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CROP BREEDING & GENETICS

Soybean Aphid Resistance in Soybean Jackson Is Controlled by a Single Dominant Gene

^a Dep. of Crop Sciences, Univ. of Illinois, 1101 West Peabody Drive, Urbana, IL 61801
^b USDA-ARS and Dep. of Crop Sciences, Univ. of Illinois, 1101 West Peabody Drive, Urbana, IL 61801
^c 6029 S. Kimbark Ave. Apt. 1, Chicago, IL 60637

^* Corresponding author (curthill{at}uiuc.edu)

	ABSTRACT

TOP NOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The soybean aphid, Aphis glycines Matsumura, has become established as a serious pest of soybean, Glycine max (L.) Merr., since it was first found in North America in 2000 and has caused millions of dollars in economic losses. While the application of chemical insecticides is the only means to control the soybean aphid at present, genetic resistance to the aphid was recently discovered in soybean. A single dominant gene named Rag1 that controls resistance to the soybean aphid was found in the cultivar Dowling. Another cultivar found to have strong antibiosis-type resistance to the soybean aphid was Jackson. The primary objective of this study was to determine the inheritance of resistance to the soybean aphid in Jackson. Segregation of resistance was analyzed in F₂ and among F₂–derived F₃ (F_2:3) families produced from crosses between Jackson and the susceptible soybean cultivar Loda. Segregation of F₂ plants was 247 resistant to 97 susceptible and fit a 3:1 genetic ratio (P = 0.17). Segregation among F_2:3 families was not clear because a number of susceptible F₂ plants did not produce a sufficient amount of seed for progeny testing. Ignoring the susceptible class, the segregation of F_2:3 families fit a 1:2 (all resistant/segregating) ratio. These results indicated that a single dominant gene controlled resistance in Jackson. There is no known genetic relationship between Jackson and Dowling. The genetic relationship between Rag1 in Dowling and the gene in Jackson is unknown.

	INTRODUCTION

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THE SOYBEAN APHID was found in North America in 2000 (Hartman et al., 2001) and has spread throughout the main soybean production areas (Ragsdale et al., 2004). The pest caused extensive economic losses in soybean in several midwestern states in 2003. Nearly 1.6 million ha of soybean were damaged in Minnesota with an estimated loss of US$80 million (Associated Press, 2003). In Illinois, about 0.5 million ha were damaged with an estimated loss of US$45 million (Steffey, 2004). Nearly 3 million ha of soybeans were sprayed to control the soybean aphid in the USA in 2003 (Landis et al., 2003), with US$9 to 12 million spent in Illinois alone (Steffey, 2004). Until the recent discovery of plant resistance to the soybean aphid (Hill et al., 2004), chemical insecticide application was the only available means to control the pest.

Plant insect resistance is an important component of an integrated pest management program to control insects (Auclair, 1989; Harrewijn and Minks, 1989). It is a cost effective and environmentally safe control method (Luginbill, 1969), and it is a plant trait governed by the same genetic mechanisms that condition other plant traits (Auclair, 1989).

Strong antibiosis-type resistance to the soybean aphid was found in soybean germplasm, including the cultivars Dowling and Jackson (Hill et al., 2004; Li et al., 2004). There is no known genetic relationship between Dowling and Jackson (Hill et al., 2004). Resistance in the ancestral soybean cultivar Dowling was controlled by a single dominant gene named Rag1 (Hill et al., 2006). Inheritance of resistance in Jackson has not been determined.

Knowledge on the inheritance of insect resistance is useful in the design of appropriate breeding procedures to develop resistant cultivars and for the identification of biotypes that may already exist or develop over time (Smith, 1989). Because qualitative, or simply inherited traits, require different breeding methods than quantitative traits controlled by many genes, the objective of this study was to determine the inheritance of soybean aphid resistance in Jackson.

	MATERIALS AND METHODS

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Crosses were made between the soybean aphid resistant cultivar Jackson and the susceptible soybean cultivar Loda as previously described (Hill et al., 2006). All crosses were made in one direction; pollen from Loda was transferred onto stigmata of Jackson flowers. Seed produced from individual crosses was harvested and planted separately for F₂ seed production in a greenhouse maintained at 28°C with supplemental lighting provided by a mixture of 1000-W high intensity discharge and high pressure sodium vapor lamps set to give a 14-h photoperiod. F₁ hybrid plants were distinguished from selfs by the expression of flower color that was polymorphic among the parents. Loda had purple flowers whereas Jackson had white flowers. Purple flower is dominant over white (Takahashi and Fukuyama, 1919).

