Abstract
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.
Similar content being viewed by others
References
Affymetrix 2001. GeneChip expression analysis overview. www.Affymetrix.com.
J.M. Alonso A.N. Stepanova T.J. Leisse C.J. Kim H. Chen P. Shinn D.K. Stevenson J. Zimmerman P. Barajas R. Cheuk C. Gadrinab C. Heller A. Jeske E. Koesema C.C. Meyers H. Parker L. Prednis Y. Ansari N. Choy H. Deen M. Geralt N. Hazari E. Hom M. Karnes C. Mulholland R. Ndubaku I. Schmidt P. Guzman L. Aguilar-Henonin M. Schmid D. Weigel D.E. Carter T. Marchand E. Risseeuw D. Brogden A. Zeko W.L. Crosby C.C. Berry J.R. Ecker (2003) ArticleTitleGenome-wide insertional mutagenesis of Arabidopsis thaliana Science 301 653–657
J. Alvarez D.R. Smyth (1999) ArticleTitleCRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS Development 126 2377–2386
Arabidopsis Genome Initiative (2000) ArticleTitleAnalysis of the genome sequence of the flowering plant Arabidopsis thaliana Nature 408 796–815
Y. Azumi D. Liu D. Zhao W. Li G. Wang Y. Hu H. Ma (2002) ArticleTitleHomolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein EMBO J. 21 3081–3095
M. Bevan I. Bancroft E. Bent K. Love H. Goodman C. Dean R. Bergkamp W. Dirkse M. Staveren ParticleVan W. Stiekema L. Drost P. Ridley S.A. Hudson K. Patel G. Murphy P. Piffanelli H. Wedler E. Wedler R. Wambutt T. Weitzenegger T.M. Pohl N. Terryn J. Gielen R. Villarroel N. Chalwatzis (1998) ArticleTitleAnalysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana Nature 391 485–488
X. Chen E.M. Meyerowitz (1999) ArticleTitleHUA1 and HUA2 are two members of the floral homeotic AGAMOUS pathway Mol. Cell 3 349–360
X. Chen J. Liu Y. Cheng D. Jia (2002b) ArticleTitleHEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower Development 129 1085–1094
C.F. Chuang M.P. Running R.W. Williams E.M. Meyerowitz (1999) ArticleTitleThe PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana Genes Dev. 13 334–344
R.S.A.H.-M. Desikan J.T. Hancock S.J. Neill (2001) ArticleTitleRegulation of the Arabidopsis transcriptome by oxidative stress Plant Physiol. 127 159–172
G. Ditta A. Pinyopich P. Robles S. Pelaz M.F. Yanofsky (2004) ArticleTitleThe SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity Curr. Biol. 14 1935–1940
J. Donson Y. Fang G. Espiritu-Santo W. Xing A. Salazar S. Miyamoto V. Armendarez W. Volkmuth (2002) ArticleTitleComprehensive gene expression analysis by transcript profiling Plant Mol. Biol. 48 75–97
G.N. Drews J.L. Bowman E.M. Meyerowitz (1991) ArticleTitleNegative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product Cell 65 991–1002
T. Durfee J.L. Roe R.A. Sessions C. Inouye K. Serikawa K.A. Feldmann D. Weigel P.C. Zambryski (2003) ArticleTitleThe F-box-containing protein UFO and AGAMOUS participate in antagonistic pathways governing early petal development in Arabidopsis Proc. Natl. Acad. Sci. USA 100 8571–8576
B.S. Everitt (1980) Cluster Analysis EditionNumber2nd Heineman-Educational Books Ltd London
R. Favaro A. Pinyopich R. Battaglia M. Kooiker L. Borghi G. Ditta M.F. Yanofsky M.M. Kater L. Colombo (2003) ArticleTitleMADS-box protein complexes control carpel and ovule development in Arabidopsis Plant Cell 15 2603–2611
Felsenstein, J. 2004. Phylip: Phylogeny Inference Package V 3.6. http://evolution.genetics.washington.edu/phylip.html.
C.A. Flanagan H. Ma (1994) ArticleTitleSpatially and temporally regulated expression of the MADS-box gene AGL2 in wild-type and mutant Arabidopsis flowers Plant Mol. Biol. 26 581–595
C.A. Flanagan Y. Hu H. Ma (1996) ArticleTitleSpecific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development Plant J. 10 343–353
J.M. Franco-Zorrilla P. Cubas J.A. Jarillo B. Fernandez-Calvin J. Salinas J.M. Martinez-Zapater (2002) ArticleTitleAtREM1, a member of a new family of B3 domain-containing genes, is preferentially expressed in reproductive meristems Plant Physiol. 128 418–427
Gentleman, R.C., Carey, V.J., Bates, D.J., Bolstad, B.M., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C.S., Maechler, M., Rossini, A.J., Sawitzki, G., Smith, C., Smyth, G.K., Tierney, L., Yang, Y.H. and Zhang, J. 2004. Bioconductor: Open software development for computational biology and bioinformatics. http://www.bepress.com/bioconductor/paper1/.
