A poplar R2R3-MYB transcription factor, PtrMYB152, is involved in regulation of lignin biosynthesis during secondary cell wall formation
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Abstract
Wood is the most abundant biomass in perennial woody plants. Extensive studies have shown that R2R3-MYB transcription factors are involved in regulation of lignin biosynthesis during secondary cell wall formation in many plant species, such as Arabidopsis, rice, maize and poplar. In this study, a MYB transcription factor, named PtrMYB152, was isolated from Populus trichocarpa and encoded a protein of 321 amino acids that contained a conserved R2R3-MYB domain. Phylogenetic analysis revealed that PtrMYB152 shares high sequence homology with other known plant MYBs associated with secondary wall formation. PtrMYB152 is specifically expressed in secondary wall-forming cells in poplar. Histochemical localizations of GUS expression in the transgenic Arabidopsis plants showed that PtrMYB152 is predominantly expressed in vascular tissues. Overexpression of PtrMYB152 resulted in specific activation of lignin biosynthetic genes, and caused ectopic deposition of lignin in stem and petiole of transgenic plants. These data indicated that PtrMYB152 is a specific transcriptional activator of lignin biosynthesis during wood formation of poplar.
Keywords
Poplar R2R3-MYB Transcription factors Lignin Secondary cell wallsNotes
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31370672, 31171620), the National Key Project for Research on Transgenic Plant (2011ZX08010-003), 100 Talents Programme of The Chinese Academy of Sciences, the Natural Science Foundation Project of CQ CSTC (CSTC2013JJB8007), the program for New Century Excellent Talents in University (NCET-11-0700), the Fundamental Research Funds for the Central Universities (XDJK2012c088, XDJK2014a005) and the Research Fund for the Doctoral Program of Higher Education (20110182110004).
Supplementary material
References
- Bedon F, Grima-Pettenati J, Mackay J (2007) Conifer R2R3-MYB transcription factors: sequence analyses and gene expression in wood-forming tissues of white spruce (Picea glauca). BMC Plant Biol 7:17PubMedCentralPubMedCrossRefGoogle Scholar
- Bedon F, Bomal C, Caron S, Levasseur C, Boyle B, Mansfield SD, Schmidt A, Gershenzon J, Grima-Pettenati J, Séguin A, MacKay J (2010) Subgroup 4 R2R3-MYBs in conifer trees: gene family expansion and contribution to the isoprenoid- and flavonoid-oriented responses. J Exp Bot 61:3847–3864PubMedCentralPubMedCrossRefGoogle Scholar
- Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546PubMedCrossRefGoogle Scholar
- Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JEK, Blais S, Tremblay L, Morency MJ, Pavy N, Grima-Pettenati J, Séguin A, MacKay J (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59:3925–3939PubMedCentralPubMedCrossRefGoogle Scholar
- Boudet AM (2000) Lignins and lignification: selected issues. Plant Physiol Biochem 38:81–96CrossRefGoogle Scholar
- Burk DH, Zhong R, Morrison WH, Ye ZH (2006) Disruption of cortical microtubules by overexpression of green fluorescent protein-tagged α-tubulin 6 causes a marked reduction in cell wall synthesis. J Integr Plant Biol 48:85–98CrossRefGoogle Scholar
- Bylesjö M, Nilsson R, Srivastava V, Grönlund A, Johansson AI, Jansson S, Karlsson J, Moritz T, Wingsle G, Trygg J (2008) Integrated analysis of transcript, protein and metabolite data to study lignin biosynthesis in hybrid aspen. J Proteome Res 8:199–210CrossRefGoogle Scholar
- Chen S, Songkumarn P, Liu J, Wang GL (2009) A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol 150:1111–1121PubMedCentralPubMedCrossRefGoogle Scholar
- Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
