Abstract
Condensed tannins (proanthocyanidins, PAs) in the seed meal of oilseed rape can potentially have a negative impact on non-ruminant livestock nutrition, particularly because of their ability to form indigestible, astringent or bitter-tasting complexes with proteins. One option to overcome this problem is the breeding of oilseed rape varieties with reduced condensed tannins in the seed coat. This might be achievable via selection of genotypes with thinner seed coats and consequently reduced condensed tannin accumulation (seed coat structural cell mutants), or alternatively by selection of genotypes with reduced biosynthesis of condensed tannins (flavonoid biosynthesis mutants). Both types of transparent testa (TT) mutants are well-characterised in Arabidopsis; however the genetic basis of the yellow-seed trait in the polyploid genome of rapeseed is still not completely understood. In this study, genetic and chemical analyses of PAs were performed in 166 doubled haploid (DH) rapeseed lines from the segregating Brassica napus doubled haploid population YE2-DH (black seed × yellow seed). Using these analyses, the relationship between seed colour and PA fractions in B. napus was investigated with a view to improving the rapeseed meal quality. Proanthocyanidin contents were estimated by vanillin and HPLC assays and the obtained values were used to identify quantitative trait loci. Closely linked molecular markers that were identified during this study for the target traits (seed colour, condensed tannins) can be valuable tools for breeding of new oilseed rape cultivars with reduced levels of antinutritive PA compounds.
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References
AOAC (1965) Official methods of analysis, 10th edn. Association of Official Analytical Chemists, Washington DC
Applequist L, Ohlson R (1972) Rapeseed cultivation, composition, processing and utilization. Elsevier, Amsterdam, pp 39–57
Badani AG, Snowdon RJ, Baetzel R, Lipsa FD, Wittkop B, Horn R, De Haro A, Font R, Lühs W, Friedt W (2006) A model for the inheritance of seed colour in oilseed rape (Brassica napus L.) based on analyses of segregation data, QTL and associated quality traits in two genetically distinct crosses. Genome 49:1499–1509. doi:10.1139/G06-091
Bate-Smith EC, Ribereau-Gayon P (1959) Leucoanthocyanidins in seeds. Qual Plant Mater Veg 5:189–198. doi:10.1007/BF01100181
Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, Lepiniec L (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39:366–380. doi:10.1111/j.1365-313X.2004.02138.x
Bell JM (1993) Factors affecting the nutritional value of canola meal: a review. Can J Anim Sci 73:679–697. doi:10.4141/cjas93-075
Blair R, Reichert RD (1984) Carbohydrate and phenolic constituents in a comprehensive range of rapeseed and canola fractions: nutritional significance for animals. J Sci Food Agr 35:29–35. doi:10.1002/jsfa.2740350106
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Clandinin D, Heard J (1968) Tannins in prepress-solvent and solvent-processed rapeseed meal. Poult Sci 47:688–689
Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination and longelivity in Arabidopsis. Plant Physiol 122:403–413. doi:10.1104/pp.122.2.403
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Durkee AB (1971) The nature of tannins in rapeseed (Brassica campestris). Phytochemistry 10:1583–1585. doi:10.1016/0031-9422(71)85028-8
Fenwick R, Hoggan S (1976) The tannin content of rapeseed meals. Br Poult Sci 17:59–62. doi:10.1080/00071667608416250
Fenwick GR, Caralyn LC, Pearson AW, Butler EJ (1984) The treatment of rapeseed meal and its effect on chemical composition and egg tainting potential. J Sci Food Agric 35:757–761. doi:10.1002/jsfa.2740350711
