Abstract
Solanum pennellii LA716, a wild relative of tomato, produces acylsugars, an insect resistance compound with activity against many tomato insect pests. Breeding of cultivated tomato using S. pennellii LA716 as a donor parent has led to the development of the elite acylsugar-producing tomato breeding line CU071026. CU071026 contains five introgressed S. pennellii genomic regions, and produces acylsugars at moderate levels that are effective against insect pests. A BC1F1 population was created by crossing the F1 CU071026 × S. pennellii LA716 with CU071026 as the recurrent parent; this BC1F1 population was used to identify additional regions of the S. pennellii genome important for further improvement of acylsugar production. This population was genotyped with 94 markers in the segregating regions and phenotyped for level of acylsugar production. Using QTLNetwork 2.1 for the detection of quantitative trait loci (QTL) and epistatic interactions, this study identified five QTL for total acylsugar level. Additionally, two epistatic interactions between QTL were found to control significant levels of total acylsugar production. Two of the QTL identified were further evaluated in silverleaf whitefly (Bemisia tabaci) field cage trials using acylsugar breeding lines that differ for the presence/absence of these QTL. While high levels of silverleaf whitefly resistance were observed in all acylsugar breeding lines, lines containing the additional QTL on either chromosomes 6 or 10 had increased levels of total acylsugar production and reduced incidence of whitefly. Acylsugar lines containing the chromosome 6 QTL also had increased density of the type IV glandular trichomes which produce and exude acylsugars.
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References
Anderson PK (2005) Introduction. In: Anderson PK, Morales FJ (eds.) Whitefly and whitefly-borne viruses in the tropics: building a knowledge base for global action. CIAT Publication no. 341, Cali, Colombia. pp 1–11
Blauth SL, Churchill GA, Mutschler MA (1998) Identification of QTL associated with acylsugar accumulation using intraspecific populations of the wild tomato Lycopersicon pennellii. Theor Appl Genet 96:458–467
Blauth SL, Steffens JC, Churchill GA, Mutschler MA (1999) QTL analysis of acylsugar fatty acid constitutents using intraspecific populations of the wild tomato Lycopersicon pennellii. Theor Appl Genet 99:373–381
Burke B, Goldsby G, Mudd JB (1987) Polar epicuticular lipids of Lycopersicon pennellii. Phytochemistry 26:2567–2571
Buta GJ, Lusby WR, Neal JW Jr, Waters RM, Pittarelli GW (1993) Sucrose esters from Nicotiana gossei active against the greenhouse whitefly Trialeuroides vaporarium. Phytochemistry 32:859–864
Churchhill GA, Doerge RW (1994) Empirical threshold for quantitative trait mapping. Genetics 138:963–971
Cutler HG, Severson RF, Cole PD, Jackson DM, Johnson AW (1986) Secondary metabolites from higher plants. Their possible role as biological control agents. In: Green MB, Hedin PA (eds) Natural resistance of plants to pests. American Chemical Society, Washington, DC, pp 178–196
Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346
Doyle JJ, Dickson EE (1987) Preservation of plant samples for DNA restriction endonuclease analysis. Taxon 36:715–722
Eshed Y, Zamir D (1996) Less-than-additive epistatic interactions of quantitative trait loci in tomato. Genetics 143:1807–1817
Fobes JF, Mudd J, Marsden M (1985) Epicuticular lipid on the leaves of L. pennellii and L. esculentum. Plant Physiol 77:567–570
Fulton T, van der Hoeven R, Eannetta N, Tanksley S (2002) Identification, analysis and utilization of a conserved ortholog set (COS) markers for comparative genomics in higher plants. Plant Cell 14:1457–1467
Gibson RW (1976) Trapping of the spider mite Tetranychus urticae by glandular hairs on the wild potato Solanum berthaultii. Potato Res 19:179–182
Gibson RJ, Valencia L (1978) A survey of potato species for resistance to the mite Polyphagotarsonemus latus, with particular reference to the protection of Solanum berthaultii and S. tarijense by glandular hairs. Potato Res 21:217–223
