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Identification and QTL mapping of whitefly resistance components in Solanum galapagense

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Abstract

Solanum galapagense is closely related to the cultivated tomato and can show a very good resistance towards whitefly. A segregating population resulting from a cross between the cultivated tomato and a whitefly resistant S. galapagense was created and used for mapping whitefly resistance and related traits, which made it possible to study the genetic basis of the resistance. Quantitative trait loci (QTL) for adult survival co-localized with type IV trichome characteristics (presence, density, gland longevity and gland size). A major QTL (Wf-1) was found for adult survival and trichome characters on Chromosome 2. This QTL explained 54.1 % of the variation in adult survival and 81.5 % of the occurrence of type IV trichomes. A minor QTL (Wf-2) for adult survival and trichome characters was identified on Chromosome 9. The major QTL was confirmed in F3 populations. Comprehensive metabolomics, based on GCMS profiling, revealed that 16 metabolites segregating in the F2 mapping population were associated with Wf-1 and/or Wf-2. Analysis of the 10 most resistant and susceptible F2 genotypes by LCMS showed that several acyl sugars were present in significantly higher concentration in the whitefly resistant genotypes, suggesting a role for these components in the resistance as well. Our results show that whitefly resistance in S. galapagense seems to inherit relatively simple compared to whitefly resistance from other sources and this offers great prospects for resistance breeding as well as elucidating the underlying molecular mechanism(s) of the resistance.

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References

  • Baldin ELL, Vendramim JD, Lourencao AL (2005) Resistance of tomato genotypes to the whitefly Bemisia tabaci (Gennadius) biotype B (Hemiptera: Aleyrodidae). Neotrop Entomol 34(3):435–441

    Article  Google Scholar 

  • Blauth SL, Churchill GA, Mutschler MA (1998) Identification of quantitative trait loci associated with acylsugar accumulation using intraspecific populations of the wild tomato, Lycopersicon pennellii. Theor Appl Genetics 96(3–4):458–467

    Article  CAS  Google Scholar 

  • Blauth SL, Steffens JC, Churchill GA, Mutschler MA (1999) Identification of QTLs controlling acylsugar fatty acid composition in an intraspecific population of Lycopersicon pennellii (Corr.) D’Arcy. Theor Appl Genetics 99(1–2):373–381

    Article  Google Scholar 

  • Bleeker PM, Diergaarde PJ, Ament K, Guerra J, Weidner M, Schutz S, de Both MT, Haring MA, Schuurink RC (2009) The role of specific tomato volatiles in tomato–whitefly interaction. Plant Physiol 151(2):925–935

    Article  PubMed  CAS  Google Scholar 

  • Broekgaarden C, Snoeren TAL, Dicke M, Vosman B (2011) Exploiting natural variation to identify insect-resistance genes. Plant Biotechnol J 9:819–882

    Article  PubMed  CAS  Google Scholar 

  • Burke BA, Goldsby G, Mudd JB (1987) Polar epicuticular lipids of Lycopersicon pennellii. Phytochemistry 26(9):2567–2571

    Article  CAS  Google Scholar 

  • Burton GW (1952) Quantitative inheritance in grasses. Proc Int Grassland Congr 1:277–283

    Google Scholar 

  • Channarayappa SG, Muniyappa V, Frist RH (1992) Resistance of Lycopersicon species to Bemisia tabaci, a tomato leaf curl virus vector. Can J Bot (Revue Canadienne De Botanique) 70(11):2184–2192

    Article  Google Scholar 

  • Chatzivasileiadis EA, Sabelis MW (1997) Toxicity of methyl ketones from tomato trichomes to Tetranychus urticae Koch. Exp Appl Acarol 21(6–7):473–484

    Article  CAS  Google Scholar 

  • De Vos RC, Moco S, Lommen A, Keurentjes JJ, Bino RJ, Hall RD (2007) Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry. Nat Protoc 2(4):778–791

    Article  PubMed  Google Scholar 

  • Didyk BM, Simoneit BRT, Brassell SC, Eglinton G (1978) Organic geochemical indicators of paleoenvironmental conditions of sedimentation. Nature 272:216–222

    Article  CAS  Google Scholar 

  • Dimock MB, Kennedy GG (1983) The role of glandular trichomes in the resistance of Lycopersicon hirsutum f. glabratum to Heliothis zea. Entomol Exp Appl 33(3):263–268

    Article  Google Scholar 

  • Eigenbrode SD, Trumble JT, Millar JG, White KK (1994) Topical toxicity of tomato sesquiterpenes to the beet armyworm and the role of these compounds in resistance derived from an accession of Lycopersicon hirsutum f. typicum. J Agric Food Chem 42(3):807–810

