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Evolution: Rooting the Eukaryotic Tree of Life

The root of the eukaryotic tree is a major unresolved question in evolutionary transcription and, particularly, biology. A recent study marshals mitochondrial genes to place that root translation [13]. This scenario implies between the enigmatic Excavates and all other eukaryotes, providing an that the mitochondrion was gained interesting new perspective on early eukaryotic evolution. before the radiation of all known eukaryotes, suggesting that Tom A. Williams The root of the eukaryotes has been mitochondrial genes might provide an studied intensively in recent years, interesting source of information about Eukaryotes are the group of organisms although as yet no consensus appears the eukaryotic root. The idea is that, whose cells contain a mitochondrion in sight. Published analyses have since mitochondria are descended and a nucleus. Although we often think placed the root within the Amorphea from Bacteria, trees of mitochondrial of eukaryotes as comprising animals, [7], between the Amorphea and all genes can be rooted on the bacterial plants, fungi, and the single-celled other eukaryotes [8], between the branch, polarizing the relationships protists, molecular phylogenetics has Archaeplastida (plants) and all other within the eukaryotic portion of the turned that view on its head [1]. At the eukaryotes [9], or within the Excavates tree — an approach pioneered by level of the genome, eukaryotic [10] — all with rather different Derelle and Lang [8] and developed biodiversity is largely microbial, with implications for the history and the in the recent study of He et al. [6]. each of the familiar multicellular groups process of eukaryotic evolution. While this work is unlikely to settle the arising independently from unicellular One reason for this lack of agreement debate for good, He et al. employ ancestors [2]. In this emerging view, may be the intrinsic difficulty of rooting state-of-the-art methods, and their which is based mainly on phylogenetic the eukaryotic tree. The great analyses focus attention on the most analyses of large sets of broadly evolutionary distance that separates important challenges remaining in this distributed genes [3–5], most eukaryotes from their closest field. eukaryotes can be classified into one of prokaryotic relatives makes standard As a starting point for their analyses, three major lineages. These are the phylogenetic rooting approaches He et al. [6] screened genomes from Amorphea (animals, fungi, and unreliable and prone to artefact. This the Amorphea, Diaphoretickes and Amoebozoans such as the slime mould has led authors to explore alternative Excavates for mitochondrial genes. Dictyostelium), the Diaphoretickes approaches, such as using the They identified 37 genes which were (including plants and most other information from gene duplications and found in all, or almost all, eukaryotes, photosynthetic eukaryotes), and the losses [7] or slowly evolving molecular and whose closest prokaryotic Excavates — a diverse group of characters such as gene fusions [9] to homologues were among the Bacteria. unicellular eukaryotes that includes root the tree. The problem is that when They found that the protein products important parasites such as Giardia, these alternative strategies disagree, of most of these genes were targeted Trichomonas, and Trypanosoma. it is difficult to determine the best to the mitochondria of modern Despite this rapid progress, some of approach. As an added difficulty, the eukaryotes, consistent with the idea the most interesting questions about interior branches of the eukaryotic tree that the genes originally entered the eukaryotic evolution remain separating the major groups often eukaryotic lineage with the ancestor of unresolved. Foremost among these appear to be rather short, perhaps the mitochondrion. Note that these is the position of the root of the suggesting that the Amorphea, genes are often not encoded by the eukaryotic tree, a critical point Diaphoretickes and Excavates mitochondrial genome, because many about which there is currently little diverged from each other over a mitochondrial genes have been consensus. A new study by He et al. [6] relatively short period of time following transferred to the nucleus during reported in this issue of Current Biology the origin of eukaryotes — the eukaryotic evolution [14]. Importantly, represents an important contribution to so-called ‘big bang’ of eukaryotic He et al. were able to show that their this ongoing debate. evolution [11,12]. set of genes contained a consistent The root of a phylogenetic tree Despite these difficulties in inferring phylogenetic signal within the is fundamental to its biological the root, recent discoveries have eukaryotes — that is, that they interpretation, defining the starting fleshed out our understanding of generally agreed on the structure of the point and polarizing the subsequent eukaryotic origins and the ancestral eukaryotic tree. Since each gene on its divergence events within the tree. For eukaryote. The balance of evidence own did not provide much rooting the eukaryotic tree, the root position is now favours a symbiogenic origin for information, the authors combined all critical for identifying the genes and the eukaryotic cell, in which an 37 genes and inferred a single tree. traits that may have been present in the Alpha-proteobacterium — the ancestor Assuming that the mitochondrion was ancestral eukaryote, for tracing the of the mitochondrion — formed a acquired before the diversification of evolution of these traits throughout partnership with an Archaeon, the main eukaryotic lineages, this tree the eukaryotic radiation, and for whose trace in modern eukaryotes could then be rooted on the branch establishing the deep relationships is found mainly in the genetic leading to the bacterial outgroups among the major eukaryotic groups. apparatus of DNA synthesis, (Figure 1). Following this logic, He et al. Current Biology Vol 24 No 4 R152

Excavates have much to learn about the earliest period of eukaryotic evolution, and will surely stimulate further debate.

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A recent study by Derelle and of He et al. is a thorough and interesting Lang [8] applied a similar strategy to He contribution to the rooting question, Institute for Cell and Molecular Biosciences, et al., using mitochondrial genes to root although it is unlikely to provide the University of Newcastle, Newcastle upon Tyne NE2 4HH, UK. the eukaryotic tree — but their analyses final word on this topic. The fact that E-mail: [email protected] instead supported a root on the similar approaches can produce very amorphean branch. The difference different results indicates that we still http://dx.doi.org/10.1016/j.cub.2014.01.026