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Cinnamyl Alcohol Dehydrogenase Deficiency Causes the Brown Midrib Phenotype in Rice

  • Toshiaki Umezawa
  • Masahiro Sakamoto
  • Taichi Koshiba
Chapter

Abstract

Because lignin encrusts lignocellulose polysaccharides, it presents obstacles to chemical pulping, forage digestion, and enzymatic hydrolysis of plant cell wall polysaccharides for biorefining. Hence, it would be beneficial for plant materials to either contain less lignin or to have lignin that is easier to remove for these processes. Grass mutants known as brown midrib (bm) mutants generally show a reduced lignin content and higher in vitro digestibility compared with wild-type plants. Several bm mutants have been isolated only from the C4 grasses, maize, sorghum, and pearl millet, but have not been detected in C3 grasses including rice (Oryza sativa). Recently, the cad2 (cinnamyl alcohol dehydrogenase 2) null mutant isolated from retrotransposon Tos17 insertion lines of O. sativa ssp. japonica cv. Nipponbare was observed to exhibit brown-colored midribs in addition to hulls and internodes, clearly showing both bm and gold hull and internode (gh) phenotypes. In addition, chemical analysis of the mutant indicated that the coloration was probably due to the accumulation of cinnamaldehyde-related structures in the lignin. The lignin content of the cad2 null mutant was lower than that of the control plants, while the enzymatic saccharification efficiency in the culm of cad2 null mutant was increased compared with that of the control plants. This mutation could be applied to breed forage paddy rice cultivars and other grass biomass plants that are suitable for use as fodder and industrial feedstock.