    Article  CAS  Google Scholar 

  • Erb WA, Lindquist RK, Flickinger NJ, Casey ML (1994) Resistance of selected interspecific Lycopersicon hybrids to greenhouse whitefly (Homoptera: Aleurodidae). Fla Entomologist 77(1):104–116

    Article  Google Scholar 

  • Erdogan C, Moores GD, Gurkan MO, Gorman KJ, Denholm I (2008) Insecticide resistance and biotype status of populations of the tobacco whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) from Turkey. Crop Prot 27(3–5):600–605

    Article  CAS  Google Scholar 

  • Fancelli M, Vendramim JD (2002) Development of Bemisia tabaci (Gennadius,1889) biotype B on Lycopersicon spp. genotypes. Scientia Agricola 59:665–669

    Google Scholar 

  • Fancelli M, Vendramim JD, Frighetto RTS, Lourencao AL (2005) Glandular exudate of tomato genotypes and development of Bemisia tabaci (Genn.) (Sternorryncha: Aleyrodidae) biotype B. Neotrop Entomol 34(4):659–665

    Article  Google Scholar 

  • Farrar RR, Kennedy G (1991) Inhibition of Telenomus sphingis an egg parasitoid of Manduca spp. by trichome 2-tridecanone-based host plant-resistance in tomato. Entomol Exp Appl 60(2):157–166

    Article  CAS  Google Scholar 

  • Firdaus S, van Heusden AW, Hidayati N, Supena EDJ, Visser RGF, Vosman B (2012) Resistance to Bemisia tabaci in tomato wild relatives. Euphytica 187:31–45

    Article  Google Scholar 

  • Firdaus S, Vosman B, Hidayati N, Supena EDJ, Visser RGF, van Heusden AW (2013) The Bemisia tabaci species complex: additions from different parts of the world. Insect Sci 00:1–11. doi:10.1111/1744-7917.12001

    Google Scholar 

  • Freitas JA, Maluf WR, Cardoso MD, Gomes LAA, Bearzotti E (2002) Inheritance of foliar zingiberene contents and their relationship to trichome densities and whitefly resistance in tomatoes. Euphytica 127(2):275–287

    Article  CAS  Google Scholar 

  • Frelichowski JE, Juvik JA (2001) Sesquiterpene carboxylic acids from a wild tomato species affect larval feeding behavior and survival of Helicoverpa zea and Spodoptera exigua (Lepidoptera: Noctuidae). J Econ Entomol 94(5):1249–1259

    Article  PubMed  CAS  Google Scholar 

  • Fridman E, Wang J, Iijima Y, Froehlich JE, Gang DR, Ohlrogge J, Pichersky E (2005) Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynthesis of methylketones. Plant Cell 17(4):1252–1267

    Article  PubMed  CAS  Google Scholar 

  • Hirano K, Budiyanto E, Swastika N, Fujii K (1995) Population dynamics of the whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), in Java, Indonesia, with special reference to spatiotemporal changes in the quantity of food resources. Ecol Res 10(1):75–85

    Article  Google Scholar 

  • Hogenboom NG (1972) Breaking breeding barriers in Lycopersicon. 1. Genus Lycopersicon, its breeding barriers and importance of breaking these barriers. Euphytica 21(2):221–227

    Article  Google Scholar 

  • Janmaat AF, de Kogel WJ, Woltering EJ (2002) Enhanced fumigant toxicity of p-cymene against Frankliniella occidentalis by simultaneous application of elevated levels of carbon dioxide. Pest Manag Sci 58(2):167–173

    Article  PubMed  CAS  Google Scholar 

  • Kehr J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J Exp Bot 57:767–774

    Article  PubMed  CAS  Google Scholar 

  • Kennedy GG, Farrar RR, Kashyap RK (1991) 2-Tridecanone glandular trichome-mediated insect resistance in tomato: effect on parasitoids and predators of Heliothis zea. ACS Symp Ser Am Chem Soc 449:150–165

    Article  CAS  Google Scholar 

  • Lawson DM, Lunde CF, Mutschler MA (1997) Marker-assisted transfer of acylsugar-mediated pest resistance from the wild tomato, Lycopersicon pennellii, to the cultivated tomato, Lycopersicon esculentum. Mol Breed 3(4):307–317

    Article  CAS  Google Scholar 

  • Leckie BM, De Jong DM, Mutschler MA (2012) Quantitative trait loci increasing acylsugars in tomato breeding lines and their impacts on silverleaf whiteflies. Mol Breed 30(4):1621–1634. doi:10.1007/s11032-012-9746-3

