Skip to main content

Advertisement

Log in

Genome-wide analysis of gene expression in soybean shoot apical meristem

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The shoot apical meristem (SAM) contains undifferentiated stem cells that are responsible for the initiation of above-ground organs. The nature of genetic programs and the regulatory networks underlying SAM function in a major legume crop, soybean was investigated here. We used soybean GeneChip® (containing 37,744 probe sets) to examine the transcript profiles associated with micro-dissected, actively growing SAMs or growth arrested axillary meristems (AMs) experiencing apical dominance, in comparison to that of non-meristem (NM) tissue. A total of 1,090 and 1,523 transcripts were identified to be significantly up- or down-regulated in the SAM in comparison to the NM. RT-PCR and in situ hybridization analysis were also carried out to verify the experimental approach. The resulting gene expression profiles point to the combinatorial role of diverse regulatory pathways including those associated with cell division and proliferation, epigenetic regulation, auxin-mediated responses and microRNA regulation in meristem function. In situ hybridization analysis on selected transcripts has implicated their roles in SAM maintenance and the establishment of organ polarity. We also identified a gene, ANGUSITFOLIA3 that could potentially serve as a novel marker for differentiating cells in the meristem. Computational analysis on the promoter regions of Arabidopsis thaliana orthologs of genes with high expression in the soybean SAM revealed a conserved over-representation of three cis-acting regulatory motifs. Our data show that plant meristems possess a unique transcriptional profile, with shared “molecular signatures” in apical and axillary meristems providing a rich source of novel target genes for further studies into a fundamental process that impacts plant growth and crop productivity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769. doi:10.1105/tpc.107.051706

    Article  PubMed  CAS  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373. doi:10.1093/nar/gkl303

    Article  PubMed  CAS  Google Scholar 

  • Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana—an analysis of development in the wild-type and in the shoot meristemless mutant. Development 119:823–831

    Google Scholar 

  • Bennett T, Leyser O (2006) Something on the Side: axillary meristems and plant development. Plant Mol Biol 60:843–854. doi:10.1007/s11103-005-2763-4

    Article  PubMed  CAS  Google Scholar 

  • Bhalla PL, Singh MB (2006) Molecular control of stem cell maintenance in shoot apical meristem. Plant Cell Rep 25:249–256. doi:10.1007/s00299-005-0071-8

    Article  PubMed  CAS  Google Scholar 

  • Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575

    PubMed  CAS  Google Scholar 

  • Dievart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131:251–261. doi:10.1242/dev.00998

    Article  PubMed  CAS  Google Scholar 

  • Domoney C, Duc G, Ellis THN, Ferrandiz C, Firnhaber C, Gallardo K, Hofer J, Kopka J, Kuster H, Madueno F, Munier-Jolain NG, Mayer K, Thompson R, Udvardi M, Salon C (2006) Genetic and genomic analysis of legume flowers and seeds. Curr Opin Plant Biol 9:133–141

    Article  PubMed  CAS  Google Scholar 

  • Douglas SJ, Chuck G, Dengler RE, Pelecanda L, Riggs CD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14:547–558. doi:10.1105/tpc.010391

    Article  PubMed  CAS  Google Scholar 

  • Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot (Lond) 99:787–822. doi:10.1093/aob/mcl255

    Article  CAS  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    Article  PubMed  CAS  Google Scholar 

  • Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979. doi:10.1046/j.1365-313X.1996.10060967.x

    Article  PubMed  CAS  Google Scholar 

  • Eyuboglu B, Pfister K, Haberer G, Chevalier D, Fuchs A, Mayer K, Schneitz K (2007) Molecular characterisation of the STRUBBELIG-RECEPTOR FAMILY of genes encoding putative leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. BMC Plant Biol 7:16. doi:10.1186/1471-2229-7-16

    Article  PubMed  CAS  Google Scholar 

  • Fleming A (2006) Metabolic aspects of organogenesis in the shoot apical meristem. J Exp Bot 57:1863–1870. doi:10.1093/jxb/erj178

    Article  PubMed  CAS  Google Scholar 

  • Green KA, Prigge MJ, Katzman RB, Clark SE (2005) CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17:691–704. doi:10.1105/tpc.104.026179

