RNA-seq analysis of an apical meristem time series reveals a critical point in Arabidopsis thaliana flower initiation

BMC Genomics

Aleksey A. Penin²  Sergey E. Dmitriev⁴  Maria D. Logacheva³  Anna V. Klepikova¹ 

[1] Institute for Information Transmission Problems of the Russian Academy of Sciences, Moscow 127051, Russia;Department of Genetics, Faculty of Biology, Lomonosov Moscow State University, Moscow 119991, Russia;Pirogov Russian National Research Medical University, Moscow, 117997, Russia;Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow 119991, Russia

关键词: RNA-seq;    Gene expression;    Meristem;    Flowering;    Cell cycle;    Arabidopsis thaliana;   

Others  :  1216167
DOI  :  10.1186/s12864-015-1688-9

 received in 2015-01-12, accepted in 2015-06-05,  发布年份 2015

【 摘 要 】

Background

Floral transition is a critical event in the life cycle of a flowering plant as it determines its reproductive success. Despite extensive studies of specific genes that regulate this process, the global changes in transcript expression profiles at the point when a vegetative meristem transitions into an inflorescence have not been reported. We analyzed gene expression during Arabidopsis thaliana meristem development under long day conditions from day 7 to 16 after germination in one-day increments.

Results

The dynamics of the expression of the main flowering regulators was consistent with previous reports: notably, the expression of FLOWERING LOCUS C (FLC) decreased over the course of the time series while expression of LEAFY (LFY) increased. This analysis revealed a developmental time point between 10 and 12 days after germination where FLC expression had decreased but LFY expression had not yet increased, which was characterized by a peak in the number of differentially expressed genes. Gene Ontology (GO) enrichment analysis of these genes identified an overrepresentation of genes related to the cell cycle.

Conclusions

We discovered an unprecedented burst of differential expression of cell cycle related genes at one particular point during transition to flowering. We suggest that acceleration of rate of the divisions and partial cell cycling synchronization takes place at this point.

