Lutein esterification in wheat endosperm is controlled by the homoeologous group 7, and is increased by the simultaneous presence of chromosomes 7D and 7Hch from Hordeum chilense
M. G. Mattera A B , A. Cabrera B , D. Hornero-Méndez C and S. G. Atienza A DA Institute for Sustainable Agriculture, CSIC, E-14004 Córdoba, Spain.
B Department of Genetics, ETSIAM, University of Córdoba, Campus de Excelencia Internacional Agroalimentario, ceiA3, 14071 Córdoba, Spain.
C Departament of Food Phytochemistry, Instituto de la Grasa (CSIC), Campus Universidad Pablo de Olavide, Edificio 46, Ctra. de Utrera, Km 1, E-41013 Sevilla, Spain.
D Corresponding author. Email: sgatienza@ias.csic.es
Crop and Pasture Science 66(9) 912-921 https://doi.org/10.1071/CP15091
Submitted: 17 March 2015 Accepted: 17 June 2015 Published: 19 August 2015
Abstract
The high carotenoid content in tritordeum (×Tritordeum Ascherson et Graebner) grains is derived from its wild parent, Hordeum chilense Roem. et Schulz. Phytoene synthase 1 (Psy1) is located on chromosome 7HchS and plays a major role in this trait. This study investigates the impact of the introgression of chromosome 7Hch into common wheat background on carotenoid composition, including xanthophylls esterified with fatty acids (monoesters and diesters). All of the genetic stocks carrying Psy1 from H. chilense increased their carotenoid content relative to common wheat. In addition, significant changes in the carotenoid profile were detected in different genetic stocks. The most relevant was the increase in content of lutein diesters when both 7Hch and 7D were present, which indicates the existence of genes involved in the esterification of xanthophylls in both chromosomes. Furthermore, our results suggest that 7Hch genes preferentially esterify lutein with palmitic acid, whereas 7D is either indifferent to the fatty acid or it prefers linoleic acid for lutein esterification. The involvement and complementarity of 7Hch and 7D are highly significant considering the scarcity of previous results on lutein esterification in wheat.
Additional keywords: alien Triticeae, carotenoid esters, esterification, genetic stocks, lutein esters, yellow pigment content.
References
Abdel-Aal ESM, Young JC, Wood PJ, Rabalski I, Hucl P, Falk D, Fregeau-Reid J (2002) Einkorn: A potential candidate for developing high lutein wheat. Cereal Chemistry 79, 455–457.| Einkorn: A potential candidate for developing high lutein wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjvFCmsrg%3D&md5=f5152481aed7b40f026b2d372db953aeCAS |
Ahmad FT, Asenstorfer RE, Soriano IR, Mares DJ (2013) Effect of temperature on lutein esterification and lutein stability in wheat grain. Journal of Cereal Science 58, 408–413.
| Effect of temperature on lutein esterification and lutein stability in wheat grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsV2mu7%2FO&md5=bf1d3cc11017c6d044f9c57bf85426e9CAS |
Alvarez JB, Martin LM, Martín A (1998) Chromosomal localization of genes for carotenoid pigments using addition lines of Hordeum chilense in wheat. Plant Breeding 117, 287–289.
| Chromosomal localization of genes for carotenoid pigments using addition lines of Hordeum chilense in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltFKmu7s%3D&md5=a047705971eaea7940529d1c80ef2d20CAS |
Alvarez JB, Martin LM, Martin A (1999) Genetic variation for carotenoid pigment content in the amphiploid Hordeum chilense × Triticum turgidum conv. durum. Plant Breeding 118, 187–189.
| Genetic variation for carotenoid pigment content in the amphiploid Hordeum chilense × Triticum turgidum conv. durum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFSmsr0%3D&md5=63b33fce67efad7c84703e5ca97db4f5CAS |
Atienza SG, Avila CM, Martin A (2007a) The development of a PCR-based marker for Psy1 from Hordeum chilense, a candidate gene for carotenoid content accumulation in tritordeum seeds. Australian Journal of Agricultural Research 58, 767–773.
