Stuart K. Kim,^1* Jim Lund,¹ Moni Kiraly,¹ Kyle Duke,¹ Min Jiang,¹ Joshua M. Stuart,² Andreas Eizinger,¹ Brian N. Wylie,³ George S. Davidson³

We have assembled data from Caenorhabditis elegans DNA microarray experiments involving many growth conditions, developmental stages, and varieties of mutants. Co-regulated genes were grouped together and visualized in a three-dimensional expression map that displays correlations of gene expression profiles as distances in two dimensions and gene density in the third dimension. The gene expression map can be used as a gene discovery tool to identify genes that are co-regulated with known sets of genes (such as heat shock, growth control genes, germ line genes, and so forth) or to uncover previously unknown genetic functions (such as genomic instability in males and sperm caused by specific transposons).

¹ Department of Developmental Biology and Genetics, Stanford University Medical School, Stanford, CA 94305, USA.
² Stanford Medical Informatics, 251 Campus Drive, MSOB X-215, Stanford, CA 94305, USA.
³ Computation, Computers and Mathematics Center, Sandia National Laboratories, Albuquerque, NM 87185-0318, USA.
^*   To whom correspondence should be addressed. E-mail: kim{at}cmgm.stanford.edu

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Nucleic Acids Res.
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Assembly of the Synaptonemal Complex Is a Highly Temperature-Sensitive Process That Is Supported by PGL-1 During Caenorhabditis elegans Meiosis.

C. Bilgir, C. R. Dombecki, P. F. Chen, A. M. Villeneuve, and K. Nabeshima (2013)
g3 3, 585-595
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PUF-8 and TCER-1 are essential for normal levels of multiple mRNAs in the C. elegans germline.

K. Pushpa, G. A. Kumar, and K. Subramaniam (2013)
Development 140, 1312-1320
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Systems Analysis of Plant Functional, Transcriptional, Physical Interaction, and Metabolic Networks.

G. W. Bassel, A. Gaudinier, S. M. Brady, L. Hennig, S. Y. Rhee, and I. De Smet (2012)
PLANT CELL 24, 3859-3875
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Discriminative local subspaces in gene expression data for effective gene function prediction.

T. Puelma, R. A. Gutierrez, and A. Soto (2012)
Bioinformatics 28, 2256-2264
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The nucleoporin Nup205/NPP-3 is lost near centrosomes at mitotic onset and can modulate the timing of this process in Caenorhabditis elegans embryos.

V. Hachet, C. Busso, M. Toya, A. Sugimoto, P. Askjaer, and P. Gonczy (2012)
Mol. Biol. Cell 23, 3111-3121
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Biomechanical Profiling of Caenorhabditis elegans Motility.

P. Krajacic, X. Shen, P. K. Purohit, P. Arratia, and T. Lamitina (2012)
Genetics 191, 1015-1021
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Notch Signaling Is Antagonized by SAO-1, a Novel GYF-Domain Protein That Interacts with the E3 Ubiquitin Ligase SEL-10 in Caenorhabditis elegans.

V. A. Hale, E. L. Guiney, L. Y. Goldberg, J. H. Haduong, C. S. Kwartler, K. W. Scangos, and C. Goutte (2012)
Genetics 190, 1043-1057
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Wobble base-pairing slows in vivo translation elongation in metazoans.

M. Stadler and A. Fire (2011)
RNA 17, 2063-2073
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A spatial and temporal map of C. elegans gene expression.

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Genome Res. 21, 325-341
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Multimodal RNA-seq using single-strand, double-strand, and CircLigase-based capture yields a refined and extended description of the C. elegans transcriptome.

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Genome Res. 21, 265-275
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The cell biology of disease: FSHD: copy number variations on the theme of muscular dystrophy.

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Integration of General Amino Acid Control and Target of Rapamycin (TOR) Regulatory Pathways in Nitrogen Assimilation in Yeast.

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Gene Terrain: Visual Exploration of Differential Gene Expression Profiles Organized in Native Biomolecular Interaction Networks.