Goffreda JC, Mutschler MA (1989) Inheritance of potato aphid resistance in hybrids between Lycopersicon esculentum and L. pennellii. Theor Appl Genet 78:210–216
Goffreda JC, Mutschler MA, Tingey WM (1988) Feeding behavior of potato aphid affected by glandular trichomes on wild tomato. Entomol Exp Appl 48:101–107
Goffreda JC, Mutschler MA, Steffens JC (1990) Association of epicuticular sugars with aphid resistance in hybrids with wild tomato. J Am Soc Hortic Sci 117:161–164
Hare JD (2005) Bioactivity of acylglucose esters from Datura wrightii glandular trichomes against three native insect herbivores. J Chem Ecol 31:1475–1491
Hawthorne DM, Shapiro JA, Tingey WM, Mutschler MA (1992) Trichome-borne and artificially applied acylsugars of wild tomato deter feeding and oviposition of the leafminer, Liriomyza trifolii. Entomol Exp Appl 65:65–73
Holley JD, King RR, Singh RP (1987) Glandular trichomes and the resistance of Solanum berthaultii (PI 473340) to infection from Phytophthora infestans. Can J Plant Pathol 9:291–294
Imtiaz M, Ogbonnaya FC, Oman J, van Ginkel M (2008) Characterization of quantitative trait loci controlling genetic variation for preharvest sprouting in synthetic backcross-derived wheat lines. Genetics 178:1725–1736
Juvik J, Shapiro JA, Young TE, Mutschler MA (1994) Acylglucoses of the wild tomato Lycopersicon pennellii alter behavior and reduce growth and survival of Helicoverpa zea and Spodoptera exigua. J Econ Entomol 87:482–492
Kennedy BS, Nielsen MT, Severson RF, Sisson VA, Stephenson MK, Jackson DM (1992) Leaf surface chemicals from Nicotiana affecting germination of Peronospora tabacina sporangia. J Chem Ecol 18:1467–1479
King RR, Calhoun LA (1988) 2, 3-di-O-and 1, 2, 3-tri-O-acylated glucose esters from the glandular trichomes of Datura metel. Phytochemistry 27:3761–3765
King RR, Pelletier Y, Singh RP, Calhoun LA (1986) 3,4-Di-O-isobutyryl-6-O-caprylsucrose: the major component of a novel sucrose ester complex from the type B glandular trichomes of Solanum berthaultii Hawkes (PI473340). J Chem Soc Chem Commun 14:1078–1079
King RR, Singh RP, Boucher A (1987) Variation in sucrose esters from the type B glandular trichomes of certain wild potato species. Am Potato J 64:529–534
King RR, Calhoun LA, Singh RP (1988) 3, 4-di-O-and 2, 3, 4-tri-O-acylated glucose esters from the glandular trichomes of non-tuberous Solanum species. Phytochemistry 27:3765–3768
King RR, Calhoun LA, Singh RP, Boucher A (1990) Sucrose esters associated with glandular trichomes of wild Lycopersicon species. Phytochemistry 29:2115–2118
Kliebenstein DJ (2009) A quantitative genetics and ecological model system: understanding the aliphatic glucosinolate biosynthetic network via QTLs. Phytochem Rev 8:243–254
Kliebenstein DJ, Kroymann J, Mitchell-olds T (2005) The glucosinolate-myrosinase system in an ecological and evolutionary context. Curr Opin Plant Biol 8:264–271
Lark KG, Chase K, Adler F, Mansur LM, Orf JH (1995) Interactions between quantitative trait loci in soybean in which trait variation at one locus is conditional upon specific allele at another. Proc Natl Acad Sci USA 92:4656–4660
Li AX, Steffens JC (2000) An acyltransferase catalyzing the formation of diacylglucose is a serine carboxypeptidase-like protein. Proc Natl Acad Sci USA 97:6902–6907
Liedl BE, Lawson DM, White KK, Shapiro JA, Cohen DE, Carson WG, Trumble JT, Mutschler MA (1995) Acylglucoses of the wild tomato Lycopersicon pennellii alters settling and reduces oviposition of Bemisia argentifolii. J Econ Entomol 88:742–748
Lukens LN, Doebley J (1999) Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genet Res 74:291–302
Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932
McMullen MD, Byrne PF, Snook ME, Wiseman BR, Lee EA, Widstrom NW, Coe EH (1998) Quantatative trait loci and metabolic pathways. Proc Natl Acad Sci USA 95:1996–2000
McNally KL, Mutschler MA (1997) Use of introgression lines and zonal mapping to identify RAPD markers linked to QTL. Mol Breed 3:203–212
Mueller LA, Solow TH, Taylor N et al (2005) The SOL genomics network. A comparative resource for Solanaceae biology and beyond. Plant Physiol 138:1310–1317
