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Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors

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Abstract

The maize (Zea mays L.) caffeic acid O-methyl-transferase (COMT) is a key enzyme in the biosynthesis of lignin. In this work we have characterized the involvement of COMT in the lignification process through the study of the molecular mechanisms involved in its regulation. The examination of the maize COMT gene promoter revealed a putative ACIII box, typically recognized by R2R3-MYB transcription factors. We used the sequence of known R2R3-MYB factors to isolate five maize R2R3-MYB factors (ZmMYB2, ZmMYB8, ZmMYB31, ZmMYB39, and ZmMYB42) and study their possible roles as regulators of the maize COMT gene. The factors ZmMYB8, ZmMY31, and ZmMYB42 belong to the subgroup 4 of the R2R3-MYB family along with other factors associated with lignin biosynthesis repression. In addition, the induction pattern of ZmMYB31 and ZmMYB42 gene expression on wounding is that expected for repressors of the maize COMT gene. Arabidopsis thaliana plants over-expressing ZmMYB31 and ZmMYB42 down-regulate both the A. thaliana and the maize COMT genes. Furthermore, the over-expression of ZmMYB31 and ZmMYB42 also affect the expression of other genes of the lignin pathway and produces a decrease in lignin content of the transgenic plants.

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References

  • Anterola AM, Lewis NG (2002) Trends in lignin modifications: a comprehensive analysis of the effects of genetics manipulations/mutations on lignification and vascular integrity. Phytochemistry 61:221–294

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Boudet AM, Kajita S, Grima-Pettenati J, Goffner D (2003) Lignins and lignocellulosics: a better control of synthesis for new and improved uses. Trends Plant Sci 8:576–581

    Article  PubMed  CAS  Google Scholar 

  • Bugos RC, Chiang VL, Campbell WH (1991) cDNA cloning, sequence analysis and seasonal expression of lignin-bispecific caffeic acid/5-hydroxyferulic acid O-methyltransferase of aspen. Plant Mol Biol 17:1203–1215

    Article  PubMed  CAS  Google Scholar 

  • Caparrós-Ruiz D, Fornalé S, Civardi L, Puigdomènech P, Rigau J (2006) Isolation and characterisation of a family of laccases in maize. Plant Sci 171:217–225

    Article  Google Scholar 

  • Capellades M, Torres MA, Bastisch I, Stiefel V, Vignols F, Bruce WB, Peterson D, Puigdomenech P, Rigau J (1996) The maize caffeic acid O-methyltransferase gene promoter is active in transgenic tobacco and maize plant tissues. Plant Mol Biol 31:307–332

    Article  PubMed  CAS  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    PubMed  CAS  Google Scholar 

  • Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6:325–330

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Collazo P, Montoliu L, Puigdomènech P, Rigau J (1992) Structure and expression of the lignin O-methyltransferase gene from Zea mays L. Plant Mol Biol 20:857–867

    Article  PubMed  CAS  Google Scholar 

  • Cone KC, Cocciolone SM, Burr FA, Burr B (1993) Maize anthocyanin regulatory gene pI is a duplicate of c1 that functions in the plant. Plant Cell 5:1795–1805

    Article  PubMed  CAS  Google Scholar 

  • de Obeso M, Caparrós-Ruiz D, Vignols F, Puigdomènech P, Rigau J (2003) Characterisation of maize peroxidases having differential patterns of mRNA accumulation in relation to lignifying tissues. Gene 309:23–33

    Article  PubMed  CAS  Google Scholar 

  • Douglas CJ (1996) Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends Plant Sci 1:171–178

    Article  Google Scholar 

  • Feuillet C, Lauvergeat V, Deswarte C, Pilate G, Boudet A, Grima-Pettenati J (1995) Tissue- and cell-specific expression of a cinnamyl alcohol dehydrogenase promoter in transgenic poplar plants. Plant Mol Biol 27:651–667

    Article  PubMed  CAS  Google Scholar 

  • Franken P, Schrell S, Peterson PA, Saedler H, Wienand U (1989) Molecular analysis of protein domain function encoded by the myb-homologous maize genes C1, Zm 1 and Zm 38. Plant J 6:21–30

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grotewold E, Athma P, Peterson T (1991) Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proc Natl Acad Sci USA 88:4587–4591

    Article  PubMed  CAS  Google Scholar 

  • Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33(Web Server issue):W557–W559

    Article  PubMed  CAS  Google Scholar 

  • Halpin C, Holt K, Chojecki J, Olivier D, Chabbert B, Monties B, Edwards K, Barakate A, Foxon GA (1998) Brown-midrib maize (bm1): a mutation affecting cinnamyl alcohol dehydrogenase gene. Plant J 14:545–553

    Article  PubMed  CAS  Google Scholar 

  • Hauffe KD, Lee SP, Subramaniam R, Douglas CJ (1993) Combinatorial interactions between positive and negative cis-acting elements control spatial patterns of 4CL-1 expression in transgenic tobacco. Plant J 4:235–253

    Article  PubMed  CAS  Google Scholar 

  • Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000a) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832

    Article  CAS  Google Scholar 

  • Hellens R, Mullineaux P, Klee H (2000b) A guide to Agrobacterium binary Ti vectors. Trends Plant Sci 5:446–451

    Article  CAS  Google Scholar 

  • Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensibility of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. Plant J 26:205–216

    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 Bio l56:255–270

    Article  Google Scholar 

  • Kranz HD, Denekamp M, Greco R, Jin H, Leyva A, Meissner RC, Petroni K, Urzainqui A, Bevan M, Martin C, Smeekens S, Tonelli C, Paz-Ares J, Weisshaar B (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263–76

