Exploiting natural variation to identify insect-resistance genes

Plant Biotechnology Journal

Volumn 9, Issue 8, 2011, Pages 819-825

  Broekgaarden, Colette ^a   Snoeren, Tjeerd A L ^a,b   Dicke, Marcel ^a   Vosman, Ben ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Nickerson Zwaan BV   (Netherlands)

Author keywords

Arabidopsis; Crop improvement; Molecular breeding; Phloem feeders; Transcript variation

Indexed keywords

PLANT DNA;

ANIMAL; BIOLOGICAL PEST CONTROL; BREEDING; DISEASE RESISTANCE; GENETIC VARIABILITY; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; INSECT; METABOLISM; METHODOLOGY; PARASITOLOGY; PATHOGENICITY; PLANT; PLANT GENE; QUANTITATIVE TRAIT LOCUS; REVIEW; TRANSGENIC PLANT;

ANIMALS; BREEDING; DISEASE RESISTANCE; DNA, PLANT; GENES, PLANT; GENETIC VARIATION; HOST-PARASITE INTERACTIONS; INSECTS; PEST CONTROL, BIOLOGICAL; PLANTS; PLANTS, GENETICALLY MODIFIED; QUANTITATIVE TRAIT LOCI;

ARABIDOPSIS; HEXAPODA;

EID: 80052435909     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2011.00635.x     Document Type: Review

References (95)

1. Allmann, S. and Baldwin, I.T. (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science, 329, 1075-1078.
2. Ben-Israel, I., Yu, G., Austin, M.B., Bhuiyan, N., Auldridge, M., Nguyen, T., Schauvinhold, I., Noel, J.P., Pichersky, E. and Fridman, E. (2009) Multiple biochemical and morphological factors underlie the production of methylketones in tomato trichomes. Plant Physiol. 151, 1952-1964.
3. Bergelson, J. and Roux, F. (2010) Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. Nat. Rev. Genet. 11, 867-879.
4. Bonaventure, G., Vandoorn, A. and Baldwin, I.T. (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci. doi:.
5. Bos, J.I.B., Prince, D., Pitino, M., Maffei, M.E., Win, J. and Hogenhout, S.A. (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet. 6, e1001216. doi:.
6. Broekgaarden, C., Poelman, E.H., Voorrips, R.E., Dicke, M. and Vosman, B. (2010) Intraspecific variation in herbivore community composition and transcriptional profiles in field-grown Brassica oleracea cultivars. J. Exp. Bot. 61, 807-819.
7. Cambron, S.E., Buntin, G.D., Weisz, R., Holland, J.D., Flanders, K.L., Schemerhorn, B.J. and Shukle, R.H. (2010) Virulence in Hessian fly (Diptera: Cecidomyiidae) field collections from the southeastern United states to 21 resistance genes in wheat. J. Econ. Entomol. 103, 2229-2235.
8. Chan, E.K.F., Rowe, H.C. and Kliebenstein, D.J. (2010) Understanding the evolution of defense metabolites in Arabidopsis thaliana using genome-wide association mapping. Genetics, 185, 991-1007.
9. Chen, W.J., Chang, S.H., Hudson, M.E., Kwan, W.K., Li, J., Estes, B., Knoll, D., Shi, L. and Zhu, T. (2005) Contribution of transcriptional regulation to natural variations in Arabidopsis. Genome Biol. 6, R32. doi:.
10. Clark, R.M., Schweikert, G., Toomajian, C., Ossowski, S., Zeller, G., Shinn, P., Warthmann, N., Hu, T.T., Fu, G., Hinds, D.A., Chen, H., Frazer, K.A., Huson, D.H., Scholkopf, B., Nordburg, M., Ratsch, G., Ecker, J.R. and Weigel, D. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science, 317, 338-342.
11. D'Alessandro, M. and Turlings, T.C.J. (2006) Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst, 131, 24-32.
12. DeBolt, S. (2010) Copy Number Variation shapes genome diversity in Arabidopsis over immediate family generational scales. Genome Biol. Evol. 2, 441-453.
13. Degenhardt, J., Hiltpold, I., Köllner, T.G., Frey, M., Gierl, A., Gershenzon, J., Hibbard, B.E., Ellersieck, M.R. and Turlings, T.C.J. (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc. Natl Acad. Sci. USA, 106, 13213-13218.
14. Diamond, J. (2002) Evolution, consequences and future of plant and animal domestication. Nature, 418, 700-707.
15. Dicke, M. (1999) Direct and indirect effects of plants on performance of beneficial organisms. In Handbook of Pest Management (Ruberson, J.R., ed), pp. 105-153, New York: Marcel Dekker.
16. Djupedal, I. and Ekwall, K. (2009) Epigenetics: heterochromatin meets RNAi. Cell Res. 19, 282-295.
17. Dodds, P.N. and Rathjen, J.P. (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548.
18. Doerge, R.W. (2002) Mapping and analysis of quantitative trait loci in experimental populations. Nat. Rev. Genet. 3, 43-52.
19. Du, B., Zhang, W., Liu, B., Hu, J., Wei, Z., Shi, Z., He, R., Zhu, L., Chen, R., Han, B. and He, G. (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc. Natl Acad. Sci. USA, 106, 22163-22168.
20. Edwards, D. and Batley, J. (2010) Plant genome sequencing: applications for crop improvement. Plant Biotechnol. J. 8, 2-9.
21. Eveland, A.L., McCarty, D.R. and Koch, K.E. (2008) Transcript profiling by 3'-untranslated region sequencing resolves expression of gene families. Plant Physiol. 146, 32-44.
22. Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Girousse, C., Faucher, M. and Bonnemain, J.L. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. C. R. Biol. 333, 566-573.
23. Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43, 701-726.
24. Grover, P.B. (1995) Hypersensitive response of wheat to the Hessian fly. Entomol. Exp. Appl. 74, 283-294.
25. Gust, A.A., Brunner, F. and Nürnberger, T. (2010) Biotechnological concepts for improving plant innate immunity. Curr. Opin. Biotechnol. 21, 204-210.
