ZEAXANTHIN EPOXIDASE activity potentiates carotenoid degradation in maturing seed

Plant Physiology

Volumn 171, Issue 3, 2016, Pages 1837-1851

  Gonzalez Jorge, Sabrina ^a,b   Mehrshahi, Payam ^a,b   Magallanes Lundback, Maria ^a   Lipka, Alexander E ^c   Angelovici, Ruthie ^a,d   Gore, Michael A ^e   DellaPenna, Dean ^a  

^a Michigan State University   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF MISSOURI   (United States)

^e Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CAROTENOID; CCD4 PROTEIN, ARABIDOPSIS; DIOXYGENASE; OXIDOREDUCTASE; XANTHOPHYLL; ZEAXANTHIN EPOXIDASE;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GROWTH, DEVELOPMENT AND AGING; HAPLOTYPE; METABOLISM; MUTATION; PLANT SEED; QUANTITATIVE TRAIT LOCUS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CAROTENOIDS; DIOXYGENASES; GENE EXPRESSION REGULATION, PLANT; GENOME-WIDE ASSOCIATION STUDY; HAPLOTYPES; MUTATION; OXIDOREDUCTASES; QUANTITATIVE TRAIT LOCI; SEEDS; XANTHOPHYLLS;

EID: 84977579186     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00604     Document Type: Article

References (112)

