Novel bioresources for studies of Brassica oleracea: Identification of a kale MYB transcription factor responsible for glucosinolate production

Plant Biotechnology Journal

Volumn 11, Issue 8, 2013, Pages 1017-1027

  Araki, Ryoichi ^a,b,h   Hasumi, Akiko ^a   Nishizawa, Osamu Ishizaki ^a   Sasaki, Katsunori ^a   Kuwahara, Ayuko ^b,c,d   Sawada, Yuji ^b,c   Totoki, Yasushi ^e,i   Toyoda, Atsushi ^e,j   Sakaki, Yoshiyuki ^e,k   Li, Yimeng ^b,f   Saito, Kazuki ^b,c,g   Ogawa, Toshiya ^a   Hirai, Masami Yokota ^b,c,d  

^a KIRIN HOLDINGS CO LTD   (Japan)

^b RIKEN   (Japan)

^c RIKEN Center for Sustainable Resource Science   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e RIKEN YOKOHAMA INSTITUTE   (Japan)

^f NORTHEAST FORESTRY UNIVERSITY   (China)

^g CHIBA UNIVERSITY   (Japan)

^h KYOTO UNIVERSITY   (Japan)

ⁱ NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^j NATIONAL INSTITUTE OF GENETICS   (Japan)

^k TOYOHASHI UNIVERSITY OF TECHNOLOGY   (Japan)

more..

Author keywords

Aliphatic glucosinolate; Arabidopsis thaliana; Brassica oleracea; Full length cDNA library; MYB type transcription factor

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA OLERACEA; BRASSICA OLERACEA VAR. ACEPHALA; BRASSICACEAE; HEXAPODA;

ALIPHATIC GLUCOSINOLATE; GLUCOSINOLATE; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BIOSYNTHESIS; BRASSICA; BRASSICA OLERACEA; CHEMISTRY; EXPRESSED SEQUENCE TAG; FULL-LENGTH CDNA LIBRARY; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENE LIBRARY; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MYB-TYPE TRANSCRIPTION FACTOR; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

ALIPHATIC GLUCOSINOLATE; ARABIDOPSIS THALIANA; BRASSICA OLERACEA; FULL-LENGTH CDNA LIBRARY; MYB-TYPE TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARABIDOPSIS; BIOSYNTHETIC PATHWAYS; BRASSICA; CLONING, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; GENE LIBRARY; GENETIC COMPLEMENTATION TEST; GLUCOSINOLATES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN; TRANSCRIPTION FACTORS;

EID: 84884419239     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12095     Document Type: Article

References (53)