    Google Scholar 

  • Lenke CA, Mutschler MA (1984) Inheritance of glandular trichomes in crosses between Lycopersicon esculentum and Lycopersicon pennellii. J Am Soc Hortic Sci 109:592–596

    Google Scholar 

  • Lin SYH, Trumble JT, Kumamoto J (1987) Activity of volatile compounds in glandular trichomes of Lycopersicon species against 2 insect herbivores. J Chem Ecol 13(4):837–850

    Article  CAS  Google Scholar 

  • Luckwill LC (1943) The genus Lycopersicon: an historical, biological, and taxonomic survey of wild and cultivated tomatoes. Aberd Univ Study 120:44

    Google Scholar 

  • Maharijaya A, Vosman B, Verstappen F, Steenhuis-Broers G, Mumm R, Purwito A, Visser RGF, Voorrips RE (2012) Resistance factors in pepper inhibit larval development of thrips (Frankliniella occidentalis). Entomol Exp Appl 145(1):62–71

    Article  Google Scholar 

  • Maliepaard C, Bas N, van Heusden S, Kos J, Pet G, Verkerk R, Vrielink R, Zabel P, Lindhout P (1995) Mapping of QTLs for glandular trichome densities and Trialeurodes vaporariorum (greenhouse whitefly) resistance in an F2 from Lycopersicon esculentum × Lycopersicon hirsutum f. glabratum. Heredity 75:425–433

    Article  Google Scholar 

  • McCollum TG, Stoffella PJ, Powell CA, Cantliffe DJ, Hanif-Khan S (2004) Effects of silverleaf whitefly feeding on tomato fruit ripening. Postharvest Biol Technol 31(2):183–190

    Article  Google Scholar 

  • McDowell ET, Kapteyn J, Schmidt A, Li C, Kang JH, Descour A, Shi F, Larson M, Schilmiller A, An LL, Jones AD, Pichersky E, Soderlund CA, Gang DR (2011) Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol 155(1):524–539

    Article  PubMed  CAS  Google Scholar 

  • Momotaz A, Scott JW, Schuster DJ (2010) Identification of quantitative trait loci conferring resistance to Bemisia tabaci in an F2 population of Solanum lycopersicum × S. habrochaites accession LA1777. J Am Soc Hortic Sci 135(2):134–142

    Google Scholar 

  • Morales FJ, Jones PG (2004) The ecology and epidemiology of whitefly-transmitted viruses in Latin America. Virus Res 100(1):57–65

    Article  PubMed  CAS  Google Scholar 

  • Muigai SG, Bassett MJ, Schuster DJ, Scott JW (2003) Greenhouse and field screening of wild Lycopersicon germplasm for resistance to the whitefly Bemisia argentifolii. Phytoparasitica 31(1):27–38

    Article  Google Scholar 

  • Mutschler MA, Doerge RW, Liu SC, Kuai JP, Liedl BE, Shapiro JA (1996) QTL analysis of pest resistance in the wild tomato Lycopersicon pennellii: QTLs controlling acylsugar level and composition. Theor Appl Genetics 92(6):709–718

    Article  CAS  Google Scholar 

  • Neupane FP, Norris DM (1991) Alpha-tocopherol alteration of soybean antiherbivory to Trichoplusia ni larvae. J Chem Ecol 17:1941–1951

    Article  CAS  Google Scholar 

  • Oriani MA, Vendramim JD (2010) Influence of trichomes on attractiveness and ovipositional preference of Bemisia tabaci (Genn.) B biotype (Hemiptera: Aleyrodidae) on tomato genotypes. Neotrop Entomol 39(6):1002–1007

    Article  PubMed  Google Scholar 

  • Oriani MAD, Vendramim JD, Vasconcelos CJ (2011) No-choice ovipositional nonpreference of Bemisia tabaci (Gennadius) B biotype on tomato genotypes. Scientia Agricola 68(2):147–153

    Google Scholar 

  • Paul AVN, Srivastavaa M, Durejaa P, Singha AK (2008) Semiochemicals produced by tomato varieties and their role in parasitism of Corcyra cephalonica (Lepidoptera: Pyralidae) by the egg parasitoid Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Int J Trop Insect Sci 28:108–116

    Article  Google Scholar 

  • Peralta IE, Spooner DM, Knapp S (2008) Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolium, sect. Lycopersicon; Solanaceae. Syst Bot Monogr 84:1–186

