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Plastid Endosymbiosis, Genome Evolution and the Origin of Green Plants John W Opinion TRENDS in Plant Science Vol.12 No.9 Plastid endosymbiosis, genome evolution and the origin of green plants John W. Stiller Department of Biology, Howell Science Complex, N108, East Carolina University, Greenville, NC 27858, USA Evolutionary relationships among complex, multicellular origin does not necessarily imply a close evolutionary eukaryotes are generally interpreted within the frame- relationship between Viridiplantae and Rhodophyta work of molecular sequence-based phylogenies that (see Glossary) [5,6]. suggest green plants and animals are only distantly Many phylogenetic analyses based on nuclear sequence related on the eukaryotic tree. However, important data strongly reject a red–green sister relationship [5,7,8], anomalies have been reported in phylogenomic analyses, and inferred differences in RNAP II transcription are diffi- including several that relate specifically to green plant cult to reconcile with their putatively monophyletic relation- evolution. In addition, plants and animals share molecu- ship [9]. In contrast, recent phylogenomic analyses provided lar, biochemical and genome-level features that suggest a strong support for a hypothesis in which three primary relatively close relationship between the two groups. This plastid lineages (green plants, red algae and glaucocysto- article explores the impacts of plastid endosymbioses on phytes) share a common ancestor [10]. This study noted, nuclear genomes, how they can explain incongruent phy- however, that a relatively large amount of sequence is logenetic signals in molecular data sets and reconcile required to recover this relationship [10], and subsequent conflicts among different sources of comparative data. analyses of the same data showed that the tree-building Specifically, I argue that the large influx of plastid DNA signal supporting monophyly of primary plastid eukaryotes into plant and algal nuclear genomes has resulted in tree- was due to more rapidly evolving sequences [8].This building artifacts that obscure a relatively close evolution- suggests that the result might be a phylogenetic artifact ary relationship between green plants and animals. caused by rate variation in sequence evolution [8], although the source of this variation is unclear. Phylogenies and the origin of plants Glossary Phylogenetic analyses using molecular sequence data have provided influential new hypotheses regarding Amoebozoans: a group that includes Dicytostelium and diverse eukaryotic evolutionary relationships and the origin amoeboid protists, and is recovered as the sister group to opistho- konts in sequence-based phylogenies [48]. of green plants (Viridiplantae; see Glossary). Most Glaucocystophyta: a small and relatively rare group of protists sequence-based phylogenies strongly support a sister whose primary plastids (cyanelles) can be distinguished by the relationship between animals and fungi (opisthokonts; presence of a vestigial bacterial cell wall and cyanobacteria-like see Glossary), with green plants as a distant outgroup pigments. [1]. Recovery of opisthokonts is among the most robust Long-branch attraction: a catch phrase for tree-building artifacts, named for the tendency of rapidly evolving sequences to attract each results of broad-scale eukaryotic molecular systematics. other artificially in phylogenetic analyses. The correlated tendency of The grouping, now, is included in most introductory slowly evolving sequences to cluster artificially (short branch exclu- biology texts, and is used as a benchmark for interpreting sion) can be a major but underappreciated problem in phylogenetic the evolution of genome-level characters and complex analyses at great evolutionary distances. metabolic processes. Opisthokonts: a group comprising animals, fungi and their respect- ive protistan relatives, proposed originally [49] based on the pre- Comparably strong phylogenetic relationships have sence of a posterior flagellum as a synapomorphic character. beenhardertopindownforgreenplants.Molecular Primary plastids: plastids (chloroplasts) believed to be derived phylogenetics that recovered all plastids as monophyletic directly from a cyanobacterial endosymbiont based on the presence with respect to cyanobacteria led to the hypothesis of a of two surrounding membranes. single endosymbiotic origin in the common ancestor of Purifying selection: the elimination of deleterious alleles from a population or species by natural selection. green plants and red algae, the two major groups contain- Rhodophyta: commonly called red algae, a diverse and ancient ing primary plastids (see Glossary) [2,3]. Whether avail- eukaryotic group with primary plastids that contain phycobilipro- able data strongly favor a