lamps which were suspended 1.4 m above the greenhouse bench. The plants were irrigated twice a day by a mechanical overhead irrigation system with water that was heated to 36°C ± 3°.

For Levels I, II, III, and IV, each experiment was terminated {approx}30 d after inoculation when galls had developed on the susceptible checks. Following removal of plants from the cones, the roots were excised, washed free of soil, and evaluated for gall number. In Level I, any PI with 10 galls or less was advanced to Level II. In Level II and III, a gall score of 1 (few galls) to 5 (many galls) was used. The gall score was established for each experiment based on the number of galls on the various checks (Table 2). In Level IV, the number of galls were counted on each plant to accurately quantify the degree of resistance. Data for galling were analyzed by analysis of variance using Agrobase (Agronomix Software, Inc., Manitoba, Canada).

Two resistant Chinese PIs for MA, and the two PIs for MI with the highest level of galling resistance were evaluated for nematode reproduction (number of eggs produced on the soybean roots). Each PI, along with resistant and susceptible checks, were individually planted into 0.5-L polystyrene cups (three seeds per cup) in a randomized complete block experimental design with 12 replications. Each cup was filled with the methyl bromide fumigated soil described above. Seven to 10 d after planting, plants were thinned to one per cup and then inoculated with 5000 nematode eggs. Inoculum source, fertilizer, and supplemental lighting were the same as previously described. Plants were watered manually twice each day.

Thirty to 70 d after inoculation, when brown egg masses developed on the susceptible check, the experiment was terminated and roots were excised and washed. Eggs were collected from each root system by cutting the roots into {approx}25-mm sections and then mechanically shaking them with a shaker for 3 min in 300 mL of a 0.5% NaOCl solution in 500-mL polypropylene jars. Eggs per root system were determined by counting the number of eggs in an aliquot of each suspension. Egg data transformed by a log10(x + 1) conversion were analyzed by analysis of variance procedures using Agrobase.

For MI, a second nematode reproduction experiment was conducted. This experiment included PI 594470C, PI 594538A, PI 594596, and PI 594401B, along with the checks PI 96354, Haskell, and Bossier. The experimental protocol and data analysis were similar to those described for the initial MI reproduction experiment.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Meloidogyne arenaria
From the 608 PIs included in Level I, 116 PIs with <=10 galls, as well as those PIs that did not emerge, were advanced to Level II (Table 1). In Level II, 23 PIs with a gall score of 1 (0–5 galls) or 2 (16–30 galls) were advanced to Level III. In Level III, seven PIs with a gall score of 1 (0–10 galls), 2 (11–20 galls), or 3 (21–30 galls) were advanced to Level IV. Of the seven PIs evaluated in Level IV, PI 594427C and PI 594403 averaged 11 and 14 galls per plant, respectively (Table 3). In Level IV, CNS averaged 57 galls per plant, Haskell averaged 17, and PI 200538 averaged 8. Plant Introduction 594427C was as resistant to MA gall formation as the highly resistant check PI 200538. Plant Introduction 594403 produced a similar number of galls as the resistant check Haskell.


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  		Table 3. Mean Meloidogyne arenaria gall production on seven Chinese soybean plant introductions and checks evaluated in Level IV greenhouse tests and egg production on selected Chinese plant introductions and checks.

 
In a MA reproduction experiment, CNS averaged 136 000 eggs per plant, Haskell averaged 72 000, and PI 200538 averaged 102 000 (Table 3). Plant Introduction 594427C produced {approx}87 000 eggs per plant and was equal in resistance to PI 200538 (highly resistant check). Plant Introduction 594403 produced {approx}62 000 eggs per plant and was equal in resistance to Haskell.

The reproduction of MA was variable, with PI 594427C having more MA eggs than PI 594403 even though the PI 594427C had the fewest galls. Also, the highly resistant check had more eggs than Haskell. Variation in MA reproduction also occurred in the study by Luzzi et al. (1987), where although the resistant check Jackson produced 45 400 eggs per plant compared with 29 000 eggs for PI 200538, the difference (16 400) in egg number was only slightly greater than the number of eggs (15 400) required to achieve significance at the 5% level.

The MA resistance identified in PI 594427C and PI 594403 needs to be evaluated for unique MA resistance genes. Tamulonis et al. (1997a) found two QTLs in PI 200538 for MA that accounted for 51% of the variation in gall number. These newly identified sources of MA resistance are important if they contain different resistance QTLs than those previously identified in MA-resistant soybean lines. The unique MA resistance genes could be pyramided with MA resistance genes in existing soybean cultivars to produce a cultivar with a superior or broader level of MA resistance.

Meloidogyne incognita
From the 608 PIs in Level I, 71 (12%) with 10 galls or less, or those that did not germinate were advanced to Level II (Table 1). In Level II, 17 PIs with a gall score of 1 (0–4 galls) or 2 (5–8 galls) were advanced to Level III. Of the 17 PIs, seven averaged eight galls or less, and the other 10 PIs averaged four galls or less. In Level III, seven PIs with a gall score of 1 (0–5 galls) or 2 (6–10 galls) were advanced to Level IV. In Level IV, two of the seven PIs, PI 594775A and PI 594753A, each averaged zero galls on the roots (Table 4). Bossier averaged 87 galls per plant, Haskell averaged four, and PI 96354 averaged zero. Four other of the Chinese PIs, PI 594470C, PI 594538A, PI 594401B, and PI 594596 each averaged two galls or less per plant, which was less than Haskell (resistant check) but more than PI 96354 (highly resistant check).


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  		Table 4. Mean Meloidogyne incognita gall production on seven Chinese soybean plant introductions and checks evaluated in Level IV greenhouse tests and egg production on selected Chinese plant introductions and checks.

 
In the initial MI reproduction experiment, Bossier averaged 10 900 eggs per plant, Haskell averaged 3 600 eggs per plant, and PI 96354 averaged 400 (Table 4). Plant Introduction 594753A produced {approx}12 000 eggs per plant, and PI 594775A produced 16 000 eggs per plant. Both of these PIs from China produced an equal number of eggs per plant as the highly susceptible Bossier.

The Chinese accessions PI 594470C, PI 594538A, PI 594596, and PI 594401B were evaluated in the second MI reproduction experiment. Plant Introduction 594470C and PI 594538A produced an equal or greater number of MI eggs as the susceptible check Bossier. Plant Introduction 594596 and PI 594401B produced fewer eggs than the susceptible check Bossier, but more eggs than the two resistant checks Haskell and PI 96354.

The MI screening produced unexpected results. The two Chinese PIs, PI 594775A and PI 594753A, with gall resistance equal to the highly resistant check, PI 96354, both had egg numbers equal to the susceptible check Bossier. Similarly, four PIs produced fewer galls than the resistant check Haskell but supported more MI reproduction than Haskell. Further experimentation is required to investigate the genetic basis for resistance in these two PIs that show resistance to gall formation, but supported high nematode reproduction. Shepherd (1979) found that on certain cotton (Gossypium hirsutum) accessions gall index and egg counts were independent of each other, indicating the need for selection for both galling and nematode reproduction to develop a highly resistant cotton cultivar. Our results also illustrate the importance of quantifying both MI gall and reproduction resistance in the development of MI-resistant soybean cultivars.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Research supported by state and Hatch funds allocated to the Georgia Agric. Exp. Stns. and a grant from the United Soybean Board.

Received for publication July 10, 2002.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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