A Comparative Genome-Wide Analysis of GATA Transcription Factors in Fungi

GATA transcription factors are widespread eukaryotic regulators whose DNA-binding domain is a class IV zinc finger motif in the form followed by a basic region. In fungi, they act as transcriptional activators or repressors in several different processes, ranging from nitrogen source utilization to mating-type switching. Using an in-house bioinformatics portal system, we surveyed 50 fungal and 9 out-group genomes and identified 396 putative fungal GATA transcription factors. The proportion of GATA transcription factors within a genome varied among taxonomic lineages. Subsequent analyses of phylogenetic relationships among the fungal GATA transcription factors, as well as a study of their domain architecture and gene structure, demonstrated high degrees of conservation in type IVa and type IVb zinc finger motifs and the existence of distinctive clusters at least at the level of subphylum. The SFH1 subgroup with a 20-residue loop was newly identified, in addition to six well-defined subgroups in the subphylum Pezizomycotina. Furthermore, a novel GATA motif with a 2f-residue loop (, designated 'zinc finger type IVc') was discovered within the phylum Basidiomycota. Our results suggest that fungal GATA factors might have undergone multiple distinct modes of evolution resulting in diversified cellular modulation in fungi.

[1]  Yi Liu,et al.  Functional conservation of light, oxygen, or voltage domains in light sensing , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[2]  B. Cairns,et al.  Sfh1p, a component of a novel chromatin-remodeling complex, is required for cell cycle progression , 1997, Molecular and cellular biology.

[3]  P. Xu,et al.  urbs1, a gene regulating siderophore biosynthesis in Ustilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. , 1993, Molecular and cellular biology.

[4]  B. Barrell,et al.  The genome sequence of Schizosaccharomyces pombe , 2002, Nature.

[5]  William R. Atchley,et al.  Molecular Evolution of the GATA Family of Transcription Factors: Conservation Within the DNA-Binding Domain , 2000, Journal of Molecular Evolution.

[6]  P. Philippsen,et al.  The Ashbya gossypii Genome as a Tool for Mapping the Ancient Saccharomyces cerevisiae Genome , 2004, Science.

[7]  William H. Majoros,et al.  Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus , 2005, Nature.

[8]  Meriel G. Jones,et al.  Characterization of nitrogen metabolite signalling in Aspergillus via the regulated degradation of areA mRNA , 2001, Molecular microbiology.

[9]  J. Loros,et al.  A recessive circadian clock mutation at the frq locus of Neurospora crassa. , 1986, Genetics.

[10]  X. Mo,et al.  Cooperative action of the NIT2 and NIT4 transcription factors upon gene expression in Neurospora crassa , 2003, Current Genetics.

[11]  Katherine H. Huang,et al.  Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78 , 2004, Nature Biotechnology.

[12]  M. Krasnow,et al.  The Drosophila genome sequence: implications for biology and medicine. , 2000, Science.

[13]  J. Dunlap,et al.  Interconnected feedback loops in the Neurospora circadian system. , 2000, Science.

[14]  Sarah Calvo,et al.  Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis , 2006, Nature.

[15]  R. R. Samaha,et al.  Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. , 2000, Science.

[16]  George Newport,et al.  The diploid genome sequence of Candida albicans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  K. Isono,et al.  Genome sequencing and analysis of Aspergillus oryzae , 2005, Nature.

[18]  H. Haas,et al.  Overexpression of nreB, a New GATA Factor-encoding Gene of Penicillium chrysogenum, Leads to Repression of the Nitrate Assimilatory Gene Cluster* , 1997, The Journal of Biological Chemistry.

[19]  Elvira Carvajal,et al.  The role of the GATA factors Gln3p, Nil1p, Dal80p and the Ure2p on ASP3 regulation in Saccharomyces cerevisiae , 2003, Yeast.

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

[21]  G. R. Fabian,et al.  srd1, a Saccharomyces cerevisiae suppressor of the temperature-sensitive pre-rRNA processing defect of rrp1-1. , 1990, Genetics.

[22]  Laura Baxter,et al.  Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis , 2006, Science.

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

[24]  G. Coupland,et al.  Shedding light on the circadian clock and the photoperiodic control of flowering. , 2003, Current opinion in plant biology.

[25]  J. Beaudoin,et al.  Fep1 represses expression of the fission yeast Schizosaccharomyces pombe siderophore-iron transport system. , 2003, Nucleic acids research.

[26]  Christina A. Cuomo,et al.  Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae , 2005, Nature.

[27]  B. Dujon,et al.  Genome evolution in yeasts , 2004, Nature.

[28]  Terrance G. Cooper,et al.  The Saccharomyces cerevisiae GATA Factors Dal80p and Deh1p Can Form Homo- and Heterodimeric Complexes , 1998, Journal of bacteriology.

[29]  H. Haas.  Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage , 2003, Applied Microbiology and Biotechnology.

[30]  Hubertus Haas,et al.  The siderophore system is essential for viability of Aspergillus nidulans: functional analysis of two genes encoding l‐ornithine N 5‐monooxygenase (sidA) and a non‐ribosomal peptide synthetase (sidC) , 2003, Molecular microbiology.

[31]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .

[32]  J. Moss,et al.  Molecular Characterization of the GTPase-activating Domain of ADP-ribosylation Factor Domain Protein 1 (ARD1)* , 1998, The Journal of Biological Chemistry.

[33]  Ray Dixon,et al.  The PAS fold. A redefinition of the PAS domain based upon structural prediction. , 2004, European journal of biochemistry.

