Microarray challenges in ecology.

Microarrays are used to measure simultaneously the amount of mRNAs transcribed from many genes. They were originally designed for gene expression profiling in relatively simple biological systems, such as cell lines and model systems under constant laboratory conditions. This poses a challenge to ecologists who increasingly want to use microarrays to unravel the genetic mechanisms underlying complex interactions among organisms and between organisms and their environment. Here, we discuss typical experimental and statistical problems that arise when analyzing genome-wide expression profiles in an ecological context. We show that experimental design and environmental confounders greatly influence the identification of candidate genes in ecological microarray studies, and that following several simple recommendations could facilitate the analysis of microarray data in ecological settings.

[1]  Scott A. Rifkin,et al.  Evolution of gene expression in the Drosophila melanogaster subgroup , 2003, Nature Genetics.

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

[3]  L. Kruglyak,et al.  Genetics of global gene expression , 2006, Nature Reviews Genetics.

[4]  Martin Hrabé de Angelis,et al.  Assessment of a systematic expression profiling approach in ENU-induced mouse mutant lines , 2004, Mammalian Genome.

[5]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[6]  G. Barker,et al.  Development of anonymous cDNA microarrays to study changes to the Senecio floral transcriptome during hybrid speciation , 2005, Molecular ecology.

[7]  J. Borevitz,et al.  The next generation of microarray research: applications in evolutionary and ecological genomics , 2008, Heredity.

[8]  G. Robinson,et al.  Gene Expression Profiles in the Brain Predict Behavior in Individual Honey Bees , 2003, Science.

[9]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[10]  Ulrich Schurr,et al.  Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth , 2006, Planta.

[11]  Z. Bochdanovits,et al.  Antagonistic pleiotropy for life–history traits at the gene expression level , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  I. Baldwin,et al.  Solanum nigrum: A model ecological expression system and its tools , 2004, Molecular ecology.

[13]  V. Walbot,et al.  Gene Expression Profiling in Response to Ultraviolet Radiation in Maize Genotypes with Varying Flavonoid Content1[w] , 2003, Plant Physiology.

[14]  I. Baldwin,et al.  Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. , 2004, The Plant journal : for cell and molecular biology.

[15]  Z. Bochdanovits,et al.  Covariation of larval gene expression and adult body size in natural populations of Drosophila melanogaster. , 2003, Molecular biology and evolution.

[16]  D. Nott,et al.  Genetic dissection of gene regulation in multiple mouse tissues , 2006, Mammalian Genome.

[17]  T. Markow,et al.  Gene expression patterns accompanying a dietary shift in Drosophila melanogaster , 2005, Molecular ecology.

[18]  D. Allison,et al.  Microarray data analysis: from disarray to consolidation and consensus , 2006, Nature Reviews Genetics.

[19]  Zhanjiang Liu,et al.  Differential gene expression in the brain of channel catfish (Ictalurus punctatus) in response to cold acclimation , 2002, Molecular Genetics and Genomics.

[20]  Rainer Breitling,et al.  Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments , 2004, FEBS letters.

[21]  Jingyuan Fu,et al.  Mapping Determinants of Gene Expression Plasticity by Genetical Genomics in C. elegans , 2006, PLoS genetics.

[22]  I. Baldwin,et al.  Molecular Interactions between the Specialist HerbivoreManduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata: V. Microarray Analysis and Further Characterization of Large-Scale Changes in Herbivore-Induced mRNAs1 , 2003, Plant Physiology.

[23]  A. Le Quéré,et al.  Divergence in gene expression related to variation in host specificity of an ectomycorrhizal fungus , 2004, Molecular ecology.

[24]  Gene E Robinson,et al.  Pheromone-mediated gene expression in the honey bee brain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. Shields,et al.  MIAME, we have a problem. , 2006, Trends in genetics : TIG.

[26]  G. Churchill,et al.  Variation in gene expression within and among natural populations , 2002, Nature Genetics.

[27]  Gary M Hellmann,et al.  Confirming microarray data—is it really necessary? , 2003, Genomics.

[28]  G. Churchill,et al.  Statistical design and the analysis of gene expression microarray data. , 2001, Genetical research.

[29]  I. Baldwin,et al.  Molecular Interactions between the Specialist Herbivore Manduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. VII. Changes in the Plant's Proteome1[W] , 2006, Plant Physiology.

[30]  N. Smirnoff,et al.  Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation , 2006, Molecular ecology.

[31]  Dan Nettleton,et al.  Genetic Regulation of Gene Expression During Shoot Development in Arabidopsis , 2006, Genetics.

[32]  Andrew Whitehead,et al.  Variation within and among species in gene expression: raw material for evolution , 2006, Molecular ecology.

[33]  M. Lynch,et al.  The Origins of Genome Complexity , 2003, Science.

[34]  A. Whitehead,et al.  Variation in tissue-specific gene expression among natural populations , 2005, Genome Biology.

[35]  C. A. Machado,et al.  Uncovering evolutionary patterns of gene expression using microarrays. , 2006, Trends in ecology & evolution.

[36]  Linda Partridge,et al.  Genome-wide gene expression in response to parasitoid attack in Drosophila , 2005, Genome Biology.

[37]  A. Whitehead,et al.  Neutral and adaptive variation in gene expression. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  B. Barrell,et al.  Life with 6000 Genes , 1996, Science.

