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Identification and characterization of a wood-associated NAC domain transcription factor PtoVNS11 from Populus tomentosa Carr.

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Here, we isolated a NAC transcription factor PtoVNS11 from Populus tomentosa Carr. Molecular characterization showed that PtoVNS11 was involved in the regulation of secondary cell wall formation in poplar.

Abstract

NAC domain transcription factors are important regulators that activate the secondary wall biosynthesis in wood formation. In this study, we isolated a NAC domain transcription factor PtoVNS11 from Populus tomentosa Carr. PtoVNS11 shares high identity with SND1 of Arabidopsis thaliana (59.6 %) and PtrWND1B (97.9 %) of P. trichocarpa. Gene expression analyses showed that PtoVNS11 gene was mainly accumulated in xylem and stem of poplar. Further, GUS expression driven by the PtoVNS11 promoter was observed in vascular tissues of vegetative and reproductive organs in transgenic Arabidopsis. Promoter deletion analysis revealed that the fragment (−283 to −171) with the secondary wall NAC-binding element was required for tissue-specific expression of the PtoVNS11 gene. Subcellular localization analysis showed that PtoVNS11:GFP fusion protein was localized in the nucleus. Transgenic poplar plants carrying 35S:PtoVNS11 exhibited dwarf phenotypes with shorter internode as compared to wild-type plants. PtoVNS11 overexpression resulted in massive deposition of lignin and increased thickening of secondary walls in transgenic poplar. Transcription analysis showed that the expression levels of many wood-associated genes were up-regulated in transgenic plants overexpressing PtoVNS11. Taken together, our results indicate that PtoVNS11 may be involved in the regulation of the secondary wall biosynthesis during wood formation in poplar.

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References

  • Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165

    Article  PubMed  Google Scholar 

  • 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 7:17

    Article  PubMed Central  PubMed  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev plant Biol 54:519–546

    Article  CAS  PubMed  Google Scholar 

  • Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JE, Blais S, Tremblay L, Morency MJ, Pavy N (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59:3925–3939

    Article  CAS  PubMed Central  PubMed  Google 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 150:1111–1121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567

    Article  CAS  PubMed  Google Scholar 

  • Hisano H, Nandakumar R, Wang ZY (2009) Genetic modification of lignin biosynthesis for improved biofuel production. In Vitro Cell Dev Biol-Plant 45:306–313

    Article  CAS  Google Scholar 

  • Hofgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145

    Article  PubMed Central  PubMed  Google Scholar 

  • Hussey SG, Saïdi MN, Hefer C, Myburg AA, Grima-Pettenati J (2014) Structural, evolutionary and functional analysis of the NAC domain protein family in Eucalyptus. New Phytol. doi:10.1111/nph.13139

    PubMed  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jia Z, Sun Y, Yuan L, Tian Q, Luo KM (2010) The chitinase gene (Bbchit1) from Beauveria bassiana enhances resistance to Cytospora chrysosperma in Populus tomentosa Carr. Biotechnol Lett 32:1325–1332

    Article  CAS  PubMed  Google Scholar 

  • Karpinska B, Karlsson M, Srivastava M, Stenberg A, Schrader J, Sterky F, Bhalerao R, Wingsle G (2004) MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen. Plant Mol Biol 56:255–270

    Article  CAS  PubMed  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, DemuraT (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860

  • Lee C, Teng Q, Zhong R, Ye ZH (2011) Molecular dissection of xylan biosynthesis during wood formation in poplar. Mol Plant 4:730–747

    Article  CAS  PubMed  Google Scholar 

  • Li L, Osakabe Y, Joshi CP, Chiang VL (1999) Secondary xylem-specific expression of caffeoyl-coenzyme A 3-O-methyltransferase plays an important role in the methylation pathway associated with lignin biosynthesis in loblolly pine. Plant Mol Biol 40:555–565

    Article  CAS  PubMed  Google Scholar 

  • Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 100:4939–4944

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Q, Lin YC, Sun YH, Song J, Chen H, Zhang XH, Sederoff RR, Chiang VL (2012) Splice variant of the SND1 transcription factor is a dominant negative of SND1 members and their regulation in Populus trichocarpa. Proc Natl Acad Sci USA 109:14699–14704

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lloyd G, McCown B (1980) Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot tip culture. In: Combined proceedings—International Plant Propagators’ Society, USA, vol 30, pp 421–427

  • Luo K, Zheng X, Chen Y, Xiao Y, Zhao D, McAvoy R, Pei Y, Li Y (2006) The maize Knotted1 gene is an effective positive selectable marker gene for Agrobacterium-mediated tobacco transformation. Plant Cell Rep 25:403–409

