Abstract
Rhopalosiphum padi, Schizaphis graminum, and Sitobion avenae are three of the most destructive aphid species of wheat (Triticum aestivum L.). They can significantly reduce wheat yields directly by feeding and indirectly by transmitting viruses. This study aimed to search for resistance to these aphid species among lines derived from different rye (Secale cereale) origins and from Aegilops speltoides, all in the genetic background of the wheat cultivar Pavon F76. Resistance was quantified as aphid weight (R. padi, S. avenae, and S. graminum) and the number of aphids and percentage of infested leaf area exhibiting chlorosis (S. graminum). The most resistant genotypes reduced R. padi and S. avenae weight by 24.2 and 34.3 %, respectively, at the seedling stage, compared with Pavon F76 control plants. Strong S. graminum resistance was found only in A. speltoides-derived lines, the most resistant of which (7A.7S-L5) sustained just 3 % chlorosis and reduced S. graminum colony weight by 67.7 %. One line carrying the 1AL.1RSam wheat–rye translocation from Amigo wheat (originally from Insave rye) reduced S. avenae weight by 23.2 and 21.8 % in seedling and adult plants, respectively. Single genotypes carrying the complete 1R chromosome or the 1RS chromosome arm derived from E12165 wheat and Presto triticale proved to be resistant to both R. padi and S. avenae at the seedling stage. Further research should be conducted to unravel the genetic basis of resistance to these aphids in 1RS genotypes. The sources of resistance identified here may be useful for incorporating multiple aphid species resistance in wheat breeding programs, particularly for R. padi and S. avenae, to which no resistant wheats have been bred.
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References
Berzonsky WA, Ding H, Haley SD, Harris MO, Lamb RJ, McKenzie RIH, Ohm HW, Patterson FL, Peairs FB, Porter DR, Ratcliffe RH, Shanower TG (2003) Breeding wheat for resistance to insects. Plant Breed Rev 22:221–296
Blackman RL, Eastop VF (2007) Taxonomic issues. In: Van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, Oxfordshire, UK, pp 1–29
Brunell MS, Lukaszewski AJ, Whitkus R (1999) Development of arm specific RAPD markers for rye chromosome 2R in wheat. Crop Sci 39(6):1702–1706
Burd JD, Porter DR (2006) Biotypic diversity in greenbug (Hemiptera: Aphididae): characterizing new virulence and host associations. J Econ Entomol 99(3):959–965
Caillaud CM, Dedryver CA, DiPietro JP, Simon JC, Fima F, Chaubet B (1995) Clonal variability in the response of Sitobion avenae (Homoptera: Aphididae) to resistant and susceptible wheat. Bull Entomol Res 85(2):189–195
Castaneda LE, Figueroa CC, Nespolo RF (2010) Do insect pests perform better on highly defended plants? Costs and benefits of induced detoxification defences in the aphid Sitobion avenae. J Evol Biol 23(11):2474–2483. doi:10.1111/j.1420-9101.2010.02112.x
Copaja SV, Nicol D, Wratten SD (1999) Accumulation of hydroxamic acids during wheat germination. Phytochemistry 50(1):17–24. doi:10.1016/s0031-9422(98)00479-8
Di Pietro JP, Caillaud CM, Chaubet B, Pierre JS, Trottet M (1998) Variation in resistance to the grain aphid, Sitobion avenae (Sternorhynca : Aphididae), among diploid wheat genotypes: Multivariate analysis of agronomic data. Plant Breed 117(5):407–412. doi:10.1111/j.1439-0523.1998.tb01964.x
