Differential accumulation of phenolic compounds and expression of related genes in black- and yellow-seeded Brassica napus

Journal of Experimental Botany

Volumn 64, Issue 10, 2013, Pages 2885-2898

  Qu, Cunmin ^a   Fu, Fuyou ^b   Lu, Kun ^a   Zhang, Kai ^a   Wang, Rui ^a   Xu, Xinfu ^a   Wang, Min ^a   Lu, Junxing ^a   Wan, Huafang ^a   Zhanglin, Tang ^a   Li, Jiana ^a  

^a SOUTHWEST UNIVERSITY   (China)

^b SASKATOON RESEARCH CENTRE   (Canada)

Author keywords

Brassica napus; expression profile; flavonoid pathway; phenolic compounds; regulatory mechanism; seed coat colour.

Indexed keywords

FLAVONOID; PHENOL DERIVATIVE; VEGETABLE PROTEIN;

ARTICLE; BIOSYNTHESIS; CLASSIFICATION; EXPRESSION PROFILE; FLAVONOID PATHWAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOLIC COMPOUNDS; PLANT SEED; RAPESEED; REGULATORY MECHANISM; SEED COAT COLOUR.;

BRASSICA NAPUS; EXPRESSION PROFILE; FLAVONOID PATHWAY; PHENOLIC COMPOUNDS; REGULATORY MECHANISM; SEED COAT COLOUR.;

BRASSICA NAPUS; FLAVONOIDS; GENE EXPRESSION REGULATION, PLANT; PHENOLS; PLANT PROTEINS; SEEDS;

BRASSICA NAPUS;

EID: 84879973766     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert148     Document Type: Article

References (75)