【 授权许可】

   
2015 Klepikova et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

【 参考文献 】

• [1]Casal JJ, Fankhauser C, Coupland G, Blázquez MA. Signalling for developmental plasticity. Trends Plant Sci. 2004; 9:309-14.
• [2]Amasino R. Seasonal and developmental timing of flowering. Plant J Cell Mol Biol. 2010; 61:1001-13.
• [3]Greenup A, Peacock WJ, Dennis ES, Trevaskis B. The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot. 2009; 103:1165-72.
• [4]Kim D-H, Doyle MR, Sung S, Amasino RM. Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol. 2009; 25:277-99.
• [5]Shrestha R, Gómez-Ariza J, Brambilla V, Fornara F: Molecular control of seasonal flowering in rice, Arabidopsis and temperate cereals. Ann Bot 2014;114(7):1445–58.
• [6]Giakountis A, Cremer F, Sim S, Reymond M, Schmitt J, Coupland G. Distinct Patterns of Genetic Variation Alter Flowering Responses of Arabidopsis Accessions to Different Daylengths. Plant Physiol. 2010; 152:177-91.
• [7]Turck F, Fornara F, Coupland G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol. 2008; 59:573-94.
• [8]Koornneef M, Hanhart CJ, van der Veen JH. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet MGG. 1991; 229:57-66.
• [9]Kobayashi Y, Weigel D. Move on up, it’s time for change–mobile signals controlling photoperiod-dependent flowering. Genes Dev. 2007; 21:2371-84.
• [10]Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature. 2001; 410:1116-20.
• [11]Mk C. New facts in support of the hormonal theory of plant development. Compt Rend Acad Sci URSS. 1936; 13:79-83.
• [12]Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science. 2000; 288:1613-6.
• [13]Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science. 2005; 309:1052-6.
• [14]Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D. Integration of spatial and temporal information during floral induction in Arabidopsis. Science. 2005; 309:1056-9.
• [15]Borner R, Kampmann G, Chandler J, Gleissner R, Wisman E, Apel K, Melzer S. A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J Cell Mol Biol. 2000; 24:591-9.
• [16]Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I. The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 2000; 14:2366-76.
• [17]Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev. 2006; 20:898-912.
• [18]Blázquez MA, Soowal LN, Lee I, Weigel D. LEAFY expression and flower initiation in Arabidopsis. Dev Camb Engl. 1997; 124:3835-44.
• [19]Hempel FD, Weigel D, Mandel MA, Ditta G, Zambryski PC, Feldman LJ, Yanofsky MF. Floral determination and expression of floral regulatory genes in Arabidopsis. Dev Camb Engl. 1997; 124:3845-53.
• [20]Busch MA, Bomblies K, Weigel D. Activation of a floral homeotic gene in Arabidopsis. Science. 1999; 285:585-7.
• [21]Kempin SA, Savidge B, Yanofsky MF. Molecular basis of the cauliflower phenotype in Arabidopsis. Science. 1995; 267:522-5.
• [22]Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature. 1992; 360:273-7.
• [23]Ng M, Yanofsky MF. Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell. 2001; 13:739-53.
• [24]Michaels SD, Amasino RM. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell. 1999; 11:949-56.
• [25]De Lucia F, Crevillen P, Jones AME, Greb T, Dean C. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A. 2008; 105:16831-6.
• [26]Sung S, Amasino RM. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature. 2004; 427:159-64.
• [27]Noh B, Lee S-H, Kim H-J, Yi G, Shin E-A, Lee M, Jung K-J, Doyle MR, Amasino RM, Noh Y-S. Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell. 2004; 16:2601-13.
• [28]Simpson GG. The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr Opin Plant Biol. 2004; 7:570-4.
• [29]Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU. Dissection of floral induction pathways using global expression analysis. Dev Camb Engl. 2003; 130:6001-12.
• [30]Hartmann U, Höhmann S, Nettesheim K, Wisman E, Saedler H, Huijser P. Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J Cell Mol Biol. 2000; 21:351-60.
• [31]Mantegazza O, Gregis V, Chiara M, Selva C, Leo G, Horner DS, Kater MM. Gene coexpression patterns during early development of the native Arabidopsis reproductive meristem: novel candidate developmental regulators and patterns of functional redundancy. Plant J Cell Mol Biol. 2014; 79:861-77.
• [32]Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, Wong W-K, Mockler TC. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res. 2010; 20:45-58.
• [33]Jiao Y, Tausta SL, Gandotra N, Sun N, Liu T, Clay NK, Ceserani T, Chen M, Ma L, Holford M, Zhang H, Zhao H, Deng X-W, Nelson T. A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat Genet. 2009; 41:258-63.