1. Abbo S, Bonfil DJ, Kerem Z, Berkovitch Z, Reifen R (2010) Towards enhancing lutein concentration in chickpea, cultivar and management effects. Plant Breed 129: 407-411
2. Abbo S, Molina C, Jungmann R, Grusak MA, Berkovitch Z, Reifen R, Kahl G, Winter P, Reifen R (2005) Quantitative trait loci governing carotenoid concentration and weight in seeds of chickpea (Cicer arietinum L.). Theor Appl Genet 111: 185-195
3. Alboresi A, Dall'Osto L, Aprile A, Carillo P, Roncaglia E, Cattivelli L, Bassi R (2011) Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein. BMC Plant Biol 11: 62-83
4. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348-1351
5. Angelovici R, Lipka AE, Deason N, Gonzalez-Jorge S, Lin H, Cepela J, Buell R, Gore MA, DellaPenna D (2013) Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 25: 4827-4843
6. Arango J, Wüst F, Beyer P, Welsch R (2010) Characterization of phytoene synthases from cassava and their involvement in abiotic stress-mediated responses. Planta 232: 1251-1262
7. Audran C, Borel C, Frey A, Sotta B,Meyer C, Simonneau T,Marion-Poll A (1998) Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol 118: 1021-1028
8. Audran C, Liotenberg S, Gonneau M, North H, Frey A, Tap-Waksman K, Vartanian N, Marion-Poll A (2001) Localisation and expression of zeaxanthin epoxidase mRNA in Arabidopsis in response to drought stress and during seed development. Funct Plant Biol 28: 1161-1173
9. Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, Magallanes-Lundback M, DellaPenna D, McCarty DR, Klee HJ (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J 45: 982-993
10. Avendaño-Vázquez AO, Cordoba E, Llamas E, San Román C, Nisar N, De la Torre S, Ramos-Vega M, Gutiérrez-Nava MD, Cazzonelli CI, Pogson BJ, et al (2014) An uncharacterized apocarotenoid-derived signal generated in ζ-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis. Plant Cell 26: 2524-2537
11. Bailey S, Grossman A (2008) Photoprotection in cyanobacteria: regulation of light harvesting. Photochem Photobiol 84: 1410-1420
12. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265
13. Baxter I, Brazelton JN, Yu D, Huang YS, Lahner B, Yakubova E, Li Y, Bergelson J, Borevitz JO, Nordborg M, Vitek O, Salt DE (2010) A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet 6: e1001193
14. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57: 289-300
15. Bensmihen S, Rippa S, Lambert G, Jublot D, Pautot V, Granier F, Giraudat J, Parcy F (2002) The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14: 1391-1403
16. 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. J Cereal Sci 54: 255-264
17. Botella-Pavía P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40: 188-199
18. Box GEP, Cox DR (1964) An analysis of transformations. J R Stat Soc Ser B Stat Methodol 26: 211-252
19. Bradbury LM, Shumskaya M, Tzfadia O, Wu SB, Kennelly EJ, Wurtzel ET (2012) Lycopene cyclase paralog CruP protects against reactive oxygen species in oxygenic photosynthetic organisms. Proc Natl Acad Sci USA 109: E1888-E1897
20. Brocard IM, Lynch TJ, Finkelstein RR (2002) Regulation and role of the Arabidopsis abscisic acid-insensitive 5 gene in abscisic acid, sugar, and stress response. Plant Physiol 129: 1533-1543
21. Busch M, Seuter A, Hain R (2002) Functional analysis of the early steps of carotenoid biosynthesis in tobacco. Plant Physiol 128: 439-453
22. Campbell R, Ducreux LJ, Morris WL, Morris JA, Suttle JC, Ramsay G, Bryan GJ, Hedley PE, Taylor MA (2010) The metabolic and developmental roles of carotenoid cleavage dioxygenase4 from potato. Plant Physiol 154: 656-664
23. Carol P, Kuntz M (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci 6: 31-36
24. Carretero-Paulet L, Cairó A, Botella-Pavía P, Besumbes O, Campos N, Boronat A, Rodríguez-Concepción M (2006) Enhanced flux through the methylerythritol 4-phosphate pathway in Arabidopsis plants overexpressing deoxyxylulose 5-phosphate reductoisomerase. Plant Mol Biol 62: 683-695
25. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15: 266-274
26. Chandler K, Lipka AE, Owens BF, Li H, Buckler ES, Rocheford T, Gore MA (2013) Genetic analysis of visually scored orange kernel color in maize. Crop Sci 53: 189-200
27. Chen J, Chen Z (2008) Extended Bayesian information criteria for model selection with large model spaces. Biometrika 95: 759-771
28. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, et al (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14: 2723-2743
29. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971
30. Cook JP, McMullen MD, Holland JB, Tian F, Bradbury P, Ross-Ibarra J, Buckler ES, Flint-Garcia SA (2012) Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol 158: 824-834
31. Couso I, Cordero BF, Vargas MA, Rodríguez H (2012) Efficient heterologous transformation of Chlamydomonas reinhardtii npq2 mutant with the zeaxanthin epoxidase gene isolated and characterized from Chlorella zofingiensis. Mar Drugs 10: 1955-1976
32. Cuttriss AJ, Cazzonelli CI, Wurtzel ET, Pogson BJ (2011) Carotenoids. Adv Bot Res 58: 1-36
33. Dall'Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R (2007) The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 19: 1048-1064
34. Davison PA, Hunter CN, Horton P (2002) Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418: 203-206
35. DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57: 711-738
36. Dong H, Deng Y, Mu J, Lu Q, Wang Y, Xu Y, Chu C, Chong K, Lu C, Zuo J (2007) The Arabidopsis Spontaneous Cell Death1 gene, encoding a zetacarotene desaturase essential for carotenoid biosynthesis, is involved in chloroplast development, photoprotection and retrograde signalling. Cell Res 17: 458-470
