MAIZEWALL. Database and Developmental Gene Expression Profiling of Cell Wall Biosynthesis and Assembly in Maize 1[W]

An extensive search for maize (Zea mays) genes involved in cell wall biosynthesis and assembly has been performed and 735 sequences have been centralized in a database, MAIZEWALL (http://www.polebio.scsv.ups-tlse.fr/MAIZEWALL). MAIZEWALL contains a bioinformatic analysis for each entry and gene expression data that are accessible via a user-friendly interface. A maize cell wall macroarray composed of a gene-specific tag for each entry was also constructed to monitor global cell wall-related gene expression in different organs and during internode development. By using this macroarray, we identified sets of genes that exhibit organ and internode-stage preferential expression profiles. These data provide a comprehensive fingerprint of cell wall-related gene expression throughout the maize plant. Moreover, an in-depth examination of genes involved in lignin biosynthesis coupled to biochemical and cytological data from different organs and stages of internode development has also been undertaken. These results allow us to trace spatially and developmentally regulated, putative preferential routes of monolignol biosynthesis involving specific gene family members and suggest that, although all of the gene families of the currently accepted monolignol biosynthetic pathway are conserved in maize, there are subtle differences in family size and a high degree of complexity in spatial expression patterns. These differences are in keeping with the diversity of lignified cell types throughout the maize plant.

[1]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[2]  R. Zhong,et al.  Dual Methylation Pathways in Lignin Biosynthesis , 1998, Plant Cell.

[3]  Chung-Jui Tsai,et al.  Differential Substrate Inhibition Couples Kinetically Distinct 4-Coumarate:Coenzyme A Ligases with Spatially Distinct Metabolic Roles in Quaking Aspen1 , 2002, Plant Physiology.

[4]  K. Edwards,et al.  Brown-midrib maize (bm1)--a mutation affecting the cinnamyl alcohol dehydrogenase gene. , 1998, The Plant journal : for cell and molecular biology.

[5]  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.

[6]  P. Ranocha,et al.  Novel Markers of Xylogenesis in Zinnia Are Differentially Regulated by Auxin and Cytokinin1[W] , 2005, Plant Physiology.

[7]  Armand Séguin,et al.  CINNAMYL ALCOHOL DEHYDROGENASE-C and -D Are the Primary Genes Involved in Lignin Biosynthesis in the Floral Stem of Arabidopsisw⃞ , 2005, The Plant Cell Online.

[8]  V. Seltzer,et al.  A coumaroyl-ester-3-hydroxylase Insertion Mutant Reveals the Existence of Nonredundant meta-Hydroxylation Pathways and Essential Roles for Phenolic Precursors in Cell Expansion and Plant Growth1[W][OA] , 2005, Plant Physiology.

[9]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[10]  Dimitra L. Milioni,et al.  Early Gene Expression Associated with the Commitment and Differentiation of a Plant Tracheary Element Is Revealed by cDNA–Amplified Fragment Length Polymorphism Analysis , 2002, The Plant Cell Online.

[11]  Shoshi Kikuchi,et al.  Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Burkhard Morgenstern,et al.  DIALIGN2: Improvement of the segment to segment approach to multiple sequence alignment , 1999, German Conference on Bioinformatics.

[13]  E. Jamet,et al.  Cell wall proteins: a new insight through proteomics. , 2006, Trends in plant science.

[14]  D. Delmer,et al.  A comparative analysis of the plant cellulose synthase (CesA) gene family. , 2000, Plant physiology.

[15]  R. E. Sharp,et al.  Growth Maintenance of the Maize Primary Root at Low Water Potentials Involves Increases in Cell-Wall Extension Properties, Expansin Activity, and Wall Susceptibility to Expansins , 1996, Plant physiology.

[16]  Jérôme Gouzy,et al.  The ProDom database of protein domain families , 1998, Nucleic Acids Res..

[17]  C. Lamb,et al.  Cloning and properties of a rice gene encoding phenylalanine ammonia-lyase , 1995, Plant Molecular Biology.

[18]  J. Schmid,et al.  Maize Phenylalanine Ammonia-Lyase Has Tyrosine Ammonia-Lyase Activity , 1997, Plant physiology.

[19]  J. Laroche,et al.  Large-scale statistical analysis of secondary xylem ESTs in pine , 2004, Plant Molecular Biology.

[20]  Roland Arnold,et al.  MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource based on the first complete plant genome , 2002, Nucleic Acids Res..

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

[22]  K. Mendgen,et al.  xyloglucans, and pectic components into walls, wall appositions, cell plates and plasmodesmata , 1995 .

[23]  V. Walbot,et al.  Rapid transcriptome responses of maize (Zea mays) to UV-B in irradiated and shielded tissues , 2004, Genome Biology.