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P. Krajacic, J. Hermanowski, O. Lozynska, T. S. Khurana, and T. Lamitina (2009)
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Comparison of diverse developmental transcriptomes reveals that coexpression of gene neighbors is not evolutionarily conserved.

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Genome Res. 19, 2214-2220
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A Caenorhabditis elegans RNA-Directed RNA Polymerase in Sperm Development and Endogenous RNA Interference.

J. I. Gent, M. Schvarzstein, A. M. Villeneuve, S. G. Gu, V. Jantsch, A. Z. Fire, and A. Baudrimont (2009)
Genetics 183, 1297-1314
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Universal function-specificity of codon usage.

H. S. Najafabadi, H. Goodarzi, and R. Salavati (2009)
Nucleic Acids Res. 37, 7014-7023
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Identification of a Basic Helix-Loop-Helix-Type Transcription Regulator Gene in Aspergillus oryzae by Systematically Deleting Large Chromosomal Segments.

F. J. Jin, T. Takahashi, M. Machida, and Y. Koyama (2009)
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Honey bee aggression supports a link between gene regulation and behavioral evolution.

C. Alaux, S. Sinha, L. Hasadsri, G. J. Hunt, E. Guzman-Novoa, G. DeGrandi-Hoffman, J. L. Uribe-Rubio, B. R. Southey, S. Rodriguez-Zas, and G. E. Robinson (2009)
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Evolution of the Caenorhabditis elegans Genome.

A. D. Cutter, A. Dey, and R. L. Murray (2009)
Mol. Biol. Evol. 26, 1199-1234
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Massively parallel sequencing of the polyadenylated transcriptome of C. elegans.

L. W. Hillier, V. Reinke, P. Green, M. Hirst, M. A. Marra, and R. H. Waterston (2009)
Genome Res. 19, 657-666
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Cluster Analysis and Comparison of Various Chloroplast Transcriptomes and Genes in Arabidopsis thaliana.

W. K. Cho, S. Geimer, and J. Meurer (2009)
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RNA interference and retinoblastoma-related genes are required for repression of endogenous siRNA targets in Caenorhabditis elegans.

A. Grishok, S. Hoersch, and P. A. Sharp (2008)
PNAS 105, 20386-20391
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Caenorhabditis elegans: An Emerging Model in Biomedical and Environmental Toxicology.

M. C. K. Leung, P. L. Williams, A. Benedetto, C. Au, K. J. Helmcke, M. Aschner, and J. N. Meyer (2008)
Toxicol. Sci. 106, 5-28
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Characterization of a Novel Caenorhabditis elegans Prolyl 4-Hydroxylase with a Unique Substrate Specificity and Restricted Expression in the Pharynx and Excretory Duct.

K. Keskiaho, L. Kukkola, A. P. Page, A. D. Winter, J. Vuoristo, R. Sormunen, R. Nissi, P. Riihimaa, and J. Myllyharju (2008)
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Patterns of Molecular Evolution in Caenorhabditis Preclude Ancient Origins of Selfing.

A. D. Cutter, J. D. Wasmuth, and N. L. Washington (2008)
Genetics 178, 2093-2104
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Evolutionary dynamics of nematode operons: Easy come, slow go.

W. Qian and J. Zhang (2008)
Genome Res. 18, 412-421
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The Caenorhabditis elegans ekl (Enhancer of ksr-1 Lethality) Genes Include Putative Components of a Germline Small RNA Pathway.

C. E. Rocheleau, K. Cullison, K. Huang, Y. Bernstein, A. C. Spilker, and M. V. Sundaram (2008)
Genetics 178, 1431-1443
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Hypothesis-based RNAi screening identifies neuroprotective genes in a Parkinson's disease model.

S. Hamamichi, R. N. Rivas, A. L. Knight, S. Cao, K. A. Caldwell, and G. A. Caldwell (2008)
PNAS 105, 728-733
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A Genome-wide Survey and Systematic RNAi-based Characterization of Helicase-like Genes in Caenorhabditis elegans.

T. Eki, T. Ishihara, I. Katsura, and F. Hanaoka (2007)
DNA Res
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Automated data integration for developmental biological research.

