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Horizontal Gene Transfers in Plants life Review Horizontal Gene Transfers in Plants Emilie Aubin, Moaine El Baidouri * and Olivier Panaud * Laboratoire Génome et Développement des Plantes, UMR 5096 UPVD/CNRS, Université de Perpignan Via Domitia, 52, Avenue, Paul Alduy, CEDEX, 66860 Perpignan, France; [email protected] * Correspondence: [email protected] (M.E.B.); [email protected] (O.P.) Abstract: In plants, as in all eukaryotes, the vertical transmission of genetic information through reproduction ensures the maintenance of the integrity of species. However, many reports over the past few years have clearly shown that horizontal gene transfers, referred to as HGTs (the interspecific transmission of genetic information across reproductive barriers) are very common in nature and concern all living organisms including plants. The advent of next-generation sequencing technologies (NGS) has opened new perspectives for the study of HGTs through comparative genomic approaches. In this review, we provide an up-to-date view of our current knowledge of HGTs in plants. Keywords: horizontal transfer; transposable elements; plants; genome 1. Introduction In living organisms, the vertical transmission of genetic information through reproduc- tion ensures the maintenance of the self within populations and guarantees the integrity of species. Meanwhile, in most eukaryotic species, sexual reproduction also contributes to Citation: Aubin, E.; El Baidouri, M.; Panaud, O. Horizontal Gene sustain adaptive diversity through the maintenance of diversity within populations. This Transfers in Plants. Life 2021, 11, 857. duality of the living, i.e., the diversity of the self, is at the origin of the neo-Darwinian theory https://doi.org/10.3390/life11080857 of evolution and has nourished generations of scholars in the field of evolutionary biology for over a century. In this context, horizontal gene transfers (HGTs), i.e., the transmission of Academic Editors: Kousuke Hanada, genetic material across reproductive barriers, have long been considered as rare, anecdotal Alfredo Conti, Dirk Schulze-Makuch, phenomena that could in no way constitute a major evolutionary force in multicellular Michael Russell, Hiroki Nishikawa organisms. However, HGTs were discovered decades ago in prokaryotes [1] and have since and Stefanos Roumeliotis been shown to be major players in their adaptive process, such as in the case of the dissemi- nation of antibiotic resistance [2]. HGTs occur at such an extent among bacteria and archaea Received: 9 July 2021 that they impede robust phylogenetic reconstructions, leading to questioning about the Accepted: 16 August 2021 taxonomic concept of species in these kingdoms [3]. In eukaryotes, unlike in prokaryotes, Published: 21 August 2021 HGTs have long been considered as anecdotal, although the first documented cases of transfer involving a eukaryotic species were published more than 30 years ago [4,5]. Since Publisher’s Note: MDPI stays neutral these pioneering studies, however, hundreds of reports have evidenced the occurrence with regard to jurisdictional claims in of HGTs involving protists [6] and multicellular organisms such as plants [7], animals [8], published maps and institutional affil- and fungi [9], therefore suggesting that, unlike it was previously thought, gene flows iations. among distinct taxa occur frequently within ecosystems. Among all genomic components, transposable elements (TEs) appear to be particularly prone to horizontal transfers [10]. Whether this could be explained by the fact that they exist as extrachromosomal forms during the transposition cycle [11] remains to be demonstrated. Nevertheless, horizontal Copyright: © 2021 by the authors. transfers may play an important role in the survival and dissemination of TEs in plant Licensee MDPI, Basel, Switzerland. genomes, as we will discuss in this review. This article is an open access article In order to ascertain that HGTs are an important process in eukaryotes evolution, distributed under the terms and one should address both the questions of the causes (mechanisms) and the consequences conditions of the Creative Commons (biological impact) of HGTs. Parasitism is often brought forward as an ecological niche that Attribution (CC BY) license (https:// could favor HGTs [12]. Indeed, several documented cases of transfers concern host/parasite creativecommons.org/licenses/by/ interactions, either directly or through an intermediate host [13], but many reports of HGTs 4.0/). Life 2021, 11, 857. https://doi.org/10.3390/life11080857 https://www.mdpi.com/journal/life Life 2021, 11, x FOR PEER REVIEW 2 of 12 that could favor HGTs [12]. Indeed, several documented cases of transfers concern host/parasite interactions, either directly or through an intermediate host [13], but many reports of HGTs do not involve parasitism, which leads to questioning about the alterna- tive routes for interspecific gene flows. As for the consequences of HGTs, the main ques- Life 2021, 11, 857 2 of 12 tions are whether the transferred genetic material remains functional in new genetic back- grounds and/or whether it could be at the origin of new functions, thus contributing to biological novelty. Theredo not involveare numerous parasitism, exam whichples leads of to questioningHGT-mediated about the acquisition alternative routes of new for functions in higher eukaryotesinterspecific gene that flows. involv As fore plants the consequences as donors of HGTs, or receptors the main questions [14,15]. are whether The latest developmentsthe transferred in geneticsequencing material tec remainshnologies functional (referred in new geneticto as NGS: backgrounds next-gener- and/or whether it could be at the origin of new functions, thus contributing to biological novelty. ation sequencing technologies)There are numerous have examples opened of HGT-mediatednew perspectives acquisition to study of new functionsHGTs through in higher genomic strategies, whicheukaryotes lead that to involve an accelera plants astion donors of their or receptors discoveries [14,15]. through comparative genomic approaches (seeThe Box latest 1 developments for the princi in sequencingples of technologies HGT detection (referred to based as NGS: on next-generation sequence sequencing technologies) have opened new perspectives to study HGTs through genomic information). In thisstrategies, review, which we leadwill to presen an accelerationt the current of their discoveries knowledge through of comparativeHGTs in genomicplants, based on these latestapproaches discoveries. (see Figure We1 willfor the focus principles on ofpossible HGT detection mechanisms based on sequence for these information). trans- fers, some of which Inare this plant-specific, review, we will present and the di currentscuss knowledgethe impact of HGTs of these in plants, interspecific based on these gene latest discoveries. We will focus on possible mechanisms for these transfers, some of which are flows in plant evolution.plant-specific, and discuss the impact of these interspecific gene flows in plant evolution. BoxFigure 1. 1.TheThe three three criteriacriteria used used for HGT for detectionHGT detection through comparative through genomics:comparative high similarity genomics: (HS), high phylogenetic similarity (HS),incongruence phylogenetic (PI) and patchy incongruence distribution (P in phylogeniesI) and patchy (PD) [distribution9]. The HS criterion in ph requiresylogenies access (PD) to genomic [9]. The data ofHS the crