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

Volumn 84, Issue 6, 2014, Pages 659-673

  Rodríguez Suárez, Cristina ^a   Mellado Ortega, Elena ^b   Hornero Méndez, Dámaso ^b   Atienza, Sergio G ^a  

^a INSTITUTO DE AGRICULTURA SOSTENIBLE   (Spain)

^b INSTITUTO DE LA GRASA   (Spain)

Author keywords

Carotenoids; Durum wheat; e Lcy; Esterification; Psy1; Tritordeum

Indexed keywords

HORDEUM; HORDEUM CHILENSE; HORDEUM VULGARE SUBSP. SPONTANEUM; TRITICUM TURGIDUM; TRITICUM TURGIDUM SUBSP. DURUM; X TRITORDEUM;

CAROTENOID; PLANT RNA; PRIMER DNA; TERPENE; VEGETABLE PROTEIN;

ALLELE; ARTICLE; BIOSYNTHESIS; CEREAL; CHIMERA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HORDEUM; HUMAN; METABOLISM; PLANT SEED; POACEAE; SPECIES DIFFERENCE; WHEAT;

ALLELES; BIOSYNTHETIC PATHWAYS; CAROTENOIDS; CEREALS; CHIMERA; DNA PRIMERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; HORDEUM; HUMANS; PLANT PROTEINS; POACEAE; RNA, PLANT; SEEDS; SPECIES SPECIFICITY; TERPENES; TRITICUM;

EID: 84896055680     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-013-0160-y     Document Type: Article

References (74)