    Article  PubMed  CAS  Google Scholar 

  • Grigg SP, Canales C, Hay A, Tsiantis M (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437:1022–1026. doi:10.1038/nature04052

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. Embo J 17:1405–1411

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131:1089–1100

    Article  PubMed  CAS  Google Scholar 

  • Hecht V, Foucher F, Ferrandiz C, Macknight R, Navarro C, Morin J, Vardy ME, Ellis N, Beltran JP, Rameau C, Weller JL (2005) Conservation of Arabidopsis flowering genes in model legumes. Plant Physiol 137:1420–1434

    Article  PubMed  CAS  Google Scholar 

  • Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78. doi:10.1111/j.1365-313X.2005.02429.x

    Article  PubMed  CAS  Google Scholar 

  • Huntley R, Healy S, Freeman D, Lavender P, de Jager S, Greenwood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutierrez C, Doonan JH, Murray JAH (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol Biol 37:155–169. doi:10.1023/A:1005902226256

    Article  PubMed  CAS  Google Scholar 

  • Kaya H, Shibahara K, Taoka K, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–142. doi:10.1016/S0092-8674(01)00197-0

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451. doi:10.1038/nature03542

    Article  PubMed  CAS  Google Scholar 

  • Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573. doi:10.1105/tpc.105.039107

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Choi DS, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104. doi:10.1046/j.1365-313X.2003.01862.x

    Article  PubMed  CAS  Google Scholar 

  • Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153

    Article  PubMed  CAS  Google Scholar 

  • Kwon CS, Chen C, Wagner D (2005) WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev 19:992–1003. doi:10.1101/gad.1276305

    Article  PubMed  CAS  Google Scholar 

  • Laufs P, Grandjean O, Jonak C, Kieu K, Traas J (1998) Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10:1375–1390

    Article  PubMed  CAS  Google Scholar 

  • Lehmann M (2004) Anything else but GAGA: a nonhistone protein complex reshapes chromatin structure. Trends Genet 20:15–22. doi:10.1016/j.tig.2003.11.005

    Article  PubMed  CAS  Google Scholar 

  • Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035

    PubMed  CAS  Google Scholar 

  • Long J, Barton MK (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev Biol 218:341–353. doi:10.1006/dbio.1999.9572

    Article  PubMed  CAS  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947

    Article  PubMed  CAS  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195. doi:10.1105/tpc.104.161220

    Article  PubMed  CAS  Google Scholar 

  • Moussian B, Schoof H, Haecker A, Jurgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 17:1799–1809. doi:10.1093/emboj/17.6.1799

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki H, Itoh J-I, Hayashi K, Hibara K-I, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104:14867–14871. doi:10.1073/pnas.0704339104

    Article  PubMed  CAS  Google Scholar 

  • Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14:1847–1857. doi:10.1105/tpc.002550

    Article  PubMed  CAS  Google Scholar 

  • Nardmann J, Werr W (2007) The evolution of plant regulatory networks: what Arabidopsis cannot say for itself. Curr Opin Plant Biol 10:653–659. doi:10.1016/j.pbi.2007.07.009

    Article  PubMed  CAS  Google Scholar 

  • Newman KL, Fernandez AG, Barton MK (2002) Regulation of axis determinacy by the Arabidopsis PINHEAD gene. Plant Cell 14:3029–3042. doi:10.1105/tpc.005132

    Article  PubMed  CAS  Google Scholar 

  • Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M (2002) OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J 30:189–201. doi:10.1046/j.1365-313X.2002.01279.x

    Article  PubMed  CAS  Google Scholar 

  • Nole-Wilson S, Krizek BA (2006) AINTEGUMENTA contributes to organ polarity and regulates growth of lateral organs in combination with YABBY genes. Plant Physiol 141:977–987

    Article  PubMed  CAS  Google Scholar 

  • Ohtsu K, Smith MB, Emrich SJ, Borsuk LA, Zhou R, Chen T, Zhang X, Timmermans MCP, Beck J, Buckner B, Janick-Buckner D, Nettleton D, Scanlon MJ, Schnable PS (2007) Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant J 52:391–404. doi:10.1111/j.1365-313X.2007.03244.x