single plastid endosymbiosis teins as the major accessory pigments. has been addressed elsewhere, and the issue remains Synapomorphy: a derived evolutionary character that is believed to difficult to resolve [4]; however, even a single plastid have originated in the common ancestor of two or more taxa. Viridiplantae: the monophyletic group comprising all green algae and land plants. It is used synonymously with the term green plants Corresponding author: Stiller, J.W. ([email protected]). in this article. Available online 16 August 2007. www.sciencedirect.com 1360-1385/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2007.08.002 392 Opinion TRENDS in Plant Science Vol.12 No.9 A persistent artifact related to green plant origins date. The evolution of such complex genomic features and The difficulty in recovering a well-supported sister metabolic networks generally are interpreted within the relationship with red algae is not the only phylogenetic framework of sequence-based phylogenies, which pre- curiosity relating to green plants origins. Early attempts at sumes a relatively distant relationship between green multigene phylogenies of major eukaryotic lineages typi- plants and animals. This can sometimes lead to more cally recovered animals and fungi as sister taxa, or placed complicated and even strained evolutionary assumptions animals with green plants, but seldom suggested a close (Box 1). Thus, even as strong consensus relationships relationship between green plants and fungi [11,12]. The emerge from sequence-based phylogenomics, serious ques- presence of a second directional tree-building signal was tions remain [1]. This is particularly true for inferences at characterized as a persistent artifact of phylogenetic re- great genetic distances, such as those relating to green construction [11]; the fact that animals and fungi were plant origins, where lineage-specific biases can confound recovered as sister taxa by most sequences led to the tree-building algorithms [1,7,31–33]. presumption that trees supporting a plant–animal relationship reflect this artifact [11]. After this preliminary The impact of plastid endosymbioses on nuclear characterization, most multigene investigations of eukar- genomes yotic relationships have not examined the problem further; Although the common presence of plastids has influenced those that have provide evidence that these two conflicting hypotheses about eukaryotic phylogenetic relationships, phylogenetic signals are a consistent feature of molecular the potential biases these plastids might introduce into sequence data [13,14]. nuclear phylogenomic inference require more scrutiny. In In addition to sequence-based phylogenies, an particular, it is important to explore whether their pre- animal–fungi relationship is supported by a number of sence can explain existing conflicts among molecular data putatively shared-derived characters (synapomorphies). sets, and/or the tree-building anomalies outlined above. These include an insertion in the elongation factor-1a gene [11], the fusion of the dihydrofolate and thymidylate synthase genes [15], the acquisition of archael tyrosyl- Box 1. Precursors or remnants of complex metabolic tRNA synthetase by horizontal gene transfer [16],and pathways? the presence of orthologous genes absent from most other The evolution of a complex molecular or biochemical feature is eukaryotes [17]. Interestingly, comparable molecular fea- generally interpreted in light of sequence-based trees. When any tures that could be considered synapomorphic have been genes involved in a given pathway are found in a member of a reported for green plants and animals, suggesting that lineage, it is assumed that the entire pathway is present, or at least the two competing phylogenetic signals are not limited to was ancestrally in the group. This can lead to the construction of tree-building algorithms. The pre-mRNA capping path- assumptions and complicated scenarios to explain characters that appear to be synapomorphic for green plants and animals. Such way is perhaps the most compelling example. Green explanations might not be realistic biologically. plants and animals are unique in their use of a different A prime example is the Rb–E2F pathway, which controls G1–S cell class of triphosphatase enzyme that also is fused to cycle progression and cell differentiation. The pathway is conserved guanylyl transferase, thereby producing a multifunc- across animals and plants, including the unicellular green algal tional capping enzyme (CE) [18]. Additional evidence of Ostreococcus [50], but has not been reported from any of the numerous fungal genomes sequenced to date. Although also absent a close animal–green plant relationship includes sim- from most protistan genomes, possible Rb homologs have been
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