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Impact of gene molecular evolution on phylogenetic reconstruction: a case study in the rosids (Superorder Rosanae, Angiosperms).

ABSTRACT: Rate of substitution of genomic regions is among the most debated intrinsic features that impact phylogenetic informativeness. However, this variable is also coupled with rates of nonsynonymous substitutions that underscore the nature and degree of selection on the selected genes. To empirically address these variables, we constructed four completely overlapping data sets of plastid matK, atpB, rbcL, and mitochondrial matR genes and used the rosid lineage (angiosperms) as a working platform. The genes differ in combinations of overall rates of nucleotide and amino acid substitutions. Tree robustness, homoplasy, accuracy in contrast to a reference tree, and phylogenetic informativeness are evaluated. The rapidly evolving/unconstrained matK faired best, whereas remaining genes varied in degrees of contribution to rosid phylogenetics across the lineage's 108 million years evolutionary history. Phylogenetic accuracy was low with the slowly evolving/unconstrained matR despite least amount of homoplasy. Third codon positions contributed the highest amount of parsimony informative sites, resolution and informativeness, but magnitude varied with gene mode of evolution. These findings are in clear contrast with the views that rapidly evolving regions and the 3rd codon position have inevitable negative impact on phylogenetic reconstruction at deep historic level due to accumulation of multiple hits and subsequent elevation in homoplasy and saturation. Relaxed evolutionary constraint in rapidly evolving genes distributes substitutions across codon positions, an evolutionary mode expected to reduce the frequency of multiple hits. These findings should be tested at deeper evolutionary histories.

SUBMITTER: Hilu KW

PROVIDER: S-EPMC4059714 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Impact of gene molecular evolution on phylogenetic reconstruction: a case study in the rosids (Superorder Rosanae, Angiosperms).

Hilu Khidir W KW Black Chelsea M CM Oza Dipan D

PloS one 20140616 6

Rate of substitution of genomic regions is among the most debated intrinsic features that impact phylogenetic informativeness. However, this variable is also coupled with rates of nonsynonymous substitutions that underscore the nature and degree of selection on the selected genes. To empirically address these variables, we constructed four completely overlapping data sets of plastid matK, atpB, rbcL, and mitochondrial matR genes and used the rosid lineage (angiosperms) as a working platform. The ...[more]

PMID: 24932884

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Project description:BackgroundGene duplication has been a fundamental process in the evolution of eukaryotic genomes. After duplication one copy (or both) can undergo divergence in sequence, expression pattern, and function. Two divergent copies of the ribosomal protein S13 gene (rps13) of chloroplast origin are found in the nucleus of the rosids Arabidopsis, Gossypium, and Glycine. One encodes chloroplast-imported RPS13 (nucp rps13), while the other encodes mitochondria-imported RPS13 (numit rps13). The rps13 gene has been lost from mitochondrial DNA (mt rps13) of many rosids.ResultsWe studied sequence evolution of numit rps13 in comparison with nucp rps13 in seven rosid genera. Ka/Ks analysis and likelihood ratio tests showed considerably higher Ka values and Ka/Ks ratios in numit rps13 than in nucp rps13, indicating increased amino acid sequence divergence in numit rps13. Two positively selected codons were detected in numit RPS13 in regions that are inferred to interact with the 16S rRNA. Several amino acids in numit RPS13 have changed from the one present in nucp RPS13 to the one present in mt RPS13, showing that numit rps13 is becoming more like mt rps13. Comparison of expression patterns and levels of numit rps13 and nucp rps13 in Arabidopsis using microarray data indicated divergence in gene expression. We discovered that in addition to numit rps13, Malus (apple) contains a transcribed mt rps13 gene. To determine if partitioning of expression takes place between numit rps13 and mt rps13, expression of both copies and RNA editing of mt rps13 were examined by RT-PCR, qRT-PCR, and sequencing from 14 different organ types plus seedlings subjected to five different abiotic stresses. Co-expression of numit rps13 and mt rps13 was observed in all the organs and various stress treatments. We determined that purifying selection is acting on both numit rps13 and mt rps13 in Malus.ConclusionOur data provide evidence that numit rps13 genes in rosids have experienced adaptive sequence evolution and convergent evolution with mt rps13. Co-expression of numit rps13 and mt rps13 and purifying selection on both genes in Malus suggest that both are functional. The three organellar rps13 genes in rosids provide a distinctive case of gene duplication involving the co-evolution of the nuclear and cytoplasmic genomes.

Project description:BackgroundRosids are a major clade in the angiosperms containing 13 orders and about one-third of angiosperm species. Recent molecular analyses recognized two major groups (i.e., fabids with seven orders and malvids with three orders). However, phylogenetic relationships within the two groups and among fabids, malvids, and potentially basal rosids including Geraniales, Myrtales, and Crossosomatales remain to be resolved with more data and a broader taxon sampling. In this study, we obtained DNA sequences of the mitochondrial matR gene from 174 species representing 72 families of putative rosids and examined phylogenetic relationships and phylogenetic utility of matR in rosids. We also inferred phylogenetic relationships within the "rosid clade" based on a combined data set of 91 taxa and four genes including matR, two plastid genes (rbcL, atpB), and one nuclear gene (18S rDNA).ResultsComparison of mitochondrial matR and two plastid genes (rbcL and atpB) showed that the synonymous substitution rate in matR was approximately four times slower than those of rbcL and atpB; however, the nonsynonymous substitution rate in matR was relatively high, close to its synonymous substitution rate, indicating that the matR has experienced a relaxed evolutionary history. Analyses of our matR sequences supported the monophyly of malvids and most orders of the rosids. However, fabids did not form a clade; instead, the COM clade of fabids (Celastrales, Oxalidales, Malpighiales, and Huaceae) was sister to malvids. Analyses of the four-gene data set suggested that Geraniales and Myrtales were successively sister to other rosids, and that Crossosomatales were sister to malvids.ConclusionCompared to plastid genes such as rbcL and atpB, slowly evolving matR produced less homoplasious but not less informative substitutions. Thus, matR appears useful in higher-level angiosperm phylogenetics. Analysis of matR alone identified a novel deep relationship within rosids, the grouping of the COM clade of fabids and malvids, which was not resolved by any previous molecular analyses but recently suggested by floral structural features. Our four-gene analysis supported the placements of Geraniales, Myrtales at basal nodes of the rosid clade and placed Crossosomatales as sister to malvids. We also suggest that the core part of rosids should include fabids, malvids and Crossosomatales.

Dataset Information

Impact of gene molecular evolution on phylogenetic reconstruction: a case study in the rosids (Superorder Rosanae, Angiosperms).

Publications

Impact of gene molecular evolution on phylogenetic reconstruction: a case study in the rosids (Superorder Rosanae, Angiosperms).

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