    Article  PubMed  CAS  Google Scholar 

  • Ono T, Kaya H, Takeda S, Abe M, Ogawa Y, Kato M, Kakutani T, Scheid OM, Araki T, Shibahara K (2006) Chromatin assembly factor 1 ensures the stable maintenance of silent chromatin states in Arabidopsis. Genes Cells 11:153–162

    Article  PubMed  CAS  Google Scholar 

  • Perez-Perez JM, Ponce MR, Micol JL (2004) The ULTRACURVATA2 gene of Arabidopsis encodes an FK506-binding protein involved in auxin and brassinosteroid signaling. Plant Physiol 134:101–117. doi:10.1104/pp.103.032524

    Article  PubMed  CAS  Google Scholar 

  • Prigge MJ, Wagner DR (2001) The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13:1263–1280

    Article  PubMed  CAS  Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    Article  PubMed  CAS  Google Scholar 

  • Reyes JC (2006) Chromatin modifiers that control plant development. Curr Opin Plant Biol 9:21–27. doi:10.1016/j.pbi.2005.11.010

    Article  PubMed  CAS  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    Article  PubMed  CAS  Google Scholar 

  • Rothstein SJ (2007) Returning to our roots: making plant biology research relevant to future challenges in agriculture. Plant Cell 19:2695–2699. doi:10.1105/tpc.107.053074

    Article  PubMed  CAS  Google Scholar 

  • Sablowski R (2007) The dynamic plant stem cell niches. Curr Opin Plant Biol 10:639–644. doi:10.1016/j.pbi.2007.07.001

    Article  PubMed  CAS  Google Scholar 

  • Sangwan I, O’Brian MR (2002) Identification of a soybean protein that interacts with GAGA element dinucleotide repeat DNA. Plant Physiol 129:1788–1794. doi:10.1104/pp.002618

    Article  PubMed  CAS  Google Scholar 

  • Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354. doi:10.1038/nrm2164

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506. doi:10.1038/ng1543

    Article  PubMed  CAS  Google Scholar 

  • Shiu S-H, Karlowski WM, Pan R, Tzeng Y-H, Mayer KFX, Li W-H (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234. doi:10.1105/tpc.020834

    Article  PubMed  CAS  Google Scholar 

  • Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15:1095–1110. doi:10.1105/tpc.010413

    Article  PubMed  CAS  Google Scholar 

  • Singh MB, Bhalla PL (2006) Plant stem cells carve their own niche. Trends Plant Sci 11:241–246. doi:10.1016/j.tplants.2006.03.004

    Article  PubMed  CAS  Google Scholar 

  • Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (eds) Bioinformatics and computational biology solutions using R and Bioconductor. Springer, New York, pp 397–420

    Chapter  Google Scholar 

  • Stahl Y, Simon R (2005) Plant stem cell niches. Int J Dev Biol 49:479–489. doi:10.1387/ijdb.041929ys

    Article  PubMed  Google Scholar 

  • Steeves TA, Sussex IM (1989) Patterns in plant development, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Stuurman J, Jaggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218. doi:10.1101/gad.230702

    Article  PubMed  CAS  Google Scholar 

  • Tao LZ, Cheung AY, Wu HM (2002) Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. Plant Cell 14:2745–2760. doi:10.1105/tpc.006320

    Article  PubMed  CAS  Google Scholar 

  • Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8:735–746

    Article  PubMed  CAS  Google Scholar 

  • Tucker MR, Laux T (2007) Connecting the paths in plant stem cell regulation. Trends Cell Biol 17:403–410. doi:10.1016/j.tcb.2007.06.002

    Article  PubMed  CAS  Google Scholar 

  • Ueda M, Matsui K, Ishiguro S, Sano R, Wada T, Paponov I, Palme K, Okada K (2004) The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems. Development 131:2101–2111. doi:10.1242/dev.01096

    Article  PubMed  CAS  Google Scholar 

  • Umemura Y, Ishiduka T, Yamamoto R, Esaka M (2004) The Dof domain, a zinc finger DNA-binding domain conserved only in higher plants, truly functions as a Cys2/Cys2 Zn finger domain. Plant J 37:741–749. doi:10.1111/j.1365-313X.2003.01997.x

    Article  PubMed  CAS  Google Scholar 

  • van Steensel B, Delrow J, Bussemaker HJ (2003) Genomewide analysis of Drosophila GAGA factor target genes reveals context-dependent DNA binding. Proc Natl Acad Sci USA 100:2580–2585. doi:10.1073/pnas.0438000100