Dubcovsky J, Lukaszewski AJ, Echaide M, Antonelli EF, Porter DR (1998) Molecular characterization of two Triticum speltoides interstitial translocations carrying leaf rust and greenbug resistance genes. Crop Sci 38(6):1655–1660
Franzen LD, Gutsche AR, Heng-Moss TM, Higley LG, Macedo TB (2008) Physiological responses of wheat and barley to Russian wheat aphid, Diuraphis noxia (Mordvilko) and bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera: Aphididae). Arthropod Plant Interact 2(4):227–235. doi:10.1007/s11829-008-9048-1
Friebe B, Mukai Y, Dhaliwal HS, Martin TJ, Gill BS (1991) Identification of alien chromatin specifying resistance to wheat streak mosaic and greenbug in wheat germ plasm by C-banding and in situ hybridization. Theor Appl Genet 81(3):381–389. doi:10.1007/bf00228680
Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat–alien translocations conferring resistance to diseases and pests: current status. Euphytica 91(1):59–87
Givovich A, Niemeyer HM (1994) Effect of hydroxamic acids on feeding behaviour and performance of cereal aphids (Hemiptera: Aphididae) on wheat. Eur J Entomol 91:371–374
Haley SD, Peairs FB, Walker CB, Rudolph JB, Randolph TL (2004) Occurrence of a new Russian wheat aphid biotype in Colorado. Crop Sci 44(5):1589–1592
Hansen LM (2006) Effect of 6-methoxybenzoxazolin-2-one (MBOA) on the reproduction rate of the grain aphid (Sitobion avenae F.). J Agric Food Chem 54(4):1031–1035. doi:10.1021/jf0509005
Hesler LS (2005) Resistance to Rhopalosiphum padi (Homoptera: Aphididae) in three triticale accessions. J Econ Entomol 98(2):603–610
Hesler LS, Tharp CI (2005) Antibiosis and antixenosis to Rhopalosiphum padi among triticale accessions. Euphytica 143(1–2):153–160. doi:10.1007/s10681-005-3060-7
Hesler LS, Haley SD, Nkongolo KK, Peairs FB (2007) Resistance to Rhopalosiphum padi (Homoptera: Aphididae) in triticale and triticale-derived wheat lines resistant to Diuraphis noxia (Homoptera: Aphididae). J Entomol Sci 42(2):217–227
Hu X, Zhao H, Heimbach U, Thieme T, Li J, Zhang Y, Liu B, Li D, Hu Z (2004) Study on cereal aphid resistance on three winter wheat cultivars introduced into China. Acta Bot Boreali Occidentalia Sinica 24(7):1221–1226
Kieckhefer RW, Gellner JL (1992) Yield losses in winter wheat caused by low-density cereal aphid populations. Agron J 84(2):180–183
Kim W, Johnson JW, Baenziger PS, Lukaszewski AJ, Gaines CS (2004) Agronomic effect of wheat-rye translocation carrying rye chromatin (1R) from different sources. Crop Sci 44(4):1254–1258
Kumlay AM, Baezinger PS, Gill KS, Shelton DR, Graybosch RA, Lukaszewski AJ, Wesenberg DM (2003) Understanding the effect of rye chromatin in bread wheat. Crop Sci 43(5):1643–1651
Leszczynski B, Dixon AFG (1992) Resistance of cereals to aphids - the interaction between hydroxamic acids and glutathione S-transferases in the grain aphid Sitobion avenae (F) (Hom., Aphididae). J Appl Entomol 113(1):61–67
Liu X, Yang X, Wang C, Wang Y, Zhang H, Ji W (2012) Molecular mapping of resistance gene to English grain aphid (Sitobion avenae F.) in Triticum durum wheat line C273. Theor Appl Genet 124(2):1–7
Lowe H (1981) Resistance and susceptibility to colour forms of the aphid Sitobion avenae in spring and winter wheats (Triticum aestivum). Ann Appl Biol 99(1):87–98
Lu H, Rudd JC, Burd JD, Weng Y (2010) Molecular mapping of greenbug resistance genes Gb2 and Gb6 in T1AL.1RS wheat-rye translocations. Plant Breed 129(5):472–476
