Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa)

BackgroundCCCH zinc finger proteins contain a typical motif of three cysteines and one histidine residues and serve regulatory functions at all stages of mRNA metabolism. In plants, CCCH type zinc finger proteins comprise a large gene family represented by 68 members in Arabidopsis and 67 in rice. These CCCH proteins have been shown to play diverse roles in plant developmental processes and environmental responses. However, this family has not been studied in the model tree species Populus to date.ResultsIn the present study, a comprehensive analysis of the genes encoding CCCH zinc finger family in Populus was performed. Using a thorough annotation approach, a total of 91 full-length CCCH genes were identified in Populus, of which most contained more than one CCCH motif and a type of non-conventional C-X11-C-X6-C-X3-H motif was unique for Populus. All of the Populus CCCH genes were phylogeneticly clustered into 13 distinct subfamilies. In each subfamily, the gene structure and motif composition were relatively conserved. Chromosomal localization of these genes revealed that most of the CCCHs (81 of 90, 90 %) are physically distributed on the duplicated blocks. Thirty-four paralogous pairs were identified in Populus, of which 22 pairs (64.7 %) might be created by the whole genome segment duplication, whereas 4 pairs seem to be resulted from tandem duplications. In 91 CCCH proteins, we also identified 63 putative nucleon-cytoplasm shuttling proteins and 3 typical RNA-binding proteins. The expression profiles of all Populus CCCH genes have been digitally analyzed in six tissues across different developmental stages, and under various drought stress conditions. A variety of expression patterns of CCCH genes were observed during Populus development, of which 34 genes highly express in root and 22 genes show the highest level of transcript abundance in differentiating xylem. Quantitative real-time RT-PCR (RT-qPCR) was further performed to confirm the tissue-specific expression and responses to drought stress treatment of 12 selected Populus CCCH genes.ConclusionsThis study provides the first systematic analysis of the Populus CCCH proteins. Comprehensive genomic analyses suggested that segmental duplications contribute significantly to the expansion of Populus CCCH gene family. Transcriptome profiling provides first insights into the functional divergences among members of Populus CCCH gene family. Particularly, some CCCH genes may be involved in wood development while others in drought tolerance regulation. Our results presented here may provide a starting point for the functional dissection of this family of potential RNA-binding proteins.

[1]  P. Blackshear,et al.  The Arabidopsis Tandem Zinc Finger Protein AtTZF1 Traffics between the Nucleus and Cytoplasmic Foci and Binds Both DNA and RNA12[C][W][OA] , 2009, Plant Physiology.

[2]  John Quackenbush,et al.  Genesis: cluster analysis of microarray data , 2002, Bioinform..

[3]  C. Douglas,et al.  Populus: a model system for plant biology. , 2007, Annual review of plant biology.

[4]  Ingo Dreyer,et al.  PlnTFDB: an integrative plant transcription factor database , 2007, BMC Bioinformatics.

[5]  Wilfred W. Li,et al.  MEME: discovering and analyzing DNA and protein sequence motifs , 2006, Nucleic Acids Res..

[6]  L. Hurst The Ka/Ks ratio: diagnosing the form of sequence evolution. , 2002, Trends in genetics : TIG.

[7]  S. Iuchi Zinc Finger Proteins: From Atomic Contact to Cellular Function , 2010 .

[8]  François Tardieu,et al.  Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours , 1998 .

[9]  F. B. Pickett,et al.  Splitting pairs: the diverging fates of duplicated genes , 2002, Nature Reviews Genetics.

[10]  Z. Peng,et al.  Consensus-derived structural determinants of the ankyrin repeat motif , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[12]  Erin T. Hamanishi,et al.  Intraspecific variation in the Populus balsamifera drought transcriptome. , 2010, Plant, cell & environment.

[13]  Lei Wang,et al.  OsLIC, a Novel CCCH-Type Zinc Finger Protein with Transcription Activation, Mediates Rice Architecture via Brassinosteroids Signaling , 2008, PloS one.

[14]  Peer Bork,et al.  SMART 4.0: towards genomic data integration , 2004, Nucleic Acids Res..

[15]  Y. Kamiya,et al.  SOMNUS, a CCCH-Type Zinc Finger Protein in Arabidopsis, Negatively Regulates Light-Dependent Seed Germination Downstream of PIL5[W] , 2008, The Plant Cell Online.

[16]  An-Yuan Guo,et al.  [GSDS: a gene structure display server]. , 2007, Yi chuan = Hereditas.