1. Abrahams S, Lee E, Walker AR, Tanner GJ, Larkin PJ, Ashton AR. 2003. The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. The Plant Journal 35, 624-636
2. Akhov LAL, Ashe PAP, Tan YTY, Datla RDR, Selvaraj GSG. 2009. Proanthocyanidin biosynthesis in the seed coat of yellow-seeded, canola quality Brassica napus YN01-429 is constrained at the committed step catalyzed by dihydroflavonol 4-reductase. Botany 87, 616-625
3. Albert S, Delseny M, Devic M. 1997. BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat. The Plant Journal 11, 289-299
4. Arsovski AA, Haughn GW, Western TL. 2010. Seed coat mucilage cells of Arabidopsis thaliana as a model for plant cell wall research. Plant Signaling and Behavior 5, 796
5. Auger B, Baron C, Lucas MO, Vautrin S, Bergès H, Chalhoub B, Fautrel A, Renard M, Nesi N. 2009. Brassica orthologs from BANYULS belong to a small multigene family, which is involved in procyanidin accumulation in the seed. Planta 230, 1167-1183
6. Auger, B, Marnet N, Gautier V, Maia-Grondard A, Leprince F, Renard M, Guyot S, Nesi N, Routaboul JM. 2010. A detailed survey of seed coat flavonoids in developing seeds of Brassica napus L. Journal of Agricultural and Food Chemistry 58, 6246-6256
7. 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. The Plant Journal 39, 366-380
8. Bharti AK, Khurana JP. 2003. Molecular characterization of transparent testa (tt) mutants of Arabidopsis thaliana (ecotype Estland) impaired in flavonoid biosynthetic pathway. Plant Science 165, 1321-1332
9. Blount JW, Korth KL, Masoud SA, Rasmussen S, Lamb C, Dixon RA. 2000. Altering expression of cinnamic acid 4-hydroxylase in transgenic plants provides evidence for a feedback loop at the entry point into the phenylpropanoid pathway. Plant Physiology 122, 107-116
10. Burbulis IE, Winkel-Shirley B. 1999. Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proceedings of the National Academy of Sciences, USA 96, 12929-12934
11. Chai YR, Lei B, Huang HL, Li JN, Yin JM, Tang ZL, Wang R, Chen L. 2009. TRANSPARENT TESTA12 genes from Brassica napus and parental species: Cloning, evolution, and differential involvement in yellow seed trait. Molecular Genetics and Genomics 281, 109-123
12. Chen AH, Chai YR, Li JN, Chen L. 2007. Molecular cloning of two genes encoding cinnamate 4-hydroxylase (C4H) from oilseed rape (Brassica napus). Journal of Biochemistry and Molecular Biology 40, 247-260
13. Chiu LW, Zhou X, Burke S, Wu X, Prior RL, Li L. 2010. The purple cauliflower arises from activation of a MYB transcription factor. Plant Physiology 154, 1470-1480
14. Debeaujon I, Peeters AJ M, Léon-Kloosterziel KM, Koornneef M. 2001. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. The Plant Cell 13, 853
15. Devic M, Guilleminot J, Debeaujon I, Bechtold N, Bensaude E, Koornneef M, Pelletier G, Delseny M. 1999. The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. The Plant Journal 19, 387-398
16. Deynze AEV, Beversdorf WD, Pauls KP. 1993. Temperature effects on seed color in black-And yellow-seeded rapeseed. Canadian Journal of Plant Science 73, 383-387
17. Fricker M, Messelhausser U, Busch U, Scherer S, Ehling-Schulz M. 2007. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Applied and Environmental Microbiology 73, 1892
18. Fu F-Y, Lie-Zhao L, Chai Y-R, Chen L, Yang T, Jin M-Y, Ma A-F, Yan X-Y, Zhang Z-S. 2007. Localization of QTLs for seed color using recombinant inbred lines of Brassica napus in different environments. Genome 50, 840-854
19. Gachon C, Langlois-Meurinne M, Henry Y, Saindrenan P. 2005. Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: Functional and evolutionary implications. Plant Molecular Biology 58, 229-245
20. Gallardo K, Firnhaber C, Zuber H, Héricher D, Belghazi M, Henry C, Küster H, Thompson R. 2007. A combined proteome and transcriptome analysis of developing Medicago truncatula seeds. Molecular and Cellular Proteomics 6, 2165-2179
21. Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annual Review of Plant Biology 57, 761-780
22. Hoffmann T, Kalinowski G, Schwab W. 2006. RNAi-induced silencing of gene expression in strawberry fruit (Fragaria×ananassa) by agroinfiltration: A rapid assay for gene function analysis. The Plant Journal 48, 818-826
23. Holton TA, Cornish EC. 1995. Genetics and biochemistry of anthocyanin biosynthesis. The Plant Cell 7, 1071-1083
24. Jiang Y, Deyholos MK. 2010. Transcriptome analysis of secondarywall-enriched seed coat tissues of canola (Brassica napus L.). Plant Cell Reports 29, 327-342
