Skip to main content

Advertisement

Log in

Transcriptional profiling of wheat caryopsis development using cDNA microarrays

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The expression of 7,835 genes in developing wheat caryopses was analyzed using cDNA arrays. Using a mixed model analysis of variance (ANOVA) method, 29% (2,237) of the genes on the array were identified to be differentially expressed at the 6 different time-points examined, which covers the developmental stages from coenocytic endosperm to physiological maturity. Comparison of genes differentially expressed between two time-points revealed a dynamic transcript accumulation profile with major re-programming events that occur at 3–7, 7–14 and 21–28 DPA. A k-means clustering algorithm grouped the differentially expressed genes into 10 clusters, revealing co-expression of genes involved in the same pathway such as carbohydrate and protein synthesis or preparation for desiccation. Functional annotation of genes that show peak expression at specific time-points correlated with the developmental events associated with the respective stages. Results provide information on the temporal expression during caryopsis development for a significant number of differentially expressed genes with unknown function.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alba R, Fei ZJ, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D’Ascenzo M, Gordon JS, Rose JKC, Martin G, Tanksley SD, Bouzayen M, Jahn MM, Giovannoni J (2004) ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J 39:697–714

    Article  PubMed  CAS  Google Scholar 

  • Albani D, Hammond-Kosack MC, Smith C, Conlan S, Colot V, Holdsworth M, Bevan MW (1997) The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9:171–184

    Article  PubMed  CAS  Google Scholar 

  • Alexandrov NN, Troukhan ME, Brover VV, Tatarinova T, Flavell RB, Feldmann KA (2006) Features of Arabidopsis genes and genome discovered using full-length cDNAs. Plant Mol Biol 60:69–85

    Article  PubMed  CAS  Google Scholar 

  • Altenbach SB, DuPont FM, Kothari KM, Chan R, Johnson EL, Lieu D (2003) Temperature, water and fertilizer influence the timing of key events during grain development in a US spring wheat. J Cereal Sci 37:9–20

    Article  Google Scholar 

  • Altenbach SB, Kothari KM (2004) Transcript profiles of genes expressed in endosperm tissue are altered by high temperature during wheat grain development. J Cereal Sci 40:115–126

    Article  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Appels R, Francki M, Chibbar R (2003) Advances in cereal functional genomics. Funct Integr Genom 3:1–24

    CAS  Google Scholar 

  • Aquino P, Carron F, Calvo R (1999) Selected wheat statistics. CIMMYT, Mexico

  • Bechtel DB, Zayas I, Kaleikau L, Pomeranz Y (1990) Size-distribution of wheat–starch granules during endosperm development. Cereal Chem 67:59–63

    Google Scholar 

  • Bhullar SS, Jenner CF (1986) Effects of temperature on the conversion of sucrose to starch in the developing wheat endosperm. Aust J Plant Physiol 13:605

    CAS  Google Scholar 

  • Bilecen K, Ozturk UH, Duru AD, Sutlu T, Petoukhov MV, Svergun DI, Koch MH, Sezerman UO, Cakmak I, Sayers Z (2005) Triticum durum metallothionein. Isolation of the gene and structural characterization of the protein using solution scattering and molecular modeling. J Biol Chem 280:13701–13711

    Article  PubMed  CAS  Google Scholar 

  • Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, Gaasterland T, Glenisson P, Holstege FCP, Kim IF, Markowitz V, Matese JC, Parkinson H, Robinson A, Sarkans U, Schulze-Kremer S, Stewart J, Taylor R, Vilo J, Vingron M (2001) Minimum information about a microarray experiment (MIAME) – toward standards for microarray data. Nat Genet 29:365–371

    Article  PubMed  CAS  Google Scholar 

  • Brooks A, Jenner CF, Aspinall D (1982) Effects of water deficit on endosperm starch granules and on grain physiology of wheat and barley. Aust J Plant Physiol 9:423

    Article  Google Scholar 

  • Bruckner PL, Frohberg RC (1987) Rate and duration of grain fill in spring wheat. Crop Science 27:451–455

    Article  Google Scholar 

  • Bruix M, Jimenez MA, Santoro J, Gonzalez C, Colilla FJ, Mendez E, Rico M (1993) Solution structure of gamma 1-H and gamma 1-P thionins from barley and wheat endosperm determined by 1H-NMR: a structural motif common to toxic arthropod proteins. Biochemistry 32:715–724

    Article  PubMed  CAS  Google Scholar 

  • Calderini DF, Abeledo LG, Slafer GA (2000) Physiological maturity in wheat based on kernel water and dry matter. Agron J 92:895–901

