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Structure of the cinnamyl-alcohol dehydrogenase gene family in rice and promoter activity of a member associated with lignification

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Abstract

Analysis of lignification in rice has been facilitated by the availability of the recently completed rice genome sequence, and rice will serve as an important model for understanding the relationship of grass lignin composition to cell wall digestibility. Cinnamyl-alcohol dehydrogenase (CAD) is an enzyme important in lignin biosynthesis. The rice genome contains 12 distinct genes present at nine different loci that encode products with significant similarity to CAD. The rice gene family is diverse with respect to other angiosperm and gymnosperm CAD genes isolated to date and includes one member (OsCAD6) that contains a peroxisomal targeting signal and is substantially diverged relative to other family members. Four closely related family members (OsCAD8A–D) are present at the same locus and represent the product of a localized gene duplication and inversion. Promoter-reporter gene fusions to OsCAD2, an orthologue of the CAD gene present at the bm1 (brown midrib 1) locus of maize, reveal that in rice expression is associated with vascular tissue in aerial parts of the plant and is correlated with the onset of lignification. In root tissue, expression is primarily in the cortical parenchyma adjacent to the exodermis and in vascular tissue.

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References

  • Altschul SF, Gish W, Miller W, Myers E, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Baker AJ (1983) Wood fuel properties and fuel products from woods. In: Proceedings. Fuel wood management and utilization seminar. Michigan State University, East Lansing, Mich., 152:14–25

  • Baucher M, Chabbert B, Pilate G, Van Doorsselaere J, Tollier MT, Petit-Conil M, Cornu D, Monties B, Van Montagu M, Inze D, Jouanin L, Boerjan W (1996) Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol 112:1479–1490

    Google Scholar 

  • Baucher M, Bernard-Vailhe MA, Chabbert B, Besle JM, Opsomer C, Van Montagu M, Botterman J (1999) Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility. Plant Mol Biol 39:437–447

    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 

  • Buxton DR, Russell JR (1988) Lignin constituents and cell-wall digestibility of grass and legume stems. Crop Sci 28:553–558

    CAS  Google Scholar 

  • Carver TLW, Zeyen RJ, Bushnell WR, Robbins MP (1994) Inhibition of phenylalanine ammonia lyase and cinnamyl alcohol dehydrogenase increases quantitative susceptibility of barley to powdery mildew (Erysiphe graminis D.C.). Physiol Mol Plant Pathol 44:261–272

    CAS  Google Scholar 

  • Chen L, Auh C-K, Dowling P, Bell J, Chen F, Hopkins A, Dixon RA, Wang Z-Y (2003) Improved forage digestibility of tall fescue (Festuca arundinacea) by transgenic down-regulation of cinnamyl alcohol dehydrogenase. Plant Biotechnol J 1:437–449

    Article  CAS  Google Scholar 

  • Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689

    CAS  PubMed  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    CAS  PubMed  Google Scholar 

  • Costa MA, Collins RE, Anterola AM, Cochrane FC, Davin LB, Lewis NG (2003) An in silico assessment of gene function and organization of the phenylpropanoid pathway metabolic networks in Arabidopsis thaliana and limitations thereof. Phytochemistry 64:1097–1112

    Article  CAS  PubMed  Google Scholar 

  • Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective and adaptive system for expressing rice development. Crop Sci 40:436–443

    Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNA from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002

    CAS  PubMed  Google Scholar 

  • Greene B, Walko R, Hake S (1994) Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics 138:1275–1285

    CAS  PubMed  Google Scholar 

  • Gregg D, Saddler JN (1996) A techno-economic assessment of the pretreatment and fractionation steps of a biomass-to-ethanol process. Appl Biochem Biotechnol 57/58:711–727

    Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    CAS  PubMed  Google Scholar 

  • Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet AM, Boon JJ, Chabbert B, Tollier MT, Schuch W (1994) Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J 6:339–350

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harrison MJ, Lawton MA, Lamb CJ, Dixon RA (1991) Characterization of a nuclear protein that binds to three elements within the silencer region of a bean chalcone synthase gene promoter. Proc Natl Acad Sci USA 88:2515–2519

