Gene expression in the developing aleurone and starchy endosperm of wheat
Corresponding Author
Susan A. Gillies
Southern Cross Plant Science, Southern Cross University, Lismore, NSW, Australia
(Tel (61-2) 6620 3466; fax (61-2) 6622 2080; email [email protected])Search for more papers by this authorAgnelo Futardo
Southern Cross Plant Science, Southern Cross University, Lismore, NSW, Australia
Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Qld, Australia
Search for more papers by this authorRobert J. Henry
Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Qld, Australia
Search for more papers by this authorCorresponding Author
Susan A. Gillies
Southern Cross Plant Science, Southern Cross University, Lismore, NSW, Australia
(Tel (61-2) 6620 3466; fax (61-2) 6622 2080; email [email protected])Search for more papers by this authorAgnelo Futardo
Southern Cross Plant Science, Southern Cross University, Lismore, NSW, Australia
Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Qld, Australia
Search for more papers by this authorRobert J. Henry
Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, Qld, Australia
Search for more papers by this authorAccession number for National Centre for Biotechnology Information/Gene Expression Omnibus No: X.
Summary
Wheat is a critical food source globally. Food security is an increasing concern; current production levels are not expected to keep pace with global demand. New technologies have provided a vast array of wheat genetic data; however, best use of this data requires placing it within a framework in which the various genes, pathways and interactions can be examined. Here we present the first systematic comparison of the global transcriptomes of the aleurone and starchy endosperm of the developing wheat seed (Triticum aestivum), at time points critical to the development of the aleurone layer; 6-, 9- and 14-day post-anthesis. Illumina sequencing gave 25—55 million sequence reads per tissue, of the trimmed reads, 70%—81% mapped to reference expressed sequence transcripts. Transcript abundance was analysed by performing RNA-Seq normalization to generate reads per kilobase of exon model per million mapped reads values, and these were used in comparative analyses between the tissues at each time point using Kal’s Z-test. This identified 9414—13 202 highly differentially expressed transcripts that were categorized on the basis of tissue and time point expression and functionally analysed revealing two very distinct tissues. The results demonstrate the fundamental biological reprogramming of the two major biologically and economically significant tissues of the wheat seed over this time course. Understanding these changes in gene expression profiles is essential to mining the potential these tissues hold for human nutrition and contributing to the systems biology of this important crop plant.
Supporting Information
Figure S1 Level 4 Gene Ontology analysis of all differentially expressed transcripts at each time point (Total) in comparison with transcripts DE at one time point (Only) and those common to all time points (All). A, Biological process terms; B, molecular function terms; C, cellular component terms. Al, aleurone; En, starchy endosperm.
Dataset S1 NCBI/GEO Submission. Raw Illumina sequencing data files and RNA-Seq analysis files are provided.
Filename | Description |
---|---|
PBI_705_sm_FigS1.tif7.7 MB | Supporting info item |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Becraft, P.W. (2001) Cell fate specification in the cereal endosperm. Semin. Cell Dev. Biol. 12, 387–394.
- Becraft, P.W. and Asuncion-Crabb, Y. (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development, 127, 4039–4048.
- Becraft, P.W. and Yi, G. (2011) Regulation of aleurone development in cereal grains. J. Exp. Bot., 62, 1669–1675.
- Becraft, P.W., Stinard, P.S. and McCarty, D.R. (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science, 273, 1406–1409.
- Botton, A., Galla, G., Conesa, A., Bachem, C., Ramina, A. and Barcaccia, G. (2008) Large-scale Gene Ontology analysis of plant transcriptome-derived sequences retrieved by AFLP technology. BMC Genomics, 9, 347.
- Brown, R.C., Lemmon, B.E. and Olsen, O.A. (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell, 6, 1241–1252.
- Conesa, A. and Gotz, S. (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics, 2008, 619832.
- Conesa, A., Gotz, S., Garcia- Gomez, J.M., Terol, J., Talon, M. and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674–3676.
