Co-ordination and divergence of cell-specific transcription and translation of genes in arabidopsis root cells

Background and Aims A key challenge in biology is to systematically investigate and integrate the different levels of information available at the global and single-cell level. Recent studies have elucidated spatiotemporal expression patterns of root cell types in Arabidopsis thaliana, and genome-wide quantification of polysome-associated mRNA levels, i.e. the translatome, has also been obtained for corresponding cell types. Translational control has been increasingly recognized as an important regulatory step in protein synthesis. The aim of this study was to investigate coupled transcription and translation by use of publicly available root datasets. Methods Using cell-type-specific datasets of the root transcriptome and translatome of arabidopsis, a systematic assessment was made of the degree of co-ordination and divergence between these two levels of cellular organization. The computational analysis considered correlation and variation of expression across cell types at both system levels, and also provided insights into the degree of co-regulatory relationships that are preserved between the two processes. Key Results The overall correlation of expression and translation levels of genes resemble an almost bimodal distribution (mean/median value of 0·08/0·12), with a second, less strongly pronounced ‘mode’ for negative Pearson's correlation coefficient values. The analysis conducted also confirms that previously identified key transcriptional activators of secondary cell wall development display highly conserved patterns of transcription and translation across the investigated cell types. Moreover, the biological processes that display conserved and divergent patterns based on the cell-type-specific expression and translation levels were identified. Conclusions In agreement with previous studies in animal cells, a large degree of uncoupling was found between the transcriptome and translatome. However, components and processes were also identified that are under co-ordinated transcriptional and translational control in plant root cells.

[1]  Ottoline Leyser,et al.  An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root , 1999, Cell.

[2]  M. Hirai,et al.  Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. , 2005, The Plant journal : for cell and molecular biology.

[3]  K. Sjölander,et al.  The Arabidopsis thaliana Chloroplast Proteome Reveals Pathway Abundance and Novel Protein Functions , 2004, Current Biology.

[4]  S. Persson,et al.  Co-expression of cell-wall related genes: new tools and insights , 2012, Front. Plant Sci..

[5]  Staffan Persson,et al.  Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Fatima Sanchez-Cabo,et al.  Global Gene Expression Profiling Reveals Widespread yet Distinctive Translational Responses to Different Eukaryotic Translation Initiation Factor 2B-Targeting Stress Pathways , 2005, Molecular and Cellular Biology.

[7]  Tal Nawy,et al.  Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞ , 2005, The Plant Cell Online.

[8]  Isaac S. Kohane,et al.  Relevance Networks: A First Step Toward Finding Genetic Regulatory Networks Within Microarray Data , 2003 .

[9]  Pablo Tamayo,et al.  Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Bailey-Serres,et al.  Profiling of Translatomes of in Vivo–Grown Pollen Tubes Reveals Genes with Roles in Micropylar Guidance during Pollination in Arabidopsis[W][OPEN] , 2014, Plant Cell.

[11]  M. Bevan,et al.  The Arabidopsis genome: a foundation for plant research. , 2005, Genome research.

[12]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[13]  Mark M. Davis,et al.  Cell type–specific gene expression differences in complex tissues , 2010, Nature Methods.

[14]  Bairong Shen,et al.  Systematic investigation of global coordination among mRNA and protein in cellular society , 2010, BMC Genomics.

[15]  Kirsten Jørgensen,et al.  Integrative Analysis of Metabolomics and Transcriptomics Data: A Unified Model Framework to Identify Underlying System Pathways , 2013, PloS one.

[16]  Xiuxin Deng,et al.  An integrative analysis of transcriptome and proteome provides new insights into carotenoid biosynthesis and regulation in sweet orange fruits. , 2012, Journal of proteomics.

[17]  L. Williams,et al.  Sugar transporters in higher plants--a diversity of roles and complex regulation. , 2000, Trends in plant science.

[18]  S. Brandt,et al.  Microgenomics: gene expression analysis at the tissue-specific and single-cell levels. , 2005, Journal of experimental botany.