K. Goto E. Meyerowitz (1994) ArticleTitleFunction and regulation of the Arabidopsis floral homeotic gene PISTILLATA Genes Dev. 8 1548–1560
C. Gustafson-Brown B. Savidge M.F. Yanofsky (1994) ArticleTitleRegulation of the Arabidopsis floral homeotic gene APETALA1 Cell 76 131–143
L. Hennig M. Menges J.A. Murray W. Gruissem (2003) ArticleTitleArabidopsis transcript profiling on Affymetrix GeneChip arrays Plant Mol. Biol. 53 457–465
L. Hennig W. Gruissem U. Grossniklaus C. Kohler (2004) ArticleTitleTranscriptional programs of early reproductive stages in Arabidopsis Plant Physiol. 135 1765–1775
T. Higginson S.F. Li R.W. Parish (2003) ArticleTitleAtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana Plant J. 35 177–192
H. Huang M. Tudor C.A. Weiss Y. Hu H. Ma (1995) ArticleTitleThe Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein Plant Mol. Biol. 28 549–567
T.R. Hughes D.D. Shoemaker (2001) ArticleTitleDNA microarrays for expression profiling Curr. Opin. Chem. Biol. 5 21–25
R. Ihaka R. Gentleman (1996) ArticleTitleR: A language for data analysis and graphics: J. Comput. Graph. Stat. 5 299–314
G.C. Ingram J. Goodrich M.D. Wilkinson R. Simon G.W. Haughn E.S. Coen (1995) ArticleTitleParallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum Plant Cell 7 1501–1510
Irizarry (2003) ArticleTitleExploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 4 249–264
T. Jack L.L. Brockman E.M. Meyerowitz (1992) ArticleTitleThe homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens Cell 68 683–697
T. Jack (2002) ArticleTitleNew members of the floral organ identity AGAMOUS pathway Trends Plant Sci. 7 286–287
K.D. Jofuku B.G. Boer Particleden M. Montagu ParticleVan J.K. Okamuro (1994) ArticleTitleControl of Arabidopsis flower and seed development by the homeotic gene APETALA2 Plant Cell 6 1211–1225
K. Keith M. Kraml N.G. Dengler P. McCourt (1994) ArticleTitlefusca3: A heterochronic mutation affecting late embryo development in Arabidopsis Plant Cell 6 589–600
S. Kurup H.D. Jones M.J. Holdsworth (2000) ArticleTitleInteractions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds Plant J. 21 143–155
J.Z. Levin E.M. Meyerowitz (1995) ArticleTitleUFO: an Arabidopsis gene involved in both floral meristem and floral organ development Plant Cell 7 529–548
S.J. Liljegren G.S. Ditta Y. Eshed B. Savidge J.L. Bowman M.F. Yanofsky (2000) ArticleTitleSHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis Nature 404 766–770
I. Lönnstedt T.P. Speed (2002) ArticleTitleReplicated microarray data Stat/ Sinica 12 31–46
H. Luerssen V. Kirik P. Herrmann S. Misera (1998) ArticleTitleFUSCA3 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 Plant J. 15 755–764
H. Ma M.F. Yanofsky E.M. Meyerowitz (1990) ArticleTitleMolecular cloning and characterization of GPA1, a G protein α subunit gene from Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 87 3821–3825
H. Ma M.F. Yanofsky E.M. Meyerowitz (1991) ArticleTitleAGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes Genes Dev. 5 484–495
H. Ma (1994) ArticleTitleThe unfolding drama of flower development: recent results from genetic and molecular analyses Genes Dev. 8 745–756
M.A. Mandel C. Gustafson-Brown B. Savidge M.F. Yanofsky (1992) ArticleTitleMolecular characterization of the Arabidopsis floral homeotic gene APETALA1 Nature 360 273–277
B.A. Moffatt E.A. McWhinnie S.K. Agarwal D.A. Schaff (1994) ArticleTitleThe adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana Gene 143 211–216
W. Ni W. Li X. Zhang W. Hu W. Zhang G. Wang T. Han L.M. Zahn D. Zhao H. Ma (2005) Genetic control of reproductive development in flowering plants R.P. Sharma (Eds) Molecular Plant Physiology Haworth Press New York
W. Ni D. Xie L. Hobbie B. Feng D. Zhao J. Akkara H. Ma (2004) ArticleTitleRegulation of flower development in Arabidopsis by SCF complexes Plant Physiol. 134 1574–1585
