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Natural history and evolutionary principles of gene duplication in fungi

Abstract

Gene duplication and loss is a powerful source of functional innovation. However, the general principles that govern this process are still largely unknown. With the growing number of sequenced genomes, it is now possible to examine these events in a comprehensive and unbiased manner. Here, we develop a procedure that resolves the evolutionary history of all genes in a large group of species. We apply our procedure to seventeen fungal genomes to create a genome-wide catalogue of gene trees that determine precise orthology and paralogy relations across these species. We show that gene duplication and loss is highly constrained by the functional properties and interacting partners of genes. In particular, stress-related genes exhibit many duplications and losses, whereas growth-related genes show selection against such changes. Whole-genome duplication circumvents this constraint and relaxes the dichotomy, resulting in an expanded functional scope of gene duplication. By characterizing the functional fate of duplicate genes we show that duplicated genes rarely diverge with respect to biochemical function, but typically diverge with respect to regulatory control. Surprisingly, paralogous modules of genes rarely arise, even after whole-genome duplication. Rather, gene duplication may drive the modularization of functional networks through specialization, thereby disentangling cellular systems.

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Figure 1: The SYNERGY algorithm.
Figure 2: A gene ancestry catalogue for Ascomycota fungi.
Figure 3: A functional dichotomy of uniform, persistent and volatile orthogroups.
Figure 4: Evolutionary profiles correspond to the hierarchical modular organization of the yeast transcriptional system.
Figure 5: Functional conservation and innovation of paralogues in classes and networks.

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Acknowledgements

A.R. was supported by a Career Award at the Scientific Interface from the Burroughs Wellcome Fund and by NIGMS. N.F. was supported by the Israel Science Foundation. We thank E. S. Lander for discussions and D. Peer, A. Tanay and O. Rando for their comments on previous drafts of this manuscript. We are also grateful to the members of the FAS Center and the Broad Institute for their scientific and technical support, especially A. Daneau, M. Ethier and B. Mantenuto.

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Correspondence to Aviv Regev.

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Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-12 and Legends and Supplementary Notes 1-5. The notes contain: quality of genomic data sources; summary of bootstrap method; accuracy measures as compared to curated resources and simulated data; summary of selected essential S. cerevisiae genes not present in all species; and discussion of coherence in gene duplication and loss (PDF 2716 kb)

Supplementary Table 1

This file contains Supplementary Table 1 which summarizes the significant enrichments of all orthogroup classes tested (different categories are on separate tabs). (XLS 764 kb)

Supplementary Table 2

This file contains Supplementary Table 2 which includes a list of each S. cerevisiae gene’s transcription module membership. (XLS 6152 kb)

Supplementary Table 3

This file contains Supplementary Table 3 which summarizes the enrichments of all gene classes tested for the transcription modules (different categories are on separate tabs). (XLS 112 kb)

Supplementary Table 4

This file contains Supplementary Table 4 which lists the extended copy number variation profile coherences in each orthogroup class tested (different categories are on separate tabs). (XLS 766 kb)

Supplementary Table 5

This file contains Supplementary Table 5 which summarizes the gene class migrations and protein interaction network statistics for each pair of paralogous S. cerevisiae genes. (XLS 148 kb)

Supplementary Table 6

This file contains Supplementary Table 6 which lists the GEO accession numbers and references for the gene expression assays included in all our analyses. (PDF 30 kb)

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Wapinski, I., Pfeffer, A., Friedman, N. et al. Natural history and evolutionary principles of gene duplication in fungi. Nature 449, 54–61 (2007). https://doi.org/10.1038/nature06107

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