• [34]Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell. 2013; 25:1960-78.
• [35]Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP. The developmental dynamics of the maize leaf transcriptome. Nat Genet. 2010; 42:1060-7.
• [36]Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 2010; 10:160. BioMed Central Full Text
• [37]Torti S, Fornara F, Vincent C, Andrés F, Nordström K, Göbel U, Knoll D, Schoof H, Coupland G. Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell. 2012; 24:444-62.
• [38]Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell. 1990; 2:755-67.
• [39]Cardon GH, Höhmann S, Nettesheim K, Saedler H, Huijser P. Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J Cell Mol Biol. 1997; 12:367-77.
• [40]Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P. The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol. 2008; 67:183-95.
• [41]Wang J-W, Czech B, Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell. 2009; 138:738-49.
• [42]Yamaguchi A, Wu M-F, Yang L, Wu G, Poethig RS, Wagner D. The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell. 2009; 17:268-78.
• [43]Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4:44-57.
• [44]Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009; 37:1-13.
• [45]Bamburg JR. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu Rev Cell Dev Biol. 1999; 15:185-230.
• [46]Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS. Cofilin promotes actin polymerization and defines the direction of cell motility. Science. 2004; 304:743-6.
• [47]Feng Y, Liu Q, Xue Q. Comparative study of rice and Arabidopsis actin-depolymerizing factors gene families. J Plant Physiol. 2006; 163:69-79.
• [48]Ruzicka DR, Kandasamy MK, McKinney EC, Burgos-Rivera B, Meagher RB. The ancient subclasses of Arabidopsis Actin Depolymerizing Factor genes exhibit novel and differential expression. Plant J Cell Mol Biol. 2007; 52:460-72.
• [49]Huang S, Robinson RC, Gao LY, Matsumoto T, Brunet A, Blanchoin L, Staiger CJ. Arabidopsis VILLIN1 generates actin filament cables that are resistant to depolymerization. Plant Cell. 2005; 17:486-501.
• [50]Khurana P, Henty JL, Huang S, Staiger AM, Blanchoin L, Staiger CJ. Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell. 2010; 22:2727-48.
• [51]Wu Y, Yan J, Zhang R, Qu X, Ren S, Chen N, Huang S. Arabidopsis FIMBRIN5, an actin bundling factor, is required for pollen germination and pollen tube growth. Plant Cell. 2010; 22:3745-63.
• [52]Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV. Myosin XI-K Is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol. 2008; 146:1098-108.
• [53]Natesan SKA, Sullivan JA, Gray JC. Myosin XI is required for actin-associated movement of plastid stromules. Mol Plant. 2009; 2:1262-72.
• [54]Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV. Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 2008; 146:1109-16.
• [55]Prokhnevsky AI, Peremyslov VV, Dolja VV. Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A. 2008; 105:19744-9.
• [56]Sparkes IA, Teanby NA, Hawes C. Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J Exp Bot. 2008; 59:2499-512.
• [57]Tominaga M, Kojima H, Yokota E, Orii H, Nakamori R, Katayama E, Anson M, Shimmen T, Oiwa K. Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. EMBO J. 2003; 22:1263-72.
• [58]Breyne P, Dreesen R, Vandepoele K, De Veylder L, Van Breusegem F, Callewaert L, Rombauts S, Raes J, Cannoot B, Engler G, Inzé D, Zabeau M. Transcriptome analysis during cell division in plants. Proc Natl Acad Sci U S A. 2002; 99:14825-30.
• [59]Menges M, Murray JAH. Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J Cell Mol Biol. 2002; 30:203-12.
• [60]Menges M, de Jager SM, Gruissem W, Murray JAH. Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J Cell Mol Biol. 2005; 41:546-66.
• [61]Taoka K, Kaya H, Nakayama T, Araki T, Meshi T, Iwabuchi M. Identification of three kinds of mutually related composite elements conferring S phase-specific transcriptional activation. Plant J Cell Mol Biol. 1999; 18:611-23.
• [62]Cho RJ, Huang M, Campbell MJ, Dong H, Steinmetz L, Sapinoso L, Hampton G, Elledge SJ, Davis RW, Lockhart DJ. Transcriptional regulation and function during the human cell cycle. Nat Genet. 2001; 27:48-54.
• [63]Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell. 1998; 9:3273-97.
• [64]Chaubet N, Clément B, Philipps G, Gigot C. Organ-specific expression of different histone H3 and H4 gene subfamilies in developing and adult maize. Plant Mol Biol. 1991; 17:935-40.
