Parasitic plants have increased rates of molecular evolution across all three genomes

Abstract

BackgroundTheoretical models and experimental evidence suggest that rates of molecular evolution could be raised in parasitic organisms compared to non-parasitic taxa. Parasitic plants provide an ideal test for these predictions, as there are at least a dozen independent origins of the parasitic lifestyle in angiosperms. Studies of a number of parasitic plant lineages have suggested faster rates of molecular evolution, but the results of some studies have been mixed. Comparative analysis of all parasitic plant lineages, including sequences from all three genomes, is needed to examine the generality of the relationship between rates of molecular evolution and parasitism in plants.ResultsWe analysed DNA sequence data from the mitochondrial, nuclear and chloroplast genomes for 12 independent evolutionary origins of parasitism in angiosperms. We demonstrated that parasitic lineages have a faster rate of molecular evolution than their non-parasitic relatives in sequences for all three genomes, for both synonymous and nonsynonymous substitutions.ConclusionsOur results prove that raised rates of molecular evolution are a general feature of parasitic plants, not confined to a few taxa or specific genes. We discuss possible causes for this relationship, including increased positive selection associated with host-parasite arms races, relaxed selection, reduced population size or repeated bottlenecks, increased mutation rates, and indirect causal links with generation time and body size. We find no evidence that faster rates are due to smaller effective populations sizes or changes in selection pressure. Instead, our results suggest that parasitic plants have a higher mutation rate than their close non-parasitic relatives. This may be due to a direct connection, where some aspect of the parasitic lifestyle drives the evolution of raised mutation rates. Alternatively, this pattern may be driven by an indirect connection between rates and parasitism: for example, parasitic plants tend to be smaller than their non-parasitic relatives, which may result in more cell generations per year, thus a higher rate of mutations arising from DNA copy errors per unit time. Demonstration that adoption of a parasitic lifestyle influences the rate of genomic evolution is relevant to attempts to infer molecular phylogenies of parasitic plants and to estimate their evolutionary divergence times using sequence data.

On the adaptive value of cytoplasmic genomes in plants

“…Studies of organelle genome evolution in parasitic plants report extensive genome rearrangements, gene losses and increased rates of base substitution (Krause 2012). These results are consistent with evolution under relaxed purifying selection, although other factors, including positive selection, reduced effective population sizes or increased mutation rates, also appear to be at least partially implicated (Bromham et al 2013). …”

Detection and Adaptation in Parasitic Angiosperm Host Selection

“…Indeed comparative exon-intron analysis between the eight Rboh proteins from Arabidopsis thaliana confirm distinct exon-intron patterns for several of those proteins as well, although none display truncations like those in SaNOX2 or SaNOX3 [42] [43]. Such unusual truncations may reflect the accelerated rate at which mutations appear to accumulate among parasitic angiosperms, relative to their non-parasitic relatives [47]. These increased rates of mutation may well provide an adaptive advantage to parasites in dealing with the evolution of resistance in hosts.…”

The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity

“…For the first time, we investigated the birth age of parasitic cnidarians belonging to the Myxozoa, using six independent nuclear genes for the reconciliation of molecular divergence time estimates of 10 myxozoans in relation to 128 metazoan taxa. Parasitic taxa are likely to have a faster rate of molecular evolution in order to win the “arms race” against their hosts (e.g., Bromham, Cowman, & Lanfear, ; Paterson et al., ). The rate heterogeneity across genes within the Myxozoa can be as high as that between myxozoans and other organisms (Hartigan et al., ; this study), and mitochondrial gene order and organization is highly variable (Takeuchi et al., ; Yahalomi et al., ), indicating a considerably accelerated rate of molecular evolution, possibly the fastest known among eukaryotes.…”