26. Haley, S.D., Peairs, F.B., Walker, C.B., Rudolph, J.B. and Randolph, T.L. (2004) Occurrence of a New Russian Wheat Aphid Biotype in Colorado. Crop Sci. 44, 1589-1592.
27. Hao, W. and Lin Hong-Xuan, H.X. (2010) Toward understanding genetic mechanisms of complex traits in rice. J. Genet. Genomics 37, 653-666.
28. Hao, P., Liu, C., Wang, Y., Chen, R., Tang, M., Du, B., Zhu, L. and He, G. (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol. 146, 1810-1820.
29. Hilker, M. and Meiners, T. (2010) How do plants "notice" attack by herbivorous arthropods? Biol. Rev. 85, 267-280.
30. Himabindu, K., Suneetha, K., Sama, V.S.A.K. and Bentur, J.S. (2010) A new rice gall midge resistance gene in the breeding line CR57-MR1523, mapping with flanking markers and development of NILs. Euphytica, 174, 179-187.
31. Huvenne, H. and Smagghe, G. (2010) Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 56, 227-235.
32. de Ilarduya, O.M., Xie, Q. and Kaloshian, I. (2003) Aphid-Induced Defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol. Plant Microbe Interact. 16, 699-708.
33. Imelfort, M., Duran, C., Batley, J. and Edwards, D. (2009) Discovering genetic polymorphisms in next-generation sequencing data: review article. Plant Biotechnol. J. 7, 312-317.
34. Jacobs, M.M.J., Vosman, B., Vleeshouwers, V.G.A.A., Visser, R.G.F., Henken, B. and van den Berg, R.G. (2010) A novel approach to locate Phytophthora infestans resistance genes on the potato genetic map. Theor. Appl. Genet. 120, 785-796.
35. Kaloshian, I. (2004) Gene-for-gene disease resistance: bridging insect pest and pathogen defense. J. Chem. Ecol. 30, 2419-2438.
36. Kalule, T. and Wright, D.J. (2005) Effect of cultivars with varying levels of resistance to aphids on development time, sex ratio, size and longevity of the parasitoid Aphidius colemani. Biocontrol, 50, 235-246.
37. Kaplan, I., Dively, G.P. and Denno, R.F. (2009) The costs of anti-herbivore defense traits in agricultural crop plants: a case study involving leafhoppers and trichomes. Ecol. Appl. 19, 864-872.
38. Kappers, I.F., Verstappen, F.W.A., Luckerhoff, L.L.P., Bouwmeester, H.J. and Dicke, M. (2010) Genetic variation in jasmonic acid- and spider mite-induced plant volatile emission of cucumber accessions and attraction of the predator Phytoseiulus persimilis. J. Chem. Ecol. 36, 500-512.
39. Kessler, A., Halitschke, R. and Baldwin, I.T. (2004) Silencing the Jasmonate cascade: induced plant defenses and insect populations. Science, 305, 665-668.
40. Keurentjes, J.J.B., Koornneef, M. and Vreugdenhil, D. (2008) Quantitative genetics in the age of omics. Curr. Opin. Plant Biol. 11, 123-128.
41. Kliebenstein, D.J. (2009a) Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu. Rev. Plant Biol. 60, 93-114.
42. Kliebenstein, D.J. (2009b) A quantitative genetics and ecological model system: understanding the aliphatic glucosinolate biosynthetic network via QTLs. Phytochem. Rev. 8, 243-254.
43. Kliebenstein, D.J., West, M.A.L., van Leeuwen, H., Kim, K., Doerge, R.W., Michelmore, R.W. and St. Clair, D.A. (2006) Genomic survey of gene expression diversity in Arabidopsis thaliana. Genetics, 172, 1179-1189.
44. Klingler, J., Kovalski, I., Silberstein, L., Thompson, G.A. and Perl-Treves, R. (2001) Mapping of cotton-melon aphid resistance in melon. J. Am. Soc. Hortic. Sci. 126, 56-63.
45. Klingler, J.P., Nair, R.M., Edwards, O.R. and Singh, K.B. (2009) A single gene, AIN, in Medicago truncatula mediates a hypersensitive response to both bluegreen aphid and pea aphid, but confers resistance only to bluegreen aphid. J Exp Bot 60, 4115-4127.
46. Klug, A. (2010) The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 79, 213-231.
47. Kollner, T.G., Held, M., Lenk, C., Hiltpold, I., Turlings, T.C.J., Gershenzon, J. and Degenhardt, J. (2008) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20, 482-494.
48. Kosma, D.K., Nemacheck, J.A., Jenks, M.A. and Williams, C.E. (2010) Changes in properties of wheat leaf cuticle during interactions with Hessian fly. Plant J. 63, 31-43.
49. Kumar, A., Jain, A., Sahu, R.K., Shrivastava, M.N., Nair, S. and Mohan, M. (2005) Genetic analysis of resistance genes for the rice gall midge in two rice genotypes. Crop Sci. 45, 1631-1635.