[34]  Jonathan E. Allen,et al.  The Genome of the Basidiomycetous Yeast and Human Pathogen Cryptococcus neoformans , 2005, Science.

[35]  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.

[36]  G. Winkelmann,et al.  Role of siderophores in iron storage in spores of Neurospora crassa and Aspergillus ochraceus , 1987, Journal of bacteriology.

[37]  Thomas L. Madden,et al.  BLAST: at the core of a powerful and diverse set of sequence analysis tools , 2004, Nucleic Acids Res..

[38]  George Newport,et al.  Regulatory networks affected by iron availability in Candida albicans , 2004, Molecular microbiology.

[39]  Sudhir Kumar,et al.  MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment , 2004, Briefings Bioinform..

[40]  Keith Moffat,et al.  The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. , 2003, Biochemistry.

[41]  Kap-Hoon Han,et al.  The nsdD gene encodes a putative GATA‐type transcription factor necessary for sexual development of Aspergillus nidulans , 2001, Molecular microbiology.

[42]  G. Marzluf,et al.  ASD4, a new GATA factor of Neurospora crassa, displays sequence-specific DNA binding and functions in ascus and ascospore development. , 2000, Biochemistry.

[43]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

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

[45]  M. Iranzo,et al.  The SRD2 gene is involved in Saccharomyces cerevisiae morphogenesis , 2002, Archives of Microbiology.

[46]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[47]  M. Cosma.  Daughter‐specific repression of Saccharomyces cerevisiae HO: Ash1 is the commander , 2004, EMBO reports.

[48]  Hubertus Haas,et al.  A Circadian Oscillator in Aspergillus spp. Regulates Daily Development and Gene Expression , 2003, Eukaryotic Cell.

[49]  Michael Q. Zhang,et al.  Identifying cooperativity among transcription factors controlling the cell cycle in yeast. , 2003, Nucleic acids research.

[50]  G. Macino,et al.  Blue light regulation in Neurospora crassa. , 1997, Fungal genetics and biology : FG & B.

[51]  W. Shen,et al.  Blue light negatively regulates the sexual filamentation via the Cwc1 and Cwc2 proteins in Cryptococcus neoformans , 2005, Molecular microbiology.

[52]  Kenji Matsuura,et al.  Reconstructing the early evolution of Fungi using a six-gene phylogeny , 2006, Nature.

[53]  R. Jansen,et al.  Characterization of Candida albicansASH1 in Saccharomyces cerevisiae , 2002, Current Genetics.

[54]  J. Reyes,et al.  The GATA Family of Transcription Factors in Arabidopsis and Rice1 , 2004, Plant Physiology.

[55]  P. Gilmartin,et al.  Two forms of type IV zinc-finger motif and their kingdom-specific distribution between the flora, fauna and fungi. , 1998, Trends in biochemical sciences.

[56]  Diane O. Inglis,et al.  Ash1 Protein, an Asymmetrically Localized Transcriptional Regulator, Controls Filamentous Growth and Virulence of Candida albicans , 2002, Molecular and Cellular Biology.

[57]  N. Horowitz,et al.  Isolation and identification of the conidial germination factor of Neurospora crassa , 1976, Journal of bacteriology.

[58]  H. Arst,et al.  The Aspergillus nidulans GATA transcription factor gene areB encodes at least three proteins and features three classes of mutation , 2001, Molecular microbiology.

[59]  W. Nierman,et al.  The Aspergillus fumigatus StuA protein governs the up-regulation of a discrete transcriptional program during the acquisition of developmental competence. , 2005, Molecular biology of the cell.

[60]  Michael Freitag,et al.  Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism , 2004, Microbiology and Molecular Biology Reviews.

[61]  Kwangwon Lee,et al.  Light regulation of asexual development in the rice blast fungus, Magnaporthe oryzae. , 2006, Fungal genetics and biology : FG & B.

[62]  B. Barrell,et al.  Life with 6000 Genes , 1996, Science.

[63]  C. Scazzocchio.  The fungal GATA factors. , 2000, Current opinion in microbiology.

[64]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[65]  T. Cooper,et al.  The Level of DAL80 Expression Down-Regulates GATA Factor-Mediated Transcription inSaccharomyces cerevisiae , 2000, Journal of bacteriology.

[66]  L. Fulton,et al.  Finding Functional Features in Saccharomyces Genomes by Phylogenetic Footprinting , 2003, Science.

[67]  I. Herskowitz,et al.  Ash1p is a site-specific DNA-binding protein that actively represses transcription. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[68]  H. Arst,et al.  Nitrogen regulation in Aspergillus: are two fingers better than one? , 1990, Gene.

[69]  Cathryn J. Rehmeyer,et al.  The genome sequence of the rice blast fungus Magnaporthe grisea , 2005, Nature.

[70]  M. Yaniv,et al.  Chromatin modifiers and tumor suppression. , 2001, Biochimica et biophysica acta.

[71]  G. Marzluf,et al.  The NIT2 nitrogen regulatory protein of Neurospora: expression and stability of nit-2 mRNA and protein , 1999, Current Genetics.

[72]  G. Marzluf,et al.  Interaction between Major Nitrogen Regulatory Protein NIT2 and Pathway-Specific Regulatory Factor NIT4 Is Required for Their Synergistic Activation of Gene Expression in Neurospora crassa , 1998, Molecular and Cellular Biology.