Abstract
While many aspects of primary cell wall have been extensively elucidated, our current understanding of secondary wall biosynthesis is limited. Recently, transcription factor MYB46 has been identified as a master regulator of secondary wall biosynthesis in Arabidopsis thaliana. To gain better understanding of this MYB46-mediated transcriptional regulation, we analyzed the promoter region of a direct target gene, AtC3H14, of MYB46 and identified a cis-acting regulatory motif that is recognized by MYB46. This MYB46-responsive cis-regulatory element (M46RE) was further characterized and shown to have an eight-nucleotide core motif, RKTWGGTR. We used electrophoretic mobility shift assay, transient transcriptional activation assay and chromatin immunoprecipitation analysis to show that the M46RE was necessary and sufficient for MYB46-responsive transcription. Genome-wide analysis identified that the frequency of M46RE in the promoters were highly enriched among the genes upregulated by MYB46, especially in the group of genes involved in secondary wall biosynthesis.
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References
Aoyama T, Chua NH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11(3):605–612
Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17(8):2281–2295. doi:10.1105/tpc.105.031542
Brown D, Wightman R, Zhang Z, Gomez LD, Atanassov I, Bukowski JP, Tryfona T, McQueen-Mason SJ, Dupree P, Turner S (2011) Arabidopsis genes IRREGULAR XYLEM (IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall. Plant J 66(3):401–413. doi:10.1111/j.1365-313X.2011.04501.x
Fukuda H (1997) Tracheary element differentiation. Plant Cell 9(7):1147–1156. doi:10.1105/tpc.9.7.1147
Han KH, Ko JH, Yang SH (2007) Optimizing lignocellulosic feedstock for improved biofuel productivity and processing. Biofpr 1(2):135–146. doi:10.1002/bbb.14
Hatton D, Sablowski R, Yung MH, Smith C, Schuch W, Bevan M (1995) Two classes of cis sequences contribute to tissue-specific expression of a PAL2 promoter in transgenic tobacco. Plant J 7(6):859–876. doi:10.1046/j.1365-313X.1995.07060859.x
Jensen JK, Kim H, Cocuron JC, Orler R, Ralph J, Wilkerson CG (2010) The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis. Plant J 66(3):387–400. doi:10.1111/j.1365-313X.2010.04475.x
Kaneda M, Rensing K, Samuels L (2010) Secondary cell wall deposition in developing secondary xylem of poplar. J Integr Plant Biol 52(2):234–243. doi:10.1111/j.1744-7909.2010.00925.x
Ko JH, Yang SH, Park AH, Lerouxel O, Han KH (2007) ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana. Plant J 50(6):1035–1048. doi:10.1111/j.1365-313X.2007.03109.x
Ko JH, Kim WC, Han KH (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. Plant J 60(4):649–665. doi:10.1111/j.1365-313X.2009.03989.x
Lerouxel O, Cavalier DM, Liepman AH, Keegstra K (2006) Biosynthesis of plant cell wall polysaccharides: a complex process. Curr Opin Plant Biol 9(6):621–630. doi:10.1016/j.pbi.2006.09.009
Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36(6):743–754. doi:10.1046/j.1365-313X.2003.01916.x
Peña MJ, Zhong R, Zhou GK, Richardson EA, O’Neill MA, Darvill AG, York WS, Ye ZH (2007) Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell 19(2):549–563. doi:10.1105/tpc.106.049320
Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70-5 Regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20(8):744–749. doi:10.1016/j.cub.2010.02.057
Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133(3):1051–1071. doi:10.1104/pp.103.026484
Rahantamalala A, Rech P, Martinez Y, Chaubet-Gigot N, Grima-Pettenati J, Pacquit V (2010) Coordinated transcriptional regulation of two key genes in the lignin branch pathway—CAD and CCR—is mediated through MYB- binding sites. BMC Plant Biol 10:130–141. doi:10.1186/1471-2229-10-130
Rammírez V, Agorio A, Coego A, García-Andrade J, Hernández MJ, Balaguer B, Ouwerkerk PB, Zarra I, Vera P (2011) MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis. Plant Physiol 155(4):1920–1935. doi:10.1104/pp.110.171843
Romero I, Fuertes A, Benito MJ, Malpica JM, Leyva A, Paz-Ares J (1998) More than 80 R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14(3):273–284. doi:10.1046/j.1365-313X.1998.00113.x
Sheen J (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol 127(4):1466–1475. doi:10.1104/pp.010820
Shi R, Sun YH, Li Q, Heber S, Sederoff R, Chiang VL (2010) Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol 51(1):144–163. doi:10.1093/pcp/pcp175
Skriver K, Olsen FL, Rogers JC, Mundy J (1991) Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci USA 88(16):7266–7270. doi:10.1073/pnas.88.16.7266
Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78. doi:10.1146/annurev.cellbio.22.022206.160206
Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA 100(3):1450–1455. doi:10.1073/pnas.0337628100
Walker JC, Howard EA, Dennis ES, Peacock WJ (1987) DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc Natl Acad Sci USA 84(19):6624–6628. doi:10.3109/00016357.2011.568963
Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics 9:44–63
Winzell A, Aspeborg H, Wang Y, Ezcurra I (2010) Conserved CA-rich motifs in gene promoters of Pt x tMYB021-responsive secondary cell wall carbohydrate-active enzymes in Populus. Biochem Biophys Res Commun 394(3):848–853. doi:10.1016/j.bbrc.2010.03.101
Wu AM, Hörnblad E, Voxeur A, Gerber L, Rihouey C, Lerouge P, Marchant A (2010) Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiol 153(2):542–554. doi:10.1104/pp.110.154971
Ye ZH (2002) Vascular tissue differentiation and pattern formation in plants. Annu Rev Plant Biol 53:183–202. doi:10.1146/annurev.arplant.53.100301.135245
Yi SY, Liu J (2009) Combinatorial interactions of two cis-acting elements, AT-rich regions and HSEs, in the expression of tomato Lehsp23.8 upon heat and non-heat stresses. J Plant Biol 52(6):560–568. doi:10.1007/s12374-009-9072-4
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572. doi:10.1038/nprot.2007.199
Zhong R, Ye ZH (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10(6):564–572. doi:10.1016/j.pbi.2007.09.001
Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18(11):3158–3170. doi:10.1105/tpc.106.047399
Zhong R, Richardson EA, Ye ZH (2007) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19(9):2776–2792. doi:10.1105/tpc.107.053678
Zhong R, Lee C, Ye ZH (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3(6):1087–1103. doi:10.1093/mp/ssq062
Acknowledgments
This work was funded by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DR-FC02-07ER64494). This project was also funded in part by a grant from the Michigan Agriculture Experiment Station and by the Ministry of Education, Science and Technology of Korea via the World Class University Project at Chonnam National University (R31-2009-000-20025-0) and by Basic Science Research Program through the National Research Foundation of Korea (NRF) (2011-0008840).
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Kim, WC., Ko, JH. & Han, KH. Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol Biol 78, 489–501 (2012). https://doi.org/10.1007/s11103-012-9880-7
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DOI: https://doi.org/10.1007/s11103-012-9880-7