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FLEXIBLE CULM 1 encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice

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Abstract

Culm mechanical strength is an important agronomic trait in crop breeding. To understand the molecular mechanisms that control culm mechanical strength, we identified a flexible culm1 (fc1) mutant by screening a rice T-DNA insertion mutant library. This mutant exhibited an abnormal development phenotype, including late heading time, semi-dwarf habit, and flexible culm. In this study, we cloned the FLEXIBLE CULM1 (FC1) gene in rice using a T-DNA tagging approach. FC1 encodes a cinnamyl-alcohol dehydrogenase and is mainly expressed in the sclerenchyma cells of the secondary cell wall and vascular bundle region. In these types of cells, a deficiency of FC1 in the fc1 mutant caused a reduction in cell wall thickness, as well as a decrease in lignin. Extracts from the first internodes and panicles of the fc1 plants exhibited drastically reduced cinnamyl-alcohol dehydrogenase activity. Further histological and biochemical analyses revealed that the p-hydroxyphenyl and guaiacyl monomers in fc1 cell wall were reduced greatly. Our results indicated that FC1 plays an important role in the biosynthesis of lignin and the control of culm strength in rice.

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References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815. doi:10.1038/35048692

    Article  Google Scholar 

  • 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

    PubMed  CAS  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. doi:10.1023/A:1006182925584

    Article  PubMed  CAS  Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162. doi:10.1105/tpc.106.044495

    Article  PubMed  CAS  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Ann Rev Plant Biol 54:519–546. doi:10.1146/annurev.arplant.54.031902.134938

    Article  CAS  Google Scholar 

  • Brill EM, Abrahams S, Hayes CM, Jenkins CL, Watson JM (1999) Molecular characterisation and expression of a wound-inducible cDNA encoding a novel cinnamyl-alcohol dehydrogenase enzyme in lucerne (Medicago sativa L.). Plant Mol Biol 41:279–291. doi:10.1023/A:1006381630494

    Article  PubMed  CAS  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295. doi:10.1105/tpc.105.031542

    Article  PubMed  CAS  Google Scholar 

  • Campbell MM, Sederoff RR (1996) Variation in lignin content and composition: mechanisms of control and implications for the genetic improvement of plants. Plant Physiol 110:3–13

    PubMed  CAS  Google Scholar 

  • Chabannes M, Barakate A, Lapierre C, Marita JM, Ralph J, Pean M, Danoun S, Halpin C, Grima-Pettenati J, Boudet AM (2001) Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants. Plant J 28:257–270. doi:10.1046/j.1365-313X.2001.01140.x

    Article  PubMed  CAS  Google Scholar 

  • Chaturvedi GS, Misra CH, Singh CN, Pandey CB, Yadav VP, Singh AK, Divivedi JL, Singh BB, Singh RK (1995) Physiological flash flooding. International Rice Research Institute, Los Banos, pp 79–96 (Rainfed)

    Google Scholar 

  • Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255. doi:10.1101/gad.1416306

    Article  PubMed  CAS  Google Scholar 

  • De Block M, Debrouwer D (1993) RNA-RNA in situ hybridization using digoxigenin-labeled probes: the use of high-molecular-weight polyvinyl alcohol in the alkaline phosphatase indoxyl-nitroblue tetrazolium reaction. Anal Biochem 215:86–89. doi:10.1006/abio.1993.1558

    Article  PubMed  Google Scholar 

  • Donaldson LA (2001) Lignification and lignin topochemistry: an ultrastructural view. Phytochemistry 57:859–873. doi:10.1016/S0031-9422(01)00049-8

    Article  PubMed  CAS  Google Scholar 

  • Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet AM, Boon JJ, Chabbert B, Tollier M-T, Schuch W (1994) Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J 6:339–350. doi:10.1046/j.1365-313X.1994.06030339.x

    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. doi:10.1046/j.1365-313X.1998.00153.x

    Article  PubMed  CAS  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. doi:10.1046/j.1365-313X.1994.6020271.x

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800. doi:10.1038/nature03895

    Article  Google Scholar 

  • Joël Piquemal CL, Myton K, O’Connell A, Schuch W, Grima Pettenati J, Boudet AM (1998) Downregulation of cinnamoyl CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J 13:71–83. doi:10.1046/j.1365-313X.1998.00014.x

    Article  Google Scholar 

  • Jones L, Ennos AR, Turner SR (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J 26:205–216. doi:10.1046/j.1365-313x.2001.01021.x

    Article  PubMed  CAS  Google Scholar 

  • Knight ME, Halpin C, Schuch W (1992) Identification and characterisation of cDNA clones encoding cinnamyl alcohol dehydrogenase from tobacco. Plant Mol Biol 19:793–801. doi:10.1007/BF00027075

