Abstract
Heavy-ion beam irradiation is an effective technique for mutation breeding to produce new cultivars. Heavy-ion beams have high linear energy transfer capable of breaking the double-stranded DNA molecules, thus inducing stable knockout mutants. Here, we report the first application of this technology to produce hypoallergenic peanut lacking major allergens, Ara h 2 and 3, from the Japanese Nakateyutaka variety. After irradiation with either N or C heavy-ion beams at a dose of 100 Gy, seventeen knockout mutants from 11,335 screened M2 seeds were obtained, eight of which lacked either one of the two isoforms of Ara h 2, and the other nine lacked one of the isoforms of Ara h 3. This result indicates that heavy-ion beam irradiation is a powerful means of producing knockout hypoallergenic peanuts.
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Abbreviations
- HIBI:
-
Heavy-ion beam irradiation
- RIBF:
-
RIKEN Nishina Center Radioactive-Isotope Beam Factory
- IUIS:
-
International Union of Immunological Societies
- SDS-PAGE:
-
Sodium dodecyl sulfate polyacrylamide gel electrophoresis
References
Abe T, Matsuyama T, Sekido S, Yamaguchi I, Yoshida S, Kameya T (2002) Chlorophyll-deficient mutants of rice demonstrated the deletion of a DNA fragment by heavy-ion irradiation. J Radiat Res (Tokyo) 43(Suppl):S157–S161
Bannon GA, Cockrell G, Connaughton C, West CM, Helm R, Stanley JS, King N, Rabjohn P, Sampson HA, Burks AW (2001) Engineering, characterization and in vitro efficacy of the major peanut allergens for use in immunotherapy. Int Arch Allergy Immunol 124:70–72
Ben-Shoshan M, Kagan RS, Alizadehfar R, Joseph L, Turnbull E, St Pierre Y, Clarke AE (2009) Is the prevalence of peanut allergy increasing? A 5-year follow-up study in children in Montreal. J Allergy Clin Immunol 123:783–788
Ben-Shoshan M, Harrington DW, Soller L, Fragapane J, Joseph L, St Pierre Y, Godefroy SB, Elliot SJ, Clarke AE (2010) A population-based study on peanut, tree nut, fish, shellfish, and sesame allergy prevalence in Canada. J Allergy Clin Immunol 125:1327–1335
Cabanillas B, Rodríguez J, González Á, Cuadrado C, Muzquiz M, Burbano C, Crespo JF (2009) Effects of autoclaving on allergenicity of roasted peanut. J Allergy Clin Immunol 123:S31
Cecchini E, Mulligan BJ, Covey SN, Miner JJ (1998) Characterization of gamma irradiation-induced deletion mutations at a selectable locus in Arabidopsis. Mutat Res 401:199–206
Chu Y, Faustinelli P, Ramos ML, Hajduch M, Stevenson S, Thelen JJ, Maleki SJ, Cheng H, Ozias-Akins P (2008) Reduction of IgE binding and nonpromotion of Aspergillus flavus fungal growth by simultaneously silencing Ara h 2 and Ara h 6 in peanut. J Agric Food Chem 56:11225–11233
Chung S-Y, Champagne ET (2009) Reducing the allergenic capacity of peanut extracts and liquid peanut butter by phenolic compounds. Food Chem 115:1345–1349
Cooper JL, Till BJ, Laport RG, Darlow MC, Kleffner JM, Jamai A, El-Mellouki T, Liu S, Ritchie R, Nielsen N, Bilyeu KD, Meksem K, Comai L, Henikoff S (2008) TILLING to detect induced mutations in soybean. BMC Plant Biol 8:9
Dodo HW, Konan KN, Chen FC, Egnin M, Viquez OM (2008) Alleviating peanut allergy using genetic engineering: the silencing of the immunodominant allergen Ara h 2 leads to its significant reduction and a decrease in peanut allergenicity. Plant Biotechnol J 6:135–145
Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L, Henikoff S (2003) Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 64:731–740
Guo B, Liang X, Chung SY, Holbrook CC, Maleki SJ (2008) Proteomic analysis of peanut seed storage proteins and genetic variation in a potential peanut allergen. Protein Pept Lett 15:567–577
Hamatani M, Iitsuka Y, Abe T, Miyoshi K, Yamamoto M, Yoshida S (2001) Mutant flowers of dahlia (Dahlia pinnata Cav.) induced by heavy-ion beams. RIKEN Accel Prog Rep 34:169
Hayashi Y, Takehisa H, Kazama Y, Ichida H, Ryuto H, Fukunishi N, Abe T, Kamba C, Sato T (2007) Effects of ion beam irradiation on mutation induction in rice. In: Cyclotrons and their applications 2007, Eighteenth international conference, pp 1–5
Ichida H, Matsuyama T, Ryuto H, Hayashi Y, Fukunishi N, Abe T, Koba T (2008) Molecular characterization of microbial mutations induced by ion beam irradiation. Mutat Res/Fund Mol Mech Mutagen 639:101–107
Kanaya T, Saito H, Hayashi Y, Fukunishi N, Ryuto H, Miyazaki K, Kusumi T, Abe T, Suzuki K (2008) Heavy-ion beam-induced sterile mutants of verbena (Verbena hybrida) with an improved flowering habit. Plant Biotechnol 25:91–96