The parents and F₂ plants were tested for soybean aphid resistance in a choice test in the greenhouse. Methods for plant culture, aphid infestation, and experimental design were described previously (Hill et al., 2004, 2006). Seeds were planted at a rate of one seed per pot in soilless media (Sunshine Mix, LC1, Sun Gro Horticulture Inc., Bellevue, WA) in 48-pot plastic inserts, with 12 rows of four pots (Hummert International, Earth City, MO, no. 1204) contained in flats without drainage holes (Hummert International, Earth City, MO, no. F1020). Genotypes were planted in four-pot rows. Ninety rows of the F₂ population, six rows of Jackson, and 13 rows of Loda were randomized and interspersed throughout the test. Three weeks after aphid infestation, the level of aphid colonization on each individual plant was estimated by visually examining aphid density, aphid mortality, and plant damage on leaves and stems using the following 0-to-4 scale, where 0 = no aphids present; 1 = few solitary live or dead aphids (dead aphid bodies present); 2 = several transient aphids (aphids possibly probing for a suitable feeding site present) with some viviparous aptera surrounded by a few nymphs; 3 = dense colonies; and 4 = dense colonies accompanied by plant damage, including leaf distortion and stunting (Hill et al., 2006). Plants in the F₂ population were considered resistant when they had the phenotype of the resistant parent Jackson (rating 0, 1, or 2) and susceptible when they had the susceptible Loda phenotype (rating 3 or 4).

All F₂ plants were transplanted to produce F_2:3 seed (F₂–derived F₃ lines) for progeny testing and genotyping using previously described methods (Hill et al., 2006). Progeny from all F₂ plants that produced at least 12 F₃ seeds, regardless of F₂ soybean aphid resistance phenotype, were planted with the parents and tested for aphid resistance in randomized four-pot rows as described above. Of the 344 F₂ plants transplanted, 172 plants produced the minimum required 12 seeds. A minimum of 10 F_2:3 plants was required to determine the F₂ genotypes. There were 149 total F_2:3 families out of the 172 planted that had at least 10 viable plants to rate for aphid resistance.

² tests were performed to test the goodness of fit of observed segregations among F₂ plants and F_2:3 families with different genetic ratios. Segregation among F_2:3 families with a minimum of 10 plants was analyzed after classifying each family as homozygous resistant (all plants had a rating of 0 to 2), homozygous susceptible (all plants had a rating 3 to 4), and heterozygous (both resistant and susceptible plants were identified).

	RESULTS

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Expression of resistance in the Jackson x Loda F₂ and F_2:3 populations was qualitative. The frequency distribution of aphid colonization ratings was non-normal and skewed toward rating 1 (data not shown). Aphid colonization ratings for Jackson plants were 0, 1, or 2 and ratings for Loda were 3 or 4. Only the parental phenotypes were observed in the F₂. Segregation of the F₂ population was 247 resistant plants and 97 susceptible plants and fit a 3:1 ratio (P = 0.17).

From the randomly selected 149 Jackson x Loda F_2:3 families, there were only 26 F_2:3 families from F₂ plants scored as susceptible that were included in the progeny tests. The ratio of 123:26 did not fit a 3:1 ratio and did not fully represent the F₂ population. Progeny from susceptible F₂ plants were under-represented in the F₃ generation, probably because many susceptible F₂ plants did not produce the minimum 12 seeds required for the progeny test. The plants may have been weakened by the aphid feeding damage and did not recover sufficiently after killing the aphids with insecticide after transplanting. The under-representation of susceptible F₂ plants in the F₃ generation prevented testing the fit to a complete 1:2:1 ratio with F_2:3 families from susceptible F₂ plants. Therefore, the fit of the segregation of just the F_2:3 families from resistant F₂ plants to a 1:2 resistant/segregating ratio was tested. In the F₃ generation, the following were found: 42 families with all resistant plants, 86 families with both resistant and susceptible plants, and 21 families with all susceptible plants (Table 1). The ratio of 42:86 resistant/segregating or heterozygous F_2:3 families significantly fit the 1:2 resistant/segregating (heterozygote) ratio expected for a monogenic dominant gene (P < 0.001). Out of 26 F₂ plants that were scored as susceptible, four F₂ plants were actually heterozygous and one was homozygous for resistance and not susceptible, as originally scored in the F₂ generation. Therefore, there was about a 19% rate of error in scoring susceptible F₂ plants. Applying the 19% error rate for susceptible plants to the original F₂ data gives an adjusted ratio of 265:79 resistant/susceptible F₂ plants. This ratio also fit a 3:1 resistant/susceptible ratio (P = 0.38).

