Skip to main content
SpringerLink
Log in

OsCAD2 is the major CAD gene responsible for monolignol biosynthesis in rice culm

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Cinnamyl alcohol dehydrogenase (CAD) catalyzes the last step of monolignol biosynthesis. The rice genome contains 12 CAD-like genes, and whereas the proteins encoded by OsCAD2 and OsCAD7 are known to function in monolignol biosynthesis, the degree to which these enzymes contribute to this process and the involvement of the enzymes encoded by the remaining ten genes is unclear. This paper investigates the role of OsCAD2 and the nine other OsCAD-like proteins in monolignol biosynthesis. Among the OsCAD genes analyzed, OsCAD2, an enzyme belonging to the bona fide CAD phylogenetic group, was the most abundantly expressed gene in the uppermost internode, and was expressed at levels that were more than seven times greater than those of the second most abundantly expressed gene, OsCAD1. Promoter-GUS analysis of OsCAD2 (pCAD::GUS) in the internode, sheath, and roots revealed that GUS expression was strong in tissues that accumulated high levels of lignin. Furthermore, expression always preceded lignin accumulation, showing the tight correlation between OsCAD2 expression and monolignol biosynthesis. Additionally, expression of pCAD::GUS was well synchronized with that of rice caffeic acid 3-O-methyltransferase (OsCOMT::GUS), suggesting that the two enzymes function cooperatively during monolignol biosynthesis. Co-expression network analysis of eight OsCAD genes further revealed that, among the OsCAD genes, expression of OsCAD2 was most tightly associated with the transcription of lignin biosynthesis-related genes. These results suggest that OsCAD2 is largely responsible for monolignol biosynthesis in rice, which is similar to that indicated for the predominant role of other plant bona fide CAD protein to monolignol biosynthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

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

    Article  PubMed  CAS  Google Scholar 

  • Bose SK, Francis RC, Govender M, Bush T, Spark A (2009) Lignin content versus syringyl to guaiacyl ratio amongst poplars. Bioresour Technol 100:1628–1633

    Article  PubMed  CAS  Google Scholar 

  • Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Genet Genomics 269:205–214

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Eudes A, Pollet B, Sibout R, Do CT, Séguin A, Lapierre C, Jouanin L (2006) Evidence for a role of AtCAD 1 in lignification of elongating stems of Arabidopsis thaliana. Planta 225:23–39

    Article  PubMed  CAS  Google Scholar 

  • Goujon T, Sibout R, Eudes A, MacKay J, Jouanin L (2003a) Genes involved in the biosynthesis of lignin precursors in Arabidopsis thaliana. Plant Physiol Biochem 41:677–687

    Article  CAS  Google Scholar 

  • Goujon T, Sibout R, Pollet B, Maba B, Nussaume L, Bechtold N, Lu F, Ralph J, Mila I, Barrière Y, Lapierre C, Jouanin L (2003b) A new Arabidopsis thaliana mutant deficient in the expression of O-methyltransferase impacts lignins and sinapyl esters. Plant Mol Biol 51:973–989

    Article  PubMed  CAS  Google Scholar 

  • Guo DM, Ran JH, Wang XQ (2010) Evolution of the cinnamyl/sinapyl alcohol dehydrogenase (CAD/SAD) gene family: the emergence of real lignin is associated with the origin of Bona Fide CAD. J Mol Evol 71:202–218

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Hamberger B, Ellis M, Friedmann M, de Azevedo Souza C, Barbazuk B, Douglas CJ (2007) Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85:1182–1201

    Article  CAS  Google Scholar 

  • Harbron C, Chang KM, South MC (2007) RefPlus: an R package extending the RMA Algorithm. Bioinformatics 15:2493–2494

    Article  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  PubMed  CAS  Google Scholar 

  • Hirano K, Kotake T, Kamihara K, Tsuna K, Aohara T, Kaneko Y, Takatsuji H, Tsumuraya Y, Kawasaki S (2010) Rice BRITTLE CULM 3 (BC3) encodes a classical dynamin OsDRP2B essential for proper secondary cell wall synthesis. Planta 232:95–108

    Article  PubMed  CAS  Google Scholar 

  • Kim SJ, Kim MR, Bedgar DL, Moinuddin SG, Cardenas CL, Davin LB, Kang C, Lewis NG (2004) Functional reclassification of the putative cinnamyl alcohol dehydrogenase multigene family in Arabidopsis. Proc Natl Acad Sci USA 101:1455–1460