W. Zhong and P. W. Sternberg (2007)
Development 134, 3227-3238
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Caenorhabditis elegans SDF-9 Enhances Insulin/Insulin-Like Signaling Through Interaction With DAF-2.

V. L. Jensen, P. S. Albert, and D. L. Riddle (2007)
Genetics 177, 661-666
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Differential gene expression of Caenorhabditis elegans grown on unmethylated sterols or 4{alpha}-methylsterols.

M. Merris, T. Wang, P. Soteropoulos, and J. Lenard (2007)
J. Lipid Res. 48, 1159-1166
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Bacterial Postgenomics: the Promise and Peril of Systems Biology{triangledown}.

G. Suen, J. S. Jakobsen, B. S. Goldman, M. Singer, A. G. Garza, and R. D. Welch (2006)
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Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction.

N. J. Szewczyk, I. A. Udranszky, E. Kozak, J. Sunga, S. K. Kim, L. A. Jacobson, and C. A. Conley (2006)
J. Exp. Biol. 209, 4129-4139
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Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression.

T. Lamitina, C. G. Huang, and K. Strange (2006)
PNAS 103, 12173-12178
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Gene expression profiling of adult acute myeloid leukemia identifies novel biologic clusters for risk classification and outcome prediction.

C. S. Wilson, G. S. Davidson, S. B. Martin, E. Andries, J. Potter, R. Harvey, K. Ar, Y. Xu, K. J. Kopecky, D. P. Ankerst, et al. (2006)
Blood 108, 685-696
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Biologic pathways associated with relapse in childhood acute lymphoblastic leukemia: a Children's Oncology Group study.

D. Bhojwani, H. Kang, N. P. Moskowitz, D.-J. Min, H. Lee, J. W. Potter, G. Davidson, C. L. Willman, M. J. Borowitz, I. Belitskaya-Levy, et al. (2006)
Blood 108, 711-717
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Unusual DNA Structures Associated With Germline Genetic Activity in Caenorhabditis elegans.

A. Fire, R. Alcazar, and F. Tan (2006)
Genetics 173, 1259-1273
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Comparing gene expression networks in a multi-dimensional space to extract similarities and differences between organisms.

G. Lelandais, P. Vincens, A. Badel-Chagnon, S. Vialette, C. Jacq, and S. Hazout (2006)
Bioinformatics 22, 1359-1366
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Identification of novel th2-associated genes in T memory responses to allergens..

A. Bosco, K. L. McKenna, C. J. Devitt, M. J. Firth, P. D. Sly, and P. G. Holt (2006)
J. Immunol. 176, 4766-4777
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Chromosomal clustering and GATA transcriptional regulation of intestine-expressed genes in C. elegans.

F. Pauli, Y. Liu, Y. A. Kim, P.-J. Chen, and S. K. Kim (2006)
Development 133, 287-295
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Caenorhabditis elegans reporter fusion genes generated by seamless modification of large genomic DNA clones..

C. T. Dolphin and I. A. Hope (2006)
Nucleic Acids Res. 34, e72
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The Arabidopsis genome: A foundation for plant research.

M. Bevan and S. Walsh (2005)
Genome Res. 15, 1632-1642
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Genomics in C. elegans: So many genes, such a little worm.

L. W. Hillier, A. Coulson, J. I. Murray, Z. Bao, J. E. Sulston, and R. H. Waterston (2005)
Genome Res. 15, 1651-1660
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Distinct Regulatory Elements Mediate Similar Expression Patterns in the Excretory Cell of Caenorhabditis elegans.

Z. Zhao, L. Fang, N. Chen, R. C. Johnsen, L. Stein, and D. L. Baillie (2005)
J. Biol. Chem. 280, 38787-38794
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Brain Microarray: Finding Needles in Molecular Haystacks.

N. M. Lewandowski and S. A. Small (2005)
J. Neurosci. 25, 10341-10346
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De novo discovery of a tissue-specific gene regulatory module in a chordate.