Kazama Y, Saito H, Fujiwara M, Matsuyama T, Hayashi Y, Ryuto H, Fukunishi N, Abe T (2007) An effective method for detection and analysis of DNA damage induced by heavy-ion beams. Biosci Biotechnol Biochem 71:2864–2869
Kazama Y, Saito H, Yamamoto YY, Hayashi Y, Ichida H, Ryuto H, Fukunishi N, Abe T (2008) LET-dependent effects of heavy-ion beam irradiation in Arabidopsis thaliana. Plant Biotechnol 25:113–117
Kazama Y, Hirano T, Saito H, Liu Y, Ohbu S, Hayashi Y, Abe T (2011) Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. BMC Plant Biol 11:161
Kikuchi S, Saito Y, Ryuto H, Fukunishi N, Abe T, Tanaka H, Tsujimoto H (2009) Effects of heavy-ion beams on chromosomes of common wheat, Triticum aestivum. Mutat Res 669:63–66
Knoll JE, Ramos ML, Zeng Y, Holbrook CC, Chow M, Chen S, Maleki S, Bhattacharya A, Ozias-Akins P (2011) TILLING for allergen reduction and improvement of quality traits in peanut (Arachis hypogaea L.). BMC Plant Biol 11:81
Li J, Shefcheck K, Callahan J, Fenselau C (2010) Primary sequence and site-selective hydroxylation of prolines in isoforms of a major peanut allergen protein Ara h 2. Protein Sci 19:174–182
Liu AH, Jaramillo R, Sicherer SH, Wood RA, Bock SA, Burks AW, Massing M, Cohn RD, Zeldin DC (2010) National prevalence and risk factors for food allergy and relationship to asthma: results from the National Health and Nutrition Examination Survey 2005-2006. J Allergy Clin Immunol 126:798–806 e713
Mari A, Scala E (2006) Allergome: a unifying platform. Arb Paul Ehrlich Inst Bundesamt Sera Impfstoffe Frankf A M 95:29–39
Miyazaki K, Suzuki K, Abe T, Katsumoto Y, Yoshida S, Kusumi T (2002) Isolation of variegated mutants of Petunia hybrida using heavy-ion beam irradiation. RIKEN Accel Prog Rep 35:130
Miyazaki K, Suzuki K, Iwaki K, Abe T, Yoshida S, Fukui H (2006) Flower pigment mutations induced by heavy ion beam irradiation in an inter specific hybrid of Torenia. Plant Biotechnol 23:163–167
Mondoulet L, Paty E, Drumare MF, Ah-Leung S, Scheinmann P, Willemot RM, Wal JM, Bernard H (2005) Influence of thermal processing on the allergenicity of peanut proteins. J Agric Food Chem 53:4547–4553
Morita R, Kusaba M, Iida S, Yamaguchi H, Nishio T, Nishimura M (2009) Molecular characterization of mutations induced by gamma irradiation in rice. Genes Genet Syst 84:361–370
Owais WM, Kleinhofs A (1988) Metabolic activation of the mutagen azide in biological systems. Mutat Res 197:313–323
Richardson FC, Richardson KK (1990) Sequence-dependent formation of alkyl DNA adducts: a review of methods, results, and biological correlates. Mutat Res 233:127–138
RIKEN (2008) Creating novel plants using heavy-ion beams. RIKEN Res 3:18–19
Ryuto H, Fukunishi N, Hayashi Y, Ichida H, Abe T, Kase M, Yano Y (2008) Heavy-ion beam irradiation facility for biological samples in RIKEN. Plant Biotech 25:119–122
Schmitt DA, Nesbit JB, Hurlburt BK, Cheng H, Maleki SJ (2010) Processing can alter the properties of peanut extract preparations. J Agric Food Chem 58:1138–1143
Sicherer SH, Munoz-Furlong A, Godbold JH, Sampson HA (2010) US prevalence of self-reported peanut, tree nut, and sesame allergy: 11-year follow-up. J Allergy Clin Immunol 125:1322–1326
Sugiyama M, Hayashi Y, Fukunishi N, Ryuto H, Terakawa T, Abe T (2008) Development of flower color mutant of Dianthus chinensis var. semperflorens by heavy-ion beam irradiation. RIKEN Accel Prog Rep 41:229
Till BJ, Reynolds SH, Weil C, Springer N, Burtner C, Young K, Bowers E, Codomo CA, Enns LC, Odden AR, Greene EA, Comai L, Henikoff S (2004) Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol 4:12
Till BJ, Cooper J, Tai TH, Colowit P, Greene EA, Henikoff S, Comai L (2007) Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol 7:19
Venter C, Hasan Arshad S, Grundy J, Pereira B, Bernie Clayton C, Voigt K, Higgins B, Dean T (2010) Time trends in the prevalence of peanut allergy: three cohorts of children from the same geographical location in the UK. Allergy 65:103–108
Yu J, Ahmedna M, Goktepe I, Cheng H, Maleki S (2011) Enzymatic treatment of peanut kernels to reduce allergen levels. Food Chem 127:1014–1022
Acknowledgments
We thank Prof. Reiko Urade (Kyoto University) for warm encouragement. The first author also wishes to thank the Japanese Government (Monbukagakusho:MEXT) for scholarship support.
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Cabanos, C.S., Katayama, H., Urabe, H. et al. Heavy-ion beam irradiation is an effective technique for reducing major allergens in peanut seeds. Mol Breeding 30, 1037–1044 (2012). https://doi.org/10.1007/s11032-011-9687-2
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DOI: https://doi.org/10.1007/s11032-011-9687-2