Probabilistic Analysis Indicates Discordant Gene Trees in Chloroplast Evolution

Abstract

Analyses of whole-genome data often reveal that some genes have evolutionary histories that diverge from the majority phylogeny estimated for the entire genome. We present a probabilistic model that deals with heterogeneity among gene trees, implement it via the Gibbs sampler, and apply it to the plastid genome. Plastids and their genomes are transmitted as a single block without recombination, hence homogeneity among gene trees within this genome is expected. Nevertheless, previous work has revealed clear heterogeneity among plastid genes (e.g., Delwiche and Palmer 1996). Other studies, using whole plastid genomes of various algae and land plants, found little additional heterogeneity (Martin et al. 1998; Adachi et al. 2000). We augment the earlier studies by using a data set of 14 taxa: 6 land plants, 2 green algae, a diatom, 2 red algae and a cryptophyte, the cyanelle of the glaucocystophyte Cyanophora, and the blue-green alga Synechocystis as an outgroup. Contrary to the earlier analyses, we cannot find even a single, dominant consensus tree. Therefore, we formulate a probabilistic model that divides the genes into two sets: those that follow the consensus tree and those that have independent gene trees. No particular tree is supported by more than three-fourths of the genes. But the set of genes that follows a certain tree is fairly independent of data processing and the method of analysis. With one possible exception, we find no evidence for collinear or functionally related genes to follow similar trees. The phylogenetic pattern also seems independent of bias in amino acid composition. Among possible explanations for the observed phenomenon, the hypothesis that different genes have different covarion structures is difficult to assess. But gene duplication may be possible through the inverted or direct repeat regions, while horizontal gene transfer seems less likely. In contrast to green algae and land plants, inverted repeat regions in red algae and in Cyanophora show abundant differences among the copies. Thus, genes may get duplicated when they are recruited into the inverted repeat region and one of the two copies may be lost after leaving the inverted repeat region.

Comparative Analysis of the Complete Plastid Genome Sequence of the Red Alga Gracilaria tenuistipitata var. liui Provides Insights into the Evolution of Rhodoplasts and Their Relationship to Other Plastids

“…Hackett, S. Heard, D. Bhattacharya, unpublished data). The result that is apparent both here and in previous analyses (e.g., Vogl et al 2003) is that a different plastid gene(s) often supports discordant phylogenies. Despite this vexing issue, it is also clear that most of the nodes in the plastid tree are in fact well supported.…”

“…To assess if different proteins supported conflicting plastid phytogenies, we divided the data into functionally related groups under the assumption that interacting proteins could potentially share a common evolutionary history (e.g., de Queiroz et al 1995 [but see Vogl et al 2003]). The first major group was defined by photosystem (PSII + II) I and II proteins (i.e., psaX and psbX proteins) and was of total length 3498 aa and the second major group included proteins involved in transcription and translation ([T + T] i.e., ribosomal proteins and RNA polymerase subunits) and was of total length 3347 aa.…”

Biogeographic and Phylogenetic Diversity of Thermoacidophilic Cyanidiales in Yellowstone National Park, Japan, and New Zealand

“…The discrepancy between the chloroplast rbcL and nuclear 18S rDNA sequence data may indicate a difference in the time scale of chloroplast evolutionary changes (or at least of the rbcL gene) within the cyanidia of Japan and New Zealand that are independent of the nuclear DNA as characterized by 18S rDNA, which shows little divergence. There is precedence for rates of chloroplast DNA evolution differing from those of nuclear DNA (11,35). This precedence also hints at lateral transfer of the rbcL gene.…”

Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

“…It results from structural and functional constraints acting on proteins [173]. Vogl et al [174] showed that many plastid genes have significantly different phylogenies under standard substitution models and proposed that this incongruence could indeed result from heterotachy. In agreement with that, the application of heterotachy models found that many plastid genes of red and green plants are, in fact, subject to such evolution [175][176][177], and this process can cause errors in inference of phylogenetic trees leading to the LBA effect [178,179].…”