    Article  PubMed  CAS  Google Scholar 

  • Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–496

    Article  PubMed  CAS  Google Scholar 

  • Marocco A, Wissenbach M, Becker D, Paz-Ares J, Saedler H, Salamini F, Rohde W (1989) Multiple genes are transcribed in Hordeum vulgare and Zea mays that carry the DNA binding domain of the myb oncoproteins. Mol Gen Genet 216:183–187

    Article  PubMed  CAS  Google Scholar 

  • Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47:239–274

    Article  PubMed  CAS  Google Scholar 

  • Miyake K, Ito T, Senda M, Ishikawa R, Harada T, Niizeki M, Akada S (2003) Isolation of a subfamily of genes for R2R3-MYB transcription factors showing up-regulated expression under nitrogen nutrient-limited conditions. Plant Mol Biol 53:237–245

    Article  PubMed  CAS  Google Scholar 

  • Morrow MP, Mascia P, Self KP, Altschuler M (1997) Molecular characterization of a brown midrib deletion mutation in maize. Mol Breed 3:351–357

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Patzlaff A, Newman LJ, Dubos C, Whetten RW, Smith C, McInnis S, Bevan MW, Sederoff RR, Campbell MM (2003a) Characterisation of Pt MYB1, an R2R3-MYB from pine xylem. Plant Mol Biol 53:597–608

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1987) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6:3553–3558

    PubMed  CAS  Google Scholar 

  • Piquemal J, Chamayou S, Nadaud I, Beckert M, Barriere Y, Mila I, Lapierre C, Rigau J, Puigdomènech P, Jauneau A, Digonnet C, Boudet AM, Goffner D, Pichon M (2002) Down-regulation of caffeic acid o-methyltransferase in maize revisited using a transgenic approach. Plant Physiol 130:1675–1685

    Article  PubMed  CAS  Google Scholar 

  • Pilu R, Piazza P, Petroni K, Ronchi A, Martin C, Tonelli C (2003) pl-bol3, a complex allele of the anthocyanin regulatory pl1 locus that arose in a naturally occurring maize population. Plant J 36:510–521

    Article  PubMed  CAS  Google Scholar 

  • Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995

    Article  PubMed  CAS  Google 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 133:1051–1071

    Article  PubMed  CAS  Google Scholar 

  • Reichel C, Mathur J, Eckes P, Langenkemper K, Koncz C, Schell J, Reiss B, Maas C (1996) Enhanced green fluorescence by the expression of an Aequorea Victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proc Natl Acad Sci USA 93:5888–5893

    Article  PubMed  CAS  Google Scholar 

  • 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 14:273–284

    Article  PubMed  CAS  Google Scholar 

  • Sablowski RW, Moyano E, Culianez-Macia FA, Schuch W, Martin C, Bevan M (1994) A flower-specific Myb protein activates transcription of phenylpropanoid biosynthetic genes. EMBO J 13:128–37

    PubMed  CAS  Google Scholar 

  • Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K, Martin C (1998a) The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10:135–54

    Article  CAS  Google Scholar 

  • Tamagnone L, Merida A, Stacey N, Plaskitt K, Parr A, Chang CF, Lynn D, Dow JM, Roberts K, Martin C (1998b) Inhibition of phenolic acid metabolism results in precocious cell death and altered cell morphology in leaves of transgenic tobacco plants. Plant Cell 10:1801–16

    Article  CAS  Google Scholar 

  • Vignols F, Rigau J, Torres MA, Capellades M, Puigdomenech P (1995) The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7:407–416

    Article  PubMed  CAS  Google Scholar 

  • Vignols F, José-Estanyol M, Caparrós-Ruiz D, Rigau J, Puigdomènech P (1999) Involvement of a maize proline-rich protein in secondary cell wall formation as deduced from its specific mRNA localisation. Plant Mol Biol 39:945–952

    Article  PubMed  CAS  Google Scholar 

  • Whetten RW, MacKay JJ, Sederoff RR (1998) Recent advances in understanding lignin biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 49:585–609

    Article  PubMed  CAS  Google Scholar 

  • Whitmore FW (1978) Lignin-carbohydrate complex formed in isolated cell walls of callus. Phytochemistry 17:421–425

    Article  CAS  Google Scholar 

  • Ye ZH, Kneusel RE, Matern U, Varner JE (1994) An alternative methylation pathway in lignin biosynthesis in Zinnia. Plant Cell 6:1427–1439

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are indebted to Dr. Sheen (MGH, USA) for kindly providing us with the synthetic GFP (sGFP) as well as the John Innes Center (Norwich, UK) for providing us with the pGREENII-0029 vector. We want to thank Dr. Piulachs (IBMB-CSIC) for her advice and comments on the phylogenetic analyses performed in this work and Dr. Pons for the confocal microscopy analyses. We are also indebted to the sequencing and greenhouse teams of IBMB-CSIC, as well as Dr. Burgess for the English correction of this manuscript. This work was funded by the Spanish “Ministerio de Ciencia y Tecnología” (BIO2001-1140). S-F was financed by a post-doctoral grant from the Autonomous Government of Catalonia (2003PIV-A-00033). F.M-S was financed by the European Project INCO-II (ICA4-CT-2000-30017) and by the “Consorci CSIC-IRTA” laboratory. T-M was financed by the European Project MapMaize (PL 962312). D-C.R was financed by the Spanish “Ministerio de Ciencia y Tecnología” (“Ramón y Cajal” Program). This work was carried out within the framework of the “Centre de Referència de Biotecnologia” (CERBA) from the Autonomous Government of Catalonia.

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Correspondence to Joan Rigau.

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Fornalé, S., Sonbol, FM., Maes, T. et al. Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors. Plant Mol Biol 62, 809–823 (2006). https://doi.org/10.1007/s11103-006-9058-2

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