D. S. Johnson, Q. Zhou, K. Yagi, N. Satoh, W. Wong, and A. Sidow (2005)
Genome Res. 15, 1315-1324
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Dragon Plant Biology Explorer. A Text-Mining Tool for Integrating Associations between Genetic and Biochemical Entities with Genome Annotation and Biochemical Terms Lists.

V. B. Bajic, M. Veronika, P. S. Veladandi, A. Meka, M.-W. Heng, K. Rajaraman, H. Pan, and S. Swarup (2005)
Plant Physiology 138, 1914-1925
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A systematic RNAi screen for longevity genes in C. elegans.

B. Hamilton, Y. Dong, M. Shindo, W. Liu, I. Odell, G. Ruvkun, and S. S. Lee (2005)
Genes & Dev. 19, 1544-1555
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Roles of the HIF-1 Hypoxia-inducible Factor during Hypoxia Response in Caenorhabditis elegans.

C. Shen, D. Nettleton, M. Jiang, S. K. Kim, and J. A. Powell-Coffman (2005)
J. Biol. Chem. 280, 20580-20588
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Caenorhabditis elegans Geminin Homologue Participates in Cell Cycle Regulation and Germ Line Development.

K.-i. Yanagi, T. Mizuno, T. Tsuyama, S. Tada, Y. Iida, A. Sugimoto, T. Eki, T. Enomoto, and F. Hanaoka (2005)
J. Biol. Chem. 280, 19689-19694
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A web-based tool for principal component and significance analysis of microarray data.

A. A. Sharov, D. B. Dudekula, and M. S. H. Ko (2005)
Bioinformatics 21, 2548-2549
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The end of "naive reductionism": rise of systems biology or renaissance of physiology?.

K. Strange (2005)
Am J Physiol Cell Physiol 288, C968-C974
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Balancing protein similarity and gene co-expression reveals new links between genetic conservation and developmental diversity in invertebrates.

C. Lefebvre, J.-C. Aude, E. Glemet, and C. Neri (2005)
Bioinformatics 21, 1550-1558
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Identification of a nematode chemosensory gene family.

N. Chen, S. Pai, Z. Zhao, A. Mah, R. Newbury, R. C. Johnsen, Z. Altun, D. G. Moerman, D. L. Baillie, and L. D. Stein (2005)
PNAS 102, 146-151
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WormBase: a comprehensive data resource for Caenorhabditis biology and genomics.

N. Chen, T. W. Harris, I. Antoshechkin, C. Bastiani, T. Bieri, D. Blasiar, K. Bradnam, P. Canaran, J. Chan, C.-K. Chen, et al. (2005)
Nucleic Acids Res. 33, D383-D389
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Combining biological networks to predict genetic interactions.

S. L. Wong, L. V. Zhang, A. H. Y. Tong, Z. Li, D. S. Goldberg, O. D. King, G. Lesage, M. Vidal, B. Andrews, H. Bussey, et al. (2004)
PNAS 101, 15682-15687
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Shared Transcriptional Signature in Caenorhabditis elegans Dauer Larvae and Long-lived daf-2 Mutants Implicates Detoxification System in Longevity Assurance.

J. J. McElwee, E. Schuster, E. Blanc, J. H. Thomas, and D. Gems (2004)
J. Biol. Chem. 279, 44533-44543
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Genetic Models of Mechanotransduction: The Nematode Caenorhabditis elegans.

P. Syntichaki and N. Tavernarakis (2004)
Physiol Rev 84, 1097-1153
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A Gateway-Compatible Yeast One-Hybrid System.

B. Deplancke, D. Dupuy, M. Vidal, and A. J.M. Walhout (2004)
Genome Res. 14, 2093-2101
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WormBase as an Integrated Platform for the C. elegans ORFeome.

N. Chen, D. Lawson, K. Bradnam, T. W. Harris, and L. D. Stein (2004)
Genome Res. 14, 2155-2161
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A First Version of the Caenorhabditis elegans Promoterome.

D. Dupuy, Q.-R. Li, B. Deplancke, M. Boxem, T. Hao, P. Lamesch, R. Sequerra, S. Bosak, L. Doucette-Stamm, I. A. Hope, et al. (2004)
Genome Res. 14, 2169-2175
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Environmentally Induced Foregut Remodeling by PHA-4/FoxA and DAF-12/NHR.