50. Kump, K.L., Bradbury, P.J., Wisser, R.J., Buckler, E.S., Belcher, A.R., Oropeza-Rosas, M.A., Zwonitzer, J.C., Kresovich, S., McMullen, M.D., Ware, D., Balint-Kurti, P.J. and Holland, J.B. (2011) Genome-wide association study of quantitative resistance to southern late blight in the maize nested association mapping population. Nat. Genet. 43, 163-168.
51. Kusnierczyk, A., Winge, P., Midelfart, H., Armbruster, W.S., Rossiter, J.T. and Bones, A.M. (2007) Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. J Exp Bot 58, 2537-2552.
52. Lawson, D.M., Lunde, C.F. and Mutschler, M.A. (1997) Marker-assisted transfer of acylsugar-mediated pest resistance from the wild tomato, Lycopersicon pennellii, to the cultivated tomato, Lycopersicon esculentum. Mol. Breeding, 3, 307-317.
53. Lewis, W.J., Van Lenteren, J.C., Phatak, S.C. and Tumlinson Iii, J.H. (1997) A total system approach to sustainable pest management. Proc. Natl Acad. Sci. USA, 94, 12243-12248.
54. Li, Y., Hill, C.B., Carlson, S.R., Diers, B.W. and Hartman, G.L. (2007) Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Mol. Breeding, 19, 25-34.
55. Liu, X.M., Smith, C.M., Friebe, B.R. and Gill, B.S. (2005) Molecular mapping and allelic relationships of Russian wheat aphid-resistance genes. Crop Sci. 45, 2273-2280.
56. Lorang, J.M., Sweat, T.A. and Wolpert, T.J. (2007) Plant disease susceptibility conferred by a "resistance" gene. Proc. Natl Acad. Sci. USA, 104, 14861-14866.
57. Martin, B., Rahbé, Y. and Fereres, A. (2003) Blockage of stylet tips as the mechanism of resistance to virus transmission by Aphis gossypii in melon lines bearing the Vat gene. Ann. Appl. Biol. 142, 245-250.
58. Meinke, D.W., Meinke, L.K., Showalter, T.C., Schissel, A.M., Mueller, L.A. and Tzafrir, I. (2003) A sequence-based map of Arabidopsis genes with mutant phenotypes. Plant Physiol. 131, 409-418.
59. Mitchell, C., Johnson, S.N., Gordon, S.C., Birch, A.N.E. and Hubbard, S.F. (2010) Combining plant resistance and a natural enemy to control Amphorophora idaei. Biocontrol, 55, 321-327.
60. Momotaz, A., Scott, J.W. and Schuster, D.J. (2010) Identification of quantitative trait loci conferring resistance to Bemisia tabaci in an F2 population of Solanum lycopersicum x Solanum habrochaites accession LA1777. J. Am. Soc. Hortic. Sci. 135, 134-142.
61. Mooney, K.A., Halitschke, R., Kessler, A. and Agrawal, A.A. (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science, 327, 1642-1644.
62. Morozova, O. and Marra, M.A. (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics, 92, 255-264.
63. Murugan, M., Khan, S.A., Cardona, P.S., Orozco, G.V., Viswanathan, P., Reese, J., Starkey, S. and Smith, C.M. (2010) Variation of resistance in barley against biotypes 1 and 2 of the Russian wheat aphid (Hemiptera: Aphididae). J. Econ. Entomol. 103, 938-948.
64. Nombela, G., Williamson, V.M. and Muñiz, M. (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant Microbe Interact. 16, 645-649.
65. Pavan, S., Jacobsen, E., Visser, R. and Bai, Y. (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol. Breeding, 25, 1-12.
66. Peng, J., Wang, H., Haley, S.D., Peairs, F.B. and Lapitan, N.L.V. (2007) Molecular mapping of the Russian wheat aphid resistance gene Dn2414 in wheat. Crop Sci. 47, 2418-2429.
67. Poelman, E.H., Van Dam, N.M., Van Loon, J.J.A., Vet, L.E.M. and Dicke, M. (2009) Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology, 90, 1863-1877.
68. Qiu, Y., Guo, J., Jing, S., Zhu, L. and He, G. (2010) High-resolution mapping of the brown planthopper resistance gene Bph6 in rice and characterizing its resistance in the 9311 and Nipponbare near isogenic backgrounds. Theor. Appl. Genet. 121, 1601-1611.
69. Ranger, C.M., Singh, A.P., Johnson-Cicalese, J., Polavarapu, S. and Vorsa, N. (2007) Intraspecific variation in aphid resistance and constitutive phenolics exhibited by the wild blueberry Vaccinium darrowi. J. Chem. Ecol. 33, 711-729.
70. Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. and Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl Acad. Sci. USA, 95, 9750-9754.
71. Salentijn, E.M.J., Pereira, A., Angenent, G.C., vanderLinden, C.G., Krens, F., Smulders M.J.M. and Vosman, B. (2007) Plant translational genomics: from model species to crops. Mol. Breeding, 20, 1-13.