| The development of a PCR-based marker for Psy1 from Hordeum chilense, a candidate gene for carotenoid content accumulation in tritordeum seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSgt7vM&md5=f577d6f04e00b080f4651608e7eb836aCAS |
Atienza SG, Ballesteros J, Martin A, Hornero-Mendez D (2007b) Genetic variability of carotenoid concentration and degree of esterification among tritordeum (×Tritordeum Ascherson et Graebner) and durum wheat accessions. Journal of Agricultural and Food Chemistry 55, 4244–4251.
| Genetic variability of carotenoid concentration and degree of esterification among tritordeum (×Tritordeum Ascherson et Graebner) and durum wheat accessions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1elsLg%3D&md5=300054a7f1f2c99da8f391fbba46cdb8CAS | 17439153PubMed |
Ballesteros J, Ramirez MC, Martinez C, Atienza SG, Martin A (2005) Registration of HT621, a high carotenoid content tritordeum germplasm line. Crop Science 45, 2662–2663.
| Registration of HT621, a high carotenoid content tritordeum germplasm line.Crossref | GoogleScholarGoogle Scholar |
Blanco A, Colasuonno P, Gadaleta A, Mangini G, Schiavulli A, Simeone R, Digesù AM, De Vita P, Mastrangelo AM, Cattivelli L (2011) Quantitative trait loci for yellow pigment concentration and individual carotenoid compounds in durum wheat. Journal of Cereal Science 54, 255–264.
| Quantitative trait loci for yellow pigment concentration and individual carotenoid compounds in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFahsrvE&md5=1d1903950249f57447938a875bdac069CAS |
Britton G, Hornero-Mendez D (1997) Carotenoids and colour in fruit and vegetables. In ‘Phytochemistry of fruit and vegetables’. (Eds FA Tomás-Barberán, RJ Robins) pp. 11–27. (Clarendon Press: Oxford, UK)
Britton G, Liaaen-Jensen S, Pfander H (2009) ‘Carotenoids. Vol. 5: Nutrition and health.’ (Birkhäuser Verlag: Basel, Switzerland)
Ceoloni C, Kuzmanović L, Forte P, Gennaro A, Bitti A (2014) Targeted exploitation of gene pools of alien Triticeae species for sustainable and multi-faceted improvement of the durum wheat crop. Crop & Pasture Science 65, 96–111.
| Targeted exploitation of gene pools of alien Triticeae species for sustainable and multi-faceted improvement of the durum wheat crop.Crossref | GoogleScholarGoogle Scholar |
Colasuonno P, Gadaleta A, Giancaspro A, Nigro D, Giove S, Incerti O, Mangini G, Signorile A, Simeone R, Blanco A (2014) Development of a high-density SNP-based linkage map and detection of yellow pigment content QTLs in durum wheat. Molecular Breeding 34, 1563–1578.
Cuttriss AJ, Cazzonelli CI, Wurtzel ET, Pogson BJ (2011) Carotenoids. Advances in Botanical Research 58, 1–36.
| Carotenoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFalsb3K&md5=7f9060fe9c326a82bb17d3025983abdcCAS |
Digesù AM, Platani C, Cattivelli L, Mangini G, Blanco A (2009) Genetic variability in yellow pigment components in cultivated and wild tetraploid wheats. Journal of Cereal Science 50, 210–218.
| Genetic variability in yellow pigment components in cultivated and wild tetraploid wheats.Crossref | GoogleScholarGoogle Scholar |
Fernández-García E, Carvajal-Lérida I, Jarén-Galán M, Garrido-Fernández J, Pérez-Gálvez A, Hornero-Méndez D (2012) Carotenoids bioavailability from foods: From plant pigments to efficient biological activities. Food Research International 46, 438–450.
| Carotenoids bioavailability from foods: From plant pigments to efficient biological activities.Crossref | GoogleScholarGoogle Scholar |
Ficco DBM, Mastrangelo AM, Trono D, Borrelli GM, De Vita P, Fares C, Beleggia R, Platani C, Papa R (2014) The colours of durum wheat: a review. Crop & Pasture Science 65, 1–15.