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031. doi:10.1105/tpc.011775

    Article  PubMed  CAS  Google Scholar 

  • Liu YG, Mitsukawa N, Osumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463. doi:10.1046/j.1365-313X.1995.08030457.x

    Article  PubMed  CAS  Google Scholar 

  • Liu KD, Wang J, Li HB, Xu CG, Liu AM, Li XH, Zhang Q (1997) A genome-wide analysis of wide compatibility in rice and the precise location of the S5 locus in the molecular map. Theory Appl Genet 95:809–814. doi:10.1007/s001220050629

    Article  CAS  Google Scholar 

  • Lu FC, Ralph J (1997) Derivatization followed by reductive cleavage (DFRC method), a new method for lignin analysis: protocol for analysis of DFRC monomers. J Agric Food Chem 45:2590–2592. doi:10.1021/jf970258h

    Article  CAS  Google Scholar 

  • Mansell RL, Gross GG, Stoeckigt J, Franke H, Zenk MH (1974) Purification and properties of cinnamyl alcohol dehydrogenase from higher plants involved in lignin biosynthesis. Phytochemistry 13:2427–2435. doi:10.1016/S0031-9422(00)86917-4

    Article  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. doi:10.1023/A:1010699919325

    Article  PubMed  CAS  Google Scholar 

  • Mou Z, He Y, Dai Y, Liu X, Li J (2000) Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12:405–418

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325. doi:10.1093/nar/8.19.4321

    Article  PubMed  CAS  Google Scholar 

  • Nicholas NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476. doi:10.1146/annurev.arplant.47.1.445

    Article  Google Scholar 

  • Ralph J, MacKay JJ, Hatfield RD, O’Malley DM, Whetten RW, Sederoff RR (1997) Abnormal lignin in a loblolly pine mutant. Science 277:235–239. doi:10.1126/science.277.5323.235

    Article  PubMed  CAS  Google Scholar 

  • Ramaiah K, Mudaliar SD (1934) Lodging of straw and its inheritance in rice (O. sativa). Indian J Agric Sci 4:880–894

    Google Scholar 

  • Ranocha P, Chabannes M, Chamayou S, Danoun S, Jauneau A, Boudet AM, Goffner D (2002) Laccase down-regulation causes alterations in phenolic metabolism and cell wall structure in poplar. Plant Physiol 129:145–155. doi:10.1104/pp.010988

    Article  PubMed  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. doi:10.1104/pp.103.021048

    Article  PubMed  CAS  Google Scholar 

  • Sibout R, Eudes A, Mouille G, Pollet B, Lapierre C, Jouanin L, Seguin 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. doi:10.1105/tpc.105.030767

    Article  PubMed  CAS  Google Scholar 

  • Taylor NG, Gardiner JC, Whiteman R, Turner SR (2004) Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose 11:329–338. doi:10.1023/B:CELL.0000046405.11326.a8

    Article  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. doi:10.1007/s00425-004-1385-4

    Article  PubMed  CAS  Google Scholar 

  • Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701

    Article  PubMed  CAS  Google Scholar 

  • Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424. doi:10.1016/S0003-2697(69)80009-6

    Article  PubMed  CAS  Google Scholar 

  • Wu C, Li X, Yuan W, Chen G, Kilian A, Li J, Xu C, Li X, Zhou DX, Wang S, Zhang Q (2003) Development of enhancer trap lines for functional analysis of the rice genome. Plant J 35:418–427. doi:10.1046/j.1365-313X.2003.01808.x

    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. doi:10.1104/pp.105.073007

    Article  PubMed  CAS  Google Scholar 

  • Zuber M (1973) Evaluation of progress in selection for stalk quality. Corn Sorghum Res Conf Proc 28:110–122

    Google Scholar 

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Acknowledgments

We thank Dr. Zhukuan Cheng (Chinese Academy of Sciences, Beijing, China) for kindly supplying the authentic standards for DFRC analysis. We also thank Drs. Yunhai Li and J. Peter Etchells for critical comments on the manuscript. This work was supported by grants from the National Special Key Project of China on Functional Genomics of Major Plants and Animals, and the National Natural Science Foundation of China.

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  1. National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, 430070, China

    Xiangjun Li, Ying Yang, Jialing Yao, Guoxing Chen, Xianghua Li, Qifa Zhang & Changyin Wu

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  1. Xiangjun Li
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Correspondence to Changyin Wu.

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Li, X., Yang, Y., Yao, J. et al. FLEXIBLE CULM 1 encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice. Plant Mol Biol 69, 685–697 (2009). https://doi.org/10.1007/s11103-008-9448-8

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