25. Johnson CS, Kolevski B., Smyth DR. 2002. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. The Plant Cell 14, 1359-1375
26. Kasai A, Kasai K, Yumoto S, Senda, M. 2007. Structural features of GmIRCHS, candidate of the I gene inhibiting seed coat pigmentation in soybean: Implications for inducing endogenous RNA silencing of chalcone synthase genes. Plant Molecular Biology 64, 467-479
27. Kitamura S, Shikazono N, Tanaka A. 2004. TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. The Plant Journal 37, 104-114
28. Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmont M, Kirkbride R, Horvath S. 2010. Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proceedings of the National Academy of Sciences, USA 107, 8063-8070
29. Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M. 2006. Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology 57, 405-430
30. Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL. 1993. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. The Plant Cell 5, 171-179
31. Liang M, Davis E, Gardner D, Cai X, Wu Y. 2006. Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224, 1185-1196
32. Liang Y, Li JN. 2004. Relationship of the color formation and related enzymes and protein content of the spermoderms in Brassica napus. Scientia Agricultura Sinica 37, 522-527
33. Lin LZ, Harnly JM. 2009. Identification of the phenolic components of collard greens, kale, and Chinese broccoli. Journal of Agricultural and Food Chemistry 57, 7401-7408
34. Lin LZ, Harnly JM. 2010. Phenolic component profiles of mustard greens, yu choy, and 15 other Brassica vegetables. Journal of Agricultural and Food Chemistry 58, 6850-6857
35. Lipsa F, Snowdon R, Friedt W. 2007. Improving rapeseed meal quality by reduction of condensed tannins. Proceedings of the 12th International Rapeseed Congress, Wuhan, China, 135-137
36. Liu Z-w, Ting-dong F, Jin-xing T, Bao-yuan C. 2005. Inheritance of seed colour and identification of RAPD and AFLP markers linked to the seed colour gene in rapeseed (Brassica napus L.). Theoretical and Applied Genetics 110, 303-310
37. Lu K, Chai YR, Zhang K, Wang R, Chen L, Lei B, Lu J, Xu XF, Li JN. 2008. Cloning and characterization of phosphorus starvation inducible Brassica napus PURPLE ACID PHOSPHATASE12 gene family, and imprinting of a recently evolved MITE-minisatellite twin structure. Theoretical and Applied Genetics 117, 963-975
38. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M. 2007. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-Antiporter active in proanthocyanidin-Accumulating cells of the seed coat. The Plant Cell 19, 2023-2038
39. Marles M, Gruber MY. 2004. Histochemical characterisation of unextractable seed coat pigments and quantification of extractable lignin in the Brassicaceae. Journal of the Science of Food and Agriculture 84, 251-262
40. Meng J, Shi S, Gan L, Li Z, Qu X. 1998. The production of yellow-seeded Brassica napus (AACC) through crossing interspecific hybrids of B. campestris (AA) and B. carinata (BBCC) with B. napus. Euphytica 103, 329-333
41. 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. The Plant Cell 12, 1863-1878
42. 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 proanthocyanidin accumulation in developing seed. The Plant Cell 13, 2099-2114
43. Nesi N, Lucas MO, Auger B, Baron C, Lécureuil A, Guerche P, Kronenberger J, Lepiniec L, Debeaujon I, Renard M. 2009. The promoter of the Arabidopsis thaliana BAN gene is active in proanthocyanidin-Accumulating cells of the Brassica napus seed coat. Plant Cell Reports 28, 601-617
44. Ohl S, Hedrick SA, Chory J, Lamb CJ. 1990. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. The Plant Cell 2, 837-848
45. Olsson G. 1960. Species crosses within the genus Brassica. I. Artificial Brassica juncea Coss. Hereditas 46, 171-223
46. Pang JS, He MY, Liu B. 2004. Construction of the seed-coat cDNA microarray and screening of differentially expressed genes in barley. Acta Biochimica et Biophysica Sinica 36, 695-700
47. Pang Y, Peel GJ, Sharma SB, Tang Y, Dixon RA. 2008. A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula. Proceedings of the National Academy of Sciences, USA 105, 14210-14215
48. Pelletier MK, Shirley BW. 1996. Analysis of flavanone 3-hydroxylase in Arabidopsis seedlings (Coordinate regulation with chalcone synthase and chalcone isomerase). Plant Physiology 111, 339-345
49. Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I. 2005. TRANSPARENT TESTA10 encodes a laccaselike enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. The Plant Cell 17, 2966-2980
50. Romani A, Vignolini P, Isolani L, Ieri F, Heimler D. 2006. HPLCDAD/ MS characterization of flavonoids and hydroxycinnamic derivatives in turnip tops (Brassica rapa L. subsp. sylvestris L.). Journal of Agricultural and Food Chemistry 54, 1342-1346
51. Russell DW. 1971. The metabolism of aromatic compounds in higher plants. Journal of Biological Chemistry 246, 3870-3878
52. 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 and Development 16, 138-149
53. Schoenbohm C, Martens S, Eder C, Forkmann G, Weisshaar B. 2000. Identification of the Arabidopsis thaliana flavonoid 3'-hydroxylase gene and functional expression of the encoded P450 enzyme. Biological Chemistry 381, 749-753
54. Sharma SB, Dixon RA. 2005. Metabolic engineering of proanthocyanidins by ectopic expression of transcription factors in Arabidopsis thaliana. The Plant Journal 44, 62-75
55. Shirley BW. 1998. Flavonoids in seeds and grains: Physiological function, agronomic importance and the genetics of biosynthesis. Seed Science Research 8, 415-422
56. Somers DJ, Rakow G, Prabhu VK, Friesen KR. 2001. Identification of a major gene and RAPD markers for yellow seed coat colour in Brassica napus. Genome 44, 1077-1082
57. Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C. 1994. Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Molecular Biology 24, 743-755
58. Stafford HA. 1988. Proanthocyanidins and the lignin connection. Phytochemistry 27, 1-6
59. Stringam G, McGregor D, Pawlowski S. 1974. Chemical and morphological characteristics associated with seed coat color in rapeseed. In: Proceedings of the 4th International Rapeseed Congress, Giessen, Germany, June 4-8, 1974
60. Sun Y, Li H, Huang Jr. 2012. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Molecular Plant 5, 387-400
61. Tang Z, Li J, Zhang X, Chen L, Wang R. 1997. Genetic variation of yellow-seeded rapeseed lines (Brassica napus L.) from different genetic sources. Plant Breeding 116, 471-474
62. Theander O, Aman P, Miksche GE, Yasuda S. 1977. Carbohydrate, polyphenols, and lignin in seed hulls of different colours from tumip rapeseed. Journal of Agricultural and Food Chemistry 25, 270-273
63. Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC. 1999. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. The Plant Cell 11, 1337-1350
64. Wang H, Liu HL. 1996. Quantitative variation of anthocyanidins, polyphenols, trans-cinnamic acid and PAL activity in seed hulls of black-And yellow-seeded B. napus. Journal of Huazhong Agricultural University 15, 509-513
65. Wang X, Wang H, Wang J, et al. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43, 1035-1039
66. Wei YL, Li JN, Lu J, Tang ZL, Pu DC, Chai YR. 2007. Molecular cloning of Brassica napus TRANSPARENT TESTA 2 gene family encoding potential MYB regulatory proteins of proanthocyanidin biosynthesis. Molecular Biology Reports 34, 105-120
67. Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, 485
68. Winkel-Shirley B. 2002. Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218-223
69. Wisman E, Cardon GH, Fransz P, Saedler H. 1998. The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Molecular Biology 37, 989-999
70. Xiao SS, Xu JS, Li Y, Zhang L, Shi S, Shi S, Wu JS, Liu KD. 2007. Generation and mapping of SCAR and CAPS markers linked to the seed coat color gene in Brassica napus using a genome-walking technique. Genome 50, 611-618
71. Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA. 2003. Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299, 396
72. Xu BB, Li JN, Zhang XK, Wang R, Xie LL, Chai YR. 2007. Cloning and molecular characterization of a functional flavonoid 3'-hydroxylase gene from Brassica napus. Journal of Plant Physiology 164, 350-363
73. Zhang Y, Li X, Chen W, Yi B, Wen J, Shen J, Ma C, Chen B, Tu J, Fu T. 2011. Identification of two major QTL for yellow seed color in two crosses of resynthesized Brassica napus line No. 2127-17. Molecular Breeding 28, 335-342
74. Zhao J, Dixon RA. 2009. MATE transporters facilitate vacuolar uptake of epicatechin 3'-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. The Plant Cell 21, 2323-2340
75. Zhao J, Pang Y, Dixon RA. 2010. The mysteries of proanthocyanidin transport and polymerization. Plant Physiology 153, 437-443