A nematode, fungus, and aphid interact via a shared host plant: Implications for soybean management

Entomologia Experimentalis et Applicata

Volumn 143, Issue 1, 2012, Pages 55-66

  Mccarville, M T ^a   O'Neal, M ^a   Tylka, G L ^a   Kanobe, C ^a   Macintosh, G C ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Aphididae; Aphis glycines; Brown stem rot; Cadophora gregata; Glycine max; Hemiptera; Heterodera glycines; Heteroderidae; Host plant resistance; Nematoda; Soybean aphid; Soybean cyst nematode

Indexed keywords

APHID; CULTIVAR; CYST; FUNGAL DISEASE; FUNGUS; HOME RANGE; HOST PLANT; HOST-PARASITE INTERACTION; INFECTIVITY; NEMATODE; PEST SPECIES; PLANT-HERBIVORE INTERACTION; SOYBEAN;

UNITED STATES;

APHIDIDAE; APHIS GLYCINES; CADOPHORA GREGATA; FABACEAE; FUNGI; GLYCINE (ANGIOSPERM); GLYCINE MAX; HEMIPTERA; HETERODERA GLYCINES; HETERODERIDAE; NEMATODA;

EID: 84857688934     PISSN: 00138703     EISSN: 15707458     Source Type: Journal    
DOI: 10.1111/j.1570-7458.2012.01227.x     Document Type: Article

References (61)