    Article  PubMed  CAS  Google Scholar 

  • Wagner D, Meyerowitz E (2002) SPLAYED, a novel SWI/SNF ATPase homolog, controls reproductive development in Arabidopsis. Curr Biol 12:85–94. doi:10.1016/S0960-9822(01)00651-0

    Article  PubMed  CAS  Google Scholar 

  • Wang HB, Wang LJ, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y (2004) Role of histone H2A ubiquitination in polycomb silencing. Nature 431:873–878. doi:10.1038/nature02985

    Article  PubMed  CAS  Google Scholar 

  • Wettenhall JM, Smyth GK (2004) limmaGUI: A graphical user interface for linear modeling of microarray data. Bioinformatics 20:3705–3706. doi:10.1093/bioinformatics/bth449

    Article  PubMed  CAS  Google Scholar 

  • Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349. doi:10.1016/j.cell.2005.09.042

    Article  PubMed  CAS  Google Scholar 

  • Wong CE, Bhalla PL, Ottenhof H, Singh MB (2008a) Transcriptional profiling of the pea shoot apical meristem reveals processes underlying its function and maintenance. BMC Plant Biol 8:73. doi:10.1186/1471-2229-8-73

    Article  PubMed  CAS  Google Scholar 

  • Wong CE, Singh MB, Bhalla PL (2008b) Molecular processes underlying floral transition in the soybean shoot apical meristem. Plant J. doi:10.1111/j.1365-313X.2008.03730.x

    Google Scholar 

  • Woodward C, Bemis SM, Hill EJ, Sawa S, Koshiba T, Torii KU (2005) Interaction of auxin and ERECTA in elaborating arabidopsis inflorescence architecture revealed by the activation tagging of a new member of the YUCCA family putative flavin monooxygenases. Plant Physiol 139:192–203. doi:10.1104/pp.105.063495

    Article  PubMed  CAS  Google Scholar 

  • Wyrzykowska J, Schorderet M, Pien S, Gruissem W, Fleming AJ (2006) Induction of differentiation in the shoot apical meristem by transient overexpression of a retinoblastoma-related protein. Plant Physiol 141:1338–1348. doi:10.1104/pp.106.083022

    Article  PubMed  CAS  Google Scholar 

  • Yanagisawa S (2001) The transcriptional activation domain of the plant-specific Dof1 factor functions in plant, animal, and yeast cells. Plant Cell Physiol 42:813–822. doi:10.1093/pcp/pce105

    Article  PubMed  CAS  Google Scholar 

  • Ye ZH, Varner JE (1991) Tissue-specific expression of cell-wall proteins in developing soybean tissues. Plant Cell 3:23–37

    Article  PubMed  CAS  Google Scholar 

  • Yin X-J, Volk S, Ljung K, Mehlmer N, Dolezal K, Ditengou F, Hanano S, Davis SJ, Schmelzer E, Sandberg G, Teige M, Palme K, Pickart C, Bachmair A (2007) Ubiquitin lysine 63 chain forming ligases regulate apical dominance in Arabidopsis. Plant Cell 19:1898–1911. doi:10.1105/tpc.107.052035

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama R, Takahashi T, Kato A, Torii KU, Komeda Y (1998) The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordia. Plant J 15:301–310. doi:10.1046/j.1365-313X.1998.00203.x

    Article  PubMed  CAS  Google Scholar 

  • Zhou DX (1999) Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 4:210–214. doi:10.1016/S1360-1385(99)01418-1

    Article  PubMed  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632. doi:10.1104/pp.104.046367

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Andrea Morrell and Cathy Jensen for their assistance in the soybean meristem dissections, Prof. Peter Gresshoff for soybean seeds and the Australian Research Council for financially supporting this project as a part of ARC centre of Excellence grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Prem L. Bhalla.

Additional information

Farzad Haerizadeh and Chui E. Wong contributed equally.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haerizadeh, F., Wong, C.E., Singh, M.B. et al. Genome-wide analysis of gene expression in soybean shoot apical meristem. Plant Mol Biol 69, 711–727 (2009). https://doi.org/10.1007/s11103-008-9450-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-008-9450-1

Keywords

Navigation