    Article  Google Scholar 

  • Campbell SA, Close TJ (1997) Dehydrins: genes, proteins, and associations with phenotypic traits. New Phytol 137:61–74

    Article  CAS  Google Scholar 

  • Chanda SV, Narmada K, Singh YD (1999) Dry matter accumulation and associated changes in biochemical parameters during wheat grain development. J Agron Crop Sci 182:153

    Google Scholar 

  • Clarke B, Rahman S (2005) A microarray analysis of wheat grain hardness. Theor Appl Genet 110:1259–1267

    Article  PubMed  CAS  Google Scholar 

  • Clarke BC, Appels R, Hobbs M, Skylas D (2000) Genes active in developing wheat endosperm. Funct Integr Genomics 1:44

    Article  PubMed  CAS  Google Scholar 

  • Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP (2004) A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol 134:960–968

    Article  PubMed  CAS  Google Scholar 

  • Colilla FJ, Rocher A, Mendez E (1990) gamma-Purothionins: amino acid sequence of two polypeptides of a new family of thionins from wheat endosperm. FEBS Lett 270:191–194

    Article  PubMed  CAS  Google Scholar 

  • Dal Degan F, Rocher A, Cameron-Mills V, Von Wettstein D (1994) The expression of serine carboxypeptidases during maturation and germination of the barley grain. Proc Nat Acad Sci USA 91:8209

    Article  CAS  Google Scholar 

  • Daniel C, Triboi E (2000) Effects of temperature and nitrogen nutrition on the grain composition of winter wheat: effects on gliadin content and composition. J Cereal Sci 32:45

    Article  CAS  Google Scholar 

  • Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638

    Article  PubMed  CAS  Google Scholar 

  • Davies EJ, Tetlow IJ, Bowsher CG, Emes MJ (2003) Molecular and biochemical characterization of cytosolic phosphoglucomutase in wheat endosperm (Triticum aestivum L. cv. Axona). J Exp Bot 54:1351–1360

    Article  PubMed  CAS  Google Scholar 

  • Dominguez F, Gonzalez MC, Cejudo FJ (2002) A germination-related gene encoding a serine carboxypeptidase is expressed during the differentiation of the vascular tissue in wheat grains and seedlings. Planta 215:727

    Article  PubMed  CAS  Google Scholar 

  • Donson J, Fang YW, Espiritu-Santo G, Xing WM, Salazar A, Miyamoto S, Armendarez V, Volkmuth W (2002) Comprehensive gene expression analysis by transcript profiling. Plant Mol Biol 48:75–97

    Article  PubMed  CAS  Google Scholar 

  • Dupont FM, Altenbach SB (2003) Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. J Cereal Sci 38:133–146

    Article  CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Farrant JM, Bailly C, Leymarie J, Hamman B, Come D, Corbineau F (2004) Wheat seedlings as a model to understand desiccation tolerance and sensitivity. Physiol Plant 120:563–574

    Article  PubMed  CAS  Google Scholar 

  • Ferl RJ (1996) 14-3-3 Proteins and signal transduction. Ann Rev Plant Physiol Plant Mol Biol 47:49–73

    Article  CAS  Google Scholar 

  • Francki M, Appels R (2002) Wheat functional genomics and engineering crop improvement. Genome Biol 3:Rev 1013

    Article  Google Scholar 

  • Fulgosi H, Soll J, de Faria Maraschin S, Korthout HA, Wang M, Testerink C (2002) 14-3-3 Proteins and plant development. Plant Mol Biol 50:1019–1029

    Article  PubMed  CAS  Google Scholar 

  • Gachon CM, Langlois-Meurinne M, Henry Y, Saindrenan P (2005) Transcriptional co-regulation of secondary metabolism enzymes in Arabidopsis: functional and evolutionary implications. Plant Mol Biol 58:229–245

    Article  PubMed  CAS  Google Scholar 

  • Giroux MJ, Boyer C, Feix G, Hannah LC (1994) Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiol 106:713–722

    PubMed  CAS  Google Scholar 

  • Goldberg RB, Hoschek G, Kamalay JC (1978) Sequence complexity of nuclear and polysomal RNA in leaves of the tobacco plant. Cell 14:123–131

    Article  PubMed  CAS  Google Scholar 

  • Gregersen PL, Brinch-Pedersen H, Holm PB (2005) A microarray-based comparative analysis of gene expression profiles during grain development in transgenic and wild type wheat. Transgen Res 14:887–905

