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Horizontal Gene Transfer in the Evolution of Photosynthetic Eukaryotes

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Horizontal Gene Transfer in the Evolution of Photosynthetic Eukaryotes Journal of Systematics and Evolution 51 (1): 13–29 (2013) doi: 10.1111/j.1759-6831.2012.00237.x Review Horizontal gene transfer in the evolution of photosynthetic eukaryotes 1,2Jinling HUANG* 1,2Jipei YUE 1(Department of Biology, East Carolina University, Greenville, North Carolina 27858, USA) 2(Key Laboratory of Plant Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China) Abstract Horizontal gene transfer (HGT) may not only create genome mosaicism, but also introduce evolutionary novelties to recipient organisms. HGT in plastid genomes, though relatively rare, still exists. HGT‐derived genes are particularly common in unicellular photosynthetic eukaryotes and they also occur in multicellular plants. In particular, ancient HGT events occurring during the early evolution of primary photosynthetic eukaryotes were probably frequent. There is clear evidence that anciently acquired genes played an important role in the establishment of primary plastids and in the transition of plants from aquatic to terrestrial environments. Although algal genes have often been used to infer historical plastids in plastid‐lacking eukaryotes, reliable approaches are needed to distinguish endosymbionts‐derived genes from those independently acquired from preferential feeding or other activities. Key words endosymbiosis, genome evolution, plants, plastids. Gene transfer across the boundaries of species or In eukaryotes, gene transfer may occur between genomes has been widely recognized as an important genomes (mitochondrial, plastid, and nuclear) within force in the evolution of life on earth (Gogarten the cell or between distinct organisms. The former is et al., 2002; Andersson, 2005; Simonson et al., 2005; often referred to as intracellular gene transfer (IGT), Keeling & Palmer, 2008). According to Woese (2002), which is mostly unidirectional from mitochondria or the primary cellular evolution was communal and gene plastids to the nucleus and sometimes between plastids transfer was the driving force in the origin of modern and mitochondria. Because of the endosymbiotic origin cells. Thus far, an increasing amount of data shows that of mitochondria and plastids, this process is also called the impact of gene transfer extends far beyond the origin endosymbiotic gene transfer (EGT). The process of of cellular life. In prokaryotes, because mutations are genetic movement between species is termed horizontal mostly deleterious, acquisition of foreign genes is or lateral gene transfer (HGT or LGT). Although the considered the major means to gain novel genes. By role of HGT in eukaryotic evolution was poorly acquiring ready‐to‐use genes from other sources, gene appreciated historically, an increasing amount of data transfer may confer recipient organisms beneficial indicates that HGT not only is frequent in unicellular phenotypes and immediate abilities to explore new eukaryotes of various habitats and lifestyles (Andersson, resources and niches (Gogarten et al., 2002; Jain et al., 2005; Keeling & Palmer, 2008), but occurs in multi- 2003). Indeed, acquired genes are reportedly respon- cellular eukaryotes as well (Scholl et al., 2003; Pierce sible for the spread of photosynthesis, nitrogen fixation, et al., 2007; Moran & Jarvik, 2010; Ni et al., 2012; Yue bacterial pathogenesis, and antibiotic resistance. It has et al., 2012). There is also clear evidence that HGT been estimated that almost all prokaryotic genes have occurs between eukaryotic species (Rumpho et al., been affected by gene transfer in their evolution (Dagan 2008; Moran & Jarvik, 2010; Sun et al., 2010, 2011). In et al., 2008). As a result, gene transfer may not only many cases, acquisition of genes from other species has spread evolutionary success across distinct lineages, but significantly shaped the evolution of the biochemical also potentially transform the Darwinian tree‐like system of recipient organisms. phylogenesis pattern into a net over time (Doolittle, This article reviews the occurrence and impact of 2000; Bapteste et al., 2009; Martin, 2011). HGT in the evolution of photosynthetic eukaryotes. Given the availability of several reviews related to HGT in plant mitochondria (Richardson & Palmer, 2007; Keeling & Palmer, 2008), we will limit this review to Received: 15 January 2012 Accepted: 4 November 2012 * Author for correspondence. E‐mail: huangj@ecu.edu. Tel.: 252‐328‐ HGT in plastid and nuclear genomes of photosynthetic 5623. Fax: 252‐328‐4178. eukaryotes. © 2012 Institute of Botany, Chinese Academy of Sciences 14 Journal of Systematics and Evolution Vol. 51 No. 1 2013 1 Detecting horizontally acquired genes in related taxa will not be known. This