Patterns of gene expression during Arabidopsis flower development from the time of initiation to maturation

BMC Genomics

Frank Wellmer²  Marcel Quint⁴  Emmanuelle Graciet¹  Ivo Grosse⁵  Alexander Gabel⁵  Kamila Kwaśniewska²  Hajk-Georg Drost⁵  Diarmuid S. Ó’Maoiléidigh³  Patrick T. Ryan² 

[1] Department of Biology, National University of Ireland Maynooth, Maynooth, Ireland;Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland;Present address: Max Planck Institute for Plant Breeding Research, Cologne, D-50829, Germany;Leibniz Institute of Plant Biochemistry, Department of Molecular Signal Processing, Halle (Saale), Germany;Institute of Computer Science, Martin Luther University Halle–Wittenberg, Halle (Saale), Germany

关键词: Gene expression atlas;    Paralog;    Temporal gene expression;    Transcriptomics;    Organ specification;    Flower development;    Arabidopsis thaliana;   

Others  :  1219239
DOI  :  10.1186/s12864-015-1699-6

 received in 2015-02-07, accepted in 2015-06-15,  发布年份 2015

【 摘 要 】

Background

The formation of flowers is one of the main model systems to elucidate the molecular mechanisms that control developmental processes in plants. Although several studies have explored gene expression during flower development in the model plant Arabidopsis thaliana on a genome-wide scale, a continuous series of expression data from the earliest floral stages until maturation has been lacking. Here, we used a floral induction system to close this information gap and to generate a reference dataset for stage-specific gene expression during flower formation.

Results

Using a floral induction system, we collected floral buds at 14 different stages from the time of initiation until maturation. Using whole-genome microarray analysis, we identified 7,405 genes that exhibit rapid expression changes during flower development. These genes comprise many known floral regulators and we found that the expression profiles for these regulators match their known expression patterns, thus validating the dataset. We analyzed groups of co-expressed genes for over-represented cellular and developmental functions through Gene Ontology analysis and found that they could be assigned specific patterns of activities, which are in agreement with the progression of flower development. Furthermore, by mapping binding sites of floral organ identity factors onto our dataset, we were able to identify gene groups that are likely predominantly under control of these transcriptional regulators. We further found that the distribution of paralogs among groups of co-expressed genes varies considerably, with genes expressed predominantly at early and intermediate stages of flower development showing the highest proportion of such genes.

Conclusions

Our results highlight and describe the dynamic expression changes undergone by a large number of genes during flower development. They further provide a comprehensive reference dataset for temporal gene expression during flower formation and we demonstrate that it can be used to integrate data from other genomics approaches such as genome-wide localization studies of transcription factor binding sites.