    Article  CAS  Google Scholar 

  • Hanley-Bowdoin L, Lane BG (1983) A novel protein programmed by the mRNA conserved in dry wheat embryos. The principal site of cysteine incorporation during early germination. Eur J Biochem 135:9–15

    Article  PubMed  CAS  Google Scholar 

  • Hartung RC, Poneleit CG, Cornelius PL (1989) Direct and correlated responses to selection for rate and duration of grain fill in maize. Crop Science 29:740–745

    Article  Google Scholar 

  • Hughes CE (1976) The developing endosperm of Triticum aestivum (L.): an ultrastructural and morphometric study. PhD thesis, University of Nottingham, England, I–IV

  • Kawaura K, Mochida K, Yamazaki Y, Ogihara Y (2006) Transcriptome analysis of salinity stress responses in common wheat using a 22k oligo-DNA microarray. Funct Integr Genomics 6:132–142

    Article  PubMed  CAS  Google Scholar 

  • Kerk NM, Ceserani T, Tausta SL, Sussex IM, Nelson TM (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol 132:27–35

    Article  PubMed  CAS  Google Scholar 

  • Kerr MK, Churchill GA (2001a) Experimental design for gene expression microarrays. Biostatistics 2:183–201

    Article  Google Scholar 

  • Kerr MK, Churchill GA (2001b) Statistical design and the analysis of gene expression microarray data. Genet Res 77:123–128

    Article  CAS  Google Scholar 

  • Kerr MK, Martin M, Churchill GA (2000) Analysis of variance for gene expression microarray data. J Comput Biol 7:819–837

    Article  PubMed  CAS  Google Scholar 

  • Langridge P, Lagudah ES, Holton TA, Appels R, Sharp PJ, Chalmers KJ (2001) Trends in genetic and genome analyses in wheat: a review. Aust J Agric Res 52:1043–1077

    Article  CAS  Google Scholar 

  • Leader DJ (2005) Transcriptional analysis and functional genomics in wheat. J Cereal Sci 41:149–163

    Article  CAS  Google Scholar 

  • Leah R, Tommerup H, Svendsen I, Mundy J (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J Biol Chem 266:1564–1573

    PubMed  CAS  Google Scholar 

  • Lu C, Hawkesford MJ, Barraclough PB, Poulton PR, Wilson ID, Barker GL, Edwards KJ (2005) Markedly different gene expression in wheat grown with organic or inorganic fertilizer. Proc Biol Sci 272:1901–1908

    Article  PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, Cherukuri PF, De Weese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant SH (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res 33:D192–D196

    Article  PubMed  CAS  Google Scholar 

  • Massiah AJ, Hartley MR (1995) Wheat ribosome-inactivating proteins: seed and leaf forms with different specificities and cofactor requirements. Planta 197:633–640

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Galbraith DW, Nelson T, Agrawal V (2004) Methods for transcriptional profiling in plants. Be fruitful and replicate. Plant Physiol 135:637–652

    Article  PubMed  CAS  Google Scholar 

  • Morell MK, Myers AM (2005) Towards the rational design of cereal starches. Curr Opin Plant Biol 8:204–210

    Article  PubMed  CAS  Google Scholar 

  • Nielsen K, Boston RS (2001) RIBOSOME-INACTIVATING PROTEINS: A Plant Perspective. Annu Rev Plant Physiol Plant Mol Biol 52:785–816

    Article  PubMed  CAS  Google Scholar 

  • Ogihara Y, Mochida K, Kawaura K, Murai K, Seki M, Kamiya A, Shinozaki K, Carninci P, Hayashizaki Y, Shin IT, Kohara Y, Yamazaki Y (2004) Construction of a full-length cDNA library from young spikelets of hexaploid wheat and its characterization by large-scale sequencing of expressed sequence tags. Genes Genet Syst 79:227–932

    Article  PubMed  Google Scholar 

  • Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Ann Rev Plant Physiol Plant Mol Biol 52:233–267

    Article  CAS  Google Scholar 

  • Olsen OA, Linnestad C, Nichols SE (1999) Developmental biology of the cereal endosperm. Trends Plant Sci 4:253–257

    Article  PubMed  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

    Article  PubMed  CAS  Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma X-F, Miftahudin, Gustafson JP, Conley EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NL, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi DW, Fenton RD, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  PubMed  CAS  Google Scholar 

  • Schaffer R, Landgraf J, Perez-Amador M, Wisman E (2000) Monitoring genome-wide expression in plants. Curr Opin Biotechnol 11:162–167

    Article  PubMed  CAS  Google Scholar 

  • Sehnke PC, Chung HJ, Wu K, Ferl RJ (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc Natl Acad Sci USA 98:765–770