1. Adom KK, Sorrells ME, Liu RH (2005) Phytochemicals and antioxidant activity of milled fractions of different wheat varieties. J Agr Food Chem 53: 2297-2306.
2. Alvarez JB, Martin LM, Martin A (1998) Chromosomal localization of genes for carotenoid pigments using addition lines of Hordeum chilense in wheat. Plant Breed 117: 287-289.
3. Alvarez JB, Martin LM, Martin A (1999) Genetic variation for carotenoid pigment content in the amphiploid Hordeum chilense × Triticum turgidum conv. durum. Plant Breed 118: 187-189.
4. 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. Aust J Agr Res 58: 767-773.
5. Atienza SG, Ballesteros J, Martin A, Hornero-Méndez D (2007b) Genetic variability of carotenoid concentration and degree of esterification among tritordeum (xTritordeum Ascherson et Graebner) and durum wheat accessions. J Agr Food Chem 55: 4244-4251.
6. Atienza SG, Martín A, Pecchioni N, Platani C, Cattivelli L (2008) The nuclear-cytoplasmic interaction controls carotenoid content in wheat. Euphytica 159: 325-331.
7. Bai L, Kim E-H, DellaPenna D, Brutnell TP (2009) Novel lycopene epsilon cyclase activities in maize revealed through perturbation of carotenoid biosynthesis. Plant J 59: 588-599.
8. Ballesteros J, Ramirez MC, Martinez C, Atienza SG, Martin A (2005) Registration of HT621, a high carotenoid content tritordeum germplasm line. Crop Sci 45: 2662-2663.
9. Barua AB, Olson JA (2001) Xanthophyll epoxides, unlike β-carotene monoepoxides, are not detectible absorbed by humans. Human Nutrition and Metabolism Research. J Nutr 131: 3212-3215.
10. Beyer P, Al-Babili S, Ye X, Lucca P, Schaub P, Welsch R, Potrykus I (2002) Golden Rice: Introducing the β-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J Nutr 132: 506-510.
11. Britton G (1991) Carotenoids. In: Dey PM, Harborne JB (eds) Methods in Plant Biochemistry. Academic Press, London, pp 473-518.
12. Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1B., spectroscopyBirkhäuser, Basel pp, pp 13-62.
13. Britton G (2008) Functions of intact carotenoids. In: Britton G, Liaaen-Jensen S, Pfander H (eds) carotenoids, vol 4., Natural functionsBirkhäuser, Basel pp, pp 189-212.
14. Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoid Handbook. Birkhäuser Verlag, Basel.
15. Carpentier S, Knaus M, Suh M (2009) Associations between lutein, zeaxanthin, and age-related macular degeneration: an overview. Crit Rev Food Sci 49: 313-326.
16. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15: 266-274.
17. Chung SM, Staub JE (2003) The development and evaluation of consensus chloroplast primer pairs that possess highly variable sequence regions in a diverse array of plant taxa. Theor Appl Genet 107: 757-767.
18. Crawford A, Francki M (2013) Lycopene-ε-cyclase (e-LCY3A) is functionally associated with quantitative trait loci for flour b* colour on chromosome 3A in wheat (Triticum aestivum L.). Mol Breed 31: 737-741.
19. Cuttriss AJ, Cazzonelli CI, Wurtzel ET, Pogson BJ (2011) Carotenoids. Adv Bot Res 58: 1-36.
20. Digesù AM, Platani C, Cattivelli L, Mangini G, Blanco A (2009) Genetic variability in yellow pigment components in cultivated and wild tetraploid wheats. J Cereal Sci 50: 210-218.
21. Dong CH, Ma ZY, Xia XC, Zhang LP, He ZH (2012) Allelic variation at the TaZds-A1 locus on wheat chromosome 2A and development of a functional marker in common wheat. J Integr Agric 11: 1067-1074.
22. Fishwick MJ, Wright AJ (1980) Isolation and characterization of amyloplast envelope membranes from Solanum tuberosum. Phytochemistry 19: 55-59.
23. Gallagher CE, Matthews PD, Li F, Wurtzel ET (2004) Gene duplication in the carotenoid biosynthetic pathway preceded evolution of the grasses. Plant Physiol 135: 1776-1783.
24. Giménez MJ, Pistón F, Atienza SG (2011) Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta 233: 163-173.
25. Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26: 139-145.
26. Graham RD, Humphries JM, Kitchen JL (2000) Nutritionally enhanced cereals: a sustainable foundation for a balanced diet. Asia Pac J Clinic Nut 9: S91-S96.
27. Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, Yan J, Buckler ES (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-333.
28. He XY, Zhang YL, He ZH, Wu YP, Xiao YG, Ma CX, Xia XC (2008) Characterization of phytoene synthase 1 gene (Psy1) located on common wheat chromosome 7A and development of a functional marker. Theor Appl Genet 116: 213-221.
29. He XY, He ZH, Ma W, Appels R, Xia XC (2009a) Allelic variants of phytoene synthase 1 (Psy1) genes in Chinese and CIMMYT wheat cultivars and development of functional markers for flour colour. Mol Breed 23: 553-563.
30. He XY, Wang JW, Ammar K, Pena RJ, Xia XC, He ZH (2009b) Allelic variants at the Psy-A1 and Psy-B1 loci in durum wheat and their associations with grain yellowness. Crop Sci 49: 2058-2064.
31. 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. J Agr Food Chem 50: 6663-6668.
32. Hidalgo A, Brandolini A, Pompei C, Piscozzi R (2006) Carotenoids and tocols of einkorn wheat (Triticum monococcum ssp. monococcum L.). J Cereal Sci 44: 182-193.
33. Hornero-Méndez D, Mínguez-Mosquera MI (2000) Xanthophyll esterification accompanying carotenoid overaccumulation in chromoplast of Capsicum annuum ripening fruits is a constitutive process and useful for ripeness index. J Agr Food Chem 48: 1617-1622.
34. Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant, Cell Environ 29: 435-445.
35. 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. Funct Integr Genomics 9: 363-376.
36. 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 Physiol 147: 1334-1346.
37. Li F, Tsfadia O, Wurtzel ET (2009) The phytoene synthase gene family in the Grasses: subfunctionalization provides tissue-specific control of carotenogenesis. Plant Signal Behav 4: 208-211.
38. Martin A, Sánchez-Monge E (1982) Cytology and morphology of the amphiploid Hordeum chilense × Triticum turgidum conv Durum. Euphytica 31: 261-267.
