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      The hidden duplication past of the plant pathogen Phytophthora and its consequences for infection

      research-article
      1 , 2 , 1 , 2 ,
      BMC Genomics
      BioMed Central

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          Abstract

          Background

          Oomycetes of the genus Phytophthora are pathogens that infect a wide range of plant species. For dicot hosts such as tomato, potato and soybean, Phytophthora is even the most important pathogen. Previous analyses of Phytophthora genomes uncovered many genes, large gene families and large genome sizes that can partially be explained by significant repeat expansion patterns.

          Results

          Analysis of the complete genomes of three different Phytophthora species, using a newly developed approach, unveiled a large number of small duplicated blocks, mainly consisting of two or three consecutive genes. Further analysis of these duplicated genes and comparison with the known gene and genome duplication history of ten other eukaryotes including parasites, algae, plants, fungi, vertebrates and invertebrates, suggests that the ancestor of P. infestans, P. sojae and P. ramorum most likely underwent a whole genome duplication (WGD). Genes that have survived in duplicate are mainly genes that are known to be preferentially retained following WGDs, but also genes important for pathogenicity and infection of the different hosts seem to have been retained in excess. As a result, the WGD might have contributed to the evolutionary and pathogenic success of Phytophthora.

          Conclusions

          The fact that we find many small blocks of duplicated genes indicates that the genomes of Phytophthora species have been heavily rearranged following the WGD. Most likely, the high repeat content in these genomes have played an important role in this rearrangement process. As a consequence, the paucity of retained larger duplicated blocks has greatly complicated previous attempts to detect remnants of a large-scale duplication event in Phytophthora. However, as we show here, our newly developed strategy to identify very small duplicated blocks might be a useful approach to uncover ancient polyploidy events, in particular for heavily rearranged genomes.

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          Most cited references53

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          A codon-based model of nucleotide substitution for protein-coding DNA sequences.

          (1994)
          A codon-based model for the evolution of protein-coding DNA sequences is presented for use in phylogenetic estimation. A Markov process is used to describe substitutions between codons. Transition/transversion rate bias and codon usage bias are allowed in the model, and selective restraints at the protein level are accommodated using physicochemical distances between the amino acids coded for by the codons. Analyses of two data sets suggest that the new codon-based model can provide a better fit to data than can nucleotide-based models and can produce more reliable estimates of certain biologically important measures such as the transition/transversion rate ratio and the synonymous/nonsynonymous substitution rate ratio.
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            • Article: not found

            Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition.

            Each mode of gene duplication (tandem, tetraploid, segmental, transpositional) retains genes in a biased manner. A reciprocal relationship exists between plant genes retained postpaleotetraploidy versus genes retained after an ancient tandem duplication. Among the models (C, neofunctionalization, balanced gene drive) and ideas that might explain this relationship, only balanced gene drive predicts reciprocity. The gene balance hypothesis explains that more "connected" genes--by protein-protein interactions in a heteromer, for example--are less likely to be retained as a tandem or transposed duplicate and are more likely to be retained postpaleotetraploidy; otherwise, selectively negative dosage effects are created. Biased duplicate retention is an instant and neutral by-product, a spandrel, of purifying selection. Balanced gene drive expanded plant gene families, including those encoding proteasomal proteins, protein kinases, motors, and transcription factors, with each paleotetraploidy, which could explain trends involving complexity. Balanced gene drive is a saltation mechanism in the mutationist tradition.
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              Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution.

              To study the evolutionary effects of polyploidy on plant gene functions, we analyzed functional genomics data for a large number of duplicated gene pairs formed by ancient polyploidy events in Arabidopsis thaliana. Genes retained in duplicate are not distributed evenly among Gene Ontology or Munich Information Center for Protein Sequences functional categories, which indicates a nonrandom process of gene loss. Genes involved in signal transduction and transcription have been preferentially retained, and those involved in DNA repair have been preferentially lost. Although the two members of each gene pair must originally have had identical transcription profiles, less than half of the pairs formed by the most recent polyploidy event still retain significantly correlated profiles. We identified several cases where groups of duplicated gene pairs have diverged in concert, forming two parallel networks, each containing one member of each gene pair. In these cases, the expression of each gene is strongly correlated with the other nonhomologous genes in its network but poorly correlated with its paralog in the other network. We also find that the rate of protein sequence evolution has been significantly asymmetric in >20% of duplicate pairs. Together, these results suggest that functional diversification of the surviving duplicated genes is a major feature of the long-term evolution of polyploids.

                Author and article information

                Journal
                BMC Genomics
                BMC Genomics
                BioMed Central
                1471-2164
                2010
                3 June 2010
                : 11
                : 353
                Affiliations
                [1 ]Department of Plant Systems Biology, VIB, Technologiepark 927, B-9052 Ghent, Belgium
                [2 ]Bioinformatics and Evolutionary Genomics, Department of Molecular Genetics, Technologiepark 927, Ghent University, B-9052 Ghent, Belgium
                Article
                1471-2164-11-353
                10.1186/1471-2164-11-353
                2996974
                20525264
                cd0ae71b-fa36-4e2d-ae25-f71ce0ae59ed
                Copyright ©2010 Martens and Van de Peer; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 4 February 2010
                : 3 June 2010
                Categories
                Research Article

                Genetics
                Genetics

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