Fu FY, Liu LZ, Chai YR, Chen L, Yang T, Meng-Yang J, Ma AF, Yan ZY, Zhang ZS, Li JN (2007) Localization of QTLs for seed color using recombinant inbred lines of Brassica napus in different environments. Genome 50:840–854. doi:10.1139/G07-068
He F, Pan QH, Shi Y, Duan CQ (2008) Biosynthesis and genetic regualtion of proanthocyanidins in plants. Molecules 13:674–2703. doi:10.3390/molecules13102674
Jensen S, Liu Y, Eggum B (1995) The influence of variations in seed size and hull content on composition and digestibility of rapeseed, vol II., pp 188–190
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Leung J, Fenton TW, Mueller MM, Clandinin DR (1979) Condensed tannins of rapeseed meals. J Food Sci 44:1313–1316. doi:10.1111/j.1365-2621.1979.tb06427.x
Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171–179
Lowe AJ, Moule C, Trick M, Edwards KJ (2004) Efficient largescale development of microsatellites for marker and mapping applications in Brassica crop species. Theor Appl Genet 108:1103–1112. doi:10.1007/s00122-003-1522-7
Matthäus B (1998) Isolation, fractionable and HPLC analysis of neutral phenolic compounds in rapeseeds. Nahrung 42:75–80
Mitaru BN, Blair R, Bell TM, Reichert RD (1982) Tannin and fiber contents of rapeseed and canola hulls. Can J Anim Sci 62:661–663
Mittasch J, Mikolajewski S, Breuer F, Strack D, Milkowski C (2010) Genomic microstructure and differential expression of the genes encoding UDP-glucose:sinapate glucosyltransferase (UGT84A9) in oilseed rape (Brassica napus). Theor Appl Genet 120:1485–1500
Mueller-Harvey I, Mcallan AB (1992) Tannins: their biochemistry and nutritional properties. Adv Plant Cell Biochem Biotechnol 1:151–217
Naczk M, Nichols T, Pink D, Sosulski F (1994) Condensed tannins in canola hulls. J Agric Food Chem 42:2196–2200. doi:10.1021/jf00046a022
Naczk M, Amarowic R, Sullivan A, Shahidi F (1998) Current research developments on polyphenolics of rapeseed/canola: a review. Food Chem 62:489–502
Naczk M, Amarowicz R, Pink D, Shahidi F (2000) Insoluble tannins of canola/rapeseed. J Agric Food Chem 48:1758–1762. doi:10.1021/jf9908401
Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L (2000) The TT8 gene encodes a basic helix–loop–helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12:1863–1878. doi:10.1105/tpc.12.10.1863
Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for the proanthocyanidin accumulation in developing seed. Plant Cell 13:2099–2114. doi:10.1105/tpc.13.9.2099
Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L (2002) The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14:2463–2479. doi:10.1105/tpc.004127
Piotrowska A, Krymanski J, Bartkowiak-Broda I, Krotka K (2003) Characteristic of yellow-seeded lines of winter oilseed rape. In: Proc 11th Int Rapeseed Congr, Frederiksberg, Denmark, vol I, pp 247–249
Piquemal J, Cinquin E, Couton F, Rondeau C, Seignoret E, Doucet I, Perret D, Villeger MJ, Vincourt P, Blanchard P (2005) Construction of an oilseed rape (Brassica napus L.) genetic map with SSR markers. Theor Appl Genet 111:1514–1523
Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17:2966–2980. doi:10.1105/tpc.105.035154
Price ML, Van Scoyoc S, Butler LG (1978) A critical evaluation of the vanillin reaction as an assay for tannin in sorghum grain. J Agric Food Chem 26:1214–1218. doi:10.1021/jf60219a031
Ragan MA, Glombitza K (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:177–241
Rezaeizad A, Wittkop B, Snowdon R, Hasan M, Mohammadi V, Zali A, Friedt W (2011) Identification of QTLs for phenolic compounds in oilseed rape (Brassica napus L.) by association mapping using SSR markers. Euphytica 177:335–342. doi:10.1007/s10681-010-0231-y