W. Ao, J. Gaudet, W. J. Kent, S. Muttumu, and S. E. Mango (2004)
Science 305, 1743-1746
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Gene co-regulation is highly conserved in the evolution of eukaryotes and prokaryotes.

B. Snel, V. van Noort, and M. A. Huynen (2004)
Nucleic Acids Res. 32, 4725-4731
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Increased measurement accuracy for sequence-verified microarray probes.

B. H. Mecham, D. Z. Wetmore, Z. Szallasi, Y. Sadovsky, I. Kohane, and T. J. Mariani (2004)
Physiol Genomics 18, 308-315
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cis-Regulatory and Protein Evolution in Orthologous and Duplicate Genes.

C. I. Castillo-Davis, D. L. Hartl, and G. Achaz (2004)
Genome Res. 14, 1530-1536
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Dragon TF Association Miner: a system for exploring transcription factor associations through text-mining.

H. Pan, L. Zuo, V. Choudhary, Z. Zhang, S. H. Leow, F. T. Chong, Y. Huang, V. W. S. Ong, B. Mohanty, S. L. Tan, et al. (2004)
Nucleic Acids Res. 32, W230-W234
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Sockeye: A 3D Environment for Comparative Genomics.

S. B. Montgomery, T. Astakhova, M. Bilenky, E. Birney, T. Fu, M. Hassel, C. Melsopp, M. Rak, A. G. Robertson, M. Sleumer, et al. (2004)
Genome Res. 14, 956-962
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Mapping knowledge domains: Characterizing PNAS.

K. W. Boyack (2004)
PNAS 101, 5192-5199
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FRG1P is localised in the nucleolus, Cajal bodies, and speckles.

S van Koningsbruggen, R W Dirks, A M Mommaas, J J Onderwater, G Deidda, G W Padberg, R R Frants, and S M van der Maarel (2004)
J. Med. Genet. 41, e46
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Concerted and Nonconcerted Evolution of the Hsp70 Gene Superfamily in Two Sibling Species of Nematodes.

N. Nikolaidis and M. Nei (2004)
Mol. Biol. Evol. 21, 498-505
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The Caenorhabditis elegans Cathepsin Z-like Cysteine Protease, Ce-CPZ-1, Has a Multifunctional Role during the Worms' Development.

S. Hashmi, J. Zhang, Y. Oksov, and S. Lustigman (2004)
J. Biol. Chem. 279, 6035-6045
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Comparative Genomics of Gene Expression in the Parasitic and Free-Living Nematodes Strongyloides stercoralis and Caenorhabditis elegans.

M. Mitreva, J. P. McCarter, J. Martin, M. Dante, T. Wylie, B. Chiapelli, D. Pape, S. W. Clifton, T. B. Nutman, and R. H. Waterston (2004)
Genome Res. 14, 209-220
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A Map of the Interactome Network of the Metazoan C. elegans.

S. Li, C. M. Armstrong, N. Bertin, H. Ge, S. Milstein, M. Boxem, P.-O. Vidalain, J.-D. J. Han, A. Chesneau, T. Hao, et al. (2004)
Science 303, 540-543
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Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans.

V. Reinke, I. S. Gil, S. Ward, and K. Kazmer (2004)
Development 131, 311-323
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RNAiDB and PhenoBlast: web tools for genome-wide phenotypic mapping projects.

K. C. Gunsalus, W.-C. Yueh, P. MacMenamin, and F. Piano (2004)
Nucleic Acids Res. 32, D406-410
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WormBase: a multi-species resource for nematode biology and genomics.

T. W. Harris, N. Chen, F. Cunningham, M. Tello-Ruiz, I. Antoshechkin, C. Bastiani, T. Bieri, D. Blasiar, K. Bradnam, J. Chan, et al. (2004)
Nucleic Acids Res. 32, D411-417
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High throughput gene expression profiling: a molecular approach to integrative physiology.