[24]  F. Legeai,et al.  Predotar: A tool for rapidly screening proteomes for N‐terminal targeting sequences , 2004, Proteomics.

[25]  Amos Bairoch,et al.  PROSITE: A Documented Database Using Patterns and Profiles as Motif Descriptors , 2002, Briefings Bioinform..

[26]  Rex L. Smith,et al.  Improvement of Forage Quality by Downregulation of Maize O‐Methyltransferase , 2003 .

[27]  L. Donaldson Lignification and lignin topochemistry - an ultrastructural view. , 2001, Phytochemistry.

[28]  Investigating the role of 99mTc-TRODAT-1 SPECT imaging in idiopathic Parkinson's disease. , 2005, Journal of Zhejiang University. Science. B.

[29]  J. Grima-Pettenati,et al.  EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. , 2005, The Plant journal : for cell and molecular biology.

[30]  D. J. Peterson,et al.  The maize caffeic acid O-methyltransferase gene promoter is active in transgenic tobacco and maize plant tissues , 1996, Plant Molecular Biology.

[31]  R. E. Sharp,et al.  The Maize Root Transcriptome by Serial Analysis of Gene Expression1[w] , 2005, Plant Physiology.

[32]  Michael D. Gonzales,et al.  Functional genomics of cell elongation in developing cotton fibers , 2004, Plant Molecular Biology.

[33]  S. Maury,et al.  Purification, Cloning, and Properties of an Acyltransferase Controlling Shikimate and Quinate Ester Intermediates in Phenylpropanoid Metabolism* , 2003, The Journal of Biological Chemistry.

[34]  R. Dixon,et al.  Substrate preferences of O-methyltransferases in alfalfa suggest new pathways for 3-O-methylation of monolignols. , 2008, The Plant Journal.

[35]  D. Ohta,et al.  Isolation of a cDNA and a Genomic Clone Encoding Cinnamate 4-Hydroxylase from Arabidopsis and Its Expression Manner in Planta , 1997, Plant physiology.

[36]  T. Girke,et al.  The Cell Wall Navigator Database. A Systems-Based Approach to Organism-Unrestricted Mining of Protein Families Involved in Cell Wall Metabolism1 , 2004, Plant Physiology.

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

[38]  Richard D. Thompson,et al.  Changes in gene expression in maize kernel in response to water and salt stress , 2006, Plant Cell Reports.

[39]  T. Umezawa,et al.  Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[40]  L. Montoliu,et al.  Structure and expression of the lignin O-methyltransferase gene from Zea mays L. , 1992, Plant Molecular Biology.

[41]  Deborah Goffner,et al.  Lignins and lignocellulosics: a better control of synthesis for new and improved uses. , 2003, Trends in plant science.

[42]  S. Maury,et al.  Repression of O-methyltransferase genes in transgenic tobacco affects lignin synthesis and plant growth. , 2001, Phytochemistry.

[43]  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.

[44]  Y. Barrière,et al.  Genetic variation and breeding strategies for improved cell wall digestibility in annual forage crops. A review , 2003 .

[45]  R. E. Sharp,et al.  Cell Wall Proteome in the Maize Primary Root Elongation Zone. II. Region-Specific Changes in Water Soluble and Lightly Ionically Bound Proteins under Water Deficit1[W][OA] , 2007, Plant Physiology.

[46]  A. Chesson,et al.  The newly extended maize internode: A model for the study of secondary cell wall formation and consequences for digestibility , 1993 .

[47]  J. Craig,et al.  The Xylem and Phloem Transcriptomes from Secondary Tissues of the Arabidopsis Root-Hypocotyl1[w] , 2005, Plant Physiology.

[48]  T. Umezawa,et al.  The Last Step of Syringyl Monolignol Biosynthesis in Angiosperms Is Regulated by a Novel Gene Encoding Sinapyl Alcohol Dehydrogenase , 2001, The Plant Cell Online.

[49]  S. Brunak,et al.  Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. , 2000, Journal of molecular biology.

[50]  A. Meijer,et al.  Pattern formation in the vascular system of monocot and dicot plant species. , 2004, The New phytologist.

[51]  Monika S. Doblin,et al.  Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family , 2004 .

[52]  Keith Roberts,et al.  Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices , 1990, Planta.

[53]  Y. Barrière,et al.  Nucleotide diversity of the ZmPox3 maize peroxidase gene: Relationships between a MITE insertion in exon 2 and variation in forage maize digestibility , 2004, BMC Genetics.

[54]  L. Schreiber,et al.  Chemical analysis and immunolocalisation of lignin and suberin in endodermal and hypodermal/rhizodermal cell walls of developing maize (Zea mays L.) primary roots , 1999, Planta.

[55]  Peer Bork,et al.  SMART: a web-based tool for the study of genetically mobile domains , 2000, Nucleic Acids Res..

