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TaDIR13, a Dirigent Protein from Wheat, Promotes Lignan Biosynthesis and Enhances Pathogen Resistance

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Abstract

Dirigent is proposed to be involved in either lignan or lignin biosynthesis. In the present study, sequences for dirigent and dirigent-like proteins from the wheat genome were analyzed. We obtained wheat dirigent (TaDIR13), and dirigent-like (TaDIR4 and TaJA1) recombinant proteins used for biochemical assays. It was shown that TaDIR13 could effectively direct coniferyl alcohol coupling into (+)-pinoresinol. In contrast, TaDIR4 and TaJA1 did not exhibit this activity. In accordance with this role of TaDIR13, overexpression of TaDIR13 in transgenic tobacco increased total lignan accumulation. Lignan extracts from TaDIR13 transgenic plants had enhanced antibacterial effects to Pseudomonas syringae. Furthermore, these plants did show strong resistance to P. syringae and Phytophthora parasitica. On the contrary, TaDIR4 transgenics did not show noticeable changes in either lignan accumulation or pathogen resistance. Overexpression of TaJA1 did not increase lignan accumulation either. Unlike TaDIR4 plants though, TaJA1 plants exhibited high pathogen resistance; yet, this was achieved through its jacalin-related lectins domain and not its dirigent domain. Lignin content and gene expression were not affected in all transgenic plants. Interestingly, expression of the pinoresinol-lariciresinol reductase gene (NtPLR) was increased in TaDIR13 transgenic plant; this is apparently owing to a favored metabolic flux from coniferyl alcohol into the lignan pathway. These data collectively suggest that TaDIR13 is mainly involved in regulating lignan biosynthesis which, in turn, responsible for the observed roles in pathogen resistance. TaDIR4 and TaJA1, both being dirigent-like proteins, have little functional overlap with dirigent proteins.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman JD (1997) Gapped Blast and PSI-Blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • An G, Watson BG, Stachel S, Gordon MP, Nester EW (1985) New cloning vehicles for transformation of higher plants. EMBO J 4:277–284

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ayella AK, Trick HN, Wang W (2007) Enhancing lignan biosynthesis by over-expressing pinoresinol lariciresinol reductase in transgenic wheat. Mol Nutr Food Res 51:1518–1526

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–63

    Article  CAS  PubMed  Google Scholar 

  • Casu RE, Dimmock CM, Chapman SC, Grof CPL, McIntyre CL, Bonnett GD, Manners JM (2004) Identification of differentially expressed transcripts from maturing stem of sugarcane by in silico analysis of stem expressed sequence tags and gene expression profiling. Plant Mol Biol 54:503–517

    Article  PubMed  Google Scholar 

  • Chen Y, Shi Z-W, Huang X-M (2010) Ultrasonic assisted extraction of total lignans and its content analysis in soybeans. Soybean Sci 29:168–170

    Article  Google Scholar 

  • Damaj MB, Kumpatla SP, Emani C, Emani C, Beremand PD, Reddy AS, Rathore KS, Buenrostro-Nava MT, Curtis IS, Thomas TL, Mirkov TK (2010) Sugarcane dirigent and O-methyltransferase promoters confer stem-regulated gene expression in diverse monocots. Planta 231:1439–1458

    Article  CAS  PubMed  Google Scholar 

  • Davin LB, Lewis NG (2003) An historical perspective on lignan biosynthesis: monolignol, allylphenol and hydroxycinnamic acid coupling and downstream metabolism. Phytochem Rev 2:257–288

    Article  CAS  Google Scholar 

  • Davin LB, Wang H-B, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275:362–366

    Article  CAS  PubMed  Google Scholar 

  • Davin LB, Jourdes M, Patten AM, Kim K-W, Vassaǒ DG, Lewis NG (2008) Dissection of lignin macromolecular configuration and assembly: comparison to related biochemical processes in allyl/propenyl phenol and lignan biosynthesis. Nat Prod Rep 25:1015–1090

    Article  CAS  PubMed  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gang DR, Costa MA, Fujita M, Dinkova-Kostova AT, Wang H-B, Burlat V, Martin W, Sarkanen S, Davin LB, Lewis NG (1999) Regiochemical control of monolignol radical coupling: a new paradigm for lignin and lignan biosynthesis. Chem Biol 6:143–151

    Article  CAS  PubMed  Google Scholar 

  • Geng S, Hills FG (1989) Biometrics in agriculture science. Kendell Hunt Publisher, Dubuque

    Google Scholar 

  • Guo Z-J, Chen X-J, Wu X-L, Ling J-Q, Xu P (2004) Overexpression of the AP2/EREBP transcription factor OPBP1 enhances disease resistance and salt tolerance in tobacco. Plant Mol Biol 55:607–618

    Article  CAS  PubMed  Google Scholar 

  • Hano C, Martin I, Fliniaux O, Legrand B, Gutierrez L, Arroo RRJ, Mesnard F, Lamblin F, Lainé E (2006) Pinoresinol–lariciresinol reductase gene expression and secoisolariciresinol diglucoside accumulation in developing flax (Linum usitatissimum) seeds. Planta 224:1291–1301

    Article  CAS  PubMed  Google Scholar 

  • Harmatha J, Dinan L (2003) Biological activities of lignans and stilbenoids associated with plant-insect chemical interaction. Phytochem Rev 2:321–330

    Article  CAS  Google Scholar 

  • Kim HJ, Ono E, Morimoto K, Yamagaki T, Okazawa A, Kobayashi A, Satake H (2009) Metabolic engineering of lignan biosynthesis in Forsythia cell culture. Plant Cell Physiol 50:2200–2209