Keywords

Brown midrib Lignin Cinnamyl alcohol dehydrogenase Gold hull and internode Rice 

References

  1. Ali F, Scott P, Bakht J, Chen Y, Lübberstedt T (2010) Identification of novel brown midrib genes in maize by tests of allelism. Plant Breed 129:724–726Google Scholar
  2. Barrière Y, Argillier O (1993) Brown-midrib genes of maize: a review. Agronomie 13:865–876CrossRefGoogle Scholar
  3. Barrière Y, Ralph J, Méchin V, Guillaumie S, Grabber JH, Argillier O, Chabbert B, Lapiere C (2004) Genetic and molecular basis of grass cell wall biosynthesis and degradability. II. Lessons from brown-midrib mutants. C R Biol 327:847–860CrossRefGoogle Scholar
  4. Baucher M, Chabbert B, Pilate G, Van Doorsselaere J, Tollier M-T, Petit-Conil M, Cornu D, Monties B, Van Montagu M, Inzé D, Jouanin L, Boerjan W (1996) Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol 112:1479–1490Google Scholar
  5. Baucher M, Bernard-Vailhé MA, Chabbert B, Besle J-M, 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 39:437–447Google Scholar
  6. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546Google Scholar
  7. Bout S, Vermerris W (2003) A candidate-gene approach to clone the sorghum Brown midrib gene encoding caffeic acid O-methyltransferase. Mol Gen Genomics 269:205–214Google Scholar
  8. Carle J, Holmgren P (2008) Wood from planted forests, a global outlook 2005–2030. Forest Prod J 58:6–18Google Scholar
  9. Chabannes M, Barakate A, Lapierre C, Mrita 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 28:257–270CrossRefGoogle Scholar
  10. Cherney JH, Cherney DJR, Akin DE, Axtell JD (1991) Potential of brown-midrib low-lignin mutants for improving forage quality. Adv Agron 46:157–198Google Scholar
  11. Chiang VL (2006) Monolignol biosynthesis and genetic engineering of lignin in trees, a review. Environ Chem Lett 4:143–146CrossRefGoogle Scholar
  12. Dixon RA, Reddy MSS (2003) Biosynthesis of monolignols. Genomic and reverse genetic approaches. Phytochem Rev 2:289–306CrossRefGoogle Scholar
  13. FAO Forest products statistics. http://www.fao.org/forestry/statistics/80938/en/.
  14. Guillaumie S, Pichon M, Martinant J-P, Bosio M, Goffner D, Barrière Y (2007) Differential expression of phenylpropanoid and related genes in brown-midrib bm1, bm2, bm3, and bm4 young near-isogenic maize plants. Planta 226:235–250Google Scholar
  15. Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet AM, Boon JJ, Chabbert B, Tollier M-T, Schuch W (1994) Manipulation of lignin quality of downregulation of cinnamyl alcohol dehydrogenase. Plant J 6:339–350CrossRefGoogle Scholar
  16. 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 14:545–553Google Scholar
  17. He X, Hall MB, Gallo-Meagher M, Smith RL (2003) Improvement of forage quality by downregulation of maize O-methyltransferase. Crop Sci 43:2240–2251CrossRefGoogle Scholar
  18. 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 59:929–931CrossRefGoogle Scholar
  19. Higuchi T, Ito T, Umezawa T, Hibino T, Shibata D (1994) Red-brown color of lignified tissues of transgenic plants with antisense CAD gene: wine-red lignin from coniferyl aldehyde. J Biotechnol 37:151–158CrossRefGoogle Scholar
  20. Hirochika H (2010) Insertional mutagenesis with Tos17 for functional analysis of rice genes. Breed Sci 60:486–492CrossRefGoogle Scholar
  21. Hong L, Qian Q, Tang D, Wang K, Li M, Cheng Z (2012) A mutation in the rice chalcone isomerase gene causes the golden hull and internode 1 phenotype. Planta 236:141–151CrossRefGoogle Scholar
  22. Iwata N, Omura T (1971) Linkage analysis by reciprocal translocation method in rice plants (Oryza sativa L.) II linkage groups corresponding to the chromosomes 5, 6, 8, 9, 10, and 11. Sci Bull Fac Agric Kyushu Univ 25:137–153Google Scholar
  23. Jorgenson LR (1931) Brown midrib in maize and its linkage relations. J Am Soc Agron 23:549–557CrossRefGoogle Scholar
  24. Kajita S, Katayama Y, Omori S (1996) Alteration in the biosynthesis of lignin in transgenic plants with chimeric genes for 4-coumarate: coenzyme a ligase. Plant Cell Physiol 37:957–965CrossRefGoogle Scholar
  25. Kim H, Ralph J, Lu F, Pilate G, Leplé J-C, Pollet B, Lapierre C (2002) Identification of the structure and origin of thioacidolysis marker compounds for cinnamyl alcohol dehydrogenase deficiency in angiosperms. J Biol Chem 277:47412–47419CrossRefGoogle Scholar
  26. Kim H, Ralph J, Lu F, Ralph SA, Boudet A-M, MacKay JJ, Sederoff RR, Ito T, Kawai S, Ohashi H, Higuchi T (2003) NMR analysis of lignins in CAD-deficient plants. Part 1. Incorporation of hydroxylcinnamaldehydes and hydroxybenzaldehydes into lignins. Org Biomol Chem 1:268–281Google Scholar
  27. Koshiba T, Murakami S, Hattori T, Mukai M, Takahashi A, Miyao A, Hirochika H, Suzuki S, Sakamoto M, Umezawa T (2013) CAD2deficiency causes both brown midrib and gold hull and internode phenotypes in Oryza sativa L. cv. Nipponbare. Plant Biotechnol 30:365–373Google Scholar