37. Estévez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-Deoxy-Dxylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276: 22901-22909
38. Fang J, Chai C, Qian Q, Li C, Tang J, Sun L, Huang Z, Guo X, Sun C, Liu M, et al (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J 54: 177-189
39. Fernandez MGS, Hamblin MT, Li L, Rooney WL, Tuinstra MR, Kresovich S (2008) Quantitative trait loci analysis of endosperm color and carotenoid content in sorghum grain. Crop Sci 48: 1732-1743
40. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609
41. Fiore A, Dall'Osto L, Fraser PD, Bassi R, Giuliano G (2006) Elucidation of the beta-carotene hydroxylation pathway in Arabidopsis thaliana. FEBS Lett 580: 4718-4722
42. Fraser PD, Kiano JW, Truesdale MR, Schuch W, Bramley PM (1999) Phytoene synthase-2 enzyme activity in tomato does not contribute to carotenoid synthesis in ripening fruit. Plant Mol Biol 40: 687-698
43. Fray RG, Wallace A, Fraser PD, Valero D, Hedden P, Bramley PM, Grierson D (1995) Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. Plant J 8: 693-701
44. Frey A, Boutin JP, Sotta B, Mercier R, Marion-Poll A (2006) Regulation of carotenoid and ABA accumulation during the development and germination of Nicotiana plumbaginifolia seeds. Planta 224: 622-632
45. Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70: 501-512
46. Frey A, Godin B, Bonnet M, Sotta B, Marion-Poll A (2004) Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta 218: 958-964
47. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53: 717-730
48. Gilliland LU, Magallanes-Lundback M, Hemming C, Supplee A, Koornneef M, Bentsink L, DellaPenna D (2006) Genetic basis for natural variation in seed vitamin E levels in Arabidopsis thaliana. Proc Natl Acad Sci USA 103: 18834-18841
49. Giuliano G, Bartley GE, Scolnik PA (1993) Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5: 379-387
50. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, et al (2008) Strigolactone inhibition of shoot branching. Nature 455: 189-194
51. Gonzalez-Jorge S, Ha SH, Magallanes-Lundback M, Gilliland LU, Zhou A, Lipka AE, Nguyen YN, Angelovici R, Lin H, Cepela J, et al (2013) Carotenoid cleavage dioxygenase4 is a negative regulator of β-carotene content in Arabidopsis seeds. Plant Cell 25: 4812-4826
52. Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, et al (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-333
53. Hobbs RP, Bernstein PS (2014) Nutrient supplementation for age-related macular degeneration, cataract, and dry eye. J Ophthalmic Vis Res 9: 487-493
54. Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S, Auton A, Muliyati NW, Platt A, Sperone FG, Vilhjálmsson BJ, et al (2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat Genet 44: 212-216
55. Howitt CA, Pogson BJ (2006) Carotenoid accumulation and function in seeds and non-green tissues. Plant Cell Environ 29: 435-445
56. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817: 182-193
57. Jourdan M, Gagné S, Dubois-Laurent C, Maghraoui M, Huet S, Suel A, Hamama L, Briard M, Peltier D, Geoffriau E (2015) Carotenoid content and root color of cultivated carrot: a candidate-gene association study using an original broad unstructured population. PLoS ONE 10: e0116674
58. Kandianis CB, Stevens R, Liu W, Palacios N, Montgomery K, Pixley K, White WS, Rocheford T (2013) Genetic architecture controlling variation in grain carotenoid composition and concentrations in two maize populations. Theor Appl Genet 126: 2879-2895
59. Kim J, Smith JJ, Tian L, DellaPenna D (2009) The evolution and function of carotenoid hydroxylases in Arabidopsis. Plant Cell Physiol 50: 463-479
60. Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5: 33-36
61. Koornneef M, Jorna ML, Brinkhorst-van der Swan DL, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 61: 385-393
62. Kramer CY (1956) Extension of multiple range tests to group means with unequal numbers of replications. Biometrics 12: 307-310
63. Krinsky NI, Johnson EJ (2005) Carotenoid actions and their relation to health and disease. Mol Aspects Med 26: 459-516
64. Kutner MH, Nachtsheim CJ, Neter J (2004) Applied Linear Regression Models. McGraw-Hill Education, Boston
65. Landrum JT, Bone RA (2004) Dietary lutein & zeaxanthin: reducing the risk for macular degeneration. Agro Food Ind Hi-Tech 15: 22-25
66. Lätari K, Wüst F, Hübner M, Schaub P, Beisel KG, Matsubara S, Beyer P, Welsch R (2015) Tissue-specific apocarotenoid glycosylation contributes to carotenoid homeostasis in Arabidopsis leaves. Plant Physiol 168: 1550-1562
67. Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45: 309-319
68. Lindgren LO, Stålberg KG, Höglund AS (2003) Seed-specific overexpression of an endogenous Arabidopsis phytoene synthase gene results in delayed germination and increased levels of carotenoids, chlorophyll, and abscisic acid. Plant Physiol 132: 779-785
69. Lipka AE, Gore MA, Magallanes-Lundback M, Mesberg A, Lin H, Tiede T, Chen C, Buell CR, Buckler ES, Rocheford T, et al (2013) Genomewide association study and pathway-level analysis of tocochromanol levels in maize grain. G3 (Bethesda) 3: 1287-1299
70. Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: Genome Association and Prediction Integrated Tool. Bioinformatics 28: 2397-2399
71. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic-structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82: 1420-1425
72. Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15: 2331-2342
73. McCarty DR (1995) Genetic control and integration of maturation and germination pathways in seed development. Annu Rev Plant Physiol Plant Mol Biol 46: 71-93
74. Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41: 697-709