| The colours of durum wheat: a review.Crossref | GoogleScholarGoogle Scholar |
Gallagher CE, Matthews PD, Li F, Wurtzel ET (2004) Gene duplication in the carotenoid biosynthetic pathway preceded evolution of the grasses. Plant Physiology 135, 1776–1783.
| Gene duplication in the carotenoid biosynthetic pathway preceded evolution of the grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqtrs%3D&md5=cd074c3637684ae180f5a6fa84281f02CAS | 15247400PubMed |
Hentschel V, Kranl K, Hollmann J, Lindhauer MG, Bohm V, Bitsch R (2002) Spectrophotometric determination of yellow pigment content and evaluation of carotenoids by high-performance liquid chromatography in durum wheat grain. Journal of Agricultural and Food Chemistry 50, 6663–6668.
| Spectrophotometric determination of yellow pigment content and evaluation of carotenoids by high-performance liquid chromatography in durum wheat grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsFWmurs%3D&md5=916015e883c910c1bea1b2cef7a8e497CAS | 12405758PubMed |
Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Current Opinion in Plant Biology 4, 210–218.
| Carotenoid biosynthesis in flowering plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFOlu7c%3D&md5=38aea8af875c1049b5ff4088065ce9a7CAS | 11312131PubMed |
Howitt CA, Cavanagh CR, Bowerman AF, Cazzonelli C, Rampling L, Mimica JL, Pogson BJ (2009) Alternative splicing, activation of cryptic exons and amino acid substitutions in carotenoid biosynthetic genes are associated with lutein accumulation in wheat endosperm. Functional & Integrative Genomics 9, 363–376.
| Alternative splicing, activation of cryptic exons and amino acid substitutions in carotenoid biosynthetic genes are associated with lutein accumulation in wheat endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXns1Chur4%3D&md5=2833d4a464b47540e99db0368bec9febCAS |
Kaneko S, Oyanagi A (1995) Varietal differences in the rate of esterification of endosperm lutien during the storage of wheat seeds. Bioscience, Biotechnology, and Biochemistry 59, 2312–2313.
| Varietal differences in the rate of esterification of endosperm lutien during the storage of wheat seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitFalsA%3D%3D&md5=479ef4bf7828274b25fabe642247350fCAS |
Kaneko S, Nagamine T, Yamada T (1995) Esterification of endosperm lutein with fatty acids during the storage of wheat seeds. Bioscience, Biotechnology, and Biochemistry 59, 1–4.
| Esterification of endosperm lutein with fatty acids during the storage of wheat seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjslKrsbY%3D&md5=090b603b5fafae9f238b94ab018967aaCAS |
Khlestkina E (2014) Current applications of wheat and wheat–alien precise genetic stocks. Molecular Breeding 34, 273–281.
| Current applications of wheat and wheat–alien precise genetic stocks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFCqt7%2FM&md5=a87f980c2e7d1b65aef9d5ebfd12f726CAS |
Landrum JT, Bone RA (2004) Dietary lutein and zeaxanthin: reducing the risk for macular degeneration. Agro Food Industry Hi-Tech 15, 22–25.
Li FQ, Vallabhaneni R, Yu J, Rocheford T, Wurtzel ET (2008) The maize phytoene synthase gene family: Overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance. Plant Physiology 147, 1334–1346.
| The maize phytoene synthase gene family: Overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslyisb4%3D&md5=c88943fd9e4297cecbd4412f2f848e79CAS |
Li F, Tzfadia O, Wurtzel ET (2009) The phytoene synthase gene family in the grasses: Subfunctionalization provides tissue-specific control of carotenogenesis. Plant Signaling & Behavior 4, 208–211.
| The phytoene synthase gene family in the grasses: Subfunctionalization provides tissue-specific control of carotenogenesis.Crossref | GoogleScholarGoogle Scholar |
Lippold F, Dorp Kv, Abraham M, Hölzl G, Wewer V, Yilmaz JL, Lager I, Montandon C, Besagni C, Kessler F, Stymne S, Dörmann P (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. The Plant Cell 24, 2001–2014.
| Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOktb7O&md5=6e4374b3a1bd5cc57987cb540461d3b8CAS | 22623494PubMed |
Marais GF (1992) The modification of a common wheat–Thinopyrum distichum translocated chromosome with a locus homeoallelic to Lr19. Theoretical and Applied Genetics 85, 73–78.
| The modification of a common wheat–Thinopyrum distichum translocated chromosome with a locus homeoallelic to Lr19.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c7jslSitw%3D%3D&md5=38794a771c8a2c5252c97296af21f4bfCAS | 24197231PubMed |
Mares DJ, Campbell AW (2001) Mapping components of flour colour in Australian wheat. Australian Journal of Agricultural Research 52, 1297–1309.
| Mapping components of flour colour in Australian wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlOmtw%3D%3D&md5=0f3abf20c369fa6a71151544dbb8e601CAS |
Martin A, Sánchez-Monge E (1982) Cytology and morphology of the amphiploid Hordeum chilense × Triticum turgidum conv. durum. Euphytica 31, 261–267.
| Cytology and morphology of the amphiploid Hordeum chilense × Triticum turgidum conv. durum.Crossref | GoogleScholarGoogle Scholar |
Mattera MG, Avila CM, Atienza SG, Cabrera A (2015) Cytological and molecular characterization of wheat–Hordeum chilense chromosome 7Hch introgression lines. Euphytica 203, 165–176.
| Cytological and molecular characterization of wheat–Hordeum chilense chromosome 7Hch introgression lines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFWktLnN&md5=8780f7c5137f802ea20b7067b5115577CAS |
Mellado-Ortega E, Hornero-Méndez D (2012) Isolation and identification of lutein esters, including their regioisomers, in tritordeum (×Tritordeum Ascherson et Graebner) grains: Evidence for a preferential xanthophyll acyltransferase activity. Food Chemistry 135, 1344–1352.
| Isolation and identification of lutein esters, including their regioisomers, in tritordeum (×Tritordeum Ascherson et Graebner) grains: Evidence for a preferential xanthophyll acyltransferase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlSmur%2FM&md5=0dcfe4988f068ebba725d48671cb8462CAS | 22953864PubMed |
Mellado-Ortega E, Hornero-Méndez D (2015) Carotenoid profiling of Hordeum chilense grains: The parental proof for the origin of the high carotenoid content and esterification pattern of tritordeum. Journal of Cereal Science 62, 15–21.
| Carotenoid profiling of Hordeum chilense grains: The parental proof for the origin of the high carotenoid content and esterification pattern of tritordeum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVClu70%3D&md5=c95db1116504032f5c8d15a1bbab29acCAS |
Mellado-Ortega E, Atienza SG, Hornero-Méndez D (2015) Carotenoid evolution during postharvest storage of durum wheat (Triticum turgidum conv. durum) and tritordeum (×Tritordeum Ascherson et Graebner) grains. Journal of Cereal Science 62, 134–142.
| Carotenoid evolution during postharvest storage of durum wheat (Triticum turgidum conv. durum) and tritordeum (×Tritordeum Ascherson et Graebner) grains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjslyms7o%3D&md5=61a2117785901c925f981d51c409699fCAS |
Mínguez-Mosquera MI, Hornero-Méndez D (1993) Separation and quantification of the carotenoid pigments in red peppers (Capsicum annuum L.), paprika and oleoresin by reversed-phase HPLC. Journal of Agricultural and Food Chemistry 41, 1616–1620.
| Separation and quantification of the carotenoid pigments in red peppers (Capsicum annuum L.), paprika and oleoresin by reversed-phase HPLC.Crossref | GoogleScholarGoogle Scholar |
Murray YHG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4326.
| Rapid isolation of high molecular weight plant DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtVSmtL8%3D&md5=f805ca18a94e62c037a6cfba2837f642CAS |
Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. The Plant Cell 15, 1795–1806.
| Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1WlsLc%3D&md5=929930eca9be2aa9ade07e7402a28328CAS | 12897253PubMed |
Panfili G, Fratianni A, Irano M (2004) Improved normal-phase high-performance liquid chromatography procedure for the determination of carotenoids in cereals. Journal of Agricultural and Food Chemistry 52, 6373–6377.
