Gene expression in a paleopolyploid: a transcriptome resource for the ciliate Paramecium tetraurelia

Abstract

Background: The genome of Paramecium tetraurelia, a unicellular model that belongs to the ciliate phylum, has been shaped by at least 3 successive whole genome duplications (WGD). These dramatic events, which have also been documented in plants, animals and fungi, are resolved over evolutionary time by the loss of one duplicate for the majority of genes. Thanks to a low rate of large scale genome rearrangement in Paramecium, an unprecedented large number of gene duplicates of different ages have been identified, making this organism an outstanding model to investigate the evolutionary consequences of polyploidization. The most recent WGD, with 51% of pre-duplication genes still in 2 copies, provides a snapshot of a phase of rapid gene loss that is not accessible in more ancient polyploids such as yeast.

Results: We designed a custom oligonucleotide microarray platform for P. tetraurelia genome-wide expression profiling and used the platform to measure gene expression during 1) the sexual cycle of autogamy, 2) growth of new cilia in response to deciliation and 3) biogenesis of secretory granules after massive exocytosis. Genes that are differentially expressed during these time course experiments have expression patterns consistent with a very low rate of subfunctionalization (partition of ancestral functions between duplicated genes) in particular since the most recent polyploidization event.

Conclusions: A public transcriptome resource is now available for Paramecium tetraurelia. The resource has been integrated into the ParameciumDB model organism database, providing searchable access to the data. The microarray platform, freely available through NimbleGen Systems, provides a robust, cost-effective approach for genome-wide expression profiling in P. tetraurelia. The expression data support previous studies showing that at short evolutionary times after a whole genome duplication, gene dosage balance constraints and not functional change are the major determinants of gene retention.

Figure 1

Hierarchical clusterization of genes differentially expressed during autogamy. The 2467 genes most differentially expressed during autogamy (treat model fold-change of 2, FDR < 0.05) were hierarchically clustered as described in Methods. The heatmap displays the samples as columns and the genes as rows. The color code goes from dark blue for the lowest expression to dark red for the highest expression. The clusterization of the samples corresponds to the classification based on nuclear morphology, although the DEV2 and DEV3 samples are not resolved. The 6 clusters of co-expressed genes were obtained by cutting the gene dendrogram on the left of the heatmap as indicated. On the right hand side, the average expression profile and standard deviation for each cluster are drawn as they appear in ParameciumDB [65].

Figure 2

Genes differentially expressed in more than one experiment. The Venn diagrams show the overlap between differentially expressed genes identified by each of the 3 experiments. For the autogamy experiment, the set of 2467 most differentially expressed genes was used. A) All differentially expressed genes B) Up-regulated genes.