[17]  Wenying Xu,et al.  A Novel Nuclear-Localized CCCH-Type Zinc Finger Protein, OsDOS, Is Involved in Delaying Leaf Senescence in Rice1[W] , 2006, Plant Physiology.

[18]  P. Blackshear,et al.  Tandem CCCH Zinc Finger Proteins in mRNA Binding , 2005 .

[19]  M. Filipecki,et al.  Characterization of CsSEF1 gene encoding putative CCCH-type zinc finger protein expressed during cucumber somatic embryogenesis. , 2009, Journal of plant physiology.

[20]  A. Déjardin,et al.  Genome-Wide Analysis of LIM Gene Family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa , 2007, DNA research : an international journal for rapid publication of reports on genes and genomes.

[21]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[22]  Rolf Apweiler,et al.  InterProScan: protein domains identifier , 2005, Nucleic Acids Res..

[23]  W. Yin,et al.  The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana , 2010, Journal of experimental botany.

[24]  H. Takatsuji,et al.  Zinc-finger transcription factors in plants , 1998, Cellular and Molecular Life Sciences CMLS.

[25]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[26]  G. Seydoux,et al.  PIE-1 is a bifunctional protein that regulates maternal and zygotic gene expression in the embryonic germ line of Caenorhabditis elegans. , 2001, Genes & development.

[27]  D. Weston,et al.  Populus Responses to Edaphic and Climatic Cues: Emerging Evidence from Systems Biology Research , 2009 .

[28]  W. Stemmer,et al.  Directed evolution of proteins by exon shuffling , 2001, Nature Biotechnology.

[29]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[30]  N. Kuldell,et al.  Zinc Finger Proteins: From Atomic Contact to Cellular Function , 2010 .

[31]  P. Blackshear,et al.  Necrosis Factor Alpha Mrna Deadenylation and Destabilization of Tumor Au-rich Elements and Promotes the Evidence That Tristetraprolin Binds To , 1999 .

[32]  V. Solovyev,et al.  Ab initio gene finding in Drosophila genomic DNA. , 2000, Genome research.

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

[34]  J. Lykke-Andersen,et al.  TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. , 2007, Genes & development.

[35]  Palitha Dharmawardhana,et al.  Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa , 2010, BMC Genomics.

[36]  Synan F. AbuQamar,et al.  Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. , 2006, The Plant journal : for cell and molecular biology.

[37]  Ge Gao,et al.  DPTF: a database of poplar transcription factors , 2007, Bioinform..

[38]  Rainer Breitling,et al.  Iterative Group Analysis (iGA): A simple tool to enhance sensitivity and facilitate interpretation of microarray experiments , 2004, BMC Bioinformatics.

[39]  T. Hinckley,et al.  Biology of populus and its implications for management and conservation , 1996 .

[40]  Andrew Jewell,et al.  TIS11 Family Proteins and Their Roles in Posttranscriptional Gene Regulation , 2009, Journal of biomedicine & biotechnology.

[41]  Michael Moore,et al.  Recent developments in the engineering of zinc finger proteins. , 2003, Briefings in functional genomics & proteomics.

[42]  Kyung-Hwan Han,et al.  Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[43]  Guodong Yang,et al.  Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice , 2008, BMC Genomics.

[44]  Nicholas J Provart,et al.  Genotype and time of day shape the Populus drought response. , 2009, The Plant journal : for cell and molecular biology.

[45]  Gerald A Tuskan,et al.  Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa , 2007, BMC Plant Biology.

[46]  Jesús Vicente-Carbajosa,et al.  Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families , 2003, BMC Evolutionary Biology.

[47]  T. Thomas,et al.  PEI1, an Embryo-Specific Zinc Finger Protein Gene Required for Heart-Stage Embryo Formation in Arabidopsis , 1998, Plant Cell.

[48]  P. Blackshear,et al.  Interactions of CCCH Zinc Finger Proteins with mRNA , 2000, The Journal of Biological Chemistry.

[49]  M. Carrington,et al.  Genome-wide in silico screen for CCCH-type zinc finger proteins of Trypanosoma brucei, Trypanosoma cruzi and Leishmania major , 2010, BMC Genomics.

[50]  Feng Chen,et al.  OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups , 2005, Nucleic Acids Res..

[51]  Y. Kohara,et al.  Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans , 2003, Development.

[52]  Paul Horton,et al.  Nucleic Acids Research Advance Access published May 21, 2007 WoLF PSORT: protein localization predictor , 2007 .