M. Liang, A. W. Cowley Jr, and A. S. Greene (2004)
J. Physiol. 554, 22-30
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Genome-Scale Analysis of the Uses of the Escherichia coli Genome: Model-Driven Analysis of Heterogeneous Data Sets.

T. E. Allen, M. J. Herrgard, M. Liu, Y. Qiu, J. D. Glasner, F. R. Blattner, and B. O. Palsson (2003)
J. Bacteriol. 185, 6392-6399
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Quantitative Classification and Natural Clustering of Caenorhabditis elegans Behavioral Phenotypes.

W. Geng, P. Cosman, J.-H. Baek, C. C. Berry, and W. R. Schafer (2003)
Genetics 165, 1117-1126
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A Gene-Coexpression Network for Global Discovery of Conserved Genetic Modules.

J. M. Stuart, E. Segal, D. Koller, and S. K. Kim (2003)
Science 302, 249-255
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Experimental Determination and System Level Analysis of Essential Genes in Escherichia coli MG1655.

S. Y. Gerdes, M. D. Scholle, J. W. Campbell, G. Balazsi, E. Ravasz, M. D. Daugherty, A. L. Somera, N. C. Kyrpides, I. Anderson, M. S. Gelfand, et al. (2003)
J. Bacteriol. 185, 5673-5684
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The Evolutionary Duplication and Probable Demise of an Endodermal GATA Factor in Caenorhabditis elegans.

T. Fukushige, B. Goszczynski, H. Tian, and J. D. McGhee (2003)
Genetics 165, 575-588
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Asymmetric Sequence Divergence of Duplicate Genes.

G. C. Conant and A. Wagner (2003)
Genome Res. 13, 2052-2058
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A Gene Recommender Algorithm to Identify Coexpressed Genes in C. elegans.

A. B. Owen, J. Stuart, K. Mach, A. M. Villeneuve, and S. Kim (2003)
Genome Res. 13, 1828-1837
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Subsystem Identification Through Dimensionality Reduction of Large-Scale Gene Expression Data.

P. M. Kim and B. Tidor (2003)
Genome Res. 13, 1706-1718
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TagA, a putative serine protease/ABC transporter of Dictyostelium that is required for cell fate determination at the onset of development.

J. R. Good, M. Cabral, S. Sharma, J. Yang, N. Van Driessche, C. A. Shaw, G. Shaulsky, and A. Kuspa (2003)
Development 130, 2953-2965
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Direct and Indirect Transcriptional Targets of DAF-16.

P. L. Larsen (2003)
Sci. Aging Knowl. Environ. 2003, pe9-9
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Global analysis of dauer gene expression in Caenorhabditis elegans.

J. Wang and S. K. Kim (2003)
Development 130, 1621-1634
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DNA microarrays and development.

L. Smith and A. Greenfield (2003)
Hum. Mol. Genet. 12, R1-8
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From Genes to Integrative Physiology: Ion Channel and Transporter Biology in Caenorhabditis elegans.

K. Strange (2003)
Physiol Rev 83, 377-415
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A Potassium Channel-MiRP Complex Controls Neurosensory Function in Caenorhabditis elegans.

L. Bianchi, S.-M. Kwok, M. Driscoll, and F. Sesti (2003)
J. Biol. Chem. 278, 12415-12424
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Coexpression of Neighboring Genes in Caenorhabditis Elegans Is Mostly Due to Operons and Duplicate Genes.

M. J. Lercher, T. Blumenthal, and L. D. Hurst (2003)
Genome Res. 13, 238-243
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WormBase: a cross-species database for comparative genomics.

T. W. Harris, R. Lee, E. Schwarz, K. Bradnam, D. Lawson, W. Chen, D. Blasier, E. Kenny, F. Cunningham, R. Kishore, et al. (2003)
Nucleic Acids Res. 31, 133-137
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Statistical Approach to DNA Chip Analysis.

N.M. Svrakic, O. Nesic, M.R.K. Dasu, D. Herndon, and J.R. Perez-Polo (2003)
Recent Prog. Horm. Res. 58, 75-93
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