Abstract
The aim of this study was to assess the genetic basis of rust mite (Aculus schlechtendali) resistance in apple (Malus × domestica). A. schlechtendali infestation of apple trees has increased as a consequence of reduced side effects of modern fungicides on rust mites. An analysis of quantitative trait loci (QTLs) was carried out using linkage map data available for F1 progeny plants of the cultivars ‘Fiesta’ × ‘Discovery’. Apple trees representing 160 different genotypes were surveyed for rust mite infestation, each at three different sites in two consecutive years. The distribution of rust mites on the individual apple genotypes was aggregated and significantly affected by apple genotype and site. We identified two QTLs for A. schlechtendali resistance on linkage group 7 of ‘Fiesta’. The AFLP marker E35M42-0146 (20.2 cM) and the RAPD marker AE10-400 (45.8 cM) were closest positioned to the QTLs and explained between 11.0% and 16.6% of the phenotypic variability. Additionally, putative QTLs on the ‘Discovery’ chromosomes 4, 5 and 8 were detected. The SSR marker Hi03a10 identified to be associated to one of the QTLs (AFLP marker E35M42-0146) was traced back in the ‘Fiesta’ pedigree to the apple cultivar ‘Wagener’. This marker may facilitate the breeding of resistant apple cultivars by marker assisted selection. Furthermore, the genetic background of rust mite resistance in existing cultivars can be evaluated by testing them for the identified SSR marker.
Similar content being viewed by others
References
Brown SK, Maloney KE (2003) Genetic improvement of apple: breeding, markers, mapping and biotechnology. In: Ferree DC, Warrington IJ (eds) Apples: botany, production and uses. CABI, Wallingford, UK, pp 31–61
Bus VGM, Chagné D, Bassett HCM, Bowatte D, Calenge F, Celton J-M, Durel C-E, Malone MT, Patocchi A, Ranatunga AC, Rikkerink EHA, Tustin DS, Zhou J, Gardiner SE (2008) Genome mapping of three major resistance genes to woolly apple aphid (Eriosoma lanigerum Hausm.). Tree Genet Genom 4:223–236
Calenge F, Drouet D, Denance C, van de Weg WE, Brisset MN, Paulin JP, Durel C-E (2005) Identification of a major QTL together with several minor additive or epistatic QTLs for resistance to fire blight in apple in two related progenies. Theor Appl Genet 111:128–135
Calenge F, Durel C-E (2006) Both stable and unstable QTLs for resistance to powdery mildew are detected in apple after four years of field assessment. Mol Breed 17:329–339
Calenge F, Faure A, Goerre M, Gebhardt C, van de Weg WE, Parisi L, Durel C-E (2004) Quantitative trait loci (QTL) analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196
Conner PJ, Brown SK, Weeden NF (1998) Molecular-marker analysis of quantitative traits for growth and development in juvenile apple trees. Theor Appl Genet 96:1027–1035
Downing RS, Moilliet TK (1967) Relative densities of predacious and phytophagous mites on three cultivars of apple trees. Can Entomol 99:733–741
Duso C, Pasini M, Pellegrini M (2003) Distribution of the predatory mite Typhlodromus pyri (Acari: Phytoseiidae) on different apple cultivars. Biocontrol Sci Technol 13:671–681
Easterbrook MA (1984) The biology and control of the rust mites (Aculus schlechtendali) and (Epitrimerus piri) on apple and pear in England. In: Griffiths DA, Bowman CE (eds) Acarology VI. Horwood, Chichester, UK, pp 797–803
Easterbrook MA, Fuller MM (1986) Russeting of apples caused by apple rust mite (Aculus schlechtendali) (Acarina: Eriophyidae). Ann Appl Biol 109:1–9
Easterbrook MA, Palmer JW (1996) The relationship between early-season leaf feeding by apple rust mite (Aculus schlechtendali Nal.), and fruit set and photosynthesis of apple. J Hortic Sci 71:939–944
Fischer C (1994) Breeding apple cultivars with multiple resistance. In: Schmidt H, Kellerhals M (eds) Progress in temperate fruit breeding. Kluwer, Dordrecht, NL, pp 43–48
Francia E, Tacconi G, Crosatti C, Barabaschi D, Bulgarelli D, Dall’Aglio E, Valè G (2005) Marker assisted selection in crop plants. Plant Cell, Tissue Organ Cult 82:317–342
Frei A, Blair MW, Cardona C, Beebe SE, Gu H, Dorn S (2005) QTL mapping of resistance to Thrips palmi (Karny) in common bean. Crop Sci 45:379–387
Frey JE, Frey B, Sauer C, Kellerhals M (2004) Efficient low-cost DNA extraction and multiplex fluorescent PCR method for marker-assisted selection in breeding. Plant Breed 123:554–557
Goonewardene HF, Janick J, Kwolek WF, Bailey CH, Hough LF (1982) Pedigree analysis of apple clones with differences in preference to European red mite (Panonychus ulmi Koch). Hortscience 17:63–65
Graf B, Höpfli HU, Höhn H, Kellerhals M, Krebs C (1998) Schorfresistente Apfelsorten: Wie steht’s mit der Schädlingsanfälligkeit? Schweiz Z Obst-Weinbau 3:71–73
Herbert HJ (1974) Notes on the biology of the apple rust mite (Aculus schlechtendali) (Prostigmata: Eriophyoidae), and its density on several cultivars of apple in Nova Scotia. Can Entomol 106:1035–1038
Höhn H, Höpli HU (1990) Die Apfelrostmilbe: Oft überschätzt, aber kaum prognostizierbar!. Schweiz Z Obst-Weinbau 126:259–266
Kellerhals M, Bertschinger L, Gessler C (2004) Use of genetic resources in apple breeding and for sustainable fruit production. J Fruit Ornam Plant Res 12:53–62
Khan MA, Duffy B, Gessler C, Patocchi A (2006) QTL mapping of fire blight resistance in apple. Mol Breed 17:299–306
