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a Division of Plant Sciences, Univ. of Missouri-Delta Center, P.O. Box 160, Portageville, MO 63873
b Division of Plant Sciences, 271-F Life Sciences Center, Univ. of Missouri-Columbia, Columbia, MO 65211
c USDA-ARS, ORADC, Ohio State Univ., 107A Williams Hall, 1680 Madison Ave, Wooster, OH 44691
d Dep. of Plant Soils and General Agriculture, Southern Illinois Univ., Carbondale, IL 62901
e Univ. of Arkansas, 2501 N Young Ave, Fayetteville, AR 72704
* Corresponding author (shannong{at}missouri.edu).
ABSTRACT
Soybean [Glycine max (L.) Merr.] germplasm line S99-2281 (Reg. No. GP-361, PI 654356) was developed at the University of Missouri–Delta Center and released by the University of Missouri Agricultural Experiment Station. It is an F4 plant selection composited in the F5 generation from the cross of N90-516 x S92-1069. S99-2281 is a productive, early group V (relative maturity 5.2) soybean line with broad resistance to soybean cyst nematode (Heterodera glycines Ichinohe) HG types (races), southern root knot nematode [Meloidogyne incognita (Kofoid & White) Chitwood], and reniform nematode [Rotylenchulus reniformis (Linford and Oliveira)]. It also carries the Rcs3 gene for resistance to all known races of frogeye leaf spot, caused by Cercospora sojina K. Hara. In combined analyses over 3 yr, S99-2281 yielded 3 and 7% more than ‘Manokin’ in southeast Missouri trials (15 tests) and in Uniform Group IVs Tests–Southern States (39 tests), respectively. It will be useful as an elite parent in soybean breeding programs to develop productive soybean cultivars with broad resistance to frogeye leaf spot and resistance to multiple nematode species.
Abbreviations: indel, insertion deletion • RKN, root knot nematode • SCN, soybean cyst nematode • SNP, single nucleotide polymorphism • SSR, simple sequence repeats
Soybean [Glycine max (L.) Merr.] germplasm line S99-2281 (Reg. No. GP-361, PI 654356), an early group V (relative maturity 5.2) line, was developed at the University of Missouri–Delta Center, Portageville, MO. It was released because it is a productive soybean line with excellent resistance to frogeye leaf spot, caused by Cercospora sojina K. Hara, and resistance to three important nematode species. It was derived from the cross of N90-516 x S92-1069. The plant population was advanced from the F2 to F5 generations by the pedigree method. S99-2281 traces to a soybean cyst nematode (SCN, Heterodera glycines Ichinohe) resistant F4 selection composited in the F5 generation. As a breeding line, S99-2281 was tested in multiple environments in southeast Missouri in University of Missouri–Delta Center research tests and in the Uniform Group IV-S Tests–Southern States, where it exceeded the yield of the check cultivar Manokin. In various field and greenhouse screening trials, S99-2281 showed resistance to SCN HG types 2.5.7, 1.2.5.7, 0, 1.2.6.7, and 2.7 (races 1, 2, 3, 5, and 14), root knot nematode (RKN) [Meloidogyne incognita (Kofoid & White) Chitwood], and reniform nematode [Rotylenchulus reniformis (Linford and Oliveira)], and it has the Rcs3 gene for resistance to all known races of frogeye leaf spot. S99-2281 will be useful as an elite parent in soybean improvement programs because of its high yield potential, excellent resistance to frogeye leaf spot, and resistance to three nematodes species.
Materials and Methods
Parental Lines and Pedigree Information
S99-2281 originated from the cross of N90-516 x S92-1069 made in the field at Portageville, MO, in 1995. N90-516 is from ‘Hutcheson’ (Buss et al., 1988) x N83-1014. N83-1014 is from ‘Gasoy 17’ (Baker and Harris, 1979) x N77-940. N77-940 is from N70-1540 x Centennial (Hartwig and Epps, 1977). N70-1540 is from ‘Dare’ (Brim, 1966) x D65-6765. D65-6765 is a selection from D58-3358 [Jackson (4) x D49-2491 (Lee sib)] x D59-9289 (selection from D51-4877 x D55-4168). S92-1069 is from Manokin (Kenworthy et al., 1996) x ‘Hartwig’ (Anand, 1992). The F1 was grown in Puerto Rico during the winter of 1995–1996 to produce F2 seed.
Early Generation Selection and Line Development
The population was advanced from the F2 to F5 generations from 1996 to 1999 by the pedigree method. Individual F2 plants were selected, and the F3 to F4 generations were advanced in plant rows 3 m long and 0.76 m between rows in an SCN- and RKN-infested field at the University of Missouri Rhodes farm near Clarkton, MO. Seed from individual F2 plants and seed from four F3 and F4 plants selected from each row were screened to a mixture of SCN HG types 0, 1.2.6.7, and 2.7 (races 3, 5, and 14) in the winter in the greenhouse at Portageville, MO. Only SCN-resistant plants were advanced in each succeeding generation.