Sagasser M, Lu GH, Hahlbrock K, Weisshaar B (2002) A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes Dev 16:138–149. doi:10.1101/gad.212702
Schofield P, Mbugua DM, Pell AN (2001) Analysis of condensed tannins: a review. Anim Feed Sci Technol 91:21–40. doi:10.1016/S0377-8401(01)00228-0
Shahidi F, Naczk M (1988) Effect of processing on the phenolic constituents of canola. Bulletin de Liaison Groupe Polyphenols 14:89–92
Shahidi F, Naczk M (1989) Effect of processing on the content of condensed tannins in rapeseed meals. A research note. J Food Sci 54:1082–1083. doi:10.1111/j.1365-2621.1989.tb07951.x
Shahidi F, Naczk M (1992) An overview of the phenolics of canola and rapeseed: chemical, sensory and nutritional implications. J Am Oil Chem Soc 69:917–924. doi:10.1007/BF02636344
Snowdon RJ, Wittkop B, Rezaidad A, Hasan M, Lipsa FD, Stein A, Friedt W (2010) Regional association analysis delineates a sequenced chromosome region influencing antinutritive seed meal compounds in oilseed rape. Genome 53:917–928
Sosulski F (1979) Organoleptic and nutritional effects of phenolics. J Am Oil Chem Soc 56:711–715. doi:10.1007/BF02663047
Stafford HA (1990) Flavonoid metabolism. CRC Press, Boca Raton, pp 63–93
Sun B, Leandro MC, De Freitas V, Spranger MI (2006) Fractionation of red wine polyphenols by solidphase extraction and liquid chromatography. J Chromatogr A 1128:27–38. doi:10.1016/j.chroma.2006.06.026
Theander O, Åman P, Miksche GE, Yasuda S (1977) Carbohydrates, polyphenols and lignin in seed hulls of different colors from turnip rapeseed. J Agric Food Chem 25:270–273. doi:10.1021/jf60210a042
Utz HF, Melchinger AE (1996) PLABQTL: a program for composite interval mapping of QTL. J Quant Trait Loci 2:1–5
Van Deynze AE, Beversdorf WD, Pauls KP (1993) Temperature effects on seed color in black- and yellow-seeded rapeseed. Can J Plant Sci 73:383–387. pubs.aic.ca/doi/pdf/10.4141/cjps93-057
Whetten RW, Mackay JJ, Sederoff R (1998) Recent advances in understanding lignin biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 49:585–609. doi:10.1146/annurev.arplant.49.1.585
Winkel-Shirley B (1998) Flavonoids in seeds and grains: physiological function, agronomic importance and the genetics of biosynthesis. Seed Sci Res 8:415–422. doi:10.1017/S0960258500004372
Wittkop B, Snowdon RJ, Friedt W (2009) Status and perspectives of breeding for enhanced yield and quality of oilseed crops for Europe. Euphytica 170:131–140. doi:10.1007/s10681-009-9940-5
Xiao DR, Liu HL (1982) Correlation analysis of seed colour and seed oil in Brassica napus L. Acta Agronomica Sinica 8:24–27
Acknowledgments
This work was performed with funding from the Federal Ministry of Education and Research (BMBF) as part of the collaborative research project GABI-CGAT: YelLowSin with support by the commercial partners KWS Saat AG, Deutsche Saatveredelung AG, Norddeutsche Pflanzenzucht Hans-Georg Lembke KG and SAATEN-UNION BIOTEC GmbH. Financial support from German Academic Exchange Service (DAAD) to the first author is gratefully acknowledged. We thank Susmitha Katha for unpublished data on phenolic compounds in rapeseed meal. Excellent technical assistance of Nelly Weis and Swetlana Renner is gratefully acknowledged.
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Lipsa, F.D., Snowdon, R. & Friedt, W. Quantitative genetic analysis of condensed tannins in oilseed rape meal. Euphytica 184, 195–205 (2012). https://doi.org/10.1007/s10681-011-0546-3
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DOI: https://doi.org/10.1007/s10681-011-0546-3