    CAS  PubMed  Google Scholar 

  • Hayashi M, Aoki M, Kato A, Kondo M, Nishimura M (1996) Transport of chimeric proteins that contain a carboxy-terminal targeting signal into plant microbodies. Plant J 10:225–234

    Article  CAS  PubMed  Google Scholar 

  • Hibino T, Takabe K, Kawazu T, Shibata D, Higuchi T (1995) Increase of cinnamaldehyde groups in lignin of transgenic tobacco plants carrying an antisense gene for cinnamyl alcohol dehydrogenase. Biosci Biotechnol Biochem 59:929–931

    CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Jorgensen LR (1931) Brown midrib in maize and its linkage relations. J Am Soc Agron 23:549–557

    Google Scholar 

  • Jornvall H, Person B, Jeffery J (1987) Characterization of alcohol/polyol dehydrogenases: the zinc-containing long chain alcohol dehydrogenases. Eur J Biochem 167:195–201

    CAS  PubMed  Google Scholar 

  • Jung HG, Mertens DR, Payne AJ (1997) Correlation of acid detergent lignin and klason lignin with disgestibility of forage dry matter and neutral detergent fiber. J Dairy Sci 80:1622–1628

    CAS  PubMed  Google Scholar 

  • Kawaoka A, Kaothien P, Yoshida K, Endo S, Yamada K, Ebinuma H (2000) Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J 22:289–301

    Article  CAS  PubMed  Google Scholar 

  • Knight ME, Halpin C, Schuch W (1992) Identification and characterization of cDNA clones encoding cinnamyl alcohol dehydrogenase from tobacco. Plant Mol Biol 19:793–801

    CAS  PubMed  Google Scholar 

  • Kondo T, Watanabe T, Ohshita T, Kyuma T (1998) Physicochemical characteristics of soluble lignin fractions released from forage grasses by ruminant digestion. JARQ 32:187–195

    CAS  Google Scholar 

  • Lauvergeat V, Rech P, Jauneau A, Guez C, Coutos-Thevenot P, Grima-Pettenati J (2002) The vascular expression pattern directed by the Eucalyptus gunnii cinnamyl alcohol dehydrogenase EgCAD2 promoter is conserved among woody and herbaceous plant species. Plant Mol Biol 50:497–509

    Article  CAS  PubMed  Google Scholar 

  • Lazo GR, Stein PA, Ludwig RA (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology 9:963–967

    CAS  PubMed  Google Scholar 

  • Lois R, Dietrich A, Hahlbrock K, Schultz W (1989) A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8:1641–1648

    CAS  PubMed  Google Scholar 

  • Lynch D, Lidgett A, McInnes R, Huxley H, Jones E, Mahoney N, Spangenberg G (2002) Isolation and characterization of three cinnamyl alcohol dehydrogenase homologue cDNAs from perennial ryegrass (Lolium perenne L.). J Plant Physiol 159:653–660

    CAS  Google Scholar 

  • MacKay JJ, Liu W, Whetten R, Sederoff RR, O’Malley D (1995) Genetic analysis of cinnamyl alcohol dehydrogenase in loblolly pine: Single gene inheritance, molecular characterization and evolution. Mol Gen Genet 247:537–545

    CAS  PubMed  Google Scholar 

  • McKie JH, Jaouhari R, Douglas KT, Goffner D, Feuillet C, Grima-Pettenati J, Boudet AM, Baltas M, Gorrichon L (1993) A molecular model for cinnamyl alcohol dehydrogenase, an aromatic alcohol dehydrogenase involved in lignification. Biochim Biophys Acta 1202:61–69

    Article  CAS  PubMed  Google Scholar 

  • Mitchell HJ, Hall JL, Barber MS (1994) Elicitor-induced cinnamyl alcohol dehydrogenase activity in lignifying wheat (Triticum aestivum L.) leaves. Plant Physiol 104:551–556

    Google Scholar 

  • Nakano J, Meshitsuka G (1992) The detection of lignin. In: Lin SY, Dence CW (eds) Methods in lignin chemistry. Springer, New York Berlin Heidelberg, pp 21–32

  • Neuffer MG (1992) Location and designation of four EMS induced kernel mutants. Maize Coop News 66:39