[53]  Robert J. Schmitz,et al.  FRIGIDA-ESSENTIAL 1 interacts genetically with FRIGIDA and FRIGIDA-LIKE 1 to promote the winter-annual habit of Arabidopsis thaliana , 2005, Development.

[54]  P. Blackshear Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. , 2001, Biochemical Society transactions.

[55]  M. Martin-Magniette,et al.  Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes , 2010, BMC Genomics.

[56]  R. Zhong,et al.  Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors1[C][OA] , 2009, Plant Physiology.

[57]  Björn Sundberg,et al.  Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. , 2008, Current opinion in plant biology.

[58]  Hong Ma,et al.  Genome-Wide Analysis of Basic/Helix-Loop-Helix Transcription Factor Family in Rice and Arabidopsis1[W] , 2006, Plant Physiology.

[59]  L. Paillard,et al.  AU-rich elements and associated factors: are there unifying principles? , 2006, Nucleic acids research.

[60]  Qi Xie,et al.  The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. , 2007, Plant & cell physiology.

[61]  Justin Foong,et al.  Expansion and Diversification of the Populus R2R3-MYB Family of Transcription Factors1[W][OA] , 2008, Plant Physiology.

[62]  Andrea Barta,et al.  Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. , 2002, Nucleic acids research.

[63]  Ashutosh Kumar Singh,et al.  MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress , 2007, BMC Genomics.

[64]  E. Koonin,et al.  Orthology, paralogy and proposed classification for paralog subtypes. , 2002, Trends in genetics : TIG.

[65]  Ying Guo,et al.  GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5. , 2009, The New phytologist.

[66]  Abdelali Barakat,et al.  The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression , 2009, BMC Plant Biology.

[67]  Ting Lan,et al.  Extensive Functional Diversification of the Populus Glutathione S-Transferase Supergene Family[C][W] , 2009, The Plant Cell Online.

[68]  Liangjiang Wang,et al.  The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants , 2005, BMC Evolutionary Biology.

[69]  Maria Carmo-Fonseca,et al.  The rules and roles of nucleocytoplasmic shuttling proteins , 2001, FEBS letters.

[70]  Marcelo C Pomeranz,et al.  AtTZF gene family localizes to cytoplasmic foci , 2010, Plant signaling & behavior.

[71]  P. Puigdoménech,et al.  Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. , 2004, Gene.

[72]  Junjie Li,et al.  HUA1, a Regulator of Stamen and Carpel Identities in Arabidopsis, Codes for a Nuclear RNA Binding Protein , 2001, The Plant Cell Online.

[73]  S. Strauss,et al.  Poplar genomics comes of age. , 2004, The New phytologist.

[74]  S. Strauss,et al.  Poplar genome sequence: functional genomics in an ecologically dominant plant species. , 2004, Trends in plant science.

[75]  H. Dyson,et al.  Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d , 2004, Nature Structural &Molecular Biology.

[76]  P. Blackshear,et al.  Tristetraprolin and Its Family Members Can Promote the Cell-Free Deadenylation of AU-Rich Element-Containing mRNAs by Poly(A) Ribonuclease , 2003, Molecular and Cellular Biology.

[77]  Gerald A. Tuskan,et al.  Divergence of the Dof Gene Families in Poplar, Arabidopsis, and Rice Suggests Multiple Modes of Gene Evolution after Duplication1[W] , 2006, Plant Physiology.

[78]  P. Kosarev,et al.  Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome , 2002, Genome Biology.

[79]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[80]  T. Tschaplinski,et al.  Water-stress tolerance of black and eastern cottonwood clones and four hybrid progeny. I. Growth, water relations, and gas exchange , 1994 .

[81]  S. Yanagisawa Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. , 2004, Plant & cell physiology.

[82]  R. Dixon,et al.  Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants , 2010, Proceedings of the National Academy of Sciences.

[83]  M. Fu,et al.  Genome-Wide Survey and Expression Profiling of CCCH-Zinc Finger Family Reveals a Functional Module in Macrophage Activation , 2008, PloS one.

[84]  Qian Gao,et al.  Comprehensive Analysis of NAC Domain Transcription Factor Gene Family in Populus trichocarpa , 2010, BMC Plant Biology.

[85]  C. Barbas,et al.  Controlling gene expression in plants using synthetic zinc finger transcription factors. , 2002, The Plant journal : for cell and molecular biology.