The SCN-resistant F5 plant rows 3 m in length and 0.76 m between rows tracing to SCN-resistant F4 plants from individual F3 families were grown at Portageville in 1999. Selected SCN-resistant F4:5 rows, which included row S99-2281, were harvested individually as bulk rows to form pure lines to test for yield, disease, and other agronomic traits in subsequent years.
Evaluation of Agronomic and Seed Traits
In 2000, S99-2281 was tested in a preliminary group V yield test with three replications in two environments at the University of Missouri–Delta Center Lee farm at Portageville, MO. It was tested from 2001 to 2003 in late IV–early V advanced yield tests in southeastern Missouri at the Delta Center and in several southern states in the Uniform Preliminary Group IV-S Test in 2001 (Paris and Bell, 2002) and the Uniform Group IV-S Test in 2002 and 2003 (Paris and Bell, 2003, 2004).
In southeastern Missouri, S99-2281 was tested in advanced tests in five environments in each of 3 yr (2001–2003) for yield and other agronomic traits. Three replicate tests were conducted in each of 3 yr at the Lee farm, which included two sites on Sharkey clay (very fine, smectitic, thermic Chromic Epilaquerts) and two sites on Dundee silt loam (fine-silty, mixed, active, thermic Typic Endoaqualfs). A single three-replicate test was conducted at Clarkton in each of the 3 yr on Bosket sandy loam (fine-loamy, mixed, active, thermic, Mollic Hapludalfs) with known infestations of SCN, predominantly HG type 1.2.6.7 (race 5) and southern root knot nematode. All plots in the southeastern Missouri tests were four rows, 4 m long and 0.76 m between rows arranged in a randomized complete block design. The plant population was approximately 400 plants plot–1 or 300,000 plants ha–1. The center two rows of each four-row plot were harvested for measurements of seed yield, recorded as kilograms per hectare; maturity date; plant height in centimeters measured from the ground to the tip of the plant main stem; and lodging score from 1 to 5, where 1 = all plants erect and 5 = all plants lodged flat.
The Uniform Group IV-S Tests–Southern States that included S99-2281 were conducted over a wide range of soil and climatic conditions in up to 14 states. In the Uniform Preliminary IV-S Test, data were included from seven locations (Paris and Bell, 2002). In the Uniform Group IV-S Test, data were analyzed over 17 and 14 locations, respectively, in 2002 and 2003 (Paris and Bell, 2003, 2004). Most tests were planted in four-row plots in two (Uniform Preliminary IV-S Test) or three replications (Uniform Group IV-S Test) with the two center rows used for data collection. Row widths varied from 0.36 to 1.0 m wide, with the majority of plots planted in 0.76-m rows. Plot lengths varied, with most plots being approximately 4 to 6 m long. Data were collected for yield, maturity, height, lodging, seed quality, seed size, seed protein, and seed oil.
Evaluation for Disease Resistance
S99-2281 was evaluated for resistance to SCN HG types 2.5.7, 1.2.5.7, 0, 1.2.6.7, and 2.7 (races 1, 2, 3, 5, and 14) in the greenhouse at Portageville and Columbia, MO, according to methods by Niblack et al. (2002). Field evaluation for RKN was conducted in fields planted after potatoes (Solanum tuberosum) at two sites in each of the 3 yr near Charleston, MO, in two replicate hill plots planted at 10 seeds hill–1 spaced 0.6 m apart in rows spaced 0.76 m between rows. Roots of genotypes were rated for root knot galling, with 1 = no galls and 5 = severe galling. In addition, S99-2281 was evaluated for resistance to reniform nematode at the University of Arkansas using the screening method outlined by Robbins et al. (1999).
Frogeye leaf spot ratings were made in two replicate hill plots at the University of Missouri–Delta Center, and at Southern Illinois University, Carbondale, in 2006 and 2007 in plantings as described for the RKN screening trials above. Plots were sprayed with conidia of C. sojina, and sprinkler irrigation was applied for several days to ensure good infection. N90-516, a parent of S99-2281 traces to Dare which traces to ‘Ogden’ the source of the Rcs3 gene, which is known to condition resistance to all known races of C. sojina in the United States (Phillips and Boerma, 1982) and to all isolates from Brazil (Yorinori, 1992). Simple sequence repeats (SSR), single nucleotide polymorphism (SNP), and insertion deletion (indel) markers are available for marker-assisted selection of this gene (Mian et al., 1999; Missaoui et al., 2007). Two SNPs (AQ455GA396 and AQ166AG280), one indel (AZ573CA150), and one SSR (Satt244) marker, which are located within 2 cM of the Rcs3 gene (Missaoui et al., 2007), were used to detect the presence of the gene in S99-2281. Two genotypes known to contain the Rcs3 gene (Davis and ‘Wright-Rcs3’) and two non-Rcs3 or susceptible genotypes (‘Blackhawk’ and ‘Wright’) were included in the analysis as checks. The SNP genotyping was conducted using the Allele Specific Primer Extension assay as described by Lee et al. (2004).