72. Sanahuja, G., Banakar, R., Twyman, R.M., Capell, T. and Christou, P. (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnol. J. 9, 283-300.
73. Schoonhoven, L.M., van Loon, J.J.A. and Dicke, M. (2005) Insect-Plant Biology. New York: Oxford University Press.
74. Schuman, M.C., Heinzel, N., Gaquerel, E., Svatos, A. and Baldwin, I.T. (2009) Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytol. 183, 1134-1148.
75. Sebat, J., Lakshmi, B., Troge, J., Alexander, J., Young, J., Lundin, P., Manér, S., Massa, H., Walker, M., Chi, M., Navin, N., Lucito, R., Healy, J., Hicks, J., Ye, K., Reiner, A., Gilliam, T.C., Trask, B., Patterson, N., Zetterberg, A. and Wigler, M. (2004) Large-scale copy number polymorphism in the human genome. Science, 305, 525-528.
76. Slade, A.J. and Knauf, V.C. (2005) TILLING moves beyond functional genomics into crop improvement. Transgenic Res. 14, 109-115.
77. Snoeren, T.A.L., Kappers, I.F., Broekgaarden, C., Mumm, R., Dicke, M. and Bouwmeester, H.J. (2010) Natural variation in herbivore-induced volatiles in Arabidopsis thaliana. J. Exp. Bot. 61, 3041-3056.
78. Tester, M. and Langridge, P. (2010) Breeding technologies to increase crop production in a changing world. Science, 327, 818-822.
79. Thompson, J.N. (2005) Coevolution: the geographic mosaic of coevolutionary arms races. Curr. Biol. 15, R992-R994.
80. Todesco, M., Balasubramanian, S., Hu, T.T., Traw, M.B., Horton, M., Epple, P., Kuhns, C., Sureshkumar, S., Schwartz, C., Lanz, C., Laitinen, R.A.E., Huang, Y., Chory, J., Lipka, V., Borevitz, J.O., Dangl, J.L., Bergelson, J., Nordborg, M. and Weigel, D. (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature, 465, 632-636.
81. Van Poecke, R.M.P. (2008) Arabidopsis-Insect Interactions. In The Arabidopsis Book, pp. 1-34. Rockville, MD: The American Society of Plant Biologists.
82. Van Poecke, R.M.P. and Dicke, M. (2004) Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biol. 6, 387-401.
83. Varshney, R.K., Graner, A. and Sorrells, M.E. (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci. 10, 621-630.
84. Varshney, R.K., Nayak, S.N., May, G.D. and Jackson, S.A. (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol. 27, 522-530.
85. Vleeshouwers, V.G.A.A., Rietman, H., Krenek, P., Champouret, N., Young, C., Oh, S.K., Wang, M., Bouwmeester, K., Vosman, B., Visser, R.G.F., Jacobsen, E., Govers, F., Kamoun, S. and van der Vossen, E.A.G. (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora Infestans avirulence genes. PLoS ONE, 3, e2875. doi
86. Walling, L.L. (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146, 859-866.
87. Wang, T., Xu, S.S., Harris, M.O., Hu, J., Liu, L. and Cai, X. (2006) Genetic characterization and molecular mapping of Hessian fly resistance genes derived from Aegilops tauschii in synthetic wheat. Theor. Appl. Genet. 113, 611-618.
88. Wang, J., Song, W.K., Zhang, W.B., Liu, C.Y., Hu, G.H. and Chen, Q.S. (2009) Meta-analysis of insect-resistance QTLs in soybean. Hereditas, 31, 953-961.
89. Wu, J., Hettenhausen, C., Schuman, M.C. and Baldwin, I.T. (2008) A comparison of two Nicotiana attenuata accessions reveals large differences in signaling induced by oral secretions of the specialist herbivore Manduca sexta. Plant Physiol. 146, 927-939.
90. Yano, S. and Ohsaki, N. (1993) The phenology and intrinsic quality of wild crucifers that determine the community structure of their herbivorous insects. Res. Popul. Ecol. (Kyoto), 35, 151-170.
91. Yencho, G.C., Cohen, M.B. and Byrne, P.F. (2000) Applications of tagging and mapping insect resistance loci in plants. Annu. Rev. Entomol. 45, 393-422.
92. Yu, G.T., Cai, X., Harris, M.O., Gu, Y.Q., Luo, M.C. and Xu, S.S. (2009) Saturation and comparative mapping of the genomic region harboring hessian fly resistance gene H26 in wheat. Theor. Appl. Genet. 118, 1589-1599.
93. Zhang, G., Gu, C. and Wang, D. (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theor. Appl. Genet. 118, 473-482.
94. Zhang, G., Gu, C. and Wang, D. (2010) A novel locus for soybean aphid resistance. Theor. Appl. Genet. 120, 1183-1191.
95. Zhu, J.K. (2009) Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 43, 143-166.