[19]  Dimitra L. Milioni,et al.  Early Gene Expression Associated with the Commitment and Differentiation of a Plant Tracheary Element Is Revealed by cDNA–Amplified Fragment Length Polymorphism Analysis , 2002, The Plant Cell Online.

[20]  P. Zimmermann,et al.  Gene Expression Analysis, Proteomics, and Network Discovery1 , 2009, Plant Physiology.

[21]  Tetsuro Mimura,et al.  Transcription switches for protoxylem and metaxylem vessel formation. , 2005, Genes & development.

[22]  Masaru Tomita,et al.  Merging multiple omics datasets in silico: statistical analyses and data interpretation. , 2013, Methods in molecular biology.

[23]  E. Marcotte,et al.  Insights into the regulation of protein abundance from proteomic and transcriptomic analyses , 2012, Nature Reviews Genetics.

[24]  K. Shinozaki,et al.  Genomics and Bioinformatics Resources for Crop Improvement , 2010, Plant & cell physiology.

[25]  Ying Wang,et al.  Advances in plant cell type-specific genome-wide studies of gene expression , 2011, Frontiers in Biology.

[26]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[27]  Zoran Nikoloski,et al.  The Choice between MapMan and Gene Ontology for Automated Gene Function Prediction in Plant Science , 2012, Front. Gene..

[28]  A. Tretyn,et al.  A role for redox factors in shaping root architecture under Phosphorus deficiency , 2010, Plant signaling & behavior.

[29]  G. Coruzzi,et al.  Cell-specific gene expression in plants. , 1990, Annual review of genetics.

[30]  Olga G. Troyanskaya,et al.  A scalable method for integration and functional analysis of multiple microarray datasets , 2006, Bioinform..

[31]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[32]  B. Bainbridge,et al.  Genetics , 1981, Experientia.

[33]  B. Usadel,et al.  Transcriptional wiring of cell wall-related genes in Arabidopsis. , 2009, Molecular plant.

[34]  David W. Galbraith,et al.  Immunopurification of Polyribosomal Complexes of Arabidopsis for Global Analysis of Gene Expression1[w] , 2005, Plant Physiology.

[35]  J. Dopazo,et al.  Extensive Translatome Remodeling during ER Stress Response in Mammalian Cells , 2012, PloS one.

[36]  Uwe Ohler,et al.  Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  H. Beug,et al.  Isolation of translationally controlled mRNAs by differential screening , 2000, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[38]  V. Ivanov Oxidative stress and formation and maintenance of root stem cells , 2007, Biochemistry (Moscow).

[39]  W. Cleveland The Collected Works of John W. Tukey, Volume V, Graphics 1965-1985. , 1989 .

[40]  D. Schachtman,et al.  Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. , 2005, Plant & cell physiology.

[41]  Ron Edgar,et al.  Gene Expression Omnibus ( GEO ) : Microarray data storage , submission , retrieval , and analysis , 2008 .

[42]  Zoran Nikoloski,et al.  Integrative Comparative Analyses of Transcript and Metabolite Profiles from Pepper and Tomato Ripening and Development Stages Uncovers Species-Specific Patterns of Network Regulatory Behavior[W][OA] , 2012, Plant Physiology.

[43]  B. Palsson,et al.  The model organism as a system: integrating 'omics' data sets , 2006, Nature Reviews Molecular Cell Biology.

[44]  P. Benfey,et al.  Fluorescence-activated cell sorting in plant developmental biology. , 2010, Methods in molecular biology.

[45]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[46]  P. Benfey,et al.  The protein expression landscape of the Arabidopsis root , 2012, Proceedings of the National Academy of Sciences.

[47]  S. Stigler Francis Galton's Account of the Invention of Correlation , 1989 .

[48]  B. Snel,et al.  A global definition of expression context is conserved between orthologs, but does not correlate with sequence conservation , 2006, BMC Genomics.

