Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana

BackgroundGenome analyses have revealed that gene duplication in plants is rampant. Furthermore, many of the duplicated genes seem to have been created through ancient genome-wide duplication events. Recently, we have shown that gene loss is strikingly different for large- and small-scale duplication events and highly biased towards the functional class to which a gene belongs. Here, we study the expression divergence of genes that were created during large- and small-scale gene duplication events by means of microarray data and investigate both the influence of the origin (mode of duplication) and the function of the duplicated genes on expression divergence.ResultsDuplicates that have been created by large-scale duplication events and that can still be found in duplicated segments have expression patterns that are more correlated than those that were created by small-scale duplications or those that no longer lie in duplicated segments. Moreover, the former tend to have highly redundant or overlapping expression patterns and are mostly expressed in the same tissues, while the latter show asymmetric divergence. In addition, a strong bias in divergence of gene expression was observed towards gene function and the biological process genes are involved in.ConclusionBy using microarray expression data for Arabidopsis thaliana, we show that the mode of duplication, the function of the genes involved, and the time since duplication play important roles in the divergence of gene expression and, therefore, in the functional divergence of genes after duplication.

[1]  E. J. Williams,et al.  Coexpression of neighboring genes in the genome of Arabidopsis thaliana. , 2004, Genome research.

[2]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[3]  Guillaume Blanc,et al.  Widespread Paleopolyploidy in Model Plant Species Inferred from Age Distributions of Duplicate Genes , 2004, The Plant Cell Online.

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

[5]  T. Speed,et al.  Summaries of Affymetrix GeneChip probe level data. , 2003, Nucleic acids research.

[6]  K. Hokamp,et al.  A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. , 2003, Genome research.

[7]  D. Nicolae,et al.  Rapid divergence in expression between duplicate genes inferred from microarray data. , 2002, Trends in genetics : TIG.

[8]  X. Gu Evolution of duplicate genes versus genetic robustness against null mutations. , 2003, Trends in genetics : TIG.

[9]  V. Corces,et al.  Chromatin insulators and boundaries: effects on transcription and nuclear organization. , 2001, Annual review of genetics.

[10]  Jeroen Raes,et al.  Duplication and divergence: the evolution of new genes and old ideas. , 2004, Annual review of genetics.

[11]  Cathal Seoighe,et al.  Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. , 2004, Trends in genetics : TIG.

[12]  J. Raes,et al.  Modeling gene and genome duplications in eukaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Wendel,et al.  Novel patterns of gene expression in polyploid plants. , 2005, Trends in genetics : TIG.

[14]  D. Sankoff,et al.  Comparable rates of gene loss and functional divergence after genome duplications early in vertebrate evolution. , 1997, Genetics.

[15]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[16]  Andreas Wagner,et al.  Asymmetric functional divergence of duplicate genes in yeast. , 2002, Molecular biology and evolution.

[17]  V. Laudet,et al.  Evolutionary rates of duplicate genes in fish and mammals. , 2001, Molecular biology and evolution.

[18]  Klaas Vandepoele,et al.  The hidden duplication past of Arabidopsis thaliana , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  K. H. Wolfe Yesterday's polyploids and the mystery of diploidization , 2001, Nature Reviews Genetics.

[20]  Jan-Peter Nap,et al.  Local Coexpression Domains of Two to Four Genes in the Genome of Arabidopsis1[w] , 2005, Plant Physiology.

[21]  A. Meyer,et al.  The Ghost of Selection Past: Rates of Evolution and Functional Divergence of Anciently Duplicated Genes , 2001, Journal of Molecular Evolution.

[22]  Jonathan F Wendel,et al.  Polyploidy and Genome Evolution in Plants This Review Comes from a Themed Issue on Genome Studies and Molecular Genetics Edited , 2022 .

[23]  D. G. Brown,et al.  The origins of genomic duplications in Arabidopsis. , 2000, Science.

[24]  Yasuko Takahashi,et al.  Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events , 2022 .

[25]  Terence P. Speed,et al.  A comparison of normalization methods for high density oligonucleotide array data based on variance and bias , 2003, Bioinform..

[26]  Jonathan F. Wendel,et al.  Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Raes,et al.  Gene duplication, the evolution of novel gene functions, and detecting functional divergence of duplicates in silico. , 2003, Applied bioinformatics.

[28]  A. Fisher,et al.  Expression of alpha- and beta-globin genes occurs within different nuclear domains in haemopoietic cells. , 2001, Nature cell biology.

[29]  A. Riggs,et al.  Epigenetic Changes and Repositioning Determine the Evolutionary Fate of Duplicated Genes , 2005, Biochemistry (Moscow).

[30]  Nick James,et al.  NASCArrays: a repository for microarray data generated by NASC's transcriptomics service , 2004, Nucleic Acids Res..

[31]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[32]  A. Force,et al.  The probability of duplicate gene preservation by subfunctionalization. , 2000, Genetics.

[33]  Wei-Min Liu,et al.  Analysis of high density expression microarrays with signed-rank call algorithms , 2002, Bioinform..

[34]  J. Wendel,et al.  Duplicated genes evolve independently after polyploid formation in cotton. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[35]  S. Gasser,et al.  Nuclear compartments and gene regulation. , 1999, Current opinion in genetics & development.

[36]  Z. Gu,et al.  Evolutionary analyses of the human genome , 2001, Nature.

[37]  J. Haldane,et al.  The Part Played by Recurrent Mutation in Evolution , 1933, The American Naturalist.

[38]  Yves Van de Peer,et al.  Computational approaches to unveiling ancient genome duplications , 2004, Nature Reviews Genetics.

[39]  Austin L. Hughes,et al.  Adaptive Evolution of Genes and Genomes , 2000 .

[40]  A. Stoltzfus On the Possibility of Constructive Neutral Evolution , 1999, Journal of Molecular Evolution.

[41]  Guillaume Blanc,et al.  Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution , 2004, The Plant Cell Online.

[42]  S. Otto,et al.  Polyploid incidence and evolution. , 2000, Annual review of genetics.

[43]  A. Hughes,et al.  Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. , 1993, Molecular biology and evolution.

[44]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[45]  Benjamin M. Bolstad,et al.  affy - analysis of Affymetrix GeneChip data at the probe level , 2004, Bioinform..

[46]  Jean YH Yang,et al.  Bioconductor: open software development for computational biology and bioinformatics , 2004, Genome Biology.

[47]  O. Witte,et al.  Stomatal Size in Fossil Plants : Evidence for Polyploidy in Majority of Angiosperms , 2022 .

[48]  V. de Lorenzo,et al.  Clues and consequences of DNA bending in transcription. , 1997, Annual review of microbiology.

[49]  R. Gregory The evolution of the genome , 2005 .

[50]  J. Raes,et al.  Small-scale gene duplications , 2005 .

[51]  M. Lynch,et al.  The altered evolutionary trajectories of gene duplicates. , 2004, Trends in genetics : TIG.

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

[53]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[54]  Wen-Hsiung Li,et al.  Divergence in the spatial pattern of gene expression between human duplicate genes. , 2003, Genome research.

[55]  E. Koonin,et al.  Selection in the evolution of gene duplications , 2002, Genome Biology.

[56]  Jim Leebens-Mack,et al.  Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. , 2006, Molecular biology and evolution.

[57]  M. Wand Local Regression and Likelihood , 2001 .

[58]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[59]  Jonathan F. Wendel,et al.  Genome evolution in polyploids , 2004, Plant Molecular Biology.

[60]  Georg Haberer,et al.  Transcriptional Similarities, Dissimilarities, and Conservation of cis-Elements in Duplicated Genes of Arabidopsis1[w] , 2004, Plant Physiology.