Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis

We have used oligonucleotide microarrays to detect Arabidopsis gene expression during early flower development. Among the 22,746 genes represented on the Affymetrix ATH1 chip, approximately 14,660 (64.5%) genes were expressed with signal intensity at or more than 50 in each of the six organs/structures examined, including young inflorescences (floral stages 1–9), stage-12 floral buds, developing siliques, leaves, stems, and roots. 17,583 genes were expressed with an intensity at or above 50 in at least one tissue, including 12,245 genes that were expressed in all the six tissues. Comparison of genes expressed between young inflorescence or stage-12 floral buds with other tissues suggests that relatively large numbers of genes are expressed at similar levels in tissues that are related morphologically and/or developmentally, as supported by a cluster analysis with data from two other studies. Further analysis of the genes preferentially expressed in floral tissues has uncovered new genes potentially involved in Arabidopsis flower development. One hundred and four genes were determined to be preferentially expressed in young inflorescences, including 22 genes encoding putative transcription factors. We also identified 105 genes that were preferentially expressed in three reproductive structures (the young inflorescences, stage-12 floral buds and developing siliques), when compared with the vegetative tissues. RT-PCR results of selected genes are consistent with the results from these microarrays and suggest that the relative signal intensities detected with the Affymetrix microarray are reliable estimates of gene expression.

[1]  B. Veit,et al.  Meristematic tissues in plant growth and development. , 2002 .

[2]  M. Van Montagu,et al.  Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. , 1994, The Plant cell.

[3]  J. Franco-Zorrilla,et al.  AtREM 1 , a Member of a New Family of B 3 Domain-Containing Genes , Is Preferentially Expressed in Reproductive Meristems 1 , 2002 .

[4]  Cindy Gustafson-Brown,et al.  Molecular characterization of the Arabidopsis floral homeotic gene APETALA1 , 1992, Nature.

[5]  E. Mcwhinnie,et al.  The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana. , 1994, Gene.

[6]  J. Levin,et al.  UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. , 1995, The Plant cell.

[7]  E. Meyerowitz,et al.  Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Parish,et al.  AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. , 2003, The Plant journal : for cell and molecular biology.

[9]  Gordon K Smyth,et al.  Statistical Applications in Genetics and Molecular Biology Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments , 2011 .

[10]  European Union Chromosome 3 Arabidopsis Genome Sequencing Consortium,et al.  Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana , 2000, Nature.

[11]  Rongchen Wang,et al.  Microarray Analysis of the Nitrate Response in Arabidopsis Roots and Shoots Reveals over 1,000 Rapidly Responding Genes and New Linkages to Glucose, Trehalose-6-Phosphate, Iron, and Sulfate Metabolism1[w] , 2003, Plant Physiology.

[12]  Xuemei Chen,et al.  HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. , 2002, Development.

[13]  H. Ma,et al.  Isolation of cDNAs encoding guanine nucleotide-binding protein beta-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1). , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Jean YH Yang,et al.  Bioconductor: open software development for computational biology and bioinformatics , 2004, Genome Biology.

[15]  D. Horner,et al.  Molecular and Phylogenetic Analyses of the Complete MADS-Box Transcription Factor Family in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011544. , 2003, The Plant Cell Online.

[16]  M. West,et al.  LEAFY COTYLEDON1 Is an Essential Regulator of Late Embryogenesis and Cotyledon Identity in Arabidopsis. , 1994, The Plant cell.

[17]  M. Yanofsky Floral Meristems to Floral Organs: Genes Controlling Early Events in Arabidopsis Flower Development , 1995 .

[18]  D. Weigel,et al.  The F-box-containing protein UFO and AGAMOUS participate in antagonistic pathways governing early petal development in Arabidopsis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Hong Ma,et al.  Regulation of Flower Development in Arabidopsis by SCF Complexes1 , 2004, Plant Physiology.

[20]  Elliot M. Meyerowitz,et al.  Genome-Wide Analysis of Spatial Gene Expression in Arabidopsis Flowers , 2004, The Plant Cell Online.

[21]  P. Herrmann,et al.  FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[22]  G. Haughn,et al.  UNUSUAL FLORAL ORGANS Controls Meristem Identity and Organ Primordia Fate in Arabidopsis. , 1995, The Plant cell.

[23]  Yiwen Fang,et al.  Comprehensive gene expression analysis by transcript profiling , 2004, Plant Molecular Biology.

[24]  E. Meyerowitz,et al.  The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana. , 1999, Genes & development.

[25]  Christopher D Town,et al.  Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. , 2004, The Plant journal : for cell and molecular biology.

[26]  E. Meyerowitz,et al.  Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. , 1994, Genes & development.

[27]  W. Crosby,et al.  The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. , 1999, The Plant journal : for cell and molecular biology.

[28]  D. Soltis,et al.  The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history. , 2005, Genetics.

[29]  C. Cepko,et al.  The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation , 2002, Development.

[30]  E. Meyerowitz,et al.  HUA1 and HUA2 are two members of the floral homeotic AGAMOUS pathway. , 1999, Molecular cell.

[31]  Hong Ma,et al.  The ASK1 gene regulates development and interacts with the UFO gene to control floral organ identity in Arabidopsis. , 1999, Developmental genetics.

[32]  E. Meyerowitz,et al.  AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. , 1991, Genes & development.

[33]  Detlef Weigel,et al.  Dissection of floral induction pathways using global expression analysis , 2003, Development.

[34]  Hong Ma,et al.  Spatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant arabidopsis flowers , 1994, Plant Molecular Biology.

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

[36]  J. Bowman,et al.  Early flower development in Arabidopsis. , 1990, The Plant cell.

[37]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[38]  L. Lepiniec,et al.  LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Hong Ma,et al.  Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin‐like protein , 2002, The EMBO journal.

[40]  Rafael A Irizarry,et al.  Exploration, normalization, and summaries of high density oligonucleotide array probe level data. , 2003, Biostatistics.

[41]  Hong Ma,et al.  The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors , 1990, Nature.

[42]  J. Bowman,et al.  Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product , 1991, Cell.

[43]  Yuval Eshed,et al.  SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis , 2000, Nature.

[44]  P. Robles,et al.  The SEP4 Gene of Arabidopsis thaliana Functions in Floral Organ and Meristem Identity , 2004, Current Biology.

[45]  B. S. Everitt,et al.  Cluster analysis , 2014, Encyclopedia of Social Network Analysis and Mining.

[46]  B. Scheithauer,et al.  DNA microarrays , 2005, Endocrine.

[47]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  L. Hennig,et al.  Arabidopsis transcript profiling on Affymetrix GeneChip arrays , 2003, Plant Molecular Biology.

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

[50]  P. Piffanelli,et al.  Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana , 1998, Nature.

[51]  G. Ditta,et al.  Assessing the redundancy of MADS-box genes during carpel and ovule development , 2003, Nature.

[52]  M. Takemura,et al.  Characterization of a Novel Gene Encoding a Putative Single Zinc-finger Protein, ZIM, Expressed during the Reproductive Phase in Arabidopsis thaliana , 2000, Bioscience, biotechnology, and biochemistry.

[53]  G. Ditta,et al.  B and C floral organ identity functions require SEPALLATA MADS-box genes , 2000, Nature.

[54]  Hong Ma,et al.  The unfolding drama of flower development: recent results from genetic and molecular analyses. , 1994, Genes & development.

[55]  H. Ma,et al.  Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. , 1996, The Plant journal : for cell and molecular biology.

[56]  H. Ma,et al.  The ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in Arabidopsis. , 2001, Development.

[57]  Claude W. dePamphilis,et al.  Genome-Wide Analysis of the Cyclin Family in Arabidopsis and Comparative Phylogenetic Analysis of Plant Cyclin-Like Proteins1[w] , 2004, Plant Physiology.

[58]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[59]  Cindy Gustafson-Brown,et al.  Regulation of the arabidopsis floral homeotic gene APETALA1 , 1994, Cell.

[60]  Lucia Colombo,et al.  MADS-Box Protein Complexes Control Carpel and Ovule Development in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.015123. , 2003, The Plant Cell Online.

[61]  R. Simon,et al.  Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. , 1995, The Plant cell.

[62]  Elliot M. Meyerowitz,et al.  The ABCs of floral homeotic genes , 1994, Cell.

[63]  F. Bertucci,et al.  [DNA microarrays for gene expression profiling of breast cancer: principles and prognostic applications]. , 2006, Pathologie-biologie.

[64]  Pilar Cubas,et al.  AtREM1, a Member of a New Family of B3 Domain-Containing Genes, Is Preferentially Expressed in Reproductive Meristems1 , 2002, Plant Physiology.

[65]  J. Hancock,et al.  Regulation of the Arabidopsis transcriptome by oxidative stress. , 2001, Plant physiology.

[66]  W Ansorge,et al.  Sequence and analysis of chromosome 3 of the plant Arabidopsis thaliana. , 2000, Nature.

[67]  Hong Ma,et al.  The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein , 1995, Plant Molecular Biology.

[68]  W. McCombie,et al.  The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[69]  P. Herrmann,et al.  FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[70]  T. Jack New members of the floral organ identity AGAMOUS pathway. , 2002, Trends in plant science.

[71]  fusca3: A Heterochronic Mutation Affecting Late Embryo Development in Arabidopsis. , 1994, The Plant cell.

[72]  J. Alvarez,et al.  CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. , 1999, Development.

[73]  Elliot M. Meyerowitz,et al.  Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries , 1995, Nature.

[74]  M. Holdsworth,et al.  Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. , 2000, The Plant journal : for cell and molecular biology.

[75]  Elliot M. Meyerowitz,et al.  The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens , 1992, Cell.

[76]  Ingrid Lönnstedt Replicated microarray data , 2001 .

[77]  S. Rounsley,et al.  Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. , 1995, The Plant cell.

[78]  L. Hennig,et al.  Transcriptional Programs of Early Reproductive Stages in Arabidopsis1[w] , 2004, Plant Physiology.