Capturing flavors from Capsicum baccatum by introgression in sweet pepper

Abstract

Key message

Biochemical characterization in combination with genetic analyses in BC 2 S 1 plants and near-isogenic lines led to the detection and validation of C. baccatum loci affecting flavor, terpenoid content and Brix level.

Abstract

The species Capsicum baccatum includes the most common hot peppers of the Andean cuisine, known for their rich variation in flavors and aromas. So far the C. baccatum genetic variation remained merely concealed for Capsicum annuum breeding, due to post-fertilization genetic barriers encountered in interspecific hybridization. However, to exploit the potential flavor wealth of C. baccatum we combined interspecific crossing with embryo rescue, resulting in a multi-parent BC2S1 population. Volatile and non-volatile compounds plus some physical characters were measured in mature fruits, in combination with taste evaluation by a sensory panel. An enormous variation in biochemical composition and sensory attributes was found, with almost all traits showing transgression. A population-specific genetic linkage map was developed for QTL mapping. BC2S1 QTLs were validated in an experiment with near-isogenic lines, resulting in confirmed genetic effects for physical, biochemical and sensory traits. Three findings are described in more detail: (1) A small C. baccatum LG3 introgression caused an extraordinary effect on flavor, resulting in significantly higher scores for the attributes aroma, flowers, spices, celery and chives. In an attempt to identify the responsible biochemical compounds few consistently up- and down-regulated metabolites were detected. (2) Two introgressions (LG10.1 and LG1) had major effects on terpenoid content of mature fruits, affecting at least 15 different monoterpenes. (3) A second LG3 fragment resulted in a strong increase in Brix without negative effects on fruit size. The mapping strategy, the potential application of studied traits and perspectives for breeding are discussed.

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References

  1. Barchi L, Bonnet J, Boudet C, Signoret P, Nagy I, Lanteri S, Palloix A, Lefebvre V (2007) A high-resolution, intraspecific linkage map of pepper (C. annuum L.) and selection of reduced recombinant inbred line subsets for fast mapping. Genome 50:51–60

    CAS  PubMed  Article  Google Scholar 

  2. Black LL, Hobbs HA, Gatti JM (1991) Tomato spotted wilt virus resistance in Capsicum Chinese ‘PI 152225’ and ‘PI 159236’. Plant Dis 75:863

    Article  Google Scholar 

  3. Blum E, Liu K, Mazourek M, Yoo EY, Jahn M, Paran I (2002) Molecular mapping of the C locus for presence of pungency in Capsicum. Genome 45:702–705

    CAS  PubMed  Article  Google Scholar 

  4. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133

    CAS  PubMed  Article  Google Scholar 

  5. Boukema IW (1982) Resistance to TMV in Capsicum chacoense Hunz. is governed by an allele of the L-locus. Capsicum Newsl 3:47–48

    Google Scholar 

  6. Brand A, Borovsky Y, Meir S, Rogachev I, Aharoni A, Paran I (2012) pc8.1, a major QTL for pigment content in pepper fruit, is associated with variation in plastid compartment size. Planta 235:579–588

    CAS  PubMed  Article  Google Scholar 

  7. Bucheli P, Voirol E, de la Torre R, Lopez J, Rytz A, Tanksley SD, Petiard V (1999) Definition of non-volatile markers for flavor of tomato (Lycopersicon esculentum Mill.) as tools in selection and breeding. J Agric Food Chem 47:659–664

    CAS  PubMed  Article  Google Scholar 

  8. Cookson PJ, Kiano JW, Shipton CA, Fraser PD, Romer S, Schuch W, Bramley PM, Pyke KA (2003) Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta 217:896–903

    CAS  PubMed  Article  Google Scholar 

  9. Do Rêgo ER, Do Rêgo MM, Finger FL, Cruz CD, Casali VWD (2009) A diallel study of yield components and fruit quality in chilli chilli pepper (C. baccatum). Euphytica 168:275–287

    Article  Google Scholar 

  10. Eggink PM, Haanstra JPW, Tikunov Y, Bovy AG, Visser RGF (2010) Characterization of volatile and non-volatile compounds of fresh pepper (C. annuum). In: Advances in genetics and breeding of capsicum and eggplant. Editorial de la Universitat Politècnica de València, Spain, pp 251–259

  11. Eggink PM, Maliepaard C, Tikunov Y, Haanstra JPW, Bovy AG, Visser RGF (2012a) A taste of sweet pepper: volatile and non-volatile chemical composition of fresh sweet pepper (C. annuum) in relation to sensory evaluation of taste. Food Chem 132:301–310

