Dataset Information

Selfing in Haploid Plants and Efficacy of Selection: Codon Usage Bias in the Model Moss Physcomitrella patens.

ABSTRACT: A long-term reduction in effective population size will lead to major shift in genome evolution. In particular, when effective population size is small, genetic drift becomes dominant over natural selection. The onset of self-fertilization is one evolutionary event considerably reducing effective size of populations. Theory predicts that this reduction should be more dramatic in organisms capable for haploid than for diploid selfing. Although theoretically well-grounded, this assertion received mixed experimental support. Here, we test this hypothesis by analyzing synonymous codon usage bias of genes in the model moss Physcomitrella patens frequently undergoing haploid selfing. In line with population genetic theory, we found that the effect of natural selection on synonymous codon usage bias is very weak. Our conclusion is supported by four independent lines of evidence: 1) Very weak or nonsignificant correlation between gene expression and codon usage bias, 2) no increased codon usage bias in more broadly expressed genes, 3) no evidence that codon usage bias would constrain synonymous and nonsynonymous divergence, and 4) predominant role of genetic drift on synonymous codon usage predicted by a model-based analysis. These findings show striking similarity to those observed in AT-rich genomes with weak selection for optimal codon usage and GC content overall. Our finding is in contrast to a previous study reporting adaptive codon usage bias in the moss P. patens.

SUBMITTER: Szovenyi P

PROVIDER: S-EPMC5507605 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Selfing in Haploid Plants and Efficacy of Selection: Codon Usage Bias in the Model Moss Physcomitrella patens.

Szövényi Péter P Ullrich Kristian K KK Rensing Stefan A SA Lang Daniel D van Gessel Nico N Stenøien Hans K HK Conti Elena E Reski Ralf R

Genome biology and evolution 20170601 6

A long-term reduction in effective population size will lead to major shift in genome evolution. In particular, when effective population size is small, genetic drift becomes dominant over natural selection. The onset of self-fertilization is one evolutionary event considerably reducing effective size of populations. Theory predicts that this reduction should be more dramatic in organisms capable for haploid than for diploid selfing. Although theoretically well-grounded, this assertion received ...[more]

PMID: 28549175

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Project description:BackgroundThe moss Physcomitrella patens is an emerging plant model system due to its high rate of homologous recombination, haploidy, simple body plan, physiological properties as well as phylogenetic position. Available EST data was clustered and assembled, and provided the basis for a genome-wide analysis of protein encoding genes.ResultsWe have clustered and assembled Physcomitrella patens EST and CDS data in order to represent the transcriptome of this non-seed plant. Clustering of the publicly available data and subsequent prediction resulted in a total of 19,081 non-redundant ORF. Of these putative transcripts, approximately 30% have a homolog in both rice and Arabidopsis transcriptome. More than 130 transcripts are not present in seed plants but can be found in other kingdoms. These potential "retained genes" might have been lost during seed plant evolution. Functional annotation of these genes reveals unequal distribution among taxonomic groups and intriguing putative functions such as cytotoxicity and nucleic acid repair. Whereas introns in the moss are larger on average than in the seed plant Arabidopsis thaliana, position and amount of introns are approximately the same. Contrary to Arabidopsis, where CDS contain on average 44% G/C, in Physcomitrella the average G/C content is 50%. Interestingly, moss orthologs of Arabidopsis genes show a significant drift of codon fraction usage, towards the seed plant. While averaged codon bias is the same in Physcomitrella and Arabidopsis, the distribution pattern is different, with 15% of moss genes being unbiased. Species-specific, sensitive and selective splice site prediction for Physcomitrella has been developed using a dataset of 368 donor and acceptor sites, utilizing a support vector machine. The prediction accuracy is better than those achieved with tools trained on Arabidopsis data.ConclusionAnalysis of the moss transcriptome displays differences in gene structure, codon and splice site usage in comparison with the seed plant Arabidopsis. Putative retained genes exhibit possible functions that might explain the peculiar physiological properties of mosses. Both the transcriptome representation (including a BLAST and retrieval service) and splice site prediction have been made available on http://www.cosmoss.org, setting the basis for assembly and annotation of the Physcomitrella genome, of which draft shotgun sequences will become available in 2005.

Project description:BACKGROUND: Hexokinase catalyzes the phosphorylation of glucose and fructose, but it is also involved in sugar sensing in both fungi and plants. We have previously described two types of hexokinases in the moss Physcomitrella. Type A, exemplified by PpHxk1, the major hexokinase in Physcomitrella, is a soluble protein that localizes to the chloroplast stroma. Type B, exemplified by PpHxk2, has an N-terminal membrane anchor. Both types are found also in vascular plants, and localize to the chloroplast stroma and mitochondrial membranes, respectively. RESULTS: We have now characterized all 11 hexokinase encoding genes in Physcomitrella. Based on their N-terminal sequences and intracellular localizations, three of the encoded proteins are type A hexokinases and four are type B hexokinases. One of the type B hexokinases has a splice variant without a membrane anchor, that localizes to the cytosol and the nucleus. However, we also found two new types of hexokinases with no obvious orthologs in vascular plants. Type C, encoded by a single gene, has neither transit peptide nor membrane anchor, and is found in the cytosol and in the nucleus. Type D hexokinases, encoded by three genes, have membrane anchors and localize to mitochondrial membranes, but their sequences differ from those of the type B hexokinases. Interestingly, all moss hexokinases are more similar to each other in overall sequence than to hexokinases from other plants, even though characteristic sequence motifs such as the membrane anchor of the type B hexokinases are highly conserved between moss and vascular plants, indicating a common origin for hexokinases of the same type. CONCLUSIONS: We conclude that the hexokinase gene family is more diverse in Physcomitrella, encoding two additional types of hexokinases that are absent in vascular plants. In particular, the presence of a cytosolic and nuclear hexokinase (type C) sets Physcomitrella apart from vascular plants, and instead resembles yeast, where all hexokinases localize to the cytosol. The fact that all moss hexokinases are more similar to each other than to hexokinases from vascular plants, even though both type A and type B hexokinases are present in all plants, further suggests that the hexokinase gene family in Physcomitrella has undergone concerted evolution.

Dataset Information

Selfing in Haploid Plants and Efficacy of Selection: Codon Usage Bias in the Model Moss Physcomitrella patens.

Publications

Selfing in Haploid Plants and Efficacy of Selection: Codon Usage Bias in the Model Moss Physcomitrella patens.

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