[39]  I. Baldwin,et al.  Generalist and specialist lepidopteran larvae elicit different transcriptional responses in Nicotiana attenuata, which correlate with larval FAC profiles , 2004 .

[40]  Andreas Wagner,et al.  Energy constraints on the evolution of gene expression. , 2005, Molecular biology and evolution.

[41]  Scott A. Rifkin,et al.  Natural selection on gene expression. , 2006, Trends in genetics : TIG.

[42]  I. Baldwin,et al.  Individual variability in herbivore‐specific elicitors from the plant's perspective , 2004, Molecular ecology.

[43]  Rainer Breitling,et al.  Vector analysis as a fast and easy method to compare gene expression responses between different experimental backgrounds , 2005, BMC Bioinformatics.

[44]  Hans A. Kestler,et al.  Generalized Venn diagrams: a new method of visualizing complex genetic set relations , 2005, Bioinform..

[45]  Royston Goodacre,et al.  Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics , 2005, The Plant Cell Online.

[46]  D. Hartl,et al.  Population genetic variation in genome-wide gene expression. , 2003, Molecular biology and evolution.

[47]  P. Brown,et al.  Exploring the metabolic and genetic control of gene expression on a genomic scale. , 1997, Science.

[48]  B. Letcher,et al.  Interaction of rearing environment and reproductive tactic on gene expression profiles in Atlantic salmon. , 2005, The Journal of heredity.

[49]  Juan P. Steibel,et al.  Reassessing Design and Analysis of two-Colour Microarray Experiments Using Mixed Effects Models , 2005, Comparative and functional genomics.

[50]  S. Edwards,et al.  A cDNA macroarray approach to parasite‐induced gene expression changes in a songbird host: genetic response of house finches to experimental infection by Mycoplasma gallisepticum , 2005, Molecular ecology.

[51]  J. Warner,et al.  The economics of ribosome biosynthesis in yeast. , 1999, Trends in biochemical sciences.

[52]  P. Nilsson,et al.  The genetics and genomics of the drought response in Populus. , 2006, The Plant journal : for cell and molecular biology.

[53]  Matthew W. Hahn,et al.  The evolution of transcriptional regulation in eukaryotes. , 2003, Molecular biology and evolution.

[54]  Dan Nettleton,et al.  A Discussion of Statistical Methods for Design and Analysis of Microarray Experiments for Plant Scientists , 2006, The Plant Cell Online.

[55]  Terence P. Speed,et al.  Expression profiling in primates reveals a rapid evolution of human transcription factors , 2006, Nature.

[56]  Yudong D. He,et al.  Functional Discovery via a Compendium of Expression Profiles , 2000, Cell.

[57]  T. Juenger,et al.  Natural genetic variation in whole‐genome expression in Arabidopsis thaliana: the impact of physiological QTL introgression , 2006, Molecular ecology.

[58]  M. Blázquez,et al.  Flower development pathways. , 2000, Journal of cell science.

[59]  S. Somerville,et al.  Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[60]  J. Nap,et al.  Genetical genomics : the added value from segregation , 2001 .

[61]  M. Marra,et al.  Genomics of hybrid poplar (Populus trichocarpa× deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full‐length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect‐induced defences in poplar , 2006, Molecular ecology.

[62]  L. Rieseberg,et al.  Microarray analysis reveals differential gene expression in hybrid sunflower species , 2006, Molecular ecology.

[63]  Andrew I Su,et al.  Uncovering regulatory pathways that affect hematopoietic stem cell function using 'genetical genomics' , 2005, Nature Genetics.

[64]  G. Somero,et al.  Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus , 2004, Journal of Experimental Biology.

[65]  K. Chong,et al.  Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. , 2006, The Plant journal : for cell and molecular biology.

[66]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[67]  P. Duchesne,et al.  Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes , 2006, Molecular ecology.

[68]  D. Crawford,et al.  Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus , 2005, Nature Genetics.

[69]  D. Botstein,et al.  Systematic changes in gene expression patterns following adaptive evolution in yeast. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Robert W. Williams,et al.  Complex trait analysis of gene expression uncovers polygenic and pleiotropic networks that modulate nervous system function , 2005, Nature Genetics.

[71]  M. Goodisman,et al.  BREEDING SYSTEM, COLONY STRUCTURE, AND GENETIC DIFFERENTIATION IN THE CAMPONOTUS FESTINATUS SPECIES COMPLEX OF CARPENTER ANTS , 2005, Evolution; international journal of organic evolution.

[72]  Rainer Breitling,et al.  Biological microarray interpretation: the rules of engagement. , 2006, Biochimica et biophysica acta.

[73]  A. Le Quéré,et al.  Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays , 2005, Molecular ecology.

[74]  J. Malone,et al.  Sex-Biased Gene Expression in a ZW Sex Determination System , 2006, Journal of Molecular Evolution.

[75]  I. Baldwin,et al.  Molecular Interactions between the Specialist HerbivoreManduca sexta (Lepidoptera, Sphingidae) and Its Natural Host Nicotiana attenuata. VI. Microarray Analysis Reveals That Most Herbivore-Specific Transcriptional Changes Are Mediated by Fatty Acid-Amino Acid Conjugates1,212 , 2003, Plant Physiology.