    CAS  Article  Google Scholar 

  12. Eggink PM, Maliepaard C, Tikunov Y, Haanstra JPW, Pohu-Flament LMM, De Wit-Maljaars SC, Willeboordse-Vos F, Bos S, Benning-de Waard C, De Grauw-van Leeuwen PJ, Freymark G, Bovy AG, Visser RGF (2012b) Prediction of sweet pepper (C. annuum) flavor over different harvests. Euphytica 187:117–131

    Article  Google Scholar 

  13. Falara V, Akhtar TA, Nguyen TTH, Spyropoulou EA, Bleeker PM, Schauvinhold I, Matsuba Y, Bonini ME, Schilmiller AL, Last RL, Schuurink RC, Pichersky E (2011) The tomato terpene synthase gene family. Plant Physiol 157:770–789

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  14. Georgelis N, Scott JW, Baldwin EA (2004) Relationship of tomato fruit sugar concentration with physical and chemical traits and linkage of RAPD markers. J Amer Soc Hort Sci 129:839–845

    CAS  Google Scholar 

  15. Grandillo S, Zamir D, Tanksley SD (1999) Genetic improvement of processing tomatoes: a 20 years perspective. Euphytica 110:85–97

    Article  Google Scholar 

  16. Heiser CB (1976) Peppers: Capsicum (Solanaceae). In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 265–268

    Google Scholar 

  17. Kalemba D, Kunicka A (2003) Antibacterial and antifungal properties of essential oils. Curr Med Chem 10:813–829

    CAS  PubMed  Article  Google Scholar 

  18. Kappers IF, Hoogerbrugge H, Bouwmeester HJ, Dicke M (2011) Variation in herbivory-induced volatiles among cucumber (Cucumis sativus L.) varieties has consequences for the attraction of carnivorous natural enemies. J Chem Ecol 37:150–160

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  19. Kim S, Kim KT, Kim DH, Yang EY, Cho MC, Jamal A, Chae Y, Pae DH, Oh DG, Hwang JK (2010) Identification of quantitative trait loci associated with anthracnose resistance in chili pepper (Capsicum spp.). Korean J Horticul Sci Technol 28:1014–1024

    CAS  Google Scholar 

  20. Kollmannsberger H, Rodriguez-Burruezo A, Nitz S, Nuez F (2011) Volatile and capsaicinoid composition of aji (C. baccatum) and rocoto (C. pubescens), two Andean species of chile peppers. J Sci Food Agric 91:1598–1611

    CAS  PubMed  Article  Google Scholar 

  21. Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugenics 12:172–175

    Article  Google Scholar 

  22. Krumbein A, Auerswald H (1998) Characterization of aroma volatiles in tomatoes by sensory analyses. Nahrung 42:395–399

    CAS  PubMed  Article  Google Scholar 

  23. Lefebvre V, Kuntz M, Camara B, Palloix A (1998) The capsanthin–capsorubin synthase gene: a candidate gene for the y locus controlling the red fruit colour in pepper. Plant Mol Biol 36:785–789

    CAS  PubMed  Article  Google Scholar 

  24. Luning PA, De Rijk T, Wichers HJ, Roozen JP (1994) Gas chromatography, mass spectrometry, and sniffing port analyses of volatile compounds of fresh bell peppers (C. annuum) at different ripening stages. J Agricul Food Chem 42:977–983

    CAS  Article  Google Scholar 

  25. Nagegowda DA (2010) Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett 584:2965–2973

    CAS  PubMed  Article  Google Scholar 

  26. Pérez-Sánchez R, Infante F, Gálvez C, Ubera JL (2007) Fungitoxic activity against phytopathogenic fungi and the chemical composition of Thymus zygis essential oils. Food Sci Tech Int 13:341–347

    Article  Google Scholar 

  27. Pickersgill B (1997) Genetic resources and breeding of Capsicum spp. Euphytica 96:129–133

    Article  Google Scholar 

  28. Poulos J (1994) Pepper breeding (Capsicum spp.): achievements, challenges and possibilities. Plant Breed Abstr 64:143–155

    Google Scholar 

  29. Rodriguez-Burruezo A, Prohens J, Raigon MD, Nuez F (2009) Variation for bioactive compounds in aji (Capsicum baccatum L.) and rocoto (C. pubescens R. & P.) and implications for breeding. Euphytica 170:169–181

    CAS  Article  Google Scholar 

  30. Rodriguez-Burruezo A, Kollmannsberger H, Gonzalez-Mas MC, Nitz S, Nuez F (2010) HS-SPME comparative analysis of genotypic diversity in volatile fraction and aroma contributing compounds of Capsicum fruits from the annuum-chinese-frutescens complex. J Agricul Food Chem 58:4388–4400

