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The Endo-β-Mannanase gene families in Arabidopsis, rice, and poplar

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Abstract

Mannans are widespread hemicellulosic polysaccharides in plant cell walls. Hydrolysis of the internal β-1,4-d-mannopyranosyl linkage in the backbone of mannans is catalyzed by endo-β-mannanase. Plant endo-β-mannanase has been well studied for its function in seed germination. Its involvement in other plant biological processes, however, remains poorly characterized or elusive. The completed genome sequences of Arabidopsis (Arabidopsis thaliana), rice (Oryza sativa), and poplar (Populus trichocarpa) provide an opportunity to conduct comparative genomic analysis of endo-β-mannanase genes in these three species. In silico sequence analysis led to the identification of eight, nine and 11 endo-β-mannanase genes in the genomes of Arabidopsis, rice, and poplar, respectively. Sequence comparisons revealed the conserved amino acids and motifs that are critical for the active site of endo-β-mannanases. Intron/exon structure analysis in conjunction with phylogenetic analysis implied that both intron gain and intron loss has played roles in the evolution of endo-β-mannanase genes. The phylogenetic analysis that included the endo-β-mannanases from plants and other organisms implied that plant endo-β-mannanases have an ancient evolutionary origin. Comprehensive expression analysis of all Arabidopsis and rice endo-β-mannanase genes showed divergent expression patterns of individual genes, suggesting that the enzymes encoded by these genes, while carrying out the same biochemical reaction, are involved in diverse biological processes.

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References

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

    Article  PubMed  CAS  Google Scholar 

  • An YQ, McDowell JM, Huang S, McKinney EC, Chambliss S, Meagher RB (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10:107–121

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Arana MV, de Miguel LC, Sanchez RA (2005) A phytochrome-dependent embryhonic factor modulates gibberellin responses in the embryo and micropylar endosperm of Datura ferox seeds. Planta (in press). DOI 10.1007/s00425-005-0134-7

  • Bacic A, Harris PJ, Stone BA (1988) Structure and function of plant cell walls. In: Preiss J (ed) Carbohydrates. The biochemistry of plants, vol. 14. Academic, New York, pp 297–371

    Google Scholar 

  • Bartel B, Bartel DP (2005) MicroRNAs: at the root of plant development? Plant Physiol 132:709–717

    Article  Google Scholar 

  • Bendtsen JD, Nielsen H, Heijne G, Brunak S (2004) Improved prediction of signal peptides: Signal P 3.0. J Mol Biol 340:783–795

    Article  PubMed  Google Scholar 

  • Bewley JD, Burton RA, Morohashi Y, Fincher GB (1997) Molecular cloning of a cDNA encoding a (1–>4)-beta-mannan endohydrolase from the seeds of germinated tomato (Lycopersicon esculentum). Planta 203:454–459

    Article  PubMed  CAS  Google Scholar 

  • Bewley JD, Banik M, Bourgault R, Feurtado JA, Toorop P, Hilhorst HW (2000) Endo-β-mannanase activity increases in the skin and outer pericarp of tomato fruits during ripening. J Exp Bot 51:529–538

    Article  PubMed  CAS  Google Scholar 

  • Bourgault R, Bewley JD (2002) Variation in its C-terminal amino acids determines whether ENDO-β-MANNANASE is active or inactive in ripening tomato fruits of different cultivars. Plant Physiol 130:1254–1262

    Article  PubMed  CAS  Google Scholar 

  • Bourgault R, Oakley AJ, Bewley JD, Wilce MCJ (2005) Three-dimensional structure of (1,4)-β-d-mannan mannanohydrolase from tomato fruit. Protein Sci 14:1233–1241

    Article  PubMed  CAS  Google Scholar 

  • Bradford KJ, Chen F, Cooley MB, Dahal P, Downie B, Fukunaga KK, Gee OH, Gurusinghe S, Mella RA, Nonogaki H, Wu CT, Yim KO (2000) Gene expression before radicle emergence in imbibed tomato seeds. In: Black M, Bradford KJ, Vazquez-Ramos J (eds) Seed biology: advances and applications. CABI, Wallingford, UK, pp 231–251

    Google Scholar 

  • Brummell DA, Cin VD, Crisosto CH, Labavitch JM (2004) Cell wall metabolism during maturation, ripening and senescence of peach fruit. J Exp Bot 55:2029–2039

    Article  PubMed  CAS  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  Google Scholar 

  • Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476

    Article  PubMed  CAS  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls of flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  PubMed  CAS  Google Scholar 

  • Carpita N, McCann M (2000) The cell wall. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Biologist, Rockville, MD, pp 52–108

    Google Scholar 

  • Chen F, Bradford KJ (2000) Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiol 124:1265–1274

    Article  PubMed  CAS  Google Scholar 

  • Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E, Gershenzon J (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481–494

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (1999) Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Physiol Plant Mol Biol 50:391–417

    Article  PubMed  CAS  Google Scholar 

  • Davies GJ, Wilson KS, Henrissat B (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J 321:557–559

    PubMed  CAS  Google Scholar 

  • Dhugga KS, Barreiro R, Whitten B, Stecca K, Hazebroek J, Randhawa GS, Dolan M, Kinney AJ, Tomes D, Nichols S, Anderson P (2004) Guar seed β-mannan synthase is a member of the cellulose synthase super gene family. Science 303:363–366

    Article  PubMed  CAS  Google Scholar 

  • Filichkin SA, Leonard JM, Monteros A, Liu PP, Nonogaki H (2004) A novel endo-β-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiol 134:1080–1087

    Article  PubMed  CAS  Google Scholar 

  • Groot SPC, Karssen CM (1987) Gibberellins regulate seed germination in tomato by endosperm weakening—a study with gibberellin-deficient mutants. Planta 171:525–531