39. Martin AC, Atienza SG, Barro F (2008a) Use of ccSSR markers for the determination of the purity of alloplasmic wheat in different Hordeum cytoplasms. Plant Breed 127: 470-475.
40. Martin AC, Atienza SG, Ramirez MC, Barro F, Martin A (2008b) Male fertility restoration of wheat in Hordeum chilense cytoplasm is associated with 6H(ch)S chromosome addition. Aust J Agr Res 59: 206-213.
41. Mellado-Ortega E, Hornero-Méndez D (2012) Isolation and identification of lutein esters, including their regioisomers, in tritordeum (xTritordeum Ascherson et Graebner) grains: evidence for a preferential xanthophyll acyltransferase activity. Food Chem 135: 1344-1352.
42. 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. J Agr Food Chem 41: 1616-1620.
43. Mínguez-Mosquera MI, Gandul-Rojas B, Gallardo-Guerrero L, Roca M, Jarén-Galán M (2008a) Chlorophylls. In: Hurst WJ (ed) Methods of analysis for functional foods and nutraceuticals. CRC Press, New York, pp 337-400.
44. Mínguez-Mosquera MI, Hornero-Méndez D, Pérez-Gálvez A (2008b) Carotenoids and provitamin A in functional foods. In: Hurst WJ (ed) Methods of analysis for functional foods and nutraceuticals. CRC Press, New York, pp 277-335.
45. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321-4326.
46. Naqvi S, Zhu CF, Farre G, Ramessar K, Bassie L, Breitenbach J, Conesa DP, Ros G, Sandmann G, Capell T, Christou P (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106: 7762-7767.
47. Ndolo VU, Beta T (2013) Distribution of carotenoids in endosperm, germ, and aleurone fractions of cereal grain kernels. Food Chem 139: 663-671.
48. Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23: 482-487.
49. Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15: 1795-1806.
50. 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. Theor Appl Genet 114: 525-537.
51. Qin X, Zhang W, Dubcovsky J, Tian L (2012) Cloning and comparative analysis of carotenoid β-hydroxylase genes provides new insights into carotenoid metabolism in tetraploid (Triticum turgidum ssp. durum) and hexaploid (Triticum aestivum) wheat grains. Plant Mol Biol 80: 631-646.
52. Ramachandran A, Pozniak CJ, Clarke JM, Singh AK (2010) Carotenoid accumulation during grain development in durum wheat. J Cereal Sci 52: 30-38.
53. Randolph LF, Hand DB (1940) Relation between carotenoid content and number of genes per cell in diploid and tetraploid corn. J Agr Res 60: 0051-0064.
54. Reimer S, Pozniak CJ, Clarke FR, Clarke JM, Somers DJ, Knox RE, Singh AK (2008) Association mapping of yellow pigment in an elite collection of durum wheat cultivars and breeding lines. Genome 51: 1016-1025.
55. Rodríguez-Suárez C, Atienza SG (2012) Hordeum chilense genome, a useful tool to investigate the endosperm yellow pigment content in the Triticeae. BMC Plant Biol 12: 200.
56. Rodríguez-Suárez C, Giménez MJ, Atienza SG (2010) Progress and perspectives for carotenoid accumulation in selected Triticeae species. Crop Pasture Sci 61: 743-751.
57. Rodríguez-Suárez C, Atienza SG, Pistón F (2011a) Allelic variation, alternative splicing and expression analysis of Psy1 gene in Hordeum chilense Roem. et Schult. PLoS ONE 6: e19885.
58. Rodríguez-Suárez C, Giménez MJ, Ramírez MC, Martín AC, Gutierrez N, Ávila CM, Martín A, Atienza SG (2011b) Exploitation of nuclear and cytoplasm variability in Hordeum chilense for wheat breeding. Plant Genet Res Charact Util 9: 313-316. doi: 10. 1017/S1479262111000402.
59. Rodríguez-Suárez C, Giménez MJ, Gutiérrez N, Ávila CM, Machado A, Huttner E, Ramírez MC, Martín A, Castillo A, Kilian A, Atienza SG (2012) Development of wild barley (Hordeum chilense)-derived DArT markers and their use into genetic and physical mapping. Theor Appl Genet 124: 713-722.
60. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
61. Shumskaya M, Wurtzel ET (2013) The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci 208: 58-63.
62. Shumskaya M, Bradbury LMT, Monaco RR, Wurtzel ET (2012) Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. Plant Cell 24: 3725-3741.
63. Singh A, Reimer S, Pozniak CJ, Clarke FR, Clarke JM, Knox RE, Singh AK (2009) Allelic variation at Psy1-A1 and association with yellow pigment in durum wheat grain. Theor Appl Genet 118: 1539-1548.
64. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: W71-W74.
65. Vallabhaneni R, Wurtzel ET (2009) Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize. Plant Physiol 150: 562-572.
66. Vallabhaneni R, Gallagher CE, Licciardello N, Cuttriss AJ, Quinlan RF, Wurtzel ET (2009) Metabolite sorting of a germplasm collection reveals the hydroxylase3 locus as a new target for maize provitamin A biofortification. Plant Physiol 151: 1635-1645.
67. Vandesompele J, De Preter K, Pattyn F, Poppe B, van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034. 0031-research0034. 0011.
68. Wang J, He X, He Z, Wang H, Xia X (2009) Cloning and phylogenetic analysis of phytoene synthase 1 (Psy1) genes in common wheat and related species. Hereditas 146: 208-256.
69. WHO (2009) Global prevalence of vitamin A deficiency in populations at risk 1995-2005. In: WHO (ed) Global database on vitamin A deficiency. World Health Organization, Geneva, pp 1-55.
70. Wurtzel ET (2004) Genomics, genetics, and biochemistry of maize carotneoid biosynthesis. In: Romeo J (ed) Recent advances in phytochemistry, vol 38. Elsevier, Amsterdam, pp 85-110.
71. Wurtzel ET, Cuttriss A, Vallabhaneni R (2012) Maize provitamin A carotenoids, current resources and future metabolic engineering challenges. Front Plant Sci 3: 29.
72. Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-Carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287: 303-305.
73. Zhang W, Dubcovsky J (2008) Association between allelic variation at the Phytoene synthase 1 gene and yellow pigment content in the wheat grain. Theor Appl Genet 116: 635-645.
74. Zhang C, Dong CH, He X, Zhang L, Xia XC, He ZH (2011) Allelic variants at the TaZds-D1 locus on wheat chromosome 2DL and their association with yellow pigment content. Crop Sci 51: 1580-1590.