    Google Scholar 

  • Reina-Pinto JJ, Yephremov A (2009) Surface lipids and plant defenses. Plant Physiol Biochem 47:540–549

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez F, Wu F, Ane C, Tanksley S, Spooner DM (2009) Do potatoes and tomatoes have a single evolutionary history, and what proportion of the genome supports this history? BMC Evol Biol 9:191

    Article  PubMed  Google Scholar 

  • Rodriguez-Lopez MJ, Garzo E, Bonani JP, Fereres A, Fernandez-Munoz R, Moriones E (2011) Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behavior of Bemisia tabaci and reduce the spread of tomato yellow leaf curl virus. Phytopathology 101(10):1191–1201

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Lopez MJ, Garzo E, Bonani JP, Fernandez-Munoz R, Moriones E, Fereres A (2012) Acylsucrose-producing tomato plants forces Bemisia tabaci to shift its preferred settling and feeding site. PLoS One 7(3):e33064

    Article  PubMed  CAS  Google Scholar 

  • Schilmiller AL, Charbonneau AL, Last RL (2012) Identification of a BAHD acetyltransferase that produces protective acyl sugars in tomato trichomes. Proc Nat Acad Sci USA 109(40):16377–16382

    Article  PubMed  CAS  Google Scholar 

  • Schuster DJ, Everett PH, Price JF, Kring JB (1990) Suppression of the sweet-potato whitefly on commercial fresh-market tomatoes. Proc Fla State Hortic Soc 102:374–379

    Google Scholar 

  • Segal G, Sarfatti M, Schaffer MA, Ori N, Zamir D, Fluhr R (1992) Correlation of genetic and physical structure in the region surrounding the I2 Fusarium oxysporum resistance locus in tomato. Mol Genetic 231(2):179–185

    CAS  Google Scholar 

  • Snyder JC, Carter CD (1984) Leaf trichomes and resistance of Lycopersicon hirsutum and Lycopersicon esculentum to spider mites. J Am Soc Hortic Sci 109(6):837–843

    Google Scholar 

  • Srinivasan R, Uthamasamy S, Talekar NS (2006) Characterization of oviposition attractants of Helicoverpa armigera in two solanaceous plants, Solanum viarum and Lycopersicon esculentum. Curr Sci 90:846–850

    CAS  Google Scholar 

  • Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Toscano LC, Boiça JAL, Maruyama WI (2002) Nonpreference of whitefly for oviposition in tomato genotypes. Scientia Agricola 59:677–681

    Article  Google Scholar 

  • Valentin HE, Lincoln K, Moshiri F, Jensen PK, Qi QG, Venkatesh TV, Karunanandaa B, Baszis SR, Norris SR, Savidge B, Gruys KJ, Last RL (2006) The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18:212–22

    Google Scholar 

  • Van Ooijen JW (2009) Software for the mapping of quantitative trait loci in experimental populations of diploid species. In: Kyazma BV (ed) Wageningen, The Netherlands

  • Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genetic Res 93:343–349

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Walters DS, Steffens JC (1990) Branched-chain amino acid metabolism in the biosynthesis of Lycopersicon pennellii glucose esters. Plant Physiol 93(4):1544–1551

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J, Tanksley SD (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172(4):2529–2540

    Article  PubMed  CAS  Google Scholar 

  • Wilkens RT, Shea GO, Halbreich S, Stamp NE (1996) Resource availability and the trichome defenses of tomato plants. Oecologia 106(2):181–191

    Article  Google Scholar 

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Acknowledgments

This project was financially supported by Royal Netherlands Academy of Arts and Sciences-KNAW (High Quality Solanaceous Vegetables by Exploration of Natural Biodiversity; INDOSOL, 05-PP-21) and Senter-Novem grant SOM071010. Roland Mumm and Ric de Vos acknowledge additional funding from the Centre for Biosystems Genomics and the Netherlands Metabolomics Centre, which are both part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research. We are grateful to Ramadhani Safitri (PT East West Seed Indonesia, Purwakarta, Indonesia) for providing the non-viruliferous B. tabaci for screenings in Indonesia. We thank Roeland Voorrips for advice on statistical analysis. We are also grateful to Greet Steenhuis-Broers, Fien Meijer, Paul Dijkhuis, Martijn van Kaauwen and Koen Pelgrom for their skilful involvement in this research.

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Correspondence to Adriaan W. van Heusden.

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Firdaus, S., van Heusden, A.W., Hidayati, N. et al. Identification and QTL mapping of whitefly resistance components in Solanum galapagense . Theor Appl Genet 126, 1487–1501 (2013). https://doi.org/10.1007/s00122-013-2067-z

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