King GJ, Maliepaard C, Lynn JR, Alston FH, Durel C-E, Evans KM, Griffon B, Laurens F, Manganaris AG, Schrevens E, Tartarini S, Verhaegh J (2000) Quantitative genetic analysis and comparison of physical and sensory descriptors relating to fruit flesh firmness in apple (Malus pumila Mill.). Theor Appl Genet 100:1074–1084
Lauter N, Doebley J (2002) Genetic variation for phenotypically invariant traits detected in teosinte: implications for the evolution of novel forms. Genetics 160:333–342
Legendre P, Legendre L (1998) Numerical ecology: developments in environmental modelling. Elsevier, Amsterdam, NL
Levine N (2007) CrimeStat: a spatial statistics program for the analysis of crime incident locations (v 3.1). National Institute of Justice, Washington, DC
Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003a) Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet 106:1497–1508
Liebhard R, Koller B, Patocchi A, Kellerhals M, Pfammatter W, Jermini M, Gessler C (2003b) Mapping quantitative field resistance against apple scab in a ‘Fiesta’ × ‘Discovery’ progeny. Phytopathology 93:493–501
Liebhard R, Kellerhals M, Pfammatter W, Jermini M, Gessler C (2003c) Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol 52:511–526
Ludwig JA, Reynolds JF (1988) Statistical ecology: a primer on the methods and computing. Wiley, New York
Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225
Mody K, Eichenberger D, Dorn S (2008) Stress magnitude matters: different intensities of pulsed water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecol Entomol. doi:10.1111/j.1365-2311.2008.01053.x
Mohan M, Nair S, Bhagwat A, Krishna TG, Yano M, Bhatia CR, Sasaki T (1997) Genome mapping, molecular markers and marker-assisted selection in crop plants. Mol Breed 3:87–103
Roche P, Alston FH, Maliepaard C, Evans KM, Vrielink R, Dunemann F, Markussen T, Tartarini S, Brown LM, Ryder C, King GJ (1997) RFLP and RAPD markers linked to the rosy leaf curling aphid resistance gene (Sd1) in apple. Theor Appl Genet 94:528–533
Segura V, Cilas C, Laurens F, Costes E (2006) Phenotyping progenies for complex architectural traits: a strategy for 1-year-old apple trees (Malus × domestica Borkh.). Tree Genet Genom 2:140–151
Silfverberg-Dilworth E, Matasci CL, van de Weg WE, van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel C-E, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genom 2:202–224
Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell, Oxford, UK
Spieser F, Graf B, Walther P, Noesberger J (1998) Impact of apple rust mite (Acari: Eriophyiidae) feeding on apple leaf gas exchange and leaf color associated with changes in leaf tissue. Environ Entomol 27:1149–1156
Stoeckli S, Mody K, Gessler C, Patocchi A, Jermini M, Dorn S (2008a) QTL analysis for aphid resistance and growth traits in apple. Tree Genet Genom: doi:10.1007/s11295-11008-10156-y
Stoeckli S, Mody K, Dorn S (2008b) Influence of canopy aspect and height on codling moth (Lepidoptera: Tortricidae) larval infestation in apple, and relationship between infestation and fruit size. J Econ Entomol 101:81–89
van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL® 4.0. Software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, NL
Varshney A, Mohapatra T, Sharma RP (2004) Molecular mapping and marker assisted selection of traits for crop improvement. Anamaya, New Delhi, IN
Venables WN, Ripley BD (2002) Modern applied statistics with S-Plus. Springer, New York
Verhoeven KJF, Simonsen L, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647
Walde SJ, Hardmann JM, Magagula CN (1997) Direct and indirect species interactions influencing within season dynamics of apple rust mite (Aculus schlechtendali) (Acari, Eriophyidae). Exp Appl Acarol 21:587–614
Wearing CH, Colhoun K, McLaren GF, Attfield B, Bus VGM (2003) Evidence for single gene resistance in apple to brownheaded leafroller (Ctenopseustis obliquata) and implications for resistance to other New Zealand leafrollers. Entomol Exp Appl 108:1–10
Acknowledgments
The authors thank Mauro Jermini and Danilo Christen (Agroscope Research Station ACW) for access to the study orchards; Heinrich Höhn (Agroscope Research Station ACW) for practical comments on rust mite filtration; Joel Meier and Hansjoerg Kull (Syngenta Crop Protection Dielsdorf) for advise on survey design; Michelle Schmocker and Christoph Rohrer for assistance with fieldwork; Caroline Baumgartner for help with mite filtration; Muhammad Khan and Giovanni Broggini (ETH Zurich) and Hans Jansen (Plant Research Wageningen) for great support in QTL analysis; Hans-Rudolf Roth, Werner Eugster, Massimo Merlini, and Rahel Liesch (ETH Zurich) for statistical consulting; Davide Gobbin (ETH Zurich) for the analysis of the pedigree of ‘Fiesta’ with SSR Hi03a10; and Cesare Gessler (ETH Zurich) for relevant aid in QTL analysis and comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: A. Dandekar
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Stoeckli, S., Mody, K., Patocchi, A. et al. Rust mite resistance in apple assessed by quantitative trait loci analysis. Tree Genetics & Genomes 5, 257–267 (2009). https://doi.org/10.1007/s11295-008-0186-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-008-0186-5