    Article  CAS  PubMed  Google Scholar 

  • Kirk TK, Obst JR (1988) Lignin determination. Methods Enzymol 161:87–101

    Article  CAS  Google Scholar 

  • Lewis NG (1999) A 20th century roller coaster ride: a short account of lignification. Curr Opin Plant Biol 2:153–162

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Li J, Jiang X-J, Zhang K-F, Duan X-Q (2011) Content determination of lignans in Kadsura coccinea (Lem.) A. C. Smith. J Anhui Agri Sci 39:12152–12153

    Google Scholar 

  • Ma Q-H (2013) Monocot chimeric jacalins: a novel subfamily of plant lectins. Crit Rev Biotechnol. doi:10.3109/07388551.2013.793650

    PubMed  Google Scholar 

  • Ma Q-H, Tian B (2005) Biochemical characterization of a cinnamoyl-CoA reductase from wheat. Biol Chem 386:553–560

    Article  CAS  PubMed  Google Scholar 

  • Ma Q-H, Wang X-M, Wang Z-M (2008) Expression of isopentenyl transferase gene controlled by seed-specific lectin promoter in transgenic tobacco influences seed development. J Plant Growth Regul 27:68–76

    Article  CAS  Google Scholar 

  • Ma Q-H, Tian B, Li Y-L (2010) Overexpression of a wheat jasmonate-regulated lectin increases pathogen resistance. Biochimie 92:187–193

    Article  CAS  PubMed  Google Scholar 

  • Ma Q-H, Wang C, Zhu H-H (2011) TaMYB4 cloned from wheat regulates lignin biosynthesis through negatively controlling the transcripts of both cinnamyl alcohol dehydrogenase and cinnamoyl-CoA reductase genes. Biochimie 93:1179–1186

    Article  CAS  PubMed  Google Scholar 

  • Ma Q-H, Zhen W-B, Liu Y-C (2013) Jacalin domain in wheat jasmonate-regulated protein Ta-JA1 confers agglutinating activity and pathogen resistance. Biochimie 95:359–365

    Article  CAS  PubMed  Google Scholar 

  • Nakatsubo T, Mizutani M, Suzuki S, Hattori T, Umezawa T (2008) Characterization of Arabidopsis thaliana pinoresinol reductase, a new type of enzyme involved in lignan biosynthesis. J Biol Chem 283:15550–15557

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Önnerud H, Zhang L, Gellerstedt G, Henriksson G (2002) Polymerization of monolignols by redox shuttle-mediated enzymatic oxidation: a new model in lignin biosynthesis I. Plant Cell 14:1953–1962

    Article  PubMed Central  PubMed  Google Scholar 

  • Ralph SG, Park JY, Bohlmann J, Mansfield SD (2006) Dirigent proteins in conifer defense: gene discovery, phylogeny, and differential wound- and insect-induced expression of a family of DIR and DIR-like genes in spruce (Picea spp.). Plant Mol Biol 60:21–40

    Article  CAS  PubMed  Google Scholar 

  • Ralph SG, Jancsik S, Bohlmann J (2007) Dirigent proteins in conifer defense II: Extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry 68:1975–1991

    Article  CAS  PubMed  Google Scholar 

  • Schroeder FC, Del Campo ML, Grant JB, Weibel DB, Smedley SR, Bolton KL, Meinwald J, Eisner T (2006) Pinoresinol: a lignol of plant origin serving for defense in a caterpillar. Proc Natl Acad Sci U S A 103:15497–15501

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sederoff RR, MacKay JJ, Ralph J, Hatfield RD (1999) Unexpected variation in lignin. Curr Opin Plant Biol 2:145–152

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Umezawa T (2007) Biosynthesis of lignans and norlignans. J Wood Sci 53:273–284

    Article  CAS  Google Scholar 

  • Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang X-M, Ma Q-H (2005) Characterization of a jasmonate-regulated wheat protein related to a beta-glucosidase-aggregating factor. Plant Physiol Biochem 43:185–192

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Nowak G, Culley D, Hadwiger LA, Fristensky B (1999) Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). Mol Plant-Microbe Interact 12:410–418

    Article  CAS  Google Scholar 

  • Wu R, Wang L, Wang Z, Shang H, Liu X, Zhu Y, Qi D, Deng X (2009) Cloning and expression analysis of a dirigent protein gene from the resurrection plant Boea hygrometrica. Prog Nat Sci 19:347–352

    Article  CAS  Google Scholar 

  • Zheng J, Li H, Ding CX, Suo YR, Wang LS, Wan HL (2011) Anthocyanins composition and antioxidant activity of two major wild Nitraria tangutorun Bobr. variations from Qinghai–Tibet Plateau. Food Res Int 44:2041–2046

    Article  CAS  Google Scholar 

  • Zhu L, Zhang X, Tu L, Zeng F, Nie Y, Guo X (2007) Isolation and characterization of two novel dirigent-like genes highly induced in cotton (Gossypium barbadense and G. hirsutum) after infection by Verticillium dahliae. J Plant Pathol 89:41–45

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (No. 31170277, No. 31370336, and No. 31070235), the Natural Science Foundation of Beijing (No. 5122024), and the Innovation Project of Chinese Academy of Sciences.

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  1. Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, 20 Nanxincun, Xiangshan, Beijing, 100093, China

    Qing-Hu Ma & Yun-Chao Liu

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Correspondence to Qing-Hu Ma.

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Ma, QH., Liu, YC. TaDIR13, a Dirigent Protein from Wheat, Promotes Lignan Biosynthesis and Enhances Pathogen Resistance. Plant Mol Biol Rep 33, 143–152 (2015). https://doi.org/10.1007/s11105-014-0737-x

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