Genome-Wide Analysis of bZIP-Encoding Genes in Maize

In plants, basic leucine zipper (bZIP) proteins regulate numerous biological processes such as seed maturation, flower and vascular development, stress signalling and pathogen defence. We have carried out a genome-wide identification and analysis of 125 bZIP genes that exist in the maize genome, encoding 170 distinct bZIP proteins. This family can be divided into 11 groups according to the phylogenetic relationship among the maize bZIP proteins and those in Arabidopsis and rice. Six kinds of intron patterns (a–f) within the basic and hinge regions are defined. The additional conserved motifs have been identified and present the group specificity. Detailed three-dimensional structure analysis has been done to display the sequence conservation and potential distribution of the bZIP domain. Further, we predict the DNA-binding pattern and the dimerization property on the basis of the characteristic features in the basic and hinge regions and the leucine zipper, respectively, which supports our classification greatly and helps to classify 26 distinct subfamilies. The chromosome distribution and the genetic analysis reveal that 58 ZmbZIP genes are located in the segmental duplicate regions in the maize genome, suggesting that the segment chromosomal duplications contribute greatly to the expansion of the maize bZIP family. Across the 60 different developmental stages of 11 organs, three apparent clusters formed represent three kinds of different expression patterns among the ZmbZIP gene family in maize development. A similar but slightly different expression pattern of bZIPs in two inbred lines displays that 22 detected ZmbZIP genes might be involved in drought stress. Thirteen pairs and 143 pairs of ZmbZIP genes show strongly negative and positive correlations in the four distinct fungal infections, respectively, based on the expression profile and Pearson's correlation coefficient analysis.

[1]  D. Xie,et al.  Structural evolution and functional diversification analyses of argonaute protein , 2012, Journal of cellular biochemistry.

[2]  D. Xie,et al.  Multiple-strategy analyses of ZmWRKY subgroups and functional exploration of ZmWRKY genes in pathogen responses. , 2012, Molecular bioSystems.

[3]  Xiping Wang,et al.  bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice , 2012, Planta.

[4]  Yong Li,et al.  The Arabidopsis AtbZIP1 transcription factor is a positive regulator of plant tolerance to salt, osmotic and drought stresses , 2012, Journal of Plant Research.

[5]  Yu Li,et al.  Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis , 2012, Planta.

[6]  D. Xie,et al.  Evolution and adaptation of hemagglutinin gene of human H5N1 influenza virus , 2012, Virus Genes.

[7]  D. Xie,et al.  Molecular Phylogenetic and Expression Analysis of the Complete WRKY Transcription Factor Family in Maize , 2012, DNA research : an international journal for rapid publication of reports on genes and genomes.

[8]  Ramón Doallo,et al.  ProtTest 3: fast selection of best-fit models of protein evolution , 2011, Bioinform..

[9]  S. Ramachandran,et al.  Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. , 2011, Journal of integrative plant biology.

[10]  Ramón Doallo,et al.  ProtTest-HPC: Fast Selection of Best-Fit Models of Protein Evolution , 2010, Euro-Par Workshops.

[11]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[12]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[13]  T. Graves,et al.  The Physical and Genetic Framework of the Maize B73 Genome , 2009, PLoS genetics.

[14]  B. Han,et al.  Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice , 2009, Planta.

[15]  Ning Tang,et al.  Characterization of OsbZIP23 as a Key Player of the Basic Leucine Zipper Transcription Factor Family for Conferring Abscisic Acid Sensitivity and Salinity and Drought Tolerance in Rice1[W][OA] , 2008, Plant Physiology.

[16]  S. Chen,et al.  Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis , 2008, Planta.

[17]  Mukesh Jain,et al.  Genomic Survey and Gene Expression Analysis of the Basic Leucine Zipper Transcription Factor Family in Rice1[W][OA] , 2007, Plant Physiology.

[18]  Steven G. Schroeder,et al.  Physical and Genetic Structure of the Maize Genome Reflects Its Complex Evolutionary History , 2007, PLoS genetics.

[19]  Zhenglin Hou,et al.  delayed flowering1 Encodes a Basic Leucine Zipper Protein That Mediates Floral Inductive Signals at the Shoot Apex in Maize[W] , 2006, Plant Physiology.

[20]  David Posada,et al.  ProtTest: selection of best-fit models of protein evolution , 2005, Bioinform..

[21]  Conrad C. Huang,et al.  UCSF Chimera—A visualization system for exploratory research and analysis , 2004, J. Comput. Chem..

[22]  Klaus F. X. Mayer,et al.  Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice , 2004, The Plant Cell Online.

[23]  C. Vinson,et al.  A heterodimerizing leucine zipper coiled coil system for examining the specificity of a position interactions: amino acids I, V, L, N, A, and K. , 2002, Biochemistry.

[24]  C. Vinson,et al.  Classification of Human B-ZIP Proteins Based on Dimerization Properties , 2002, Molecular and Cellular Biology.

[25]  David Landsman,et al.  B-ZIP proteins encoded by the Drosophila genome: evaluation of potential dimerization partners. , 2002, Genome research.

[26]  E. Grotewold,et al.  MYB transcription factors in Arabidopsis. , 2002, Trends in plant science.