1. Basten, G.P., Bao, Y. and Williamson, G. (2002) Sulforaphane and its glutathione conjugate but not sulforaphane nitrile induce UDP-glucuronosyl transferase (UGT1A1) and glutathione transferase (GSTA1) in cultured cells. Carcinogenesis, 23, 1399-1404.
2. Burow, M., Halkier, B.A. and Kliebenstein, D.J. (2010) Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness. Curr. Opin. Plant Biol. 13, 347-352.
3. Carninci, P., Kvam, C., Kitamura, A., Ohsumi, T., Okazaki, Y., Itoh, M., Kamiya, M., Shibata, K., Sasaki, N., Izawa, M., Muramatsu, M., Hayashizaki, Y. and Schneider, C. (1996) High-efficiency full-length cDNA cloning by biotinylated CAP trapper. Genomics, 37, 327-336.
4. Carninci, P., Shibata, Y., Hayatsu, N., Sugahara, Y., Shibata, K., Itoh, M., Konno, H., Okazaki, Y., Muramatsu, M. and Hayashizaki, Y. (2000) Normalization and subtraction of cap-trapper-selected cDNAs to prepare full-length cDNA libraries for rapid discovery of new genes. Genome Res. 10, 1617-1630.
5. Carninci, P., Shibata, Y., Hayatsu, N., Itoh, M., Shiraki, T., Hirozane, T., Watahiki, A., Shibata, K., Konno, H., Muramatsu, M. and Hayashizaki, Y. (2001) Balanced-size and long-size cloning of full-length, cap-trapped cDNAs into vectors of the novel λ-FLC family allows enhanced gene discovery rate and functional analysis. Genomics, 77, 79-90.
6. Celenza, J.L., Quiel, J.A., Smolen, G.A., Merrikh, H., Silvestro, A.R., Normanly, J. and Bender, J. (2005) The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol. 137, 253-262.
7. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
8. Conesa, A. and Götz, S. (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Intl. J. Plant Genomics, 2008, 619832.
9. Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M. and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
10. Ewing, B. and Green, P. (1998) Base-calling of automated sequencer traces using phred II. Error probabilities. Genome Res. 8, 186-194.
11. Ewing, B., Hillier, L., Wendl, M.C. and Green, P. (1998) Base-calling of automated sequencer traces using phred I. Accuracy assessment. Genome Res. 8, 175-185.
12. Fahey, J.W., Zhang, Y. and Talalay, P. (1997) Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc. Natl Acad. Sci. USA, 94, 10367-10372.
13. Fahey, J.W., Zalcmann, A.T. and Talalay, P. (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry, 56, 5-51.
14. Gigolashvili, T., Berger, B., Mock, H-P., Müller, C., Weisshaar, B. and Flügge, U-I. (2007a) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50, 886-901.
15. Gigolashvili, T., Yatusevich, R., Berger, B., Müller, C. and Flügge, U-I. (2007b) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 51, 247-261.
16. Gigolashvili, T., Engqvist, M., Yatusevich, R., Müller, C. and Flügge, U-I. (2008) HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. New Phytol. 177, 627-642.
17. Gigolashvili, T., Berger, B. and Flügge, U-I. (2009) Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana. Phytochem. Rev. 8, 3-13.
18. Götz, S., García-Gómez, J.M., Terol, J., Williams, T.D., Nagaraj, S.H., Nueda, M.J., Robles, M., Talón, M., Dopazo, J. and Conesa, A. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36, 3420-3435.
19. Green, P. (1996) PHRAP Documentation. University of Washington, Seattle, WA. [http://bozeman.mbt.washington.edu/phrap.docs/phrap.html] Accessed May 2013.
20. Halkier, B.A. and Gershenzon, J. (2006) Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
21. Hansen, B.G., Kliebenstein, D.J. and Halkier, B.A. (2007) Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J. 50, 902-910.
22. Hirai, M.Y. (2009) A robust omics-based approach for the identification of glucosinolate biosynthetic genes. Phytochem. Rev. 8, 15-23.
23. Hirai, M.Y., Sugiyama, K., Sawada, Y., Tohge, T., Obayashi, T., Suzuki, A., Araki, R., Sakurai, N., Suzuki, H., Aoki, K., Goda, H., Nishizawa, O.I., Shibata, D. and Saito, K. (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl Acad. Sci. USA, 104, 6478-6483.
24. Hopkins, R.J., van Dam, N.M. and van Loon, J.J.A. (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57-83.
25. Hu, Z., Huang, S., Sun, M., Wang, H. and Hua, W. (2012) Development and application of single nucleotide polymorphism markers in the polyploid Brassica napus by 454 sequencing of expressed sequence tags. Plant Breed. 131, 293-299.
26. Kliebenstein, D.J. (2009) Advancing genetic theory and application by metabolic quantitative trait loci analysis. Plant Cell, 21, 1637-1646.
27. Kliebenstein, D.J., Kroymann, J., Brown, P., Figuth, A., Pedersen, D., Gershenzon, J. and Mitchell-Olds, T. (2001a) Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126, 811-825.
28. Kliebenstein, D.J., Lambrix, V.M., Reichelt, M., Gershenzon, J. and Mitchell-Olds, T. (2001b) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell, 13, 681-693.