[49]  Weiwen Zhang,et al.  Integrating multiple 'omics' analysis for microbial biology: application and methodologies. , 2010, Microbiology.

[50]  D. Galbraith,et al.  Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[51]  Gary A. Churchill,et al.  Analysis of Variance for Gene Expression Microarray Data , 2000, J. Comput. Biol..

[52]  Nathan M. Springer,et al.  Reshaping of the maize transcriptome by domestication , 2012, Proceedings of the National Academy of Sciences.

[53]  K. Oparka,et al.  Sieve Elements and Companion Cells—Traffic Control Centers of the Phloem , 1999, Plant Cell.

[54]  C. Buell,et al.  Advances in plant genome sequencing. , 2012, The Plant journal : for cell and molecular biology.

[55]  E. Kay,et al.  Introductory Graph Theory , 1978 .

[56]  P. Benfey,et al.  Cell type–specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines , 2005, Nature Methods.

[57]  A. Fernie,et al.  Combined Transcript and Metabolite Profiling of Arabidopsis Grown under Widely Variant Growth Conditions Facilitates the Identification of Novel Metabolite-Mediated Regulation of Gene Expression[C][W] , 2010, Plant Physiology.

[58]  R. Zhong,et al.  The Poplar MYB Master Switches Bind to the SMRE Site and Activate the Secondary Wall Biosynthetic Program during Wood Formation , 2013, PloS one.

[59]  Enrico Blanzieri,et al.  Widespread uncoupling between transcriptome and translatome variations after a stimulus in mammalian cells , 2012, BMC Genomics.

[60]  N. Sauer,et al.  Phloem Loading by the PmSUC2 Sucrose Carrier from Plantago major Occurs into Companion Cells. , 1995, The Plant cell.

[61]  R. Tuan,et al.  Projection Stereolithographic Fabrication of Human Adipose Stem Cell-Incorporated Biodegradable Scaffolds for Cartilage Tissue Engineering , 2015, Front. Bioeng. Biotechnol..

[62]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[63]  G. Parmigiani,et al.  The Analysis of Gene Expression Data , 2003 .

[64]  D. Schachtman,et al.  Hydrogen peroxide mediates plant root cell response to nutrient deprivation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[65]  A. Gerber,et al.  Stress-Dependent Coordination of Transcriptome and Translatome in Yeast , 2009, PLoS biology.

[66]  R. Zhong,et al.  The MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis , 2007, The Plant Cell Online.

[67]  C. Jung THE COLLECTED WORKS OF , 2014 .

[68]  S. Turner,et al.  ARABIDOPSIS : A RICH HARVEST 10 YEARS AFTER COMPLETION OF THE GENOME SEQUENCE Arabidopsis – a powerful model system for plant cell wall research , 2010 .

[69]  D. Shasha,et al.  A Gene Expression Map of the Arabidopsis Root , 2003, Science.

[70]  Léon Personnaz,et al.  Enrichment or depletion of a GO category within a class of genes: which test? , 2007, Bioinform..

[71]  U. Sauer,et al.  Getting Closer to the Whole Picture , 2007, Science.

[72]  Rafael A Irizarry,et al.  Exploration, normalization, and summaries of high density oligonucleotide array probe level data. , 2003, Biostatistics.

[73]  K. Jiang,et al.  Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment , 2003, Development.

[74]  U. Roessner,et al.  Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement , 2006, Nature Biotechnology.

[75]  C. Hack,et al.  Integrated transcriptome and proteome data: the challenges ahead. , 2004, Briefings in functional genomics & proteomics.

[76]  John Schiefelbein,et al.  ARABIDOPSIS : A RICH HARVEST 10 YEARS AFTER COMPLETION OF THE GENOME SEQUENCE Getting to the root of plant biology : impact of the Arabidopsis genome sequence on root research , 2010 .

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

[78]  S. Hanash,et al.  Global and Specific Translational Control by Rapamycin in T Cells Uncovered by Microarrays and Proteomics* , 2002, The Journal of Biological Chemistry.