- Dever, T.E. (2002) Gene-specific regulation by general translation factors. Cell, 108, 545–556.
- Dietz, K.J., Jacob, S., Oelze, M.L., Laxa, M., Tognetti, V., de Miranda, S.M., Baier, M. and Finkemeier, I. (2006) The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57, 1697–1709.
- Drea, S., Leader, D.J., Arnold, B.C., Shaw, P., Dolan, L. and Doonan, J.H. (2005) Systematic spatial analysis of gene expression during wheat caryopsis development. Plant Cell, 17, 2172–2185.
- Emes, M.J., Bowsher, C.G., Hedley, C., Burrell, M.M., Scrase- Field, E.S. and Tetlow, I.J. (2003) Starch synthesis and carbon partitioning in developing endosperm. J. Exp. Bot. 54, 569–575.
- Fenech, M., Noakes, M., Clifton, P. and Topping, D. (2005) Aleurone flour increases red-cell folate and lowers plasma homocyst(e)ine substantially in man. Br. J. Nutr. 93, 353–360.
- Geisler-Lee, J. and Gallie, D.R. (2005) Aleurone cell identity is suppressed following connation in maize kernels. Plant Physiol. 139, 204–212.
- Gruis, D.F., Guo, H., Selinger, D., Tian, Q. and Olsen, O.A. (2006) Surface position, not signaling from surrounding maternal tissues, specifies aleurone epidermal cell fate in maize. Plant Physiol. 141, 898–909.
- Jerkovic, A., Kriegel, A.M., Bradner, J.R., Atwell, B.J., Roberts, T.H. and Willows, R.D. (2010) Strategic distribution of protective proteins within bran layers of wheat protects the nutrient-rich endosperm. Plant Physiol. 152, 1459–1470.
- Laudencia- Chingcuanco, D.L., Stamova, B.S., You, F.M., Lazo, G.R., Beckles, D.M. and Anderson, O.D. (2007) Transcriptional profiling of wheat caryopsis development using cDNA microarrays. Plant Mol. Biol., 63, 651–668.
- Lid, S.E., Gruis, D., Jung, R., Lorentzen, J.A., Ananiev, E., Chamberlin, M., Niu, X., Meeley, R., Nichols, S. and Olsen, O.A. (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc. Natl. Acad. Sci. USA, 99, 5460–5465.
- Liu, K. (2011) Comparison of lipid content and fatty acid composition and their distribution within seeds of 5 small grain species. J. Food Sci. 76, C334–C342.
- Mata, J., Marguerat, S. and Bahler, J. (2005) Post-transcriptional control of gene expression: a genome-wide perspective. Trends Biochem. Sci. 30, 506–514.
- McIntosh, G.H., Royle, P.J. and Pointing, G. (2001) Wheat aleurone flour increases cecal beta-glucuronidase activity and butyrate concentration and reduces colon adenoma burden in azoxymethane-treated rats. J. Nutr. 131, 127–131.
- McIntosh, S., Watson, L., Bundock, P.C., Crawford, A.C., White, J., Cordeiro, G.M., Barbary, D., Rooke, L. and Henry, R.J. (2007) SAGE of the developing wheat Caryopsis. Plant Biotechnol. J. 5, 69–83.
- Morrison, I.N., Kuo, J. and O’ Brien, T.P. (1975a) Histochemistry and fine structure of developing wheat aleurone cells. Planta, 123, 105–116.
- Morrison, W.R., Mann, D.L., Soon, W. and Coventry, A.M. (1975b) Selective extraction and quantitative analysis of non-starch and starch lipids from wheat flour. J. Sci. Food Agric. 26, 507–521.
- Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621–628.
- Myhre, S., Tveit, H., Mollestad, T. and Laegreid, A. (2006) Additional gene ontology structure for improved biological reasoning. Bioinformatics, 22, 2020–2027.
- Olsen, O.A. (2001) ENDOSPERM DEVELOPMENT: cellularization and Cell Fate Specification. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 233–267.
