Systems Analysis of Seed Filling in Arabidopsis: Using General Linear Modeling to Assess Concordance of Transcript and Protein Expression1[C][W][OA]

Previous systems analyses in plants have focused on a single developmental stage or time point, although it is often important to additionally consider time-index changes. During seed development a cascade of events occurs within a relatively brief time scale. We have collected protein and transcript expression data from five sequential stages of Arabidopsis (Arabidopsis thaliana) seed development encompassing the period of reserve polymer accumulation. Protein expression profiling employed two-dimensional gel electrophoresis coupled with tandem mass spectrometry, while transcript profiling used oligonucleotide microarrays. Analyses in biological triplicate yielded robust expression information for 523 proteins and 22,746 genes across the five developmental stages, and established 319 protein/transcript pairs for subsequent pattern analysis. General linear modeling was used to evaluate the protein/transcript expression patterns. Overall, application of this statistical assessment technique showed concurrence for a slight majority (56%) of expression pairs. Many specific examples of discordant protein/transcript expression patterns were detected, suggesting that this approach will be useful in revealing examples of posttranscriptional regulation.

[1]  Nicolas Turenne.  Data Mining, a Tool for Systems Biology or a Systems Biology Tool , 2009 .

[2]  Karl J. Friston.  Hierarchical Models in the Brain , 2008, PLoS Comput. Biol..

[3]  M. Hills.  Control of storage-product synthesis in seeds. , 2004, Current opinion in plant biology.

[4]  N. Luscombe,et al.  Know your limits: assumptions, constraints and interpretation in systems biology. , 2009, Biochimica et biophysica acta.

[5]  David E. Misek,et al.  Discordant Protein and mRNA Expression in Lung Adenocarcinomas * , 2002, Molecular & Cellular Proteomics.

[6]  M. Lehrman,et al.  Discordance of UPR signaling by ATF6 and Ire1p-XBP1 with levels of target transcripts. , 2004, Biochemical and biophysical research communications.

[7]  Gang Wu,et al.  Integrative Analysis of Transcriptomic and Proteomic Data: Challenges, Solutions and Applications , 2007, Critical reviews in biotechnology.

[8]  J. Shendure.  The beginning of the end for microarrays? , 2008, Nature Methods.

[9]  Richard L. Degerman.  Ordered binary trees constructed through an application of Kendall's tau , 1982 .

[10]  J. Yates,et al.  An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database , 1994, Journal of the American Society for Mass Spectrometry.

[11]  J. Rodgers,et al.  Thirteen ways to look at the correlation coefficient , 1988 .

[12]  J. Froehlich,et al.  A Heteromeric Plastidic Pyruvate Kinase Complex Involved in Seed Oil Biosynthesis in Arabidopsis[W] , 2007, The Plant Cell Online.

[13]  S. Gygi,et al.  Correlation between Protein and mRNA Abundance in Yeast , 1999, Molecular and Cellular Biology.

[14]  Lourens J. Waldorp,et al.  Robust and Unbiased Variance of GLM Coefficients for Misspecified Autocorrelation and Hemodynamic Response Models in fMRI , 2009, Int. J. Biomed. Imaging.

[15]  M. Hajduch,et al.  Proteomic Analysis of Seed Filling in Brassica napus. Developmental Characterization of Metabolic Isozymes Using High-Resolution Two-Dimensional Gel Electrophoresis1[W] , 2006, Plant Physiology.

[16]  M. Hajduch,et al.  A Systematic Proteomic Study of Seed Filling in Soybean. Establishment of High-Resolution Two-Dimensional Reference Maps, Expression Profiles, and an Interactive Proteome Database1[w] , 2005, Plant Physiology.

[17]  M. Hajduch,et al.  In-Depth Investigation of the Soybean Seed-Filling Proteome and Comparison with a Parallel Study of Rapeseed1[W][OA] , 2008, Plant Physiology.

[18]  Jae K. Lee,et al.  Transcript and protein expression profiles of the NCI-60 cancer cell panel: an integromic microarray study , 2007, Molecular Cancer Therapeutics.

[19]  Zhentian Lei,et al.  Transcript and proteomic analysis of developing white lupin (Lupinus albus L.) roots , 2009, BMC Plant Biology.

[20]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[21]  David G Hendrickson,et al.  Concordant Regulation of Translation and mRNA Abundance for Hundreds of Targets of a Human microRNA , 2009, PLoS biology.

[22]  K. Edwards,et al.  A joint transcriptomic, proteomic and metabolic analysis of maize endosperm development and starch filling. , 2008, Plant biotechnology journal.

[23]  Gang Wu,et al.  Integrative Analyses of Posttranscriptional Regulation in the Yeast Saccharomyces cerevisiae Using Transcriptomic and Proteomic Data , 2008, Current Microbiology.

[24]  Kathleen Marchal,et al.  Inferring Transcriptional Networks by Mining 'Omics' Data , 2006 .

[25]  D. Cox,et al.  An Analysis of Transformations , 1964 .

[26]  Wei-Shou Hu,et al.  Uncovering Genes with Divergent mRNA-Protein Dynamics in Streptomyces coelicolor , 2008, PloS one.

[27]  Alison M. Smith,et al.  Plastidial glycolysis in developing Arabidopsis embryos. , 2010, The New phytologist.

[28]  Gregory W. Corder,et al.  Nonparametric Statistics for Non-Statisticians: A Step-by-Step Approach , 2009 .

[29]  Igor Jurisica,et al.  Integrated proteomic and transcriptomic profiling of mouse lung development and Nmyc target genes , 2007, Molecular systems biology.

[30]  L. Hood,et al.  Complementary Profiling of Gene Expression at the Transcriptome and Proteome Levels in Saccharomyces cerevisiae*S , 2002, Molecular & Cellular Proteomics.

[31]  J. A. Wagmaister,et al.  Using Genomics to Study Legume Seed Development1 , 2007, Plant Physiology.

[32]  Thomas Girke,et al.  Contrapuntal Networks of Gene Expression during Arabidopsis Seed Filling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000877. , 2002, The Plant Cell Online.

[33]  P. Nelson,et al.  Correlation of mRNA and protein levels: Cell type-specific gene expression of cluster designation antigens in the prostate , 2008, BMC Genomics.

[34]  Torben F. Ørntoft,et al.  Genome-wide Study of Gene Copy Numbers, Transcripts, and Protein Levels in Pairs of Non-invasive and Invasive Human Transitional Cell Carcinomas* , 2002, Molecular & Cellular Proteomics.

[35]  H. Hornshøj,et al.  Transcriptomic and proteomic profiling of two porcine tissues using high-throughput technologies , 2009, BMC Genomics.

[36]  B. Usadel,et al.  Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis , 2009, Molecular systems biology.

[37]  P. Zimmermann,et al.  Genome-Scale Proteomics Reveals Arabidopsis thaliana Gene Models and Proteome Dynamics , 2008, Science.

[38]  I. Simon,et al.  Reconstructing dynamic regulatory maps , 2007, Molecular systems biology.

[39]  R. Yadegari,et al.  Plant Embryogenesis: Zygote to Seed , 1994, Science.

[40]  Alexandra To,et al.  Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[41]  Yingyao Zhou,et al.  Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. , 2004, Genome research.

[42]  J. Miernyk,et al.  Shape-to-String Mapping: A Novel Approach To Clustering Time-Index Biomics Data , 2009 .