[27]  L. Lopez-Molina,et al.  A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  K. Shinozaki,et al.  Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  B. Gaut,et al.  Maize as a model for the evolution of plant nuclear genomes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  T. Lynch,et al.  The Arabidopsis Abscisic Acid Response Gene ABI5 Encodes a Basic Leucine Zipper Transcription Factor , 2000, Plant Cell.

[31]  S. Kim,et al.  ABFs, a Family of ABA-responsive Element Binding Factors* , 2000, The Journal of Biological Chemistry.

[32]  M. Guiltinan,et al.  The maize EmBP-1 orthologue differentially regulates Opaque2-dependent gene expression in yeast and cultured maize endosperm cells , 1999, Plant Molecular Biology.

[33]  M. Guiltinan,et al.  Bipartite determinants of DNA-binding specificity of plant basic leucine zipper proteins , 1999, Plant Molecular Biology.

[34]  M. Freeling,et al.  The liguleless2 gene of maize functions during the transition from the vegetative to the reproductive shoot apex. , 1999, The Plant journal : for cell and molecular biology.

[35]  M. Freeling,et al.  The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary. , 1998, Genes & development.

[36]  C. Vinson,et al.  Leucine is the most stabilizing aliphatic amino acid in the d position of a dimeric leucine zipper coiled coil. , 1997, Biochemistry.

[37]  E. Lam,et al.  DNA-binding properties, genomic organization and expression pattern of TGA6, a new member of the TGA family of bZIP transcription factors in Arabidopsis thaliana , 1997, Plant Molecular Biology.

[38]  M. Freeling,et al.  Interactions of liguleless1 and liguleless2 function during ligule induction in maize. , 1996, Genetics.

[39]  N. Suzuki,et al.  A maize DNA-binding factor with a bZIP motif is induced by low temperature , 1995, Molecular and General Genetics MGG.

[40]  R. Ferl,et al.  Characterization of a maize G-box binding factor that is induced by hypoxia. , 1995, The Plant journal : for cell and molecular biology.

[41]  B. Müller-Hill,et al.  Replacement of invariant bZip residues within the basic region of the yeast transcriptional activator GCN4 can change its DNA binding specificity. , 1994, Nucleic acids research.

[42]  C. Vinson,et al.  A thermodynamic scale for leucine zipper stability and dimerization specificity: e and g interhelical interactions. , 1994, The EMBO journal.

[43]  C. Vinson,et al.  Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. , 1993, Genes & development.

[44]  K. Thompson,et al.  Thermodynamic characterization of the structural stability of the coiled-coil region of the bZIP transcription factor GCN4. , 1993, Biochemistry.

[45]  D. Llewellyn,et al.  Isolation of a maize bZIP protein subfamily: candidates for the ocs-element transcription factor. , 1993, The Plant journal : for cell and molecular biology.

[46]  R. Foster,et al.  Plant bZIP protein DNA binding specificity. , 1993, Journal of molecular biology.

[47]  B. Müller-Hill,et al.  Identification of three residues in the basic regions of the bZIP proteins GCN4, C/EBP and TAF‐1 that are involved in specific DNA binding. , 1993, The EMBO journal.

[48]  R. Schmidt,et al.  OHP1: a maize basic domain/leucine zipper protein that interacts with opaque2. , 1993, The Plant cell.

[49]  K. Struhl,et al.  The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α Helices: Crystal structure of the protein-DNA complex , 1992, Cell.

[50]  R. Schmidt,et al.  Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. , 1992, The Plant cell.

[51]  P. Arruda,et al.  Partial purification and characterization of lysine-ketoglutarate reductase in normal and opaque-2 maize endosperms. , 1992, Plant physiology.

[52]  F. Salamini,et al.  The maize regulatory locus Opaque‐2 encodes a DNA‐binding protein which activates the transcription of the b‐32 gene. , 1991, The EMBO journal.

[53]  J. Tokuhisa,et al.  OCSBF-1, a maize ocs enhancer binding factor: isolation and expression during development. , 1990, The Plant cell.

[54]  S. McKnight,et al.  Scissors-grip model for DNA recognition by a family of leucine zipper proteins. , 1989, Science.

[55]  S. McKnight,et al.  The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. , 1988, Science.

[56]  A. Mclachlan,et al.  Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. , 1975, Journal of molecular biology.

[57]  A. Mackay,et al.  Crystals of glutamine synthetase from Escherichia coli. , 1975, Journal of molecular biology.

[58]  Ina Ruck,et al.  USA , 1969, The Lancet.

[59]  Peer Bork,et al.  Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation , 2007, Bioinform..

[60]  Sjef Smeekens,et al.  Dimerization specificity of all 67 B-ZIP motifs in Arabidopsis thaliana: a comparison to Homo sapiens B-ZIP motifs. , 2004, Nucleic acids research.

[61]  F. Parcy,et al.  bZIP transcription factors in Arabidopsis. , 2002, Trends in plant science.

[62]  D. Leister,et al.  Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. , 2002, Molecular biology and evolution.

[63]  H. Hurst,et al.  Transcription factors. 1: bZIP proteins. , 1994, Protein profile.

[64]  P. Arruda,et al.  The role of the Opaque2 transcriptional factor in the regulation of protein accumulation and amino acid metabolism in maize seeds. , 1994, Anais da Academia Brasileira de Ciencias.

[65]  B. Burr,et al.  Maize regulatory gene opaque-2 encodes a protein with a "leucine-zipper" motif that binds to zein DNA. , 1990, Proceedings of the National Academy of Sciences of the United States of America.