1. Allington WB & Chamberlain DW (1948) Brown stem rot of soybean. Phytopathology 38: 793-802.
2. Bezemer TM, De Deyn GB, Bossinga TM, van Dam NM, Harvey JA & van der Putten WH (2005) Soil community composition drives aboveground plant-herbivore-parasitoid interactions. Ecology Letters 8: 652-661.
3. Bilyeu K, Pavalli L, Sleper D & Beuselinck P (2005) Mutations in soybean microsomal omega-3 fatty acid desaturase genes reduce linolenic acid concentration in soybean seeds. Crop Science 45: 1830-1836.
4. Casteel CL, Walling LL & Paine TD (2006) Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomologia Experimentalis et Applicata 121: 67-72.
5. Chappell AS & Bilyeu KD (2007) The low linolenic acid soybean line PI361088B contains a novel GmFAD3A mutation. Crop Science 47: 1705-1710.
6. Chen YH & Welter SC (2003) Confused by domestication: incongruent behavioral responses of the sunflower moth, Homoeosoma electellum (Lepidoptera: Pyralidae) and its parasitoid, Dolichogenidea homoeosomae (Hymenoptera: Braconidae), towards wild and domesticated sunflowers. BioControl 28: 180-190.
7. Chiozza MV, O'Neal ME & MacIntosh GC (2009) Constitutive and induced differential accumulation of amino acid in leaves of susceptible and resistant soybean plants in response to the soybean aphid (Hemiptera: Aphididae). Environmental Entomology 39: 856-864.
8. Department of HHS (Health and Human Services) and USDA (United States Department of Agriculture) (2005) Dietary Guidelines for Americans. Available at: (accessed 23/01/2012).
9. Faghihi J & Ferris JM (2000) An efficient new device to release eggs from Heterodera glycines. Journal of Nematology 32: 411-413.
10. Fehr WR (2006) Breeding for modified fatty acid composition in soybean. Crop Science 47: S72-S87.
11. Fehr WR & Caviness CE (1977) Stages of soybean development. Iowa Agricultural and Home Economics Experiment Station Special Report 80: 3-11.
12. Giordanengo P, Brunissen L, Rusterucci C, Vincent C, van Bel A et al. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. Comptes Rendus Biologies 333: 516-523.
13. Glover KD, Wang D, Arelli PR, Carlson SR, Cianzio SR & Diers BW (2004) Near isogenic lines confirm a soybean cyst nematode resistance gene from PI 88788 on linkage group. Crop Science 44: 936-941.
14. Goggin FL (2007) Plant-aphid interactions: molecular and ecological perspectives. Current Opinion in Plant Biology 10: 399-408.
15. Gunduz I, Buss GR, Chen P & Tolin SA (2004) Genetic and phenotypic analysis of Soybean mosaic virus resistance in PI 88788 soybean. Phytopathology 94: 687-692.
16. Hanafi A, Radcliffe EB & Ragsdale DW (1989) Spread and control of potato leafroll virus in Minnesota. Journal of Economic Entomology 82: 1201-1206.
17. Harrington TC, Steimel J, Workneh F & Yang XB (2003) Characterization and distribution of two races of Phialophora gregata in the North-Central United States. Phytopathology 93: 901-912.
18. Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA et al. (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biological Invasions 12: 2913-2931.
19. Hill CB, Li Y & Hartman GL (2006) A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Science 46: 1601-1605.
20. Hill CB, Crull L, Herman TK, Voegtlin DJ & Hartman GL (2010) A new soybean aphid (Hemiptera: Aphididae) biotype identified. Journal of Economic Entomology 103: 509-515.
21. Hong SC, Donaldson J & Gratton C (2010) Soybean cyst nematode effects on soybean aphid preferance and performance in the laboratory. Environmental Entomology 39: 1561-1569.
22. Hong SC, MacGuidwin A & Gratton C (2011) Soybean aphid (Aphis glycines Matsumura) and soybean cyst nematode (Heterodera glycines Ichinohe) interactions in the field and effects on soybean yield. Journal of Economic Entomology 104: 1568-1574.
23. Hughes TJ, Kurtzweil NC, Diers BW & Grau CR (2004) Resistance to brown stem rot in soybean germ plasm with resistance to the soybean cyst nematode. Plant Disease 88: 761-768.
24. Hyten DL, Song Q, Zhu Y, Choi I, Nelson RL et al. (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proceedings of the National Academy of Sciences of the USA 103: 16666-16671.
25. Jenkins WR (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Report 48: 692.
26. Kaplan I, Sardanelli S & Denno RF (2009) Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecological Entomology 34: 262-270.
27. Kim KS & Diers BW (2009) The associated effects of the soybean aphid resistance locus Rag1 on soybean yield and other agronomic traits. Crop Science 49: 1726-1732.
28. Kim KS, Hill CB, Hartman GL, Mian MAR & Diers BW (2008) Discovery of soybean aphid biotypes. Crop Science 48: 923-928.
29. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M & Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689-710.
30. Mardorf JL, Fehr WR & O'Neal ME (2010) Agronomic and seed traits of soybean lines with the Rag1 gene for aphid resistance. Crop Science 50: 1891-1895.
31. Matsui K (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Current Opinion in Plant Biology 9: 274-280.
32. Mazur B, Krebbers E & Tingey S (1999) Gene discovery and product development for grain quality traits. Science 285: 372-375.
33. Mian MAR, Hammond RB & Martin SKS (2008) New plant introductions with resistance to the soybean aphid. Crop Science 48: 1055-1061.
34. Niblack TL, Lambert KN & Tylka GL (2006) A model plant pathogen from the kingdom animalia: Heterodera glycines, the soybean cyst nematode. Annual Review of Phytopathology 44: 283-303.
35. Nombela G, Williamson VM & Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Plant-Microbe Interactions 16: 645-649.
36. Patzoldt ME, Grau CR, Stephens PA, Kurtzweil NC, Carlson SR & Diers BW (2005) Localization of a quantitative trait locus providing brown stem rot resistance in the soybean cultivar Bell. Crop Science 45: 1241-1248.
37. Pimentel D, Zuniga R & Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273-288.
38. Ragsdale DW, McCornack BP, Venette RC, Potter BD, MacRae IV et al. (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). Journal of Economic Entomology 100: 1258-1267.
39. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE & Desneux N (2011) Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56: 375-399.
40. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S et al. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737.
41. SAS Institute (2001) Proc User's Manual, 6th edn. SAS Institute, Cary, NC, USA.
42. Schmitt DP, Wrather JA & Riggs RD (2004) The Biology and Management of Soybean Cyst Nematode, 2nd edn. Schmitt & Associates, Marceline, MO, USA.
43. Seah S, Telleen AC & Williamson VM (2007) Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theoretical and Applied Genetics 114: 1289-1302.
44. Sell P & Kuo-Sell HL (1990) Influence of infestation of oats by root-knot nematodes (Meloidogyne sp.) on the performance of the cereal aphid, Metopolophium dirhodum (Walk) (Homoptera: Aphididae). Journal of Applied Entomology 109: 37-43.
45. Shah J (2005) Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annual Review of Phytopathology 43: 229-260.
46. Simberloff D & Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1: 21-32.
47. Smith CM & Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122: 1-16.
48. Tabor GM, Tylka GL, Behm JE & Bronson CR (2003) Heterodera glycines infection increases incidence and severity of brown stem rot in both resistant and susceptible soybean. Plant Disease 87: 655-661.
49. Tabor GM, Tylka GL & Bronson CR (2006a) Soybean stem colonization by genotypes A and B of Cadophora gregata increases with increasing population densities of Heterodera glycines. Plant Disease 90: 1297-1301.
50. Tabor GM, Tylka GL & Bronson CR (2006b) Genotypes A and B of Cadophora gregata differ in ability to colonize susceptible soybean. Plant Disease 91: 574-580.
51. Tylka GL, Gebhart GD, Marett CC, Mullaney MP & Wiggs SN (2010) Evaluation of Soybean Varieties Resistant to Soybean Cyst Nematode in Iowa-2010. IPM 52, Iowa State University, University Extension and Iowa Soybean Association, Ames, IA, USA.
52. Vandegehuchte ML, de la Pena E & Bonte D (2010) Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field. Oikos 119: 1011-1019.
53. Venette RC & Ragsdale DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Annals of the Entomological Society of America 97: 219-226.
54. Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L et al. (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology 16: 1365-1369.
55. Walling LL (2008) Avoiding effective defenses: strategies employed by phloem feeding insects. Plant Physiology 146: 859-866.
56. Will T, Tjallingii WF, Thonnessen A & van Bel AJE (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences of the USA 104: 10536-10541.
57. Workneh F, Tylka GL, Yang XB, Faghihi J & Ferris JM (1999) Regional assessment of soybean brown stem rot, Phytophthora sojae, and Heterodera glycines using area-frame sampling: prevalence and effects of tillage. Phytopathology 89: 204-211.
58. Wurst S & van der Putten WH (2007) Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores. Basic and Applied Ecology 8: 491-499.
59. Yen JH, Niblack TL & Wiebold WJ (1995) Dormancy of Heterodera glycines in Missouri. Journal of Nematology 27: 153-163.
60. Zhang GR, Gu CH & Wang DC (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theoretical and Applied Genetics 118: 473-482.
61. Zhang G, Gu C & Wang D (2010) A novel locus for soybean aphid resistance. Theoretical and Applied Genetics 120: 1183-1191.