In the Uniform Group IV-S Tests–Southern States, reaction was assessed for various diseases, including SCN HG types 1.2.5.7, 0, and 2.7 (races 2, 3, and 14) and RKN. Details of data collection for various agronomic, seed and disease traits in the Uniform Soybean Group IV-S Tests–Southern States were given by Paris and Bell (2002, 2003, 2004).
Seed Purification
Purification of S99-2281 seed was initiated in 2002 and continued until 2006. Yield plot seed was initially planted and rouged to remove off-type plants for flower color, pubescence color, pod wall color, maturity, plant height and seed hila color in seed purification plots from 2002 to 2006. The center rows of four row seed plots of S99-2281 were harvested in each year using a plot combine that was thoroughly cleaned before harvest to ensure no contamination.
Statistical Analyses
All statistical analyses on yield and agronomic traits from the University of Missouri tests and agronomic, yield, and seed trait data for the southern uniform tests were conducted using SAS Version 9.1 (SAS Institute, Cary, NC). The statistical model included genotypes as fixed factors and locations as random factors. Means were separated for statistical significance by the Student's paired t test procedure with 
= 0.05.
Results and Discussion
Agronomic Performance
S99-2281 was compared to Manokin for yield in University of Missouri–Delta Center trials on each of three soil types from 2001 to 2003 (Table 1
). Yields of S99-2281 were significantly greater than Manokin on the medium- to coarse-textured loam and sandy soils but were significantly less on heavy clay (Table 1). This shows that S99-2281 is not well adapted to the Sharkey clay soil in which the soil is slowly drained and conditions are wetter than on lighter soils. However, S99-2281 yielded 700 kg ha–1 more than Manokin in fields at Clarkton, MO where natural infestations of SCN HG Types 1.2.5.7 and 1.2.6.7 (races 2 and 5) and southern root knot nematode were known to be present. Averaged over all soil types over the 3 yr, S99-2281 averaged 100 kg ha–1 more than Manokin, but this difference was not significant (Table 1).
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In research tests in southeastern Missouri and in the Uniform Group IV-S Tests–Southern States, S99-2281 was 2 to 3 d later in maturity, was 5 to 6 cm taller, and had similar lodging scores compared with Manokin (Tables 1 and 2 ).
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Disease Resistance
On the basis of disease trials conducted at the University of Missouri–Delta Center, and in the Uniform Group IV-S Tests-Southern States, S99-2281 has shown broad resistance to SCN HG types or races and RKN. In the Uniform Group IV-S Tests–Southern States (Paris and Bell, 2002, 2003, 2004), S99-2281 was resistant to SCN HG Types 1.2.5.7, 0, and 2.7 (races 2, 3, and 14) and RKN (Table 3
). In tests at the University of Missouri–Delta Center and at Columbia, S99-2281 also showed high resistance to SCN HG Type 2.5.7 or race 1 (female index of 2 versus 100 on the susceptible check) and HG Type 1.2.6.7 or race 5 (female index of 7 versus 100 on the susceptible check).
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S99-2281 was highly resistance (scores of 0) to frogeye leaf spot in field tests at the Delta Center and at Carbondale, IL, in 2006 and 2007. S99-2281 was predicted to carry the Rcs3 gene for frogeye leaf spot resistance because the four-marker haplotype (closely flanking the Rcs3 gene) of S99-2281 was identical to the four-marker haplotype of the two Rcs3-positive controls Davis and Wright-Rcs3 (Table 4 ).
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Availability
Seed of S99-2281 was deposited in the USDA Soybean Germplasm Collection. Small quantities of seeds for research purposes, including the development and commercialization of new cultivars, may be obtained from the corresponding author for at least 5 yr. We ask that the appropriate recognition be made if this germplasm contributes to the development of a new breeding line or cultivar.
Acknowledgments
The authors thank the North Central Soybean Research Program for the financial support in the development of this germplasm line through funding of the project "Managing frogeye leaf spot and charcoal rot in the north central region."
Footnotes
All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.
Received for publication June 2, 2008.
References
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