    CAS  Article  Google Scholar 

  31. Stevens MA, Kader AA, Albright-Holton M, Algazi M (1977) Genotypic variation for flavor and composition in fresh market tomatoes. J Am Soc Hort Sci 102:680–689

    CAS  Google Scholar 

  32. Stewart C, Kang BC, Liu K, Mazourek M, Moore SL, Yoo EY, Kim BD, Paran I, Jahn MM (2005) The Pun1 gene for pungency in pepper encodes a putative acyltransferase. Plant J 42:675–688

    CAS  PubMed  Article  Google Scholar 

  33. Tandon KS, Baldwin EA, Shewfelt RL (2000) Aroma perception of individual volatile compounds in fresh tomatoes (Lycopersicon esculentum Mill.) as affected by the medium of evaluation. Postharvest Biol Technol 20:261–268

    CAS  Article  Google Scholar 

  34. Thorup TA, Tanyolac B, Livingstone KD, Popovsky S, Paran I, Jahn M (2000) Candidate gene analysis of organ pigmentation loci in the Solanaceae. PNAS 97:11192–11197

    CAS  PubMed  Article  Google Scholar 

  35. Tikunov YM, Laptenok S, Hall RD, Bovy AG, de Vos RCH (2012) MSClust: a tool for unsupervised mass spectra extraction of chromatography–mass spectrometry ion-wise aligned data. Metabolomics 8:714–718

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  36. Van Ooijen JW (2006) JoinMap 4.0: software for the calculation of genetic linkage maps in experimental populations. Plant Research International, Wageningen

    Google Scholar 

  37. Van Ooijen JW (2009) MapQTL 6: software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen

    Google Scholar 

  38. Van Ruth SM, Roozen JP, Cozijnsen JL, Posthumus MA (1995) Volatile compounds of rehydrated French beans, bell peppers and leeks. Part II. Gas chromatography/sniffing port analysis and sensory evaluation. Food Chem 54:1–7

    Article  Google Scholar 

  39. Velterop JS, Vos F (2001) A rapid and inexpensive microplate assay for the enzymatic determination of glucose, fructose, sucrose, L-malate and citrate in tomato (Lycopersicon esculentum) extracts and in orange juice. Phytochem Anal 12:299–304

    CAS  PubMed  Article  Google Scholar 

  40. Verkerke W, Kersten M (2000) The role of fruit texture in flavour of tomato and sweet pepper. In: Spatz HC, Speck T (eds) Proceedings third plant biomechanics conference Freiburg. Thieme, Stuttgart, pp 342–347

    Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  42. Wahyuni Y, Ballester A-R, Tikunov Y, de Vos CHR, Pelgrom KTB, Maharijaya A, Sudarmonowati E, Bino RJ, Bovy AG (2013) Metabolomics and molecular marker analysis to explore pepper (Capsicum sp.) biodiversity. Metabolomics 9:130–144

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  43. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    CAS  PubMed  Google Scholar 

  44. Wu F, Eannetta NT, Xu Y, Durrett R, Mazourek M, Jahn MM, Tanksley SD (2009) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118:1279–1293

    CAS  PubMed  Article  Google Scholar 

  45. Yoon JB, Yang DC, Lee WP, Ahn SY, Park HG (2004) Genetic resources resistant to anthracnose in the genus Capsicum. J Kor Soc Hort Sci 45:318–323

    Google Scholar 

  46. Yoon JB, Yang DC, Wahng Do J, Park HG (2006) Overcoming two post-fertilization genetic barriers in interspecific hybridization between C. annuum and C. baccatum for introgression of anthracnose resistance. Breed Sci 56:31–38

    CAS  Article  Google Scholar 

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Acknowledgments

The authors kindly acknowledge Harry Jonker and Yvonne Birnbaum at Plant Research International for performing the SPME–GC–MS analyses. In addition we thank Suzanne de Wit, Femke Willeboordse, Laure Pohu, Sander Bos, Tineke Benning and Paula de Grauw for performing a massive job on sample preparation and non-volatile measurements. Finally, we are grateful to all people at Rijk Zwaan who took care of perfect greenhouse management.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiments comply with the current laws of the Netherlands.

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Correspondence to P. M. Eggink.

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Communicated by M. J. Havey.

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Eggink, P.M., Tikunov, Y., Maliepaard, C. et al. Capturing flavors from Capsicum baccatum by introgression in sweet pepper. Theor Appl Genet 127, 373–390 (2014). https://doi.org/10.1007/s00122-013-2225-3

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Keywords

  • Linkage Group
  • Terpenoid
  • Monoterpene
  • Fruit Size
  • Total Soluble Solid