- Dence CW (1992) The determination of lignin [M]//methods in lignin chemistry. Springer, Berlin, pp 33–61Google Scholar
- Derikvand MM, Sierra JB, Ruel K, Pollet B, Do CT, Thévenin J, Buffard D, Jouanin L, Lapierre C (2008) Redirection of the phenylpropanoid pathway to feruloyl malate in Arabidopsis mutants deficient for cinnamoyl-CoA reductase 1. Planta 227:943–956CrossRefGoogle Scholar
- Do CT, Pollet B, Thévenin J, Sibout R, Denoue D, Barrière Y, Lapierre C, Jouanin L (2007) Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta 226:1117–1129PubMedCrossRefGoogle Scholar
- Douglas CJ (1996) Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends Plant Sci 1:171–178CrossRefGoogle Scholar
- Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581PubMedCrossRefGoogle Scholar
- Fukushima RS, Hatfield RD (2001) Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. J Agric Food Chem 49:3133–3139PubMedCrossRefGoogle Scholar
- Goicoechea M, Lacombe E, Legay S, Milhaevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati J (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567PubMedCrossRefGoogle Scholar
- Gray J (2005) Guard cells: transcription factors regulate stomatal movements. Curr Biol 15:R593–R595PubMedCrossRefGoogle Scholar
- Iiyama K, Wallis AFA (1988) An improved acetyl bromide procedure for determining lignin in woods and wood pulps. Wood Sci Technol 22(3):271–280CrossRefGoogle Scholar
- Jia ZC, Sun YM, Yuan L, Tian QY, Luo KM (2010) The chitinase gene (Bbchit1) from Beauveria bassiana enhances resistance to Cytospora chrysosperma in Populus tomentosa Carr. Biotechnol Lett 32:1325–1332PubMedCrossRefGoogle Scholar
- Joshi CP, Bhandari S, Ranjan P, Kalluri UC, Liang X, Fujino T, Samuga A (2004) Genomics of cellulose biosynthesis in poplars. New Phytol 164:53–61CrossRefGoogle Scholar
- Kao YY, Harding SA, Tsai CJ (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol 130:796–807PubMedCentralPubMedCrossRefGoogle Scholar
- Kim WC, Ko JH, Han KH (2012) Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Mol Biol 78:489–501PubMedCrossRefGoogle Scholar
- Kim WC, Ko JH, Kim JY, Han KH (2013) MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis. Plant J 73:26–36Google Scholar
- Lee C, Teng Q, Zhong R, Ye ZH (2011) Molecular dissection of xylan biosynthesis during wood formation in poplar. Mol Plant 4:730–747PubMedCrossRefGoogle Scholar
- Legay S, Lacombe E, Goicoechea M, Brière C, Séguin A, Mackay J, Grima-Pettenati J (2007) Molecular characterization of EgMYB1, a putative transcriptional repressor of the lignin biosynthetic pathway. Plant Sci 173:542–549CrossRefGoogle Scholar
- Liang YK, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15:1201–1206PubMedCrossRefGoogle Scholar
- McCarthy RL, Zhong R, Ye ZH (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol 50:1950–1964PubMedCrossRefGoogle Scholar
- McCarthy RL, Zhong R, Fowler S, Lyskowski D, Piyasena H, Carleton K, Spicer C, Ye ZH (2010) The poplar MYB transcription factors, PtrMYB3 and PtrMYB20, are involved in the regulation of secondary wall biosynthesis. Plant Cell Physiol 51:1084–1090PubMedCrossRefGoogle Scholar
- Mellerowicz EJ, Sundberg B (2008) Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol 11:293–300PubMedCrossRefGoogle Scholar
- Meyer K, Shirley AM, Cusumano JC, Bell-Lelong DA, Chapple C (1998) Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc Natl Aca Sci USA 95:6619–6623CrossRefGoogle Scholar
- Newman LJ, Perazza DE, Juda L, Campbell MM (2004) Involvement of the R2R3-MYB, AtMYB61, in the ectopic lignification and dark-photomorphogenic components of the det3 mutant phenotype. Plant J 37:239–250PubMedCrossRefGoogle Scholar
- Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterization of a pine MYB that regulates lignification. Plant J 36:743–754PubMedCrossRefGoogle Scholar
- Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071PubMedCentralPubMedCrossRefGoogle Scholar
- Ralph J, Akiyama T, Kim H (2006) Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J Biol Chem 281(13):8843–8853PubMedCrossRefGoogle Scholar
- Ro DK, Mah N, Ellis BE, Douglas CJ (2001) Functional characterization and subcellular localization of poplar (Populus trichocarpa × Populus deltoides) cinnamate 4-hydroxylase. Plant Physiol 126:317–329PubMedCentralPubMedCrossRefGoogle Scholar
- Romano JM, Dubos C, Prouse MB, Wilkins O, Hong H, Poole M, Kang KY, Li E, Douglas CJ, Western TL, Mansfield SD, Campbell MM (2012) AtMYB61, an R2R3-MYB transcription factor, functions as a pleiotropic regulator via a small gene network. New Phytol 195:774–786PubMedCrossRefGoogle Scholar
- Sall J, Lehman A, Creighton L (1996) JMP start statistics: a guide to statistical and data analysis using JMP and JMP IN software. Duxbury Press, New YorkGoogle Scholar
- Sibout R, Eudes A, Mouille G, Pollet B, Lapierre C, Jouanin L, Séguin A (2005) Cinnamyl alcohol dehydrogenase-C and-D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell 17:2059–2076PubMedCentralPubMedCrossRefGoogle Scholar
- Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172:47–62PubMedCrossRefGoogle Scholar
- Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
- Van Soest PJ, Wine RH (1967) Use of detergents in the analysis of fibrous feeds. IV. Determination of plant cell-wall constituents. J Assoc Off Anal Chem 50:50–55Google Scholar
- Voelker SL, Lachenbruch B, Meinzer FC, Kitin P, Strauss SH (2010) Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar. Plant Physiol 154(2):874–886PubMedCentralPubMedCrossRefGoogle Scholar
- Wagner A, Ralph J, Akiyama T (2007) Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyltransferase in Pinus radiata. Proc Natl Aca Sci USA 104(28):11856–11861CrossRefGoogle Scholar
- Wang J, Wang CL, Zhu ML, Yu Y, Zhang YB, Wei ZM (2008) Generation and characterization of transgenic poplar plants overexpressing a cotton laccase gene. Plant Cell Tiss Organ Cult 93:303–310CrossRefGoogle Scholar
- Wang H, Avci U, Nakashima J, Hahn MG, Chen F, Dixon RA (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci USA 107:22338–22343PubMedCentralPubMedCrossRefGoogle Scholar
- Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993PubMedCentralPubMedCrossRefGoogle Scholar
- Zaragoza MV, Lewis LE, Sun G, Wang E, Li L, Said-Salman I, Feucht L, Huang T (2004) Identification of the TBX5 transactivating domain and the nuclear localization signal. Gene 330:9–18PubMedCrossRefGoogle Scholar
- Zeng SH, Liu YL, Zou CY, Huang WJ, Wang Y (2013) Cloning and characterization of phenylalanine ammonia-lyase in medicinal Epimedium species. Plant Cell Tiss Organ Cult 113:257–267CrossRefGoogle Scholar
- Zhang J, Elo A, Helariutta Y (2011) Arabidopsis a model for wood formation. Curr Opin Biotechnol 22:293–299PubMedCrossRefGoogle Scholar
- Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16:227–233PubMedCrossRefGoogle Scholar
- Zhong R, Peña MJ, Zhou GK, Richardson EA, O’Neill MA, Darvill AG, York WS, Ye ZH (2005) Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell 17:3390–3408PubMedCentralPubMedCrossRefGoogle Scholar
- 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 19:2776–2792PubMedCentralPubMedCrossRefGoogle Scholar
- Zhong R, Lee C, Ye ZH (2010) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol 152:1044–1055PubMedCentralPubMedCrossRefGoogle Scholar
- Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye ZH (2013) The poplar MYB master switches bind to the SMRE site and activate the secondary wall biosynthetic program during wood formation. PLoS ONE 8:e69219PubMedCentralPubMedCrossRefGoogle Scholar
- Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21(1):248–266PubMedCentralPubMedCrossRefGoogle Scholar