    Article  CAS  Google Scholar 

  • Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337–343

    Article  PubMed  CAS  Google Scholar 

  • Handford MG, Baldwin TC, Gobet F, Prime TA, Miles J, Yu X, Dupree P (2003) Localisation and characterization of cell wall mannan polysaccharides in Arabidopsis thaliana. Planta 218:27–36

    Article  PubMed  CAS  Google Scholar 

  • Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316

    PubMed  CAS  Google Scholar 

  • Henrissat B, Bairoch A (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316:695–696

    PubMed  Google Scholar 

  • Henrissat B, Coutinho PM, Davies GJ (2001) A census of carbonhydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol Biol 47:55–72

    Article  PubMed  CAS  Google Scholar 

  • Hogg D, Pell G, Dupree P, Goubet F, Martin-Orue SM, Armand S, Gilbert HJ (2003) The molecular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. Biochem J 371:1027–1043

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Liu P-P, Koizuka N, Homrichhausen TM, Hewitt JR, Martin RC, Nonogaki H (2005) Large scale screening of Arabidopsis enhancer-trap lines for seed germinationassociated genes. Plant J 41:936–944

    Article  PubMed  CAS  Google Scholar 

  • Lu SF, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203

    Article  PubMed  CAS  Google Scholar 

  • Lundqvist J, TeLeMAN A, Junel L, Zacchi G, Dahlman O, Tjerneld F, Stalbrand H (2002) Isolation and characterization of galactoglucomannan from spruce (Piceaabies). Carbohydr Polym 48:29–39

    Article  CAS  Google Scholar 

  • Marraccinni P, Rogers WJ, Allard C, André ML, Caillet V, Lacoste N, Lausanne F, Michaux S (2001) Molecular and biochemical characterization of ENDO-β-MANNANASEs from germinating coffee (Coffea arabica) grains. Planta 213:296–308

    Article  Google Scholar 

  • Nonogaki H, Morohashi Y (1996) An ENDO-β-MANNANASE develops exclusively in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiol 110:555–559

    PubMed  CAS  Google Scholar 

  • Nonogaki H, Gee OH, Bradford KJ (2000) A germination-specific ENDO-β-MANNANASE gene is expected in the micropylar endosperm cap of tomato seeds. Plant Physiol 123:1235–1245

    Article  PubMed  CAS  Google Scholar 

  • Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4:176–183

    Article  PubMed  Google Scholar 

  • Rouze P, Pavy N, Rombauts S (1999) Genome annotation: which tools do we have for it? Curr Opin Plant Biol 2:90–95

    Article  PubMed  CAS  Google Scholar 

  • Schröder R, Wegrzyn TF, Sharma NN, Atkinson RG (2006) LeMAN4 endo-β-mannanase from ripe tomato fruit can act as a mannan transglycosylase or hydrolase. Planta DOI 10.1007/s00425-006-0286-0

  • Tamaru Y, Doi RH (2000) The engL gene cluster of Clostridium cellulovorans contains a gene for cellulosomal ManA. J Bacteriol 182:244–247

    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

    PubMed  CAS  Google Scholar 

  • Wang AX, Li JR, Bewley JD (2004) Molecular cloning and characterization of an endo-β-mannanase gene expressed in the lettuce endosperm following radicle emergence. Seed Sci Res 14:267–276

    Article  CAS  Google Scholar 

  • Wang AX, Wang XF, Ren YF, Gong XM, Bewley JD (2005) Endo-β-mannanase and β-mannosidase activities in rice grains during and following germination, and the influence of gibberellin and abscisic acid. Seed Sci Res 15:219–227

    Article  CAS  Google Scholar 

  • Whitney SEC, Brigham JE, Darke AH, Reid JSG, Gidley MJ (1998) Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose. Carbohydr Res 307:299–309

    Article  CAS  Google Scholar 

  • Xu B, Hägglund P, Stålbrand H, Janson J-C (2001) Endo-β-1,4-Mannanases from blue mussel, Mytilus edulis: purification, characterization, and mode of action. J Biotechnol 92:267–277

    Article  Google Scholar 

  • Xu B, Sellos D, Janson J (2002) Cloning and expression in Pichia pastoris of a blue mussel (Mytilus edulis) β-mannanase gene. Eur J Biochem 269:1753–1760

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama R, Nishitani K (2004) Genomic basis for cell-wall diversity in plants. A comparative approach to gene families in rice and Arabidopsis. Plant Cell Physiol 45:1111–1121

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama R, Rose JKC, Nishitani K (2004) A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol 134:1088–1099

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Sciences, University of Tennessee, 2431 Joe Johnson Drive, Knoxville, TN, 37996, USA

    Joshua S. Yuan, Xiaohan Yang, Jingru Lai, Zong-Ming Cheng & Feng Chen

  2. Crop Diseases, Pests and Genetics, USDA-ARS, 9611 S. Riverbend Avenue, Parlier, CA, 93648, USA

    Hong Lin

  3. Department of Horticulture, Oregon State University, 4017 Agricultural and Life Science Building, Corvallis, OR, 97331, USA

    Hiroyuki Nonogaki

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  1. Joshua S. Yuan
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  2. Xiaohan Yang
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  3. Jingru Lai
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  4. Hong Lin
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  5. Zong-Ming Cheng
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  6. Hiroyuki Nonogaki
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  7. Feng Chen
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Correspondence to Feng Chen.

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Yuan, J.S., Yang, X., Lai, J. et al. The Endo-β-Mannanase gene families in Arabidopsis, rice, and poplar. Funct Integr Genomics 7, 1–16 (2007). https://doi.org/10.1007/s10142-006-0034-3

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  • DOI: https://doi.org/10.1007/s10142-006-0034-3

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