【 授权许可】

   
2015 Ryan et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

【 参考文献 】

• [1]Hirano HY, Tanaka W, Toriba T. Grass flower development. Methods Mol Biol. 2014; 1110:57-84.
• [2]Causier B, Davies B. Flower development in the asterid lineage. Methods Mol Biol. 2014; 1110:35-55.
• [3]Prunet N, Jack TP. Flower development in Arabidopsis: there is more to it than learning your ABCs. Methods Mol Biol. 2014; 1110:3-33.
• [4]O’Maoileidigh DS, Graciet E, Wellmer F. Gene networks controlling Arabidopsis thaliana flower development. New Phytol. 2014; 201(1):16-30.
• [5]Wellmer F, Graciet E, Riechmann JL. Specification of floral organs in Arabidopsis. J Exp Bot. 2014; 65(1):1-9.
• [6]Sablowski R: Control of patterning, growth, and differentiation by floral organ identity genes. J Exp Bot 2015;66(4):1065–72.
• [7]Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell. 1990; 2(8):755-67.
• [8]Mantegazza O, Gregis V, Chiara M, Selva C, Leo G, Horner DS et al.. Gene coexpression patterns during early development of the native Arabidopsis reproductive meristem: novel candidate developmental regulators and patterns of functional redundancy. Plant J. 2014; 79(5):861-77.
• [9]Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM. Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet. 2006; 2(7):e117.
• [10]Gomez-Mena C, de Folter S, Costa MM, Angenent GC, Sablowski R. Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development. 2005; 132(3):429-38.
• [11]Jiao Y, Meyerowitz EM. Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol Syst Biol. 2010; 6:419.
• [12]Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K et al.. Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci U S A. 2012; 109(33):13452-7.
• [13]Maoileidigh DS O, Wuest SE, Rae L, Raganelli A, Ryan PT, Kwasniewska K et al.. Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS. Plant Cell. 2013; 25(7):2482-503.
• [14]Pajoro A, Madrigal P, Muino JM, Matus JT, Jin J, Mecchia MA et al.. Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biol. 2014; 15(3):R41. BioMed Central Full Text
• [15]Alves-Ferreira M, Wellmer F, Banhara A, Kumar V, Riechmann JL, Meyerowitz EM. Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol. 2007; 145(3):747-62.
• [16]Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM. Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell. 2004; 16(5):1314-26.
• [17]Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M et al.. A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005; 37(5):501-6.
• [18]Zhang X, Feng B, Zhang Q, Zhang D, Altman N, Ma H. Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol. 2005; 58(3):401-19.
• [19]Peiffer JA, Kaushik S, Sakai H, Arteaga-Vazquez M, Sanchez-Leon N, Ghazal H et al.. A spatial dissection of the Arabidopsis floral transcriptome by MPSS. BMC Plant Biol. 2008; 8:43. BioMed Central Full Text
• [20]Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M et al.. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol. 2010; 20(6):506-12.
• [21]Sanchez-Leon N, Arteaga-Vazquez M, Alvarez-Mejia C, Mendiola-Soto J, Duran-Figueroa N, Rodriguez-Leal D et al.. Transcriptional analysis of the Arabidopsis ovule by massively parallel signature sequencing. J Exp Bot. 2012; 63(10):3829-42.
• [22]Pina C, Pinto F, Feijo JA, Becker JD. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol. 2005; 138(2):744-56.
• [23]Honys D, Twell D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 2004; 5(11):R85. BioMed Central Full Text
• [24]O’Maoileidigh DS, Wellmer F. A floral induction system for the study of early Arabidopsis flower development. Methods Mol Biol. 2014; 1110:307-14.
• [25]O’Maoileidigh DS, Thomson B, Raganelli A, Wuest SE, Ryan PT, Kwasniewska K, et al. Gene network analysis in Arabidopsis thaliana flower development through dynamic gene perturbations. Plant J. 2015;82.
• [26]Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR. Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development. 1993; 119:721-43.
• [27]Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development. 2000; 127(4):725-34.
• [28]Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS et al.. Gene expression during the life cycle of Drosophila melanogaster. Science. 2002; 297(5590):2270-5.
• [29]Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V et al.. Orchestration of floral initiation by APETALA1. Science. 2010; 328(5974):85-9.
• [30]Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990; 346(6279):35-9.
• [31]Jack T, Brockman LL, Meyerowitz EM. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell. 1992; 68(4):683-97.
• [32]Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H. Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development. 2007; 134(10):1901-10.
• [33]Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 1999; 283(5409):1911-4.
• [34]Payne T, Johnson SD, Koltunow AM. KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development. 2004; 131(15):3737-49.
• [35]Sun B, Xu YF, Ng KH, Ito T. A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Gene Dev. 2009; 23(15):1791-804.
• [36]Sakai H, Medrano LJ, Meyerowitz EM. Role of SUPERMAN in maintaining Arabidopsis floral whorl boundaries. Nature. 1995; 378(6553):199-203.
• [37]Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E et al.. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature. 2003; 424(6944):85-8.
• [38]Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D. A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet. 2009; 5(3):e1000430.
• [39]Sorensen AM, Krober S, Unte US, Huijser P, Dekker K, Saedler H. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 2003; 33(2):413-23.
• [40]Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K. Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1999; 96(20):11664-9.
• [41]Yang WC, Ye D, Xu J, Sundaresan V. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 1999; 13(16):2108-17.
• [42]Canales C, Bhatt AM, Scott R, Dickinson H. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol. 2002; 12(20):1718-27.
• [43]Zhao DZ, Wang GF, Speal B, Ma H. The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 2002; 16(15):2021-31.
• [44]Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development. 2006; 133(16):3085-95.
• [45]Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M et al.. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature. 2004; 430(6997):356-60.
• [46]Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY et al.. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod. 1999; 11:297-322.
• [47]Robinson-Beers K, Pruitt RE, Gasser CS. Ovule Development in Wild-Type Arabidopsis and Two Female-Sterile Mutants. Plant Cell. 1992; 4(10):1237-49.
• [48]Chandler JW. The hormonal regulation of flower development. J Plant Growth Regulation. 2011; 30(2):242-54.
• [49]Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM. Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci U S A. 2004; 101(20):7827-32.
• [50]Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature. 1991; 353(6339):31-7.
• [51]Bowman JL, Smyth DR, Meyerowitz EM. Genes directing flower development in Arabidopsis. Plant Cell. 1989; 1(1):37-52.
• [52]Causier B, Schwarz-Sommer Z, Davies B. Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol. 2010; 21(1):73-9.
• [53]Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J et al.. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A. 2012; 109(5):1560-5.
• [54]Moore RC, Purugganan MD. The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol. 2005; 8(2):122-8.
• [55]Deal RB, Henikoff S. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell. 2010; 18(6):1030-40.
• [56]Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004; 3:Article3.
• [57]Smyth GK, Speed T. Normalization of cDNA microarray data. Methods. 2003; 31(4):265-73.
• [58]Yi X, Du Z, Su Z. PlantGSEA: a gene set enrichment analysis toolkit for plant community. Nucleic Acids Res. 2013; 41(Web Server issue):W98-103.
• [59]Banjamini Y, Yekutieli D. False discovery rate–adjusted multiple confidence intervals for selected parameters. J Am Stat Assoc. 2005; 100(469):71-81.
• [60]Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K et al.. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10:421. BioMed Central Full Text