A. Nishii M. Takemura H. Fujita M. Shikata A. Yokota T. Kohchi (2000) ArticleTitleCharacterization of a novel gene encoding a putative single zinc-finger protein, ZIM, expressed during the reproductive phase in Arabidopsis thaliana Biosci. Biotechnol. Biochem. 64 1402–1409
L. Parenicova S. Folter Particlede M. Kieffer D.S. Horner C. Favalli J. Busscher H.E. Cook R.M. Ingram M.M. Kater B. Davies G.C. Angenent L. Colombo (2003) ArticleTitleMolecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world Plant Cell 15 1538–1551
S. Pelaz G.S. Ditta E. Baumann E. Wisman M.F. Yanofsky (2000) ArticleTitleB and C floral organ identity functions require SEPALLATA MADS-box genes Nature 405 200–203
A. Pinyopich G.S. Ditta B. Savidge S.J. Liljegren E. Baumann E. Wisman M.F. Yanofsky (2003) ArticleTitleAssessing the redundancy of MADS-box genes during carpel and ovule development Nature 424 85–88
J.C. Redman B.J. Haas G. Tanimoto C.D. Town (2004) ArticleTitleDevelopment and evaluation of an Arabidopsis whole genome Affymetrix probe array Plant J. 38 545–561
J.L. Riechmann J. Heard G. Martin L. Reuber C. Jiang J. Keddie L. Adam O. Pineda O.J. Ratcliffe R.R. Samaha R. Creelman M. Pilgrim P. Broun J.Z. Zhang D. Ghandehari B.K. Sherman G. Yu (2000) ArticleTitleArabidopsis transcription factors: genome-wide comparative analysis among eukaryotes Science 290 2105–2110
H. Sakai L.J. Medrano E.M. Meyerowitz (1995) ArticleTitleRole of SUPERMAN in maintaining Arabidopsis floral whorl boundaries Nature 378 199–203
M. Salanoubat K. Lemcke M. Rieger W. Ansorge M. Unseld B. Fartmann G. Valle H. Blocker M. Perez-Alonso B. Obermaier M. Delseny M. Boutry L.A. Grivell R. Mache P. Puigdomenech V. Simone ParticleDe N. Choisne F. Artiguenave C. Robert P. Brottier P. Wincker L. Cattolico J. Weissenbach W. Saurin F. Quetier M. Schafer S. Muller-Auer C. Gabel M. Fuchs V. Benes E. Wurmbach H. Drzonek H. Erfle N. Jordan S. Bangert R. Wiedelmann H. Kranz H. Voss R. Holland P. Brandt G. Nyakatura A. Vezzi M. D′Angelo A. Pallavicini S. Toppo B. Simionati A. Conrad K. Hornischer G. Kauer T.H. Lohnert G. Nordsiek J. Reichelt M. Scharfe O. Schon M. Bargues J. Terol J. Climent P. Navarro C. Collado A. Perez-Perez B. Ottenwalder D. Duchemin R. Cooke M. Laudie C. Berger-Llauro B. Purnelle D. Masuy M. Haan Particlede A.C. Maarse J.P. Alcaraz A. Cottet E. Casacuberta A. Monfort A. Argiriou M. Flores R. Liguori D. Vitale G. Mannhaupt D. Haase H. Schoof S. Rudd P. Zaccaria H.W. Mewes K.F. Mayer S. Kaul C.D. Town H.L. Koo L.J. Tallon J. Jenkins T. Rooney M. Rizzo A. Walts T. Utterback C.Y. Fujii T.P. Shea T.H. Creasy B. Haas R. Maiti D. Wu J. Peterson S. Aken ParticleVan G. Pai J. Militscher P. Sellers J.E. Gill T.V. Feldblyum D. Preuss X. Lin W.C. Nierman S.L. Salzberg O. White J.C. Venter C.M. Fraser T. Kaneko Y. Nakamura S. Sato T. Kato E. Asamizu S. Sasamoto T. Kimura K. Idesawa K. Kawashima Y. Kishida C. Kiyokawa M. Kohara M. Matsumoto A. Matsuno A. Muraki S. Nakayama N. Nakazaki S. Shinpo C. Takeuchi T. Wada A. Watanabe M. Yamada M. Yasuda S. Tabata (2000) ArticleTitleSequence and analysis of chromosome 3 of the plant Arabidopsis thaliana Nature 408 820–822
A. Samach J.E. Klenz S.E. Kohalmi E. Risseeuw G.W. Haughn W.L. Crosby (1999) ArticleTitleThe UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem Plant J. 20 433–445
B. Savidge S.D. Rounsley M.F. Yanofsky (1995) ArticleTitleTemporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes Plant Cell 7 721–733
M. Schmid N.H. Uhlenhaut F. Godard M. Demar R. Bressan D. Weigel J.U. Lohmann (2003) ArticleTitleDissection of floral induction pathways using global expression analysis Development 130 6001–6012
D.R. Smyth J.L. Bowman E.M. Meyerowitz (1990) ArticleTitleEarly flower development in Arabidopsis Plant Cell 2 755–767
Smyth, G.K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statist. Appl. Genet. Mol. Biol. 3: Article 3, http://www.bepress.com/sagmb/vol3/iss1/art3.