    Article  CAS  PubMed  Google 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 51:1084–1090

    Article  CAS  PubMed  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ni W, Paiva NL, Dixon RA (1994) Reduced lignin in transgenic plants containing a caffeic acidO-methyltransferase antisense gene. Transgenic Res 3:120–126

    Article  CAS  Google Scholar 

  • Ohtani M, Nishikubo N, Xu B, Yamaguchi M, Mitsuda N, Goué N, Shi F, Ohme-Takagi M, Demura T (2011) A NAC domain protein family contributing to the regulation of wood formation in poplar. Plant J 67:499–512

    Article  CAS  PubMed  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  CAS  PubMed  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

  • Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754

    Article  CAS  PubMed  Google Scholar 

  • Plomion C, Leprovost G, StokesA (2001) Wood formation in trees. Plant Physiol 127:1513–1523

  • Prassinos C, Ko JH, Yang J, Han KH (2005) Transcriptome profiling of vertical stem segments provides insights into the genetic regulation of secondary growth in hybrid aspen trees. Plant Cell Physiol 46:1213–1225

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning, a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M, Sandberg G (2004) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16:2278–2292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen H, Yin Y, Chen F, Xu Y, Dixon RA (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. BioEnerg Res 2:217–232

    Article  Google Scholar 

  • Shi R, Sun YH, Li Q, Heber S, Sederoff R, Chiang VL (2009) Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol 51:144–163

    Article  PubMed  Google Scholar 

  • Tian QY, Wang XQ, Li CF, Lu WX, Yang L, Jiang YZ, Luo KM (2013) Functional characterization of the poplar R2R3-MYB transcription factor PtoMYB216 involved in the regulation of lignin biosynthesis during wood formation. PLoS One 8:e76369

    Article  CAS  PubMed Central  PubMed  Google 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 172:47–62

    Article  CAS  PubMed  Google Scholar 

  • Wang HH, Tang RJ, Liu H, Chen HY, Liu JY, Jiang XN, Zhang HX (2013a) Chimeric repressor of PtSND2 severely affects wood formation in transgenic Populus. Tree Physiol 33:878–886

    Article  PubMed  Google Scholar 

  • Wang Z, Zhang H, Yang J, Chen Y, Xu X, Mao X, Li C (2013b) Phylogenetic, expression, and bioinformatic analysis of the ABC1 gene family in populus trichocarpa. Sci World J 2013:1–11

    Google Scholar 

  • Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16:227–233

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Sun J, Xu P, Zhang R, Li L (2014) Intron-mediated alternative splicing of PtrWND1B regulates cell wall thickening during fiber development in Populus. Plant Physiol 164:765–776

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Ye ZH (2007) Regulation of cell wall biosynthesis. Curr Opin Plant Biol 10:564–572

    Article  CAS  PubMed  Google Scholar 

  • 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. 18:3158–3170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Lee C, Ye ZH (2010) Functional characterization of poplar wood-associated NAC domain transcription factors. Plant Physiol 152:1044–1055

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, McCarthy RL, Lee C, Ye ZH (2011) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physio 157:1452–1468

    Article  CAS  Google Scholar 

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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), and the Fundamental Research Funds for the Central Universities (XDJK2014a005).

Conflict of interest

The authors declare that they have no conflict of interest.

Author contribution statement

Conceived and designed the experiments: LY ST KL. Performed the experiments: LY XZ WL. Analyzed the data: KL WL LY. Contributed reagents/materials/analysis tools: WL LY YF. Wrote the paper: KL LY ST.

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    Authors and Affiliations

    1. Key Laboratory of Eco-environments of Three Gorges Reservoir Region, Ministry of Education, Chongqing Key Laboratory of Transgenic Plant and Safety Control, Institute of Resources Botany, School of Life Sciences, Southwest University, No. 1, Tiansheng Road, Beibei, Chongqing, 400715, China

      Li Yang, Yisu Hou, Xin Zhao, Yongli Li, Fan Yang, Shaohu Tang & Keming Luo

    2. College of Horticulture and Landscape Architecture, Southwest University, Chongqing, 400716, China

      Wanxiang Lu

    3. Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810008, China

      Keming Luo

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    Correspondence to Shaohu Tang or Keming Luo.

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    Communicated by F. Canovas.

    L. Yang and Y. Hou contributed equally to this work.

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    Yang, L., Hou, Y., Zhao, X. et al. Identification and characterization of a wood-associated NAC domain transcription factor PtoVNS11 from Populus tomentosa Carr.. Trees 29, 1091–1101 (2015). https://doi.org/10.1007/s00468-015-1188-1

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