Abstract
To better understand the functional characterization of anthocyanin gene expression in black rice, we performed a detailed computational examination. The experiment was performed using the newly designed 135K Oryza sativa microarray to assess gene expression at three time points after the heading stage in Ds insertion lines. Transcription factors related to anthocyanin pigmentation biosynthesis were clustered. A total of 8,517 genes exhibited greater than 2.5-fold up- or downregulation in each comparison between three rice groups and three seed developmental stages. The resultant 82 transcription factor genes found to be associated with anthocyanin were classified into 12 groups. In addition, 12 unknown and hypothetical genes were identified from comparisons between the white cultivar and two black Ds insertion mutants tested. We identified 12 unknown and hypothetical genes involved in anthocyanin biosynthesis. These genes likely play either a regulatory role in the anthocyanin production process or are related to anthocyanin metabolism during flavonoid biosynthesis. While these genes require further characterization and validation, the results here underline the potential use of the newly designed microarray.
Similar content being viewed by others
References
Zhang, M.W., Guo, B.J. & Peng, Z.M. Genetic effects on grain characteristics of indica black rice and their uses on indirect selections for some mineral element contents in grains. Genet. Resour. Crop 52, 1121–1128 (2005).
Ryu, S.N., Park, S.Z. & Ho, C.T. High performance liquid chromatographic determination of anthocyanin pigments in some varieties of black rice. J. Food Drug Anal. 6, 729–736 (1998).
Robert, Y. & Naofumi, M. Color enhancing effect of carboxylic acids on anthocyanins. Food Chemistry 105, 421–427 (2007).
Quattrocchio, F., Wing, J.F., Leppen, H.T.C., Mol, J.N.M. & Koes, R.E. Regulatory genes controlling anthocyanin pigmentation are functionally conserved among plant species and have distinct sets of target genes. Plant Cell 5, 1497–1512 (1993).
Takahashi, M. Gene analysis and its related problems. J. Fac. Agr. Hokkaido University 61, 91–142 (1982).
Hu, J., Reddy, V.S. & Wessler, S.R. The rice R gene family, two distinct subfamilies inverted repeat transposable elements. Plant Molecular Biology 42, 667–678 (2000).
Reddy, V.S., Scheffler, B.E., Wienand, U., Wessler, S.R. & Reddy, A.R. Cloning and characterization of the rice homologue of the maize C1 anthocyanin regulatory gene. Plant Mol. Biology 36, 497–498 (1998).
Holton, T.A. & Cornish, E.C. Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7, 1071–1083 (1995).
Clifford, M.N. Anthocyanins, Nature, occurrence and dietary burden. Journal of Science Food Agriculture 80, 1063–1072 (2000).
Oki, T. et al. Polymeric procyanidins as radical-scavenging componenets in red-hulled rice. J. Agric. Food Chemistry 50, 7524–7529 (2002).
Dessimoz, C., Boeckmann, B., Roth, A.C. & Gonnet, G.H. Detecting non-orthology in the COGs database and other approaches grouping orthologs using genome-specific best hits. Nucleic Acids Res. 34, 3309–3316 (2006).
Remm, M., Storm, C. & Sonnhammer, E. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biology 314, 1041–1052 (2001).
Ashburner, M. et al. Gene ontology, tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25–29 (2000).
Ptashne, M. How eukaryotic transcriptional activators work. Nature 335, 683–689 (1988).
Li, J. et al. A subgroup of MYB transcription factor genes undergoes conserved alternative splicing in Arabidopsis and rice. Journal Experimental Botany 57, 1263–1273 (2006).
Baudry, A. et al. TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J. 39, 366–380 (2004).
Hartmann, U., Sagasser, M., Mehrtens, F., Stracke, R. & Weisshaar, B. Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol. Biol. 57, 155–171 (2005).
Reddy, A.M. et al. Novel transgenic rice overexpressing anthocyanidin synthase accumulates a mixture of flavonoids leading to an increased antioxidant potential. Metab Eng. 9, 95–111 (2007).
Hui, S.L. & David, K. Text-based over-representation analysis of microarray gene lists with annotation bias. Nucleic Acids Res. 37, e79 (2009).
Qin, H., Feng, T., Harding, S.A., Tsai, C.J. & Zhang, S. An efficient method to identify differentially expressed genes in microarray experiments. Bioinformatics 24, 1583–1589 (2008).
Park, H.W. et al. Gene expression pattern analysis of PAHs and VOCs in rat blood using HazChem rat array. BioChip J. 3, 333–338 (2009).
Kim, C.K. et al. Genetic analysis of seed-specific gene expression for pigmentation in colored rice. BioChip J. 3, 125–129 (2009).
