A gene expression atlas of the model legume Medicago truncatula.

Legumes played central roles in the development of agriculture and civilization, and today account for approximately one-third of the world's primary crop production. Unfortunately, most cultivated legumes are poor model systems for genomic research. Therefore, Medicago truncatula, which has a relatively small diploid genome, has been adopted as a model species for legume genomics. To enhance its value as a model, we have generated a gene expression atlas that provides a global view of gene expression in all major organ systems of this species, with special emphasis on nodule and seed development. The atlas reveals massive differences in gene expression between organs that are accompanied by changes in the expression of key regulatory genes, such as transcription factor genes, which presumably orchestrate genetic reprogramming during development and differentiation. Interestingly, many legume-specific genes are preferentially expressed in nitrogen-fixing nodules, indicating that evolution endowed them with special roles in this unique and important organ. Comparative transcriptome analysis of Medicago versus Arabidopsis revealed significant divergence in developmental expression profiles of orthologous genes, which indicates that phylogenetic analysis alone is insufficient to predict the function of orthologs in different species. The data presented here represent an unparalleled resource for legume functional genomics, which will accelerate discoveries in legume biology.

[1]  M. J. Harrison,et al.  MOLECULAR AND CELLULAR ASPECTS OF THE ARBUSCULAR MYCORRHIZAL SYMBIOSIS. , 1999, Annual review of plant physiology and plant molecular biology.

[2]  C. Town.  Annotating the genome of Medicago truncatula. , 2006, Current opinion in plant biology.

[3]  R. Durbin,et al.  Pfam: A comprehensive database of protein domain families based on seed alignments , 1997, Proteins.

[4]  J. Downie,et al.  Calcium, kinases and nodulation signalling in legumes , 2004, Nature Reviews Molecular Cell Biology.

[5]  W. Broughton,et al.  Control of leghaemoglobin synthesis in snake beans. , 1971, The Biochemical journal.

[6]  J. Doyle.  Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria , 1998 .

[7]  M. Udvardi,et al.  METABOLITE TRANSPORT ACROSS SYMBIOTIC MEMBRANES OF LEGUME NODULES. , 1997, Annual review of plant physiology and plant molecular biology.

[8]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[9]  M. Parniske,et al.  Evolution of signal transduction in intracellular symbiosis. , 2002, Trends in plant science.

[10]  J. Riechmann,et al.  A genomic perspective on plant transcription factors. , 2000, Current opinion in plant biology.

[11]  Leif Schauser,et al.  A plant regulator controlling development of symbiotic root nodules , 1999, Nature.

[12]  D. Redecker,et al.  Glomalean fungi from the Ordovician. , 2000, Science.

[13]  D. Kahn,et al.  Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. , 2004, Molecular plant-microbe interactions : MPMI.

[14]  Jeffrey T. Leek,et al.  Gene expression EDGE : extraction and analysis of differential gene expression , 2006 .

[15]  Kathryn A. VandenBosch,et al.  Computational Identification and Characterization of Novel Genes from Legumes1[w] , 2004, Plant Physiology.

[16]  N. J. Brewin.  Development of the legume root nodule. , 1991, Annual review of cell biology.

[17]  B. Trevaskis,et al.  Symbiotic nitrogen fixation research in the postgenomics era , 2002 .

[18]  Andrei N Lupas,et al.  PhyloGenie: automated phylome generation and analysis. , 2004, Nucleic acids research.

[19]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.

[20]  S. Tabata,et al.  Expression Islands Clustered on the Symbiosis Island of the Mesorhizobium loti Genome , 2004, Journal of bacteriology.

[21]  T. Bisseling,et al.  NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription , 2005, Science.

[22]  M. Udvardi,et al.  Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. , 2004, The Plant journal : for cell and molecular biology.

[23]  V. Smil.  Nitrogen in crop production: An account of global flows , 1999 .

[24]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[25]  Igor Dozmorov,et al.  An associative analysis of gene expression array data , 2003, Bioinform..

[26]  M. Parniske.  Molecular genetics of the arbuscular mycorrhizal symbiosis. , 2004, Current opinion in plant biology.

[27]  Rafael A. Irizarry,et al.  A Model-Based Background Adjustment for Oligonucleotide Expression Arrays , 2004 .

[28]  H. Abdi.  The Bonferonni and Šidák Corrections for Multiple Comparisons , 2006 .

[29]  E. Journet,et al.  Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. , 2001, Molecular plant-microbe interactions : MPMI.

[30]  Eva Kondorosi,et al.  A Novel Family in Medicago truncatula Consisting of More Than 300 Nodule-Specific Genes Coding for Small, Secreted Polypeptides with Conserved Cysteine Motifs1,212 , 2003, Plant Physiology.

[31]  J. Gouzy,et al.  Expression Profiling in Medicago truncatula Identifies More Than 750 Genes Differentially Expressed during Nodulation, Including Many Potential Regulators of the Symbiotic Program1[w] , 2004, Plant Physiology.

[32]  E. Kondorosi,et al.  Genomic organization and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula. , 2007, Molecular plant-microbe interactions : MPMI.

[33]  R. Dixon.  Natural products and plant disease resistance , 2001, Nature.

[34]  S. Long.  Genes and signals in the rhizobium-legume symbiosis. , 2001, Plant physiology.

[35]  J. Hofer,et al.  Legume Transcription Factors: Global Regulators of Plant Development and Response to the Environment1[W] , 2007, Plant Physiology.

[36]  G. Weiller,et al.  AffyTrees: Facilitating Comparative Analysis of Affymetrix Plant Microarray Chips1[C][OA] , 2007, Plant Physiology.

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

[38]  S. Tabata,et al.  Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases , 2003, Nature.

[39]  C. Vance,et al.  Legumes: Importance and Constraints to Greater Use , 2003, Plant Physiology.

[40]  Georg F. Weiller,et al.  Extending MapMan: application to legume genome arrays , 2006, Bioinform..

[41]  C. Li,et al.  Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Taylor,et al.  Four hundred-million-year-old vesicular arbuscular mycorrhizae. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[44]  S. Davis.  Faculty Opinions recommendation of Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. , 2006 .

[45]  P. Chomczyński,et al.  Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. , 1995, BioTechniques.

[46]  K. Silverstein,et al.  Novel paralogous gene families with potential function in legume nodules and seeds. , 2006, Current opinion in plant biology.

[47]  K. Silverstein,et al.  Accumulation of extracellular proteins bearing unique proline-rich motifs in intercellular spaces of the legume nodule parenchyma , 2005, Protoplasma.

[48]  S. Shaw,et al.  Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[49]  S. Clough,et al.  Transcriptome changes in the phenylpropanoid pathway of Glycine max in response to Pseudomonas syringae infection , 2006, BMC Plant Biology.

[50]  R. R. Samaha,et al.  Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. , 2000, Science.

[51]  J. F. Marsh,et al.  Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators , 2005, Science.

[52]  E. Kondorosi,et al.  Glycine-rich proteins encoded by a nodule-specific gene family are implicated in different stages of symbiotic nodule development in Medicago spp. , 2002, Molecular plant-microbe interactions : MPMI.

[53]  Michal Linial,et al.  Novel Unsupervised Feature Filtering of Biological Data , 2006, ISMB.

[54]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Di Liu,et al.  DATF: a database of Arabidopsis transcription factors , 2005, Bioinform..