    Google Scholar 

  • O’Malley D, Porter S, Sederoff RR (1992) Purification, characterization and cloning of cinnamyl alcohol dehydrogenase in loblolly pine (Pinus taeda L.). Plant Physiol 98:1364–1371

    Google Scholar 

  • Romero I, Fuertes A, Benito MJ, Malpica JM, Leyva A, Paz-Ares J (1998) More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14:273–284

    Article  CAS  PubMed  Google Scholar 

  • Rossmann MG, Moras D, Olsen KW (1974) Chemical and biological evolution of nucleotide-binding protein. Nature 250:194–199

    CAS  PubMed  Google Scholar 

  • Sakurai N, Katayama Y, Yamaya T (2001) Overlapping expression of cytosolic glutamine synthetase and phenylalanine ammonia-lyase in immature leaf blades of rice. Physiol Plant 113:400–408

    Google Scholar 

  • Sallaud C, Meynard D, van Boxtel J, Gay C, Be‘s M, Brizard JP, Larmande P, Ortega D, Raynal M, Portefaix M, Ouwerkerk PBF, Rueb S, Delseny M, Guiderdoni E (2003) Highly efficient production and characterization of T-DNA plants for rice (Oryza sativa L.) functional genomics. Theor Appl Genet 106:1396–1408

    CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EJ, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Sauter M, Kende H (1992) Levels of β-glucan and lignin in elongating internodes of deepwater rice. Plant Cell Physiol 33:1089–1097

    CAS  Google Scholar 

  • Sewalt V, Glasser W, Beauchemin K (1997) Lignin impact on fiber degradation. 3. Reversal of inhibition of enzymatic hydrolysis by chemical modification of lignin and by additives. J Agric Food Chem 45:1823–1828

    Article  CAS  Google Scholar 

  • Sibout R, Eudes A, Pollet B, Goujon T, Mila I, Granier F, Seguin A, Lapierre C, Jouanin L (2003) Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis. Isolation and characterization of the corresponding mutants. Plant Physiol 132:848–860

    Google Scholar 

  • Tanaka H, Tapscott SJ, Trask BJ, Yao M (2002) Short inverted repeats initiate gene amplification through the formation of a large DNA palindrome in mammalian cells. Proc Natl Acad Sci USA 99:8772–8777

    CAS  PubMed  Google Scholar 

  • Tavares R, Aubourg S, Lecharny A, Kreis M (2000) Organization and structural evolution of four multigene families in Arabidopsis thaliana: AtLCAD, AtLGT, AtMYST and AtHD-GL2. Plant Mol Biol 42:703–717

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  Google Scholar 

  • Vogel KP, Jung HG (2001) Genetic modification of herbaceous plants for feed and fuel. Crit Rev Plant Sci 20:15–49

    Article  Google Scholar 

  • Wang J, Jiang J, Oard JH (2000) Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.). Plant Sci 156:201–211

    Article  CAS  PubMed  Google Scholar 

  • Ware DH, Jaiswal P, Ni J, Yap IV, Pan X, Clark KY, Teytelman L, Schmidt SC, Zhao W, Chang K, Cartinhour S, Stein LD, McCouch SR (2002) Gramene, a tool for grass genomics. Plant Physiol 130:1606–1613

    Google Scholar 

  • Zhu Q, Dabi T, Beeche A, Yamamoto R, Lawton C, Lamb C (1995) Cloning and properties of a rice gene encoding phenylalanine ammonia-lyase. Plant Mol Biol 29:535–550

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to John Vogel, Debbie Laudencia-Chingcuanco, and Roger Thilmony for critical review of the manuscript and Devin Coleman-Derr for contributing the illustration in Fig. 4. This work was supported by the U.S. Department of Agriculture ARS CRIS 5325-21000-009-00.

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  1. Agricultural Research Service, Western Regional Research Center, United States Department of Agriculture, 800 Buchanan Street, Albany, CA 94710, USA

    Christian M. Tobias & Elaine K. Chow

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  1. Christian M. Tobias
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Correspondence to Christian M. Tobias.

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Tobias, C.M., Chow, E.K. Structure of the cinnamyl-alcohol dehydrogenase gene family in rice and promoter activity of a member associated with lignification. Planta 220, 678–688 (2005). https://doi.org/10.1007/s00425-004-1385-4

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