    Article  PubMed  CAS  Google Scholar 

  • Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958

    Article  PubMed  CAS  Google Scholar 

  • Shewry PR, Halford NG, Belton PS, Tatham AS (2002) The structure and properties of gluten: an elastic protein from wheat grain. Philos Trans R Soc Lond Ser B Biol Sci 357:133–142

    Article  CAS  Google Scholar 

  • Simmonds D, O’Brien T (1981) Morphological and biochemical development of the wheat endosperm. American Association of Cereal Chemists, St. Paul, Minnesota

    Google Scholar 

  • Simmonds NW (1995) The relation between yield and protein in cereal grain. J Sci Food Agric 67:309–315

    Article  CAS  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Ann Rev Plant Biol 55:555–590

    Article  CAS  Google Scholar 

  • Sreenivasulu N, Altschmied L, Radchuk V, Gubatz S, Wobus U, Weschke W (2004) Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains. Plant J 37:539–553

    Article  PubMed  CAS  Google Scholar 

  • Stoddard FL (1999a) Survey of starch particle-size distribution in wheat and related species. Cereal Chem 76:145–149

    CAS  Google Scholar 

  • Stoddard FL (1999b) Variation in grain mass, grain nitrogen, and starch B-granule content within wheat heads. Cereal Chem 76:139–144

    CAS  Google Scholar 

  • Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208

    Article  PubMed  CAS  Google Scholar 

  • Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55:2131–2145

    Article  PubMed  CAS  Google Scholar 

  • Triboi E, Martre P, Triboi-Blondel AM (2003) Environmentally-induced changes in protein composition in developing grains of wheat are related to changes in total protein content. J Exp Bot 54:1731–1742

    Article  PubMed  CAS  Google Scholar 

  • Triboi E, Triboi-Blondel AM (2002) Productivity and grain or seed composition: a new approach to an old problem – invited paper. Eur J Agron 16:163–186

    Article  Google Scholar 

  • Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2:e117

    Article  PubMed  CAS  Google Scholar 

  • Wilson ID, Barker GLA, Beswick RW, Shepherd SK, Lu CG, Coghill JA, Edwards D, Owen P, Lyon R, Parker JS, Lenton JR, Holdsworth MJ, Shewry PR, Edwards KJ (2004) A transcriptomics resource for wheat functional genomics. Plant Biotechnol J 2:495–506

    Article  PubMed  Google Scholar 

  • Woerdeman DL, Veraverbeke WS, Parnas RS, Johnson D, Delcour JA, Verpoest I, Plummer CJ (2004) Designing new materials from wheat protein. Biomacromolecules 5:1262–1269

    Article  PubMed  CAS  Google Scholar 

  • Wolfinger R, Gibson G, Wolfinger E, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules R (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8:625–637

    Article  PubMed  CAS  Google Scholar 

  • Xue GP, McIntyre CL, Chapman S, Bower NI, Way H, Reverter A, Clarke B, Shorter R (2006) Differential gene expression of wheat progeny with contrasting levels of transpiration efficiency. Plant Mol Biol 61:863–881

    Article  PubMed  CAS  Google Scholar 

  • Yang YH, Speed T (2002) Design issues for cDNA microarray experiments. Nat Rev Genet 3:579–588

    PubMed  CAS  Google Scholar 

  • Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44:283–301

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Feng B, Zhang Q, Zhang D, Altman N, Ma H (2005) Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol 58:401–419

    Article  PubMed  CAS  Google Scholar 

  • Zhu T, Budworth P, Chen W, Provart N, Chang H-S, Guimil S, Su W, Estes B, Zou G, Wang X (2003) Transcriptional control of nutrient partitioning during rice grain filling. Plant Biotechnol J 1:59–70

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Adaku Ude, Sarah Vela and Joseph Pham for their excellent technical assistance and Dr. Grace Chen, Dr. Michael Gitt, Dr. Kent McCue and Dr. Craig Parker for the critical reading of the manuscript. We apologize to those whose works we have not cited owing to restrictions in the length of this article. The USDA-ARS CRIS Project 5325-21000-011 funded this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Debbie L. Laudencia-Chingcuanco.

Additional information

Boryana S. Stamova share first co-authorship

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laudencia-Chingcuanco, D.L., Stamova, B.S., You, F.M. et al. Transcriptional profiling of wheat caryopsis development using cDNA microarrays. Plant Mol Biol 63, 651–668 (2007). https://doi.org/10.1007/s11103-006-9114-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-006-9114-y

Keywords

Navigation