• [65]Muskhelishvili L, Latendresse JR, Kodell RL, Henderson EB. Evaluation of cell proliferation in rat tissues with BrdU, PCNA, Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. J Histochem Cytochem Off J Histochem Soc. 2003; 51:1681-8.
• [66]Menges M, Hennig L, Gruissem W, Murray JAH. Cell cycle-regulated gene expression in Arabidopsis. J Biol Chem. 2002; 277:41987-2002.
• [67]Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, Matese JC, Perou CM, Hurt MM, Brown PO, Botstein D. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell. 2002; 13:1977-2000.
• [68]Teichmanová M, Masková P, Vojvodová P, Krekule J, Francis D, Lipavská H. The fission yeast mitotic activator cdc25 and sucrose induce early flowering synergistically in the day-neutral Nicotiana tabacum cv. Samsun New Phytol. 2007; 176:804-12.
• [69]Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y, De Bodt S, Maere S, Laukens K, Pharazyn A, Ferreira PCG, Eloy N, Renne C, Meyer C, Faure J-D, Steinbrenner J, Beynon J, Larkin JC, Van de Peer Y, Hilson P, Kuiper M, De Veylder L, Van Onckelen H, Inzé D, Witters E, De Jaeger G. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol. 2010; 6:397.
• [70]Gegas VC, Doonan JH. Expression of cell cycle genes in shoot apical meristems. Plant Mol Biol. 2006; 60:947-61.
• [71]Larkin JC, Hunsperger JP, Culley D, Rubenstein I, Silflow CD. The organization and expression of a maize ribosomal protein gene family. Genes Dev. 1989; 3:500-9.
• [72]Lebrun M, Freyssinet G. Nucleotide sequence and characterization of a maize cytoplasmic ribosomal protein S11 cDNA. Plant Mol Biol. 1991; 17:265-8.
• [73]Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis CW, Ma H. Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol. 2004; 135:1084-99.
• [74]Takahashi I, Kojima S, Sakaguchi N, Umeda-Hara C, Umeda M. Two Arabidopsis cyclin A3s possess G1 cyclin-like features. Plant Cell Rep. 2010; 29:307-15.
• [75]Ito M. Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res. 2005; 118:61-9.
• [76]Bernier G. My favourite flowering image: the role of cytokinin as a flowering signal. J Exp Bot. 2013; 64:5795-9.
• [77]Francis D. The cell cycle in plant development. New Phytol. 1992; 122:1-20.
• [78]Gonthier R, Jacqmard A, Bernier G. Changes in cell-cycle duration and growth fraction in the shoot meristem of Sinapis during floral transition. Planta. 1987; 170:55-9.
• [79]Jacqmard A, Gadisseur I, Bernier G. Cell division and morphological changes in the shoot apex of Arabidopsis thaliana during floral transition. Ann Bot. 2003; 91:571-6.
• [80]Bodson M. Variation in the rate of cell division in the apical meristem of Sinapis alba during transition to flowering. Ann Bot. 1975; 39:547-54.
• [81]Marc J, Palmer H. Variation in cell-cycle time and nuclear DNA content in the apical meristem ofHelianthus annum L. during the transition to flowering. Am J Bot. 1984; 7:588-95.
• [82]Miller MB, Lyndon RF. The cell cycle in vegetative and floral shoot meristems measured by a double labelling technique. Planta. 1975; 126:37-43.
• [83]Francis D, Lyndon RF. Synchronisation of cell division in the shoot apex of Silene in relation to flower initiation. Planta. 1979; 145:151-7.
• [84]Jacqmard A, Houssa C. DNA fiber replication during a morphogenetic switch in the shoot meristematic cells of a higher plant. Exp Cell Res. 1988; 179:454-61.
• [85]Durdan SF, Herbert RJ, Francis D. Activation of latent origins of DNA replication in florally determined shoot meristems of long-day and short-day plants: Silene coeli-rosa and Pharbitis nil. Planta. 1998; 207:235-40.
• [86]Nougarède A, Francis D, Rondet P. Location of cell cycle changes in relation to morphological changes in the shoot apex ofSilene coeli-rosa immediately before sepal initiation. Protoplasma. 1991; 165:1-10.
• [87]Grose S, Lyndon RF. Inhibition of growth and synchronised cell division in the shoot apex in relation to flowering in Silene. Planta. 1984; 161:289-94.
• [88]Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010; 11:R106. BioMed Central Full Text
• [89]Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005; 139:5-17.
• [90]Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods San Diego Calif. 2001; 25:402-8.
• [91]R Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/ 2013.
• [92]Müllner D. Fastcluster: Fast Hierarchical, Agglomerative Clustering Routines for R and Python. J Stat Softw. 2013; 53:1-18.
• [93]Langfelder P, Zhang B, Horvath S. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinforma Oxf Engl. 2008; 24:719-20.