Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants

Abstract

The importance of gene gain through duplication has long been appreciated. In contrast, the importance of gene loss has only recently attracted attention. Indeed, studies in organisms ranging from plants to worms and humans suggest that duplication of some genes might be better tolerated than that of others. Here we have undertaken a large-scale study to investigate the existence of duplication-resistant genes in the sequenced genomes of 20 flowering plants. We demonstrate that there is a large set of genes that is convergently restored to single-copy status following multiple genome-wide and smaller scale duplication events. We rule out the possibility that such a pattern could be explained by random gene loss only and therefore propose that there is selection pressure to preserve such genes as singletons. This is further substantiated by the observation that angiosperm single-copy genes do not comprise a random fraction of the genome, but instead are often involved in essential housekeeping functions that are highly conserved across all eukaryotes. Furthermore, single-copy genes are generally expressed more highly and in more tissues than non-single-copy genes, and they exhibit higher sequence conservation. Finally, we propose different hypotheses to explain their resistance against duplication

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

“…Species with or without WGD that branch within the same group, such as the deuterostomes Homo sapiens and Ciona intestinalis or the fungi Allomyces macrogynus and the chytrids, show similar TFome profiles in terms of the proportions of each TF class, suggesting that this tendency is independent of TF type. This is consistent with the finding that TFs are one of the gene classes that are most resilient to loss after WGD (28,29). As for the total number of TFs, the proportion of TFs in a genome (as a fraction of the total number of proteins) also varies considerably.…”

Genome-wide deserts for copy number variation in vertebrates

“…We identified putative dosage-sensitive singletons as genes present in single copy in all of human, chimpanzee, macaque, mouse, rat, dog, cow, opossum and chicken. We examined CNVs neighbouring these 1,151 singletons and found that they were unlikely to display CNVs (21.9%, 252/1,151; P ¼ 3.0 Â 10 À 14 , w 2 test), which is consistent with the hypothesis that these are dosage-sensitive genes 37 . We observed a strong positive correlation between P CNV of non-singletons and distance to singletons for non-singletons on a 0.0-0.5 Mb scale (Supplementary Fig.…”

“…Furthermore, non-ohnologs within ORRs were likely to be singletons in all genomes analysed (purported dosage-sensitive singletons as described above; Table 1; P ¼ 1.0 Â 10 -8 , w 2 test). The dosage-sensitive singletons within ORRs are likely to be genes that returned to single-copy status from ohnologs after WGD 37 . These results indicate that non-ohnologs within ORRs may also be dosage-sensitive genes.…”

Pollen-Specific Activation of Arabidopsis Retrogenes Is Associated with Global Transcriptional Reprogramming

“…Duplicated genes are generated by several DNA-and RNA-based mechanisms (Innan and Kondrashov, 2010;Sakai et al, 2011). Whole-genome DNA-based duplication (WGD) by polyploidization has occurred in the evolutionary history of all land plants and many animals (Dehal and Boore, 2005;De Smet et al, 2013). Since WGD amplifies the entire genome, it seems to be a solution toward major evolutionary and/or ecological challenges (Comai, 2005;Fawcett et al, 2009).…”