in turn can eukaryotes translate into difficulties distinguishing recent HGT versus ancient HGT. A good and practical Because gene transfer involves the origin of a gene approach should be a broad and balanced from another genome or species, any evidence taxonomic sample from representative groups indicative of evolutionary relationships can be used of all three domains of life (bacteria, archaea, to identify transferred genes. Such evidence, for and eukaryotes). In many cases, identification of example, may include GC content or codon usage the exact donor involves re‐sampling once the patterns that often differ between donor and recipient donor has been narrowed down. organisms. Since phylogenetic analyses investigate the (2) Organismal phylogeny. A good knowledge of relationships among sampled sequences, they are often organismal phylogeny is not only essential for considered to be the most reliable method to identify the identification of transferred genes, but also transferred genes (Andersson, 2005; Keeling & particularly important for explaining some Palmer, 2008). Theoretically, if a gene in a eukaryotic puzzling gene phylogenies resulting from differ- genome was acquired from a bacterium, it is essentially ential displacement (Huang & Gogarten, 2009). a bacterial gene in origin and should be more closely The scenario arising from differential displace- related to bacterial homologs than to other eukaryotic ment of preexisting homologs by acquired genes sequences. Therefore, evidence for gene transfer can be is potentially frequent, but largely ignored in inferred by comparing the gene phylogeny and the current studies and rarely discussed in literatures. known organismal phylogeny for incongruence. Such a scenario may have been frequently Though straightforward as it sounds, the phylo- mistaken as resulting from independent acquis- genetic approach can be subject to many potential itions, or gene duplication followed by differ- pitfalls due to data quality, methodology, differential ential losses. gene gain/loss, or other issues (Huang & Gogarten, (3) Gene distribution. Accurate information of gene 2006). In particular, long‐branch attraction due to distribution can eliminate some spurious cases unequal sequence changing rates can lead to erroneous of gene transfer, but also is extremely useful for gene tree topologies. Biased or insufficient taxonomic distinguishing horizontally acquired genes from sampling may also result in grouping unrelated those arising from other scenarios, including sequences in a clade, which is superficially similar to differential losses and IGT events. For example, cases of gene transfer. Even if the gene tree is free of a eukaryotic gene that is absent from cyanobac- artifacts, other explanations always exist. In particular, teria and proteobacteria may not have a plastid differential gene loss, sometimes associated with or mitochondrial origin. The determination of duplication and paralogy, can always be invoked as gene distribution entails extensive searches of an explanation alternative to HGT (Gogarten & many additional databases other than GenBank. Townsend, 2005; Huang & Gogarten, 2006). This (4) Gene neighborhood. Some acquired genes are alternative scenario, however, becomes increasingly functionally related, but their exact donors are less likely if more and more loss events need to be often uncertain. However, if these genes are invoked. In some other cases, independent or recurrent physically adjacent or form an operon on a gene transfer events may also lead to gene tree chromosome of the potential donor, a likely topologies that are difficult to interpret. scenario would be that these genes were To effectively reduce the number of false positives acquired together from the same donor (Ricard in HGT detection, a combined approach including et al., 2006; Sun et al., 2010). multiple lines of independent evidence is preferred. The (5) Pairwise sequence comparison. Although se- following summarizes some practical considerations in quence similarity comparison is not an accurate the identification of acquired genes in eukaryotes. approach to detect transferred genes, its sensi- tivity is high (Frickey & Lupas, 2004). For (1) Broad and balanced taxonomic sampling.A example, the vast majority of plastid genes broad and balanced sampling is not only either are highly similar to cyanobacterial important for narrowing down the donor, but homologs in pairwise sequence comparison the recipient as well. If the donor taxon is not or group with cyanobacterial homologs in sampled, it cannot be identified. On the other phylogenetic analyses (Huang J, unpublished hand, if the recipient group is not properly data). Therefore, if a eukaryotic sequence sampled, the distribution of an acquired gene in is most similar to their cyanobacterial or a‐ © 2012 Institute
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