Lukaszewski AJ (1993) Reconstruction in wheat of complete chromosomes 1B and 1R from the 1RS.1BL translocation of ‘Kavkaz’ origin. Genome 36(5):821–824
Lukaszewski AJ (1995) Physical distribution of translocation breakpoints in homoeologous recombinants induced by the absence of the Ph1 gene in wheat and triticale. Theor Appl Genet 90(5):714–719
Lukaszewski AJ (1997) Further manipulation by centric misdivision of the 1RS.1BL translocation in wheat. Euphytica 94(3):257–261. doi:10.1023/a:1002916323085
Lukaszewski AJ (2000) Manipulation of the 1RS.1BL translocation in wheat by induced homoeologous recombination. Crop Sci 40(1):216–225
Lukaszewski AJ (2006) Cytogenetically engineered rye chromosomes 1R to improve bread-making quality of hexaploid triticale. Crop Sci 46(5):2183–2194. doi:10.2135/cropsci2006.03.0135
Lukaszewski AJ (2008) Unexpected behavior of an inverted rye chromosome arm in wheat. Chromosoma 117(6):569–578. doi:10.1007/s00412-008-0174-4
Lukaszewski AJ, Rybka K, Korzun V, Malyshev SV, Lapinski B, Whitkus R (2004) Genetic and physical mapping of homoeologous recombination points involving wheat chromosome 2B and rye chromosome 2R. Genome 47(1):36–45. doi:10.1139/g03-089
Migui SM, Lamb RJ (2003) Patterns of resistance to three cereal aphids among wheats in the genus Triticum (Poaceae). Bull Entomol Res 93(4):323–333. doi:10.1079/ber2003246
Migui SM, Lamb RJ (2004) Seedling and adult plant resistance to Sitobion avenae (Hemiptera: Aphididae) in Triticum monococcum (Poaceae), an ancestor of wheat. Bull Entomol Res 94(1):35–46. doi:10.1079/ber2003278
Nicol D, Wratten SD (1997) The effect of hydoroxamic acid concentration at late growth stages of wheat on the performance of the aphid Sitobion avenae. Ann Appl Biol 130(3):387–396. doi:10.1111/j.1744-7348.1997.tb07669.x
Nicol D, Copaja SV, Wratten SD, Niemeyer HM (1992) A screen of worldwide wheat cultivars for hydroxamic acid levels and aphid antixenosis. Ann Appl Biol 121(1):11–18. doi:10.1111/j.1744-7348.1992.tb03982.x
Niemeyer HM, Jerez JM (1997) Chromosomal location of genes for hydroxamic acid accumulation in Triticum aestivum L. (wheat) using wheat aneuploids and wheat substitution lines. Heredity 79(1):10–14
Nomura TN, Ishihara AI, Imaishi HI, Endo TE, Ohkawa HO, Iwamura HI (2002) Molecular characterization and chromosomal localization of cytochrome P450 genes involved in the biosynthesis of cyclic hydroxamic acids in hexaploid wheat. Mol Genet Genomics 267(2):210–217. doi:10.1007/s00438-002-0653-x
Nomura T, Ishihara A, Imaishi H, Ohkawa H, Endo TR, Iwamura H (2003) Rearrangement of the genes for the biosynthesis of benzoxazinones in the evolution of Triticeae species. Planta 217(5):776–782. doi:10.1007/s00425-003-1040-5
Porter DR, Webster JA, Burton RL, Puterka GJ, Smith EL (1991) New sources of resistance to greenbug in wheat. Crop Sci 31(6):1502–1504
Porter DR, Burd JD, Shufran KA, Webster JA, Teetes GL (1997) Greenbug (Homoptera: Aphididae) biotypes: selected by resistant cultivars or preadapted opportunists? J Econ Entomol 90(5):1055–1065
Porter DR, Harris MO, Hesler LS, Puterka GJ (2009) Insects which challenge global wheat production. In: Carver BF (ed) Wheat science and trade. Wiley-Blackwell, Iowa, pp 189–201
Rabinovich SV (1998) Importance of wheat-rye translocations for breeding modern cultivars of Triticum aestivum L. (Reprinted from Wheat: Prospects for global improvement, 1998). Euphytica 100(1–3):323–340