  28. Kumar A, Hirochika H (2001) Applications of retrotransposons as genetic tools in plant biology. Trends Plant Sci 6:127–134Google Scholar
  29. MacKay JJ, O’Malley DM, Presnell T, Booker FL, Campbell MM, Whetten RW, Sederoff RR (1997) Inheritance, gene expression, and lignin characterization in a mutant pine deficient in cinnamyl alcohol dehydrogenase. Proc Natl Acad Sci USA 94:8255–8260Google Scholar
  30. Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780CrossRefGoogle Scholar
  31. Morrow SL, Mascia P, Self KA, Altschuler M (1997) Molecular characterization of a brown midrib3 deletion mutation in maize. Mol Breed 3:351–357Google Scholar
  32. Novaes E, Kirst M, Chiang V, Winter-Sederoff H, Sederoff R (2010) Lignin and biomass: a negative correlation for wood formation and lignin content in trees. Plant Physiol 154:555–561CrossRefGoogle Scholar
  33. Ookawa T, Tanaka S, Kato H, Hirasawa T (2008) The effect of the decrease in the density of lignin on the lodging resistance of the lignin deficient mutant, gh2, in rice. Abstracts of the 225th Meeting of the Crop Science Society of Japan, 210–211 (in Japanese)Google Scholar
  34. Park J-y, Kanda E, Fukushima A, Motobayashi K, Nagata K, Kondo M, Ohshita Y, Morita S, Tokuyasu K (2011) Contents of various sources of glucose and fructose in rice straw, a potential feedstock for ethanol production in Japan. Biomass Bioenergy 35:3733–3735Google Scholar
  35. Piquemal J, Lapierre C, Myton K, O’Connell A, Schuch W, Grima-Pettenati J, Boudet A-M (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J 13:71–83CrossRefGoogle Scholar
  36. Ralph J, Lapierre C, Marita JM, Kim H, Lu F, Hatfield RD, Ralph S, Chapple C, Franke R, Hemm MR, Van Doorsselaere J, Sederoff RR, O’Malley DM, Scott JT, MacKay JJ, Yahiaoui N, Boudet A-M, Pean M, Pilate G, Jouanin L, Boerjan W (2001) Elucidation of new structures in lignins of CAD- and COMT-deficient plants by NMR. Phytochemistry 57:993–1003CrossRefGoogle Scholar
  37. Saballos A, Vermerris W, Rivera L, Ejeta G (2008) Allelic association, chemical characterization and saccharification properties of brown midrib mutants of sorghum (Sorghum bicolor (L.) Moench). Bioenergy Res 1:193–204Google Scholar
  38. Saballos A, Ejeta G, Sanchez E, Kang C, Vermerris W (2009) A genomewide analysis of the cinnamyl alcohol dehydrogenase family in sorghum [Sorghum bicolor (L.) Moench] identifies SbCAD2 as the Brown midrib6 gene. Genetics 181:783–795Google Scholar
  39. 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 150:584–595CrossRefGoogle Scholar
  40. Sattler SE, Funnell-Harris DL, Pedersen JF (2010) Brown midrib mutations and their importance to the utilization of maize, sorghum, and pearl millet lignocellulosic tissues. Plant Sci 178:229–238Google Scholar
  41. Shiba T, Kubo K, Kawai S (2007) Down regulation of cinnamyl alcohol dehydrogenase (CAD) induces increase of cell wall digestibility in rice (Oryza sativa). Proceedings of the 52nd lignin symposium, Utsunomiya, Japan, pp 18–21Google Scholar
  42. Tsai C-J, Popko JL, Mielke MR, Hu W-J, Podila GK, Chiang VL (1998) Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol 117:101–112Google Scholar
  43. Umezawa T (2010) The cinnamate/monolignol pathway. Phytochem Rev 9:1–17CrossRefGoogle Scholar
  44. Van Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier M-T, Petit-Conil M, Leplé J-C, Pilate G, Cornu D, Monties B, Van Montagu M, Inzé D, Boerjan W, Jouanin L (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J 8:855–864CrossRefGoogle Scholar
  45. Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:278–285CrossRefGoogle Scholar
  46. 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 7:407–416CrossRefGoogle Scholar
  47. Weng J-K, Li X, Bonawitz ND, Chapple C (2008) Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr Opin Biotechnol 19:166–172CrossRefGoogle Scholar
  48. Yamamura M, Noda S, Hattori T, Shino A, Kikuchi J, Takabe K, Tagane S, Gau M, Uwatoko N, Mii M, Suzuki S, Shibata D, Umezawa T (2013) Characterization of lignocellulose of Erianthus arundinaceus in relation to enzymatic saccharification efficiency. Plant Biotechnol 30:25–35CrossRefGoogle Scholar
  49. 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 140:972–983Google Scholar
  50. Zhong R, Morrison WH III, Himmelsbach DS, Poole FL II, Ye Z-H (2000) Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol 124:563–577Google Scholar

Copyright information

© Springer (India) Pvt. Ltd. 2018

Authors and Affiliations

  • Toshiaki Umezawa
    • 1
  • Masahiro Sakamoto
    • 2
  • Taichi Koshiba
    • 1
  1. 1.Research Institute for Sustainable HumanosphereKyoto UniversityKyotoJapan
  2. 2.Graduate School of AgricultureKyoto UniversityKyotoJapan

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