[56]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[57]  C. Chapple,et al.  Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Michael A. Costa,et al.  Characterization in vitro and in vivo of the putative multigene 4-coumarate:CoA ligase network in Arabidopsis: syringyl lignin and sinapate/sinapyl alcohol derivative formation. , 2005, Phytochemistry.

[59]  Y. Barrière,et al.  In search of a maize ideotype for cell wall enzymatic degradability using histological and biochemical lignin characterization. , 2005, Journal of agricultural and food chemistry.

[60]  C. Chapple,et al.  Regulation of ferulate-5-hydroxylase expression in Arabidopsis in the context of sinapate ester biosynthesis. , 1999, Plant physiology.

[61]  M. Bennett,et al.  Hrp Mutant of Pseudomonas syringae pv phaseolicola Induces Cell Wall Alterations but Not Membrane Damage Leading to the Hypersensitive Reaction in Lettuce , 1995, Plant physiology.

[62]  G. Meshitsuka,et al.  The Detection of Lignin , 1992 .

[63]  B. Sundberg,et al.  A transcriptional roadmap to wood formation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[64]  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.

[65]  M. Morant,et al.  CYP98A3 from Arabidopsis thaliana Is a 3′-Hydroxylase of Phenolic Esters, a Missing Link in the Phenylpropanoid Pathway* , 2001, The Journal of Biological Chemistry.

[66]  F. Vignols,et al.  The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. , 1995, The Plant cell.

[67]  John L. Hall,et al.  Differential induction of cinnamyl alcohol dehydrogenase during defensive lignification in wheat (Triticum aestivum L.): characterisation of the major inducible form , 1999, Planta.

[68]  F. Corpet Multiple sequence alignment with hierarchical clustering. , 1988, Nucleic acids research.

[69]  Robert D. Finn,et al.  Pfam: clans, web tools and services , 2005, Nucleic Acids Res..

[70]  M. R. Hemm,et al.  New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[71]  W. Frommer,et al.  ARAMEMNON, a Novel Database for Arabidopsis Integral Membrane Proteins1 , 2003, Plant Physiology.

[72]  F. Sterky,et al.  MYB transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen , 2004, Plant Molecular Biology.

[73]  Chung-Jui Tsai,et al.  Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[74]  J. Grima-Pettenati,et al.  Cloning and characterization of two maize cDNAs encoding Cinnamoyl-CoA Reductase (CCR) and differential expression of the corresponding genes , 1998, Plant Molecular Biology.

[75]  W. Barz,et al.  Characterization and oxidative in vitro cross-linking of an extensin-like protein and a proline-rich protein purified from chickpea cell walls. , 2000, Phytochemistry.

[76]  C. Lamb,et al.  Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response , 1992, Cell.

[77]  S. Cutler,et al.  The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. , 1999, The Plant cell.

[78]  R. E. Sharp,et al.  Root Growth Maintenance at Low Water Potentials (Increased Activity of Xyloglucan Endotransglycosylase and Its Possible Regulation by Abscisic Acid) , 1994, Plant physiology.

[79]  C. Chapple,et al.  The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. , 2002, The Plant journal : for cell and molecular biology.

[80]  C. Chapple,et al.  Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. , 2000, The Plant journal : for cell and molecular biology.

[81]  A. de Waal,et al.  Isolation and characterization of a cDNA clone from Catharanthus roseus encoding NADPH:cytochrome P-450 reductase, an enzyme essential for reactions catalysed by cytochrome P-450 mono-oxygenases in plants. , 1993, The Plant journal : for cell and molecular biology.

[82]  Emmanuel Barillot,et al.  GénoPlante-Info (GPI): a collection of databases and bioinformatics resources for plant genomics , 2003, Nucleic Acids Res..

[83]  Y. Barrière,et al.  Down-Regulation of Caffeic Acid O-Methyltransferase in Maize Revisited Using a Transgenic Approach1 , 2002, Plant Physiology.

[84]  B. Hamberger,et al.  The 4-coumarate:CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[85]  P. Nilsson,et al.  A genomic approach to investigate developmental cell death in woody tissues of Populus trees , 2005, Genome Biology.

[86]  K. Nakai,et al.  PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. , 1999, Trends in biochemical sciences.

[87]  D. Roby,et al.  Gene expression in Nicotiana tabacum in response to compatible and incompatible isolates of Pseudomonas solanacearum , 1989 .

[88]  V. Brendel,et al.  Comparative genomics of Arabidopsis and maize: prospects and limitations , 2002, Genome Biology.

[89]  C. Lapierre,et al.  Thioacidolysis of Poplar Lignins: Identification of Monomeric Syringyl Products and Characterization of Guaiacyl-Syringyl Lignin Fractions , 1986 .

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