Riedell WE, Kieckhefer RW, Langham MAC, Hesler LS (2003) Root and shoot responses to bird cherry-oat aphids and barley yellow dwarf virus in spring wheat. Crop Sci 43(4):1380–1386
SAS Institute Inc. (2009) SAS/STAT® 9.2 User’s guide. SAS Institute Inc, Cary, NC
Sebesta E, Wood E (1978) Transfer of greenbug resistance from rye to wheat with X-rays. Agron Abstr 70:61–62
Skovmand B, Villareal RL, van Ginkel M, Rajaram S, Ortiz-Ferrara G (1997) Semidwarf bread wheats: names, parentages, pedigrees and origins. CIMMYT, Mexico, DF
Smith CM, Belay T, Stauffer C, Stary P, Kubeckova I, Starkey S (2004a) Identification of Russian wheat aphid (Homoptera: Aphididae) populations virulent to the Dn4 resistance gene. J Econ Entomol 97(3):1112–1117. doi:10.1603/0022-0493(2004)097
Smith CM, Havlickova H, Starkey S, Gill B, Holubec V (2004b) Identification of Aegilops germplasm with multiple aphid resistance. Euphytica 135(3):265–273
Thackray DJ, Wratten SD, Edwards PJ, Niemeyer HM (1990) Resistance to the aphids Sitobion avenae and Rhopalosiphum padi in Gramineae in relation to hydroxamic acid levels. Ann Appl Biol 116(3):573–582. doi:10.1111/j.1744-7348.1990.tb06640.x
Tyler JM, Webster JA, Smith EL (1985) Biotype E greenbug resistance in WSMV resistant wheat germplasm lines. Crop Sci 25(4):686–688
Tyler JM, Webster JA, Merkle OG (1987) Designations for genes in wheat germplasm conferring greenbug resistance. Crop Sci 27(3):526–527
Voss TS, Kieckhefer RW, Fuller BW, McLeod MJ, Beck DA (1997) Yield losses in maturing spring wheat caused by cereal aphids (Homoptera: Aphididae) under laboratory conditions. J Econ Entomol 90(5):1346–1350
Watt A (1979) The effect of cereal growth stages on the reproductive activity of Sitobion avenae and Metopolophium dirhodum. Ann Appl Biol 91(2):147–157
Weiland AA, Peairs FB, Randolph TL, Rudolph JB, Haley SD, Puterka GJ (2008) Biotypic diversity in Colorado Russian wheat aphid (Hemiptera: Aphididae) populations. J Econ Entomol 101(2):569–574. doi:10.1603/0022-0493(2008)101
Weng Y, Li W, Devkota RN, Rudd JC (2005) Microsatellite markers associated with two Aegilops taushii-derived greenbug resistance loci in wheat. Theor Appl Genet 110:462–469
Xu ZH, Chen JL, Cheng DF, Sun JR, Liu Y, Francis F (2011) Discovery of English grain aphid (Hemiptera: Aphididae) biotypes in China. J Econ Entomol 104(3):1080–1086
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14(6):415–421
Acknowledgments
We thank the Monsanto’s Beachell-Borlaug International Scholars Program for financing this research project. The Swedish Foundation for Strategic Environmental Research (Mistra) through the PlantComMistra program is acknowledged for support. We would also like to thank for technical support provided by Dr. Vehbo Hot (SLU) and Ms. Lina Aguirre (KSU) and to Dr. Jan-Eric Englund (SLU) for his valuable advice on the statistical analyses. Emma Quilligan provided editing assistance.
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Crespo-Herrera, L.A., Smith, C.M., Singh, R.P. et al. Resistance to multiple cereal aphids in wheat–alien substitution and translocation lines. Arthropod-Plant Interactions 7, 535–545 (2013). https://doi.org/10.1007/s11829-013-9267-y
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DOI: https://doi.org/10.1007/s11829-013-9267-y
Keywords
- Rhopalosiphum padi
- Schizaphis graminum
- Sitobion avenae
- Triticum aestivum
- Secale cereale
- Aegilops speltoides