| Improved normal-phase high-performance liquid chromatography procedure for the determination of carotenoids in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslartLY%3D&md5=6a854cdd14eb6726799938e2b52526f4CAS | 15478994PubMed |
Pozniak CJ, Knox RE, Clarke FR, Clarke JM (2007) Identification of QTL and association of a phytoene synthase gene with endosperm colour in durum wheat. Theoretical and Applied Genetics 114, 525–537.
| Identification of QTL and association of a phytoene synthase gene with endosperm colour in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFKrsw%3D%3D&md5=408c724bf8410de3c5549260ed60dda6CAS | 17131106PubMed |
Rodríguez-Suárez C, Atienza SG (2012) Hordeum chilense genome, a useful tool to investigate the endosperm yellow pigment content in the Triticeae. BMC Plant Biology 12, 200
| Hordeum chilense genome, a useful tool to investigate the endosperm yellow pigment content in the Triticeae.Crossref | GoogleScholarGoogle Scholar | 23122232PubMed |
Rodríguez-Suárez C, Giménez MJ, Atienza SG (2010) Progress and perspectives for carotenoid accumulation in selected Triticeae species. Crop & Pasture Science 61, 743–751.
| Progress and perspectives for carotenoid accumulation in selected Triticeae species.Crossref | GoogleScholarGoogle Scholar |
Rodríguez-Suárez C, Atienza SG, Pistón F (2011) Allelic variation, alternative splicing and expression analysis of Psy1 gene in Hordeum chilense Roem. et Schult. PLoS One 6, e19885
| Allelic variation, alternative splicing and expression analysis of Psy1 gene in Hordeum chilense Roem. et Schult.Crossref | GoogleScholarGoogle Scholar | 21603624PubMed |
Rodríguez-Suárez C, Mellado-Ortega E, Hornero-Méndez D, Atienza SG (2014) Increase in transcript accumulation of Psy1 and e-Lcy genes in grain development is associated with differences in seed carotenoid content between durum wheat and tritordeum. Plant Molecular Biology 84, 659–673.
| Increase in transcript accumulation of Psy1 and e-Lcy genes in grain development is associated with differences in seed carotenoid content between durum wheat and tritordeum.Crossref | GoogleScholarGoogle Scholar | 24306494PubMed |
WHO (2009) Global prevalence of vitamin A deficiency in populations at risk 1995–2005. WHO Global database on Vitamin A deficiency.
Wurtzel ET, Cuttriss A, Vallabhaneni R (2012) Maize provitamin A carotenoids, current resources and future metabolic engineering challenges. Frontiers in Plant Science 3, article no. 29
| Maize provitamin A carotenoids, current resources and future metabolic engineering challenges.Crossref | GoogleScholarGoogle Scholar |
Zhang W, Dubcovsky J (2008) Association between allelic variation at the Phytoene synthase 1 gene and yellow pigment content in the wheat grain. Theoretical and Applied Genetics 116, 635–645.
| Association between allelic variation at the Phytoene synthase 1 gene and yellow pigment content in the wheat grain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFCqtbs%3D&md5=2cc4899730cf6ef9f90a361691c303e8CAS | 18193186PubMed |
Zhang WJ, Lukaszewski AJ, Kolmer J, Soria MA, Goyal S, Dubcovsky J (2005) Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum. Theoretical and Applied Genetics 111, 573–582.
| Molecular characterization of durum and common wheat recombinant lines carrying leaf rust resistance (Lr19) and yellow pigment (Y) genes from Lophopyrum ponticum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovVKkt7k%3D&md5=211f4ea72d0f2cf5bbc3dd9797aa971dCAS |
Zhu C, Sanahuja G, Yuan D, Farré G, Arjó G, Berman J, Zorrilla-López U, Banakar R, Bai C, Pérez-Massot E, Bassie L, Capell T, Christou P (2013) Biofortification of plants with altered antioxidant content and composition: genetic engineering strategies. Plant Biotechnology Journal 11, 129–141.
| Biofortification of plants with altered antioxidant content and composition: genetic engineering strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvVOltL0%3D&md5=4b2a3fe9bc57aadb1c7898607cb6f362CAS | 22970850PubMed |