	DISCUSSION

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According to information provided in GRIN, the Germplasm Resources Information Network, Jackson and Dowling have no known genetic relationship (Hill et al., 2004). It is possible that the soybean aphid resistance gene found in Jackson and Rag1 found in Dowling are unique and nonallelic; however, genetic allelism tests that involve analysis of segregation for aphid resistance in F₂ plants from crosses between the two cultivars or lines homozygous for each gene are required to determine the genetic relationship between the genes. No known biotypes of A. glycines exist that are distinguished by the reactions of plants possessing these genes (Hill et al., 2004).

Due to the simple inheritance of the gene found in Jackson and the ease of distinguishing resistant from susceptible plants in aphid resistance bioassays, soybean breeders will be able to rapidly convert existing soybean cultivars into aphid resistant cultivars using efficient back cross breeding procedures. Breeders now have two sources of resistance with dominant soybean aphid resistance genes to use to combat the soybean aphid.

	ACKNOWLEDGMENTS

 
We thank the United Soybean Board for partial support of this research through USB Project #4243 and the undergraduate students who assisted in conducting the tests in this project.

	NOTES

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Trade and manufacturers' names are necessary to report factually on available data; however, the USDA neither guarantees nor warrants the standard of the product, and the use of the name by the USDA implies no approval of the product to the exclusion of others that may also be suitable.

Received for publication November 28, 2005.

	REFERENCES

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• Associated Press. 2003. Aphids whittling soybean farmers' profits [Online]. Available at www.cnn.com/2003/US/Midwest/11/25/soybean.aphids.ap (posted 25 November 2003; verified 24 Mar. 2006).
• Auclair, J.L. 1989. Host plant resistance. p. 225–265. In A.K. Minks and P. Harrewijn (ed.) Aphids: Their biology, natural enemies, and control. Vol. C. Elsevier, New York.
• Harrewijn, P., and A.K. Minks. 1989. Integrated aphid management: General aspects. p. 267–272. In A.K. Minks and P. Harrewijn (ed.) Aphids: Their biology, natural enemies, and control. Vol. C. Elsevier, New York.
• Hartman, G.L., L.L. Domier, L.M. Wax, C.G. Helm, D.W. Onstad, J.T. Shaw, L.F. Solter, D.J. Voegtlin, C.J. D'Arcy, M.E. Gray, K.L. Steffey, S.A. Isard, and P.L. Orwick. 2001. Occurrence and distribution of Aphis glycines on soybeans in Illinois in 2000 and its potential control [Online]. Available at www.plantmanagementnetwork.org/pub/php/. Plant Health Progress DOI 10.1094/PHP-2001-0205-01-HN.
• Hill, C.B., Y. Li, and G.L. Hartman. 2004. Resistance to the soybean aphid in soybean germplasm. Crop Sci. 44:98–106.[Abstract/Free Full Text]
• Hill, C.B., Y. Li, and G.L. Hartman. 2006. Identification of a single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Sci. 46: this issue.
• Landis, D., M. Brewer, and G. Heimpel. 2003. Soybean aphid parasitoid questionnaire 2003 [Online]. Available at www.ncera125.ent.msu.edu/StateRpts2003MI.htm (verified 23 Mar. 2006) Michigan State Univ., East Lansing.
• Li, Y., C.B. Hill, and G.L. Hartman. 2004. Effect of three resistant soybean genotypes on the fecundity, mortality, and maturation of soybean aphid (Homoptera: Aphididae). J. Econ. Entomol. 97:1106–1111.[Medline]
• Luginbill, J.P. 1969. Developing resistant plants—The ideal method of controlling insects. USDA, ARS. Prod. Res. Rep. 111. U.S. Gov. Print. Office, Washington, DC.
• Ragsdale, D.W., D.J. Voegtlin, and R.J. O'Neil. 2004. Soybean aphid biology in North America. Ann. Entomol. Soc. Am. 97:204–208.[CrossRef]
• Smith, C.M. 1989. Plant resistance to insects: A fundamental approach. John Wiley & Sons, New York.
• Steffey, K.L. 2004. Soybean aphids in Illinois [Online]. www.ipm.uiuc.edu/fieldcrops/insects/soybean_aphids/workshop/SoybeanAphidsInIllinois_Steffey.ppt (verified 18 Mar. 2006). Univ. of Illinois at Urbana-Champaign.
• Takahashi, H., and J. Fukuyama. 1919. Morphological and genetic studies on the soybean. 10. Hokkaido Agric. Exp. Stn., Hokkaido, Japan.

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This Article Abstract Full Text (PDF) Free An erratum has been published Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (7) Citing Articles via Google Scholar Google Scholar Articles by Hill, C. B. Articles by Hartman, G. L. Search for Related Content PubMed Articles by Hill, C. B. Articles by Hartman, G. L. Agricola Articles by Hill, C. B. Articles by Hartman, G. L. Related Collections Soybean Insect Resistance Crop Genetics