29. Kroymann, J., Textor, S., Tokuhisa, J.G., Falk, K.L., Bartram, S., Gershenzon, J. and Mitchell-Olds, T. (2001) A gene controlling variation in Arabidopsis glucosinolate composition is part of the methionine chain elongation pathway. Plant Physiol. 127, 1077-1088.
30. Li, G. and Quiros, C.F. (2002) Genetic analysis, expression and molecular characterization of BoGSL-ELONG, a major gene involved in the aliphatic glucosinolate pathway of Brassica species. Genetics, 162, 1937-1943.
31. Li, G. and Quiros, C.F. (2003) In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSL-ALK. Theor. Appl. Genet. 106, 1116-1121.
32. Li, G., Riaz, A., Goyal, S., Abel, S. and Quiros, C.F. (2001) Inheritance of three major genes involved in the synthesis of aliphatic glucosinolates in Brassica oleracea. J. Am. Soc. Hort. Sci. 126, 427-431.
33. Li, J., Hansen, B.G., Ober, J.A., Kliebenstein, D.J. and Halkier, B.A. (2008) Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol. 148, 1721-1733.
34. Li, Y., Sawada, Y., Hirai, A., Sato, M., Kuwahara, A., Yan, X. and Hirai, M.Y. (2013) Novel insights into the function of Arabidopsis R2R3-MYB transcription factors regulating aliphatic glucosinolate biosynthesis. Plant Cell Physiol. doi:10.1093/pcp/pct085.
35. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T. and Kimura, T. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41.
36. Nasu, S., Suzuki, J., Ohta, R., Hasegawa, K., Yui, R., Kitazawa, N., Monna, L. and Minobe, Y. (2002) Search for and analysis of single nucleotide polymorphisms (SNPs) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers. DNA Res. 9, 163-171.
37. Qiu, D., Gao, M., Li, G. and Quiros, C. (2009) Comparative sequence analysis for Brassica oleracea with similar sequences in B. rapa and Arabidopsis thaliana. Plant Cell Rep. 28, 649-661.
38. Quiros, C.F. and Farnham, M.W. (2011) The Genetics of Brassica oleracea. In: Genetics and Genomics of the Brassicaceae (Schmidt, R. and Bancroft, I., eds) pp. 261-289. New York: Springer.
39. Sawada, Y., Akiyama, K., Sakata, A., Kuwahara, A., Otsuki, H., Sakurai, T., Saito, K. and Hirai, M.Y. (2009) Widely targeted metabolomics based on large-scale MS/MS data for elucidating metabolite accumulation patterns in plants. Plant Cell Physiol. 50, 37-47.
40. Sønderby, I.E., Hansen, B.G., Bjarnholt, N., Ticconi, C., Halkier, B.A. and Kliebenstein, D.J. (2007) A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE, 2, e1322.
41. Sønderby, I.E., Burow, M., Rowe, H.C., Kliebenstein, D.J. and Halkier, B.A. (2010a) A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol., 153, 348-363.
42. Sønderby, I.E., Geu-Flores, F. and Halkier, B.A. (2010b) Biosynthesis of glucosinolates - gene discovery and beyond. Trends Plant Sci. 15, 283-290.
43. Textor, S., de Kraker, J-W., Hause, B., Gershenzon, J. and Tokuhisa, J.G. (2007) MAM3 catalyzes the formation of all aliphatic glucosinolate chain lengths in Arabidopsis. Plant Physiol. 144, 60-71.
44. The Brassica rapa Genome Sequencing Project Consortium (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035-1039.
45. Wang, H., Wu, J., Sun, S., Liu, B., Cheng, F., Sun, R. and Wang, X. (2011) Glucosinolate biosynthetic genes in Brassica rapa. Gene, 487, 135-142.
46. Wittstock, U. and Halkier, B.A. (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7, 263-270.
47. Xue, J., Jørgensen, M., Pihlgren, U. and Rask, L. (1995) The myrosinase gene family in Arabidopsis thaliana: gene organization, expression and evolution. Plant Mol. Biol. 27, 911-922.
48. Yanaka, A., Fahey, J.W., Fukumoto, A., Nakayama, M., Inoue, S., Zhang, S., Tauchi, M., Suzuki, H., Hyodo, I. and Yamamoto, M. (2009) Dietary sulforaphane-rich broccoli sprouts reduce colonization and attenuate gastritis in Helicobacter pylori-infected mice and humans. Cancer Prev. Res. 2, 353-360.
49. Zang, Y-X., Kim, J-H., Park, Y-D., Kim, D-H. and Hong, S-B. (2008) Metabolic engineering of aliphatic glucosinolates in Chinese cabbage plants expressing Arabidopsis MAM1, CYP79F1, and CYP83A1. BMB Rep. 41, 472-478.
50. Zang, Y-X., Kim, H.U., Kim, J.A., Lim, M-H., Jin, M., Lee, S.C., Kwon, S-J., Lee, S-I., Hong, J.K., Park, T-H., Mun, J-H., Seol, Y-J., Hong, S-B. and Park, B-S. (2009) Genome-wide identification of glucosinolate synthesis genes in Brassica rapa. FEBS J. 276, 3559-3574.
51. Zhang, Y., Cho, C-G., Posner, G.H. and Talalay, P. (1992) Spectroscopic quantitation of organic isothiocyanates by cyclocondensation with vicinal dithiols. Anal. Biochem. 205, 100-107.
52. Zhang, Y., Kensler, T.W., Cho, C.G., Posner, G.H. and Talalay, P. (1994) Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proc. Natl Acad. Sci. USA, 91, 3147-3150.
53. Zhang, Z., Ober, J.A. and Kliebenstein, D.J. (2006) The gene controlling the quantitative trait locus EPITHIOSPECIFIER MODIFIER1 alters glucosinolate hydrolysis and insect resistance in Arabidopsis. Plant Cell, 18, 1524-1536.