- Olsen, O.A. (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell, 16(Suppl), S214–S227.
- Price, R.K., Keaveney, E.M., Hamill, L.L., Wallace, J.M., Ward, M., Ueland, P.M., McNulty, H., Strain, J.J., Parker, M.J. and Welch, R.W. (2010) Consumption of wheat aleurone-rich foods increases fasting plasma betaine and modestly decreases fasting homocysteine and LDL-cholesterol in adults. J. Nutr. 140, 2153–2157.
- Regvar, M., Eichert, D., Kaulich, B., Gianoncelli, A., Pongrac, P., Vogel-Mikus, K. and Kreft, I. (2011) New insights into globoids of protein storage vacuoles in wheat aleurone using synchrotron soft X-ray microscopy. J. Exp. Bot. 62, 3929–3939.
- Shen, B., Li, C., Min, Z., Meeley, R.B., Tarczynski, M.C. and Olsen, O.A. (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc. Natl. Acad. Sci. USA, 100, 6552–6557.
- Stamova, B.S., Laudencia-Chingcuanco, D. and Beckles, D.M. (2009) Transcriptomic analysis of starch biosynthesis in the developing grain of hexaploid wheat. Int. J. Plant Genomics, 2009, 407426.
- Stein, K., Borowicki, A., Scharlau, D. and Glei, M. (2010) Fermented wheat aleurone induces enzymes involved in detoxification of carcinogens and in antioxidative defence in human colon cells. Br. J. Nutr. 104, 1101–1111.
- Tovar-Mendez, A., Matamoros, M.A., Bustos-Sanmamed, P., Dietz, K.J., Cejudo, F.J., Rouhier, N., Sato, S., Tabata, S. and Becana, M. (2011) Peroxiredoxins and NADPH-dependent thioredoxin systems in the model legume Lotus japonicus. Plant Physiol. 156, 1535–1547.
- Usadel, B., Nagel, A., Thimm, O., Redestig, H., Blaesing, O.E., Palacios-Rojas, N., Selbig, J., Hannemann, J., Piques, M.C., Steinhauser, D., Scheible, W.R., Gibon, Y., Morcuende, R., Weicht, D., Meyer, S. and Stitt, M. (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol. 138, 1195–1204.
- Usadel, B., Poree, F., Nagel, A., Lohse, M., Czedik-Eysenberg, A. and Stitt, M. (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant Cell Environ. 32, 1211–1229.
- Wan, Y., Poole, R.L., Huttly, A.K., Toscano-Underwood, C., Feeney, K., Welham, S., Gooding, M.J., Mills, C., Edwards, K.J., Shewry, P.R. and Mitchell, R.A. (2008) Transcriptome analysis of grain development in hexaploid wheat. BMC Genomics, 9, 121.
- Wan, Y., Underwood, C., Toole, G., Skeggs, P., Zhu, T., Leverington, M., Griffiths, S., Wheeler, T., Gooding, M., Poole, R., Edwards, K.J., Gezan, S., Welham, S., Snape, J., Mills, E.N., Mitchell, R.A. and Shewry, P.R. (2009) A novel transcriptomic approach to identify candidate genes for grain quality traits in wheat. Plant Biotechnol. J. 7, 401–410.
- Wegel, E., Pilling, E., Calder, G., Drea, S., Doonan, J., Dolan, L. and Shaw, P. (2005) Three-dimensional modelling of wheat endosperm development. New Phytol. 168, 253–262.
- Young, T.E. and Gallie, D.R. (2000) Programmed cell death during endosperm development. Plant Mol. Biol. 44, 283–301.
- Young, T.E., Meeley, R.B. and Gallie, D.R. (2004) ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J. 40, 813–825.
- Zdobnov, E.M. and Apweiler, R. (2001) InterProScan – an integration platform for the signature-recognition methods in InterPro. Bioinformatics, 17, 847–848.