Kim, C.K. et al. Genetic analysis of gene expression for pigmentation in Chinese cabbage (Brassica rapa). BioChip J. 4, 123–128 (2010).
Zhu, Q.H. et al. Transposon insertional mutants, a resource for rice functional genomics. In, Upadhyaya NM(ed) Rice functional genomics challenges progress and prospects. Springer Press 224–262 (2007).
Kolesnik, T. et al. Establishing an efficient Ac/Ds tagging system in rice, large-scale analysis of Ds flanking sequences. Plant J. 37, 301–314 (2004).
Park, D.S. et al. Genetic variation through Dissociation (Ds) insertional mutagenesis system for rice in Korea, progress and current status. Molecular Breeding 24, 1–15 (2009).
Xia, M., Ling, W.H., Ma, J., Kitts, D.D. & Zawistowski, J. Supplementation of diets with black rice pigment fraction attenuates atherosclerotic plaque formation in apolipoprotein E deficient mice. Journal Nutr. 133, 744–751 (2003).
Xia, X. et al. An anthocyanin-rich extract from black rice enhances atherosclerotic plaque stabilization in apolipoprotein E-deficient mice. Journal Nutr. 136, 2220–2225 (2006).
Guo, H. et al. Effect of anthocyanin-rich extract from black rice (Oryza sativa L. indica) on hyperlipidemia and insulin resistance in fructose-fed rats. Plant Foods Hum Nutr. 62, 1–6 (2007).
Wu, X. & Prior, R.L. Systematic identification and characterization of anthocyanins by HPLC-ESI-MS/MS in common foods in the United States, fruits and berries. Journal of Agricultural and Food Chemistry 53, 2589–2599 (2005).
Zhang, Z., Kou, X., Fugal, K. & McLaughlin, J. Comparison of HPLC methods for determination of anthocyanins and anthocyanidins in bilberry extracts. Journal of Agricultural and Food Chemistry 52, 688–691 (2004).
NCBI/COGs. [http://www.ncbi.nlm.nih.gov/COG/]
Zeeberg, B.R. et al. GoMiner, a resource for biological interpretation of genomic and proteomic data. Genome Biol. 4, R28 (2003).
IRGSP. [http://rgp.dna.affrc.go.jp/E/IRGSP/]
Martin, C. & Paz-Ares, J. MYB transcription factors in plants. Trends Genet. 13, 67–73 (1997).
Yujie, F., Kabin, X., Xin, H., Honghong, H. & Lizhong, X. Systematic analysis of GT factor family of rice reveals a novel subfamily involved in stress responses. Mol. Genet Genomics 283, 157–169 (2010).
Reddy, V.S., Scheffler, B.E., Wienand, U., Wessler, S.R. & Reddy, A.R. Cloning and characterization of the rice homologue of the maize C1 anthocyanin regulatory gene. Plant Mol. Biology 36, 497–498 (1998).
Borevitz, J.O., Xia, Y., Blount, J., Dixon, R.A. & Lamb, C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12, 2383–2393 (2000).
Sheng, T., Joost, K., Maarten, K. & Sjef, S. Sucrosespecific induction of anthocyanin biosynthesis in arabidopsis requires the MYB75/PAP1 Gene1. Plant Physiology 139, 1840–1852 (2005).
Johnson, C.S., Kolevski, B. & Smyth, D.R. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14, 1359–1375 (2002).
Morishita, T. et al. Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol. 50, 2210–2222 (2009).
Jeon, J.S. et al. Leafy hull sterile1 (lhs1) is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12, 871–884 (2000).
Antonio, G., Mingzhe, Z., John, M.L. & Alan, M.L. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant Journal 53, 814–827 (2008).
Park, S.H. et al. Analysis of gene-trap Ds rice populations in Korea. Plant Mol Biol. 65, 373–384 (2007).
RAP2 (Rice Annotation Project version 2). [http://rapdb.dna.affrc.go.jp/]
Workman, C. et al. A new non-linear normalization method for reducing variability in dna microarray experiments. Genome Biol. 3, 0048.1–0048.16 (2002).
Sadlier, D.M. et al. Sequential extracellular matrixfocused and baited-global cluster analysis of serial transcriptomic profiles identifies candidate modulators of renal tubulointerstitial fibrosis in murine adriamycininduced nephropathy. J. Biol Chem. 279, 29670–29680 (2004).
Irizarry, R.A. et al. Summaries of Affymetrix Gene-Chip probe level data. Nucleic Acids Res. 31, e15 (2003).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kim, C., Kikuchi, S., Kim, Y. et al. Computational identification of seed-specific transcription factors involved in anthocyanin production in black rice. BioChip J 4, 247–255 (2010). https://doi.org/10.1007/s13206-010-4313-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13206-010-4313-7