Mutschler MA, Doerge RW, Liu J, Kuai JP, Liedl B, Shapiro Y (1996) QTL analysis of pest resistance in the wild tomato, Lycopersicon pennellii: QTL controlling acylsugar level and composition. Theor Appl Genet 92:709–718
Neal JJ, Tingey WM, Steffens JC (1989) Glandular trichomes of Solanum berthaultii and resistance to the Colorado potato beetle. Entomol Exp Appl 51:133–140
Neal JJ, Tingey WM, Steffens JC (1990) Sucrose esters of carboxylic acids in glandular trichomes of Solanum berthaultii deter settling and probing by green peach aphid. J Chem Ecol 16:487–497
Palumbo JC, Horowitz AR, Prabhaker N (2001) Insecticidal control and resistance management for Bemisia tabaci. Crop Prot 20:739–765
Pappu HR, Jones RAC, Jain RJ (2008) Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res 141:219–236
Polston JE, Anderson PK (1997) The emergence of whitefly-transmitted geminiviruses in tomato in the western hemisphere. Plant Dis 81:1358–1369
Rodriguez AE, Tingey WM, Mutschler MA (1993) Acylsugars produced by type IV trichomes of Lycopersicon pennellii (Corr.)D’Arcy deter settling of the green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae). J Econ Entomol 86:34–39
Rowe HC, Hansen BG, Halkier BA, Kliebenstein DJ (2008) Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome. Plant Cell 20:1199–1216
Saikia AK, Muniyappa V (1989) Epidemiology and control of tomato leaf curl virus in southern India. Trop Agric (Trinidad) 66:350–354
SAS Institute Inc (2008) JMP 8 User Guide. SAS Institute Inc., Cary
Schilmiller A, Shi F, Kim J, Charbonneau A, Holmes D, Jones AD, Last RL (2010) Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant J 62:391–403
Schumacher JN (1970) The isolation of 6-O-acetyl-2,3,4-tri-O-((+)-3-methylvaleryl)-D-glucopyranose from tobacco. Carbohydrate Res 13:1–8
Schuster DJ (2001) Relationship of silverleaf whitefly population density to severity of irregular ripening of tomato. HortScience 36:1089–1090
Schuster DJ, Stansly PA, Polston JE (1996) Expressions of plant damage by Bemisia. In: Gerling D, Mayer RT (eds.), Bemisia 1995: Taxonomy, biology, damage control and management, Intercept. Ltd., Andover, Hants, UK, pp 153–165
Schuster DJ, Mann RS, Toapanta M et al (2010) Monitoring neonicotinoid resistance in biotype B of Bemisia tabaci in Florida. Pest Manag Sci 66:186–195
Segre D, DeLuna A, Church GM, Kishony R (2005) Modular epistasis in yeast metabolism. Nat Genet 37:77–83
Setter TL, Flannigan BA, Melkonian J (2001) Loss of kernel set due to water deficit and shade in maize: Carbohydrate supplies, abscisic acid, and cytokinins. Crop Sci 41:1530–1540
Severson RF, Johnson AW, Jackson DM (1985) Cuticular constituents of tobacco: factors affecting their production and their role in insect and disease resistance and smoke quality. Rec Adv Tobacco Sci 11:105–174
Shapiro J, Steffens J, Mutschler MA (1994) Acylsugars of the wild tomato Lycopersicon pennellii in relation to its geographic distribution. Biochem Syst Ecol 22:545–561
von Korff M, Leon J, Pillen K (2010) Detection of epistatic interactions between exotic alleles intrgressed from wild barley. Theor Appl Genet 121:1455–1464
Yang J, Hu C, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24:721–723
Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang QF, Maroof MAS (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231
Acknowledgments
We would like to thank for George Kennedy for advice prior to the insect cage experiment and critical reading of the manuscript. We thank Larry Robertson for loan of the cages used for the insect study. We would also like to thank Jean-Luc Jannink for the valuable discussions on epistasis. This study was funded by the Hatch Project NYC-149440) and the Cornell University Vegetable Breeding Institute.
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Leckie, B.M., De Jong, D.M. & Mutschler, M.A. Quantitative trait loci increasing acylsugars in tomato breeding lines and their impacts on silverleaf whiteflies. Mol Breeding 30, 1621–1634 (2012). https://doi.org/10.1007/s11032-012-9746-3
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DOI: https://doi.org/10.1007/s11032-012-9746-3