    Article  PubMed  CAS  Google Scholar 

  • Kim SJ, Kim KW, Cho MH, Franceschi VR, Davin LB, Lewis NG (2007) Expression of cinnamyl alcohol dehydrogenases and their putative homologues during Arabidopsis thaliana growth and development: lessons for database annotations? Phytochemistry 68:1957–1974

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto T, Chiba W, Saito K, Fukushima K, Uraki Y, Ubukata M (2010) Influence of syringyl to guaiacyl ratio on the structure of natural and synthetic lignins. J Agric Food Chem 58:895–901

    Article  PubMed  CAS  Google Scholar 

  • Li X, Weng JK, Chapple C (2008) Improvement of biomass through lignin modification. Plant J 54:569–581

    Article  PubMed  CAS  Google Scholar 

  • Li X, Yang Y, Yao J, Chen G, Li X, Zhang Q, Wu C (2009) FLEXIBLE CULM 1 encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice. Plant Mol Biol 69:685–697

    Article  PubMed  CAS  Google Scholar 

  • Ma QH (2010) Functional analysis of a cinnnamyl alcohol dehydrogenase involved in lignin biosynthesis in wheat. J Exp Bot 10:2735–2744

    Article  Google Scholar 

  • Mir Derikvand M, 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 227:943–956

    Article  PubMed  CAS  Google Scholar 

  • Murakami T, Ohashi Y (1992) Methods for histochemical detection of GUS reporter gene expression in transgenic plants. Shokubutu-Saibou-Kougaku 4:281–286

    Google Scholar 

  • Obayashi T, Kinoshita K (2011) COXPRESdb: a database to compare gene coexpression in seven model animals. Nucleic Acids Res 39:D1016–D1022

    Article  PubMed  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

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sattler SE, Saathoff AJ, Haas EJ, Palmer NA, Funnell-Harris DL, Sarath G, Pedersen JF (2009) A nonsense mutation in a cinnamyl alcohol dehydrogenase gene is responsible for the Sorghum brown midrib6 phenotype. Plant Physiol 150:584–595

    Article  PubMed  CAS  Google 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 17:2059–2076

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Tobias CM, Chow EK (2005) Structure of the cinnamyl-alcohol dehydrogenase gene family in rice and promoter activity of a member associated with lignification. Planta 220:678–688

    Article  PubMed  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 

  • Vogel J (2008) Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301–307

    Article  PubMed  CAS  Google Scholar 

  • Weng JK, Li X, Bonawitz ND, Chapple C (2008) Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr Opin Biotechnol 19:166–172

    Article  PubMed  CAS  Google Scholar 

  • Xu Z, Zhang D, Hu J, Zhou X, Ye X, Reichel KL, Stewart NR, Syrenne RD, Yang X, Gao P, Shi W, Doeppke C, Sykes RW, Burris JN, Bozell JJ, Cheng MZ, Hayes DG, Labbe N, Davis M, Stewart CN Jr, Yuan JS (2009) Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinform 10(Suppl 11):S3

    Article  Google Scholar 

  • Youn B, Camacho R, Moinuddin SG, Lee C, Davin LB, Lewis NG, Kang C (2006) Crystal structures and catalytic mechanism of the Arabidopsis cinnamyl alcohol dehydrogenases AtCAD5 and AtCAD4. Org Biomol Chem 4:1687–1697

    Article  PubMed  CAS  Google Scholar 

  • Yuan JS, Tiller KH, Al-Ahmad H, Stewart NR, Stewart CN Jr (2008) Plants to power: bioenergy to fuel the future. Trends Plant Sci 13:421–429

    Article  PubMed  CAS  Google Scholar 

  • Zhang K, Qian Q, Huang Z, Wang Y, Li M, Hong L, Zeng D, Gu M, Chu C, Cheng Z (2006) GOLD HULL AND INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice. Plant Physiol 140:972–983

    Article  PubMed  CAS  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

    Ko Hirano, Koichiro Aya, Mari Kondo, Ayako Okuno & Makoto Matsuoka

  2. Honda Research Institute Japan Co, Ltd, 2-1-4 Kazusa-Kamatari, Kisarazu, Chiba, 292-0818, Japan

    Yoichi Morinaka

Authors
  1. Ko Hirano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Koichiro Aya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mari Kondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ayako Okuno
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoichi Morinaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Makoto Matsuoka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Makoto Matsuoka.

Additional information

Communicated by L. Jouanin.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hirano, K., Aya, K., Kondo, M. et al. OsCAD2 is the major CAD gene responsible for monolignol biosynthesis in rice culm. Plant Cell Rep 31, 91–101 (2012). https://doi.org/10.1007/s00299-011-1142-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1142-7

Keywords

Search

Navigation