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

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.

[1]  D. Sellos,et al.  Cloning and expression in Pichia pastoris of a blue mussel (Mytilus edulis) β‐mannanase gene , 2002 .

[2]  N. Carpita,et al.  Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. , 1993, The Plant journal : for cell and molecular biology.

[3]  Po-Pu Liu,et al.  Large-scale screening of Arabidopsis enhancer-trap lines for seed germination-associated genes. , 2005, The Plant journal : for cell and molecular biology.

[4]  N. Lacoste,et al.  Molecular and biochemical characterization of endo-β-mannanases from germinating coffee (Coffea arabica) grains , 2001, Planta.

[5]  S. Filichkin,et al.  A Novel Endo-β-Mannanase Gene in Tomato LeMAN5 Is Associated with Anther and Pollen Development1 , 2004, Plant Physiology.

[6]  Steven B Cannon,et al.  The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana , 2004, BMC Plant Biology.

[7]  A. Darke,et al.  Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose , 1998 .

[8]  R. Burton,et al.  Molecular cloning of a cDNA encoding a (1→4)-β-mannan endohydrolase from the seeds of germinated tomato (Lycopersicon esculentum) , 1997, Planta.

[9]  N. Sharma,et al.  LeMAN4 endo-β-mannanase from ripe tomato fruit can act as a mannan transglycosylase or hydrolase , 2006, Planta.

[10]  C. J. Chamberlain The Cell Wall , 1907, Botanical Gazette.

[11]  R. Sánchez,et al.  A phytochrome-dependent embryonic factor modulates gibberellin responses in the embryo and micropylar endosperm of Datura ferox seeds , 2006, Planta.

[12]  Per Hägglund,et al.  endo-β-1,4-Mannanases from blue mussel, Mytilus edulis: purification, characterization, and mode of action , 2002 .

[13]  J. Labavitch,et al.  Cell wall metabolism during maturation, ripening and senescence of peach fruit. , 2004, Journal of experimental botany.

[14]  H. Gilbert,et al.  The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. , 2003, The Biochemical journal.

[15]  B. Henrissat,et al.  A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. , 2001 .

[16]  F. Chen,et al.  Expression of an expansin is associated with endosperm weakening during tomato seed germination. , 2000, Plant physiology.

[17]  J. Gershenzon,et al.  Biosynthesis and Emission of Terpenoid Volatiles from Arabidopsis Flowers Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007989. , 2003, The Plant Cell Online.

[18]  K. Bradford,et al.  A germination-specific endo-beta-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. , 2000, Plant physiology.

[19]  J. Bewley,et al.  Endo-beta-mannanase activity increases in the skin and outer pericarp of tomato fruits during ripening. , 2000, Journal of experimental botany.

[20]  S. Brunak,et al.  Improved prediction of signal peptides: SignalP 3.0. , 2004, Journal of molecular biology.

[21]  B Henrissat,et al.  A classification of glycosyl hydrolases based on amino acid sequence similarities. , 1991, The Biochemical journal.

[22]  Vincent L. Chiang,et al.  Novel and Mechanical Stress–Responsive MicroRNAs in Populus trichocarpa That Are Absent from Arabidopsisw⃞ , 2005, The Plant Cell Online.

[23]  H. Nonogaki,et al.  An Endo-[beta]-Mannanase Develops Exclusively in the Micropylar Endosperm of Tomato Seeds Prior to Radicle Emergence , 1996, Plant physiology.

[24]  G J Davies,et al.  Nomenclature for sugar-binding subsites in glycosyl hydrolases. , 1997, The Biochemical journal.

[25]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[26]  K. Nishitani,et al.  Genomic basis for cell-wall diversity in plants. A comparative approach to gene families in rice and Arabidopsis. , 2004, Plant & cell physiology.

[27]  A. Kinney,et al.  Guar Seed ß-Mannan Synthase Is a Member of the Cellulose Synthase Super Gene Family , 2004, Science.

[28]  G. Zacchi,et al.  Isolation and characterization of galactoglucomannan from spruce (Picea abies) , 2002 .

[29]  N. Carpita STRUCTURE AND BIOGENESIS OF THE CELL WALLS OF GRASSES. , 1996, Annual review of plant physiology and plant molecular biology.

[30]  李佩芳 International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. , 2005 .

[31]  Antony Bacic,et al.  8 – Structure and Function of Plant Cell Walls , 1988 .

[32]  A. Bennett,et al.  Polygalacturonases: many genes in search of a function. , 1998, Plant physiology.

[33]  Takuji Sasaki,et al.  The map-based sequence of the rice genome , 2005, Nature.

[34]  C. M. Karssen,et al.  Gibberellins regulate seed germination in tomato by endosperm weakening: a study with gibberellin-deficient mutants , 1987, Planta.

[35]  Aaron J. Oakley,et al.  Three‐dimensional structure of (1,4)‐β‐d‐mannan mannanohydrolase from tomato fruit , 2005 .

[36]  R. Doi,et al.  The engL Gene Cluster ofClostridium cellulovorans Contains a Gene for Cellulosomal ManA , 2000, Journal of bacteriology.

[37]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[38]  J. McDowell,et al.  Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. , 1996, The Plant journal : for cell and molecular biology.

[39]  Xiaofen Wang,et al.  Endo-β-mannanase and β-mannosidase activities in rice grains during and following germination, and the influence of gibberellin and abscisic acid , 2005, Seed Science Research.

[40]  P. Rouzé,et al.  Genome annotation: which tools do we have for it? , 1999, Current opinion in plant biology.

[41]  A Bairoch,et al.  Updating the sequence-based classification of glycosyl hydrolases. , 1996, The Biochemical journal.

[42]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[43]  J. Bewley,et al.  Molecular cloning and characterization of an endo-β-mannanase gene expressed in the lettuce endosperm following radicle emergence , 2004, Seed Science Research.

[44]  J. Bewley,et al.  Variation in Its C-Terminal Amino Acids Determines Whether Endo-β-Mannanase Is Active or Inactive in Ripening Tomato Fruits of Different Cultivars1 , 2002, Plant Physiology.

[45]  K. Nishitani,et al.  A Surprising Diversity and Abundance of Xyloglucan Endotransglucosylase/Hydrolases in Rice. Classification and Expression Analysis1 , 2004, Plant Physiology.

[46]  D J Cosgrove,et al.  Enzymes and other agents that enhance cell wall extensibility. , 1999, Annual review of plant physiology and plant molecular biology.

[47]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[48]  S. Karita,et al.  A Large Gene Cluster for the Clostridium cellulovorans Cellulosome , 2000, Journal of bacteriology.

[49]  F. Goubet,et al.  Localisation and characterisation of cell wall mannan polysaccharides in Arabidopsis thaliana , 2003, Planta.

[50]  David P. Bartel,et al.  MicroRNAs: At the Root of Plant Development?1 , 2003, Plant Physiology.

[51]  A. Bennett,et al.  Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. , 1999, Trends in plant science.