S.L. Stone L.W. Kwong K.M. Yee J. Pelletier L. Lepiniec R.L. Fischer R.B. Goldberg J.J. Harada (2001) ArticleTitleLEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development Proc. Natl. Acad. Sci. USA 98 11806–11811
J.D. Storey R. Tibshirani (2003) ArticleTitleStatistical significance for genome-wide studies Proc. Natl. Acad. Sci. USA 100 9440–9445
G. Wang H. Kong Y. Sun X. Zhang W. Zhang N. Altman C.W. DePamphilis H. Ma (2004) ArticleTitleGenome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins Plant Physiol 135 1084–1099
R. Wang M. Okamoto X. Xing N.M. Crawford (2003) ArticleTitleMicroarray 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 metabolism Plant Physiol. 132 556–567
D. Weigel E.M. Meyerowitz (1994) ArticleTitleThe ABCs of floral homeotic genes Cell 78 203–209
C.A. Weiss C.W. Garnaat K. Mukai Y. Hu H. Ma (1994) ArticleTitleIsolation of cDNAs encoding guanine nucleotide-binding protein beta-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1) Proc. Natl. Acad. Sci. USA 91 9554–9558
F. Wellmer J.L. Riechmann M. Alves-Ferreira E.M. Meyerowitz (2004) ArticleTitleGenome-wide analysis of spatial gene expression in Arabidopsis flowers Plant Cell 16 1314–1326
M. West K.M. Yee J. Danao J.L. Zimmerman R.L. Fischer R.B. Goldberg J.J. Harada (1994) ArticleTitleLEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis Plant Cell 6 1731–1745
M.D. Wilkinson G.W. Haughn (1995) ArticleTitleUNUSUAL FLORAL ORGANS controls meristem identity and floral organ primordia fate in Arabidopsis Plant Cell 7 1485–1499
M. Yang Y. Hu M. Lodhi R. McCombie H. Ma (1999) ArticleTitleThe Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation Proc. Natl. Acad. Sci. USA 96 11416–11421
M.F. Yanofsky H. Ma J.L. Bowman G.N. Drews K.A. Feldmann E.M. Meyerowitz (1990) ArticleTitleThe protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors Nature 346 35–39
M.F. Yanofsky (1995) ArticleTitleFloral meristems to floral organs: genes controlling early events in Arabidopsis flower development Annu. Rev. Plant Physiol. Plant Mol. Biol. 46 167–188
Zahn, L.M., Kong, H., Leebens-Mack, J.H., Kim, S., Soltis, P.S., Landherr, L.L., Soltis, D.E., dePamphilisa, C. W. and Ma, H. 2005. The evolution of the SEPALLATA subfamily of MADS-box genes: a pre-angiosperm origin with multiple duplications throughout angiosperm history. Genetics In press
D. Zhao M. Yang J. Solava H. Ma (1999) ArticleTitleThe ASK1 gene regulates development and interacts with the UFO gene to control floral organ identity in Arabidopsis Dev. Genet. 25 209–223
D. Zhao Q. Yu M. Chen H. Ma (2001a) ArticleTitleThe ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in Arabidopsis Development 128 2735–2746
Zhao, D.Z., Yu, Q.L., Chen, C.B. and Ma, H. 2001b. Genetic control of reproductive meristems. In: M.T. McManus and B.E. Veit, (Eds), Meristematic Tissues in Plant Growth and Development. Shefield Academic Press Ltd, pp. 89–141.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Zhang, X., Feng, B., Zhang, Q. et al. Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol 58, 401–419 (2005). https://doi.org/10.1007/s11103-005-5434-6
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-005-5434-6