75. Nambara E, Marion-Poll A (2003) ABA action and interactions in seeds. Trends Plant Sci 8: 213-217
76. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165-185
77. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8: 68-82
78. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359
79. Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10: 1121-1134
80. Owens BF, Lipka AE, Magallanes-Lundback M, Tiede T, Diepenbrock CH, Kandianis CB, Kim E, Cepela J, Mateos-Hernandez M, Buell CR, et al (2014) A foundation for provitamin A biofortification of maize: genome-wide association and genomic prediction models of carotenoid levels. Genetics 198: 1699-1716
81. Paran I, van der Knaap E (2007) Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J Exp Bot 58: 3841-3852
82. Park HY, Seok HY, Park BK, Kim SH, Goh CH, Lee BH, Lee CH, Moon YH (2008) Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochem Biophys Res Commun 375: 80-85
83. Platt A, Horton M, Huang YS, Li Y, Anastasio AE, Mulyati NW, Agren J, Bossdorf O, Byers D, Donohue K, et al (2010) The scale of population structure in Arabidopsis thaliana. PLoS Genet 6: e1000843
84. 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
85. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904-909
86. Qin G,Gu H, Ma L, Peng Y, Deng XW, Chen Z,Qu LJ (2007) Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Res 17: 471-482
87. Rock CD, Zeevaart JA (1991) The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc Natl Acad Sci USA 88: 7496-7499
88. Ruiz-Sola MA, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. The Arabidopsis Book 10: e0158, doi: 10.1199/tab.0158
89. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6: 461-464
90. Schwarz N, Armbruster U, Iven T, Brückle L, Melzer M, Feussner I, Jahns P (2015) Tissue-specific accumulation and regulation of zeaxanthin epoxidase in Arabidopsis reflect the multiple functions of the enzyme in plastids. Plant Cell Physiol 56: 346-357
91. Segura V, Vilhjálmsson BJ, Platt A, Korte A, Seren Ü, Long Q, Nordborg M (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44: 825-830
92. Shewmaker CK, Sheehy JA, Daley M, Colburn S, Ke DY (1999) Seedspecific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J 20: 401-412X
93. Simon M, Loudet O, Durand S, Bérard A, Brunel D, Sennesal FX, Durand-Tardif M, Pelletier G, Camilleri C (2008) Quantitative trait loci mapping in five new large recombinant inbred line populations of Arabidopsis thaliana genotyped with consensus single-nucleotide polymorphism markers. Genetics 178: 2253-2264
94. Smolikova GN, Laman NA, Boriskevich OV (2011) Role of chlorophylls and carotenoids in seed tolerance to abiotic stressors. Russ J Plant Physiol 58: 965-973
95. Sonah H, O'Donoughue L, Cober E, Rajcan I, Belzile F (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol J 13: 211-221
96. Sun G, Zhu C, Kramer MH, Yang SS, Song W, Piepho HP, Yu J (2010) Variation explained in mixed-model association mapping. Heredity (Edinb) 105: 333-340
97. Suwarno WB, Pixley KV, Palacios-Rojas N, Kaeppler SM, Babu R (2015) Genome-wide association analysis reveals new targets for carotenoid biofortification in maize. Theor Appl Genet 128: 851-864
98. Tian L, Magallanes-Lundback M, Musetti V, DellaPenna D (2003) Functional analysis of beta-and epsilon-ring carotenoid hydroxylases in Arabidopsis. Plant Cell 15: 1320-1332
99. Toledo-Ortiz G, Huq E, Rodríguez-Concepción M (2010) Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc Natl Acad Sci USA 107: 11626-11631
100. Tukey JW (1953) The problem of multiple comparisons. In The Collected Works of John W. Tukey, Vol 8, 1994. Chapman & Hall, New York
101. Utz HF,Melchinger AE (1996) PLABQTL: a program for composite interval mapping of QTL. Journal of Quantitative Trait Loci 2: 1-5
102. Vallabhaneni R, Wurtzel ET (2009) Timing and biosynthetic potential for carotenoid accumulation in genetically diverse germplasm of maize. Plant Physiol 150: 562-572
103. Weigel D, Mott R (2009) The 1001 Genomes Project for Arabidopsis thaliana. Genome Biol 10: 107-112
104. Welsch R, Arango J, Bär C, Salazar B, Al-Babili S, Beltrán J, Chavarriaga P, Ceballos H, Tohme J, Beyer P (2010) Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. Plant Cell 22: 3348-3356
105. Wen W, Li D, Li X, Gao Y, Li W, Li H, Liu J, Liu H, Chen W, Luo J, et al (2014) Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat Commun 5: 3438-3448
106. Wong JC, Lambert RJ, Wurtzel ET, Rocheford TR (2004) QTL and candidate genes phytoene synthase and zeta-carotene desaturase associated with the accumulation of carotenoids in maize. Theor Appl Genet 108: 349-359
107. Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, et al (2010) Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat Genet 42: 322-327
108. Young AJ (1993) Factors that affect the carotenoid composition of higher plants and algae. In Carotenoids in Photosynthesis, AJ Young and G Britton, eds. Springer, Dordrecht, The Netherlands, pp 160-205
109. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38: 203-208
110. Zhou X, McQuinn R, Fei Z, Wolters AM, van Eck J, Brown C, Giovannoni JJ, Li L (2011) Regulatory control of high levels of carotenoid accumulation in potato tubers. Plant Cell Environ 34: 1020-1030
111. Zhou Y, Han Y, Li Z, Fu Y, Fu Z, Xu S, Li J, Yan J, Yang X (2012) ZmcrtRB3 encodes a carotenoid hydroxylase that affects the accumulation of α-carotene in maize kernel. J Integr Plant Biol 54: 260-269
112. Zuber H, Davidian JC, Wirtz M, Hell R, Belghazi M, Thompson R, Gallardo K (2010) Sultr4;1 mutant seeds of Arabidopsis have an enhanced sulphate content and modified proteome suggesting metabolic adaptations to altered sulphate compartmentalization. BMC Plant Biol 10: 78-91