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Outline. Arabidopsis gene expression (MPSS) Two evolutionary issues in the evolution of expression profiles: Physical clustering of co-expressed genes Divergence of duplicated genes. Physical clustering of co-expression. Caenorhabditis elegans Roy et al., (2002) Nature 418, 975

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  1. Outline • Arabidopsis gene expression (MPSS) • Two evolutionary issues in the evolution of expression profiles: • Physical clustering of co-expressed genes • Divergence of duplicated genes

  2. Physical clustering of co-expression Caenorhabditis elegans Roy et al., (2002) Nature 418, 975 Lercher et al (2003) Genome Research 13, 238 Drosophila melanogaster Boutanaev et al (2002) Nature 420, 666 Spellman and Rubin (2002) J Biology 1, 5 Homo sapiens Caron et al (2001) Science 291, 1289 Lercher et al (2002) Nature Genetics 31, 180 Saccharomyces cerevisiae Cohen et al (2000) Nature Genetics 26, 183 Hurst et al (2002) Trends in Genetics 18, 604 Mannila et al (2002) Bioinformatics 18, 482 ‘ • What are the proximate explanations? • shared cis-regulatory elements • chromatin packaging, etc. • What are the ultimate explanations? • Adaptive: greater transcriptional efficiency/accuracy? • Maladaptive: mutational rain chipping away at insulators and other mechanisms that over-ride regional controllers of gene expression?

  3. library 2 library 1 library 3 Measuring expression distance

  4. Clustering of tissue-specific expression Chromosome 1 Flower (red)Silique (violet)Leaf (green)Root (blue)Callus (white)

  5. Statistical tests of coexpression clustering • Measured median pairwise expression distance (MPED) in non-overlapping windows of 20 genes • Summed unique class 1 and 2 signatures for each gene • Only one gene within each tandemly arrayed family was counted • Out of 100 shuffles of gene order • Zero shuffles had as many windows with small MPED (less than 1.5) as the unshuffled data • Zero shuffles had as large a variance in MPED among windows as the unshuffled data

  6. Coexpression in Arabidopsis

  7. Coexpression in Arabidopsis

  8. Coexpression in Arabidopsis

  9. Selection and recombination • In regions of low recombination • deleterious mutations can hitch-hike to high frequency along with favorable ones • favorable mutations are kept at low frequency by linkage to deleterious ones • Therefore, the effectiveness of natural selection is causally related to recombination rate • Are clusters more concentrated in regions of • high recombination (i.e. are they adaptive) • low (i.e. are they maladaptive)?

  10. Measuring recombination rate Chromosome 1

  11. Co-expression is greater in low recombination regions

  12. Co-expression clusters • MPSS data provides evidence for clusters of co-expression among non-related genes in Arabidopsis • Co-expression is greater in regions of low recombination • Thus, co-expression clusters may be maladapative, at least on average

  13. Outline • Arabidopsis gene expression (MPSS) • Two evolutionary issues in the evolution of expression profiles: • Physical clustering of co-expressed genes • Divergence of duplicated genes

  14. Divergence of duplicated genes Expression distance Age of duplication

  15. Duplicated genes in Arabidopsis

  16. Modes of gene duplication • Tandem (unequal crossing-over) • Dispersed (transposition) • Segmental (polyploidy)

  17. Divergence of duplicated genes • All gene families of size 2 in Arabidopsis were classified as ‘dispersed’, ‘segmental’ or ‘tandem’ • Expression distance was calculated for each • The number of silent (i.e. synonymous) substitutions per site was calculated for each (as a proxy for age since duplication)

  18. Divergence and mode of duplication

  19. Divergence of duplicated genes • Almost all expression divergence occurs during (or immediately following) duplication • Initial expression divergence is more extreme for tandem than dispersed duplicates • Tandem and dispersed duplicates with the most divergent expression profiles are quickly lost • Segmental duplicates plateau at a lower level of expression divergence than dispersed duplicates • The average divergence in relative expression level in each tissue is about 8-fold.

  20. Lessons learned • Clusters of co-expression in Arabidopsis may be largely the result of a rain of weakly deleterious mutations that homogenize the expression profiles of neighboring genes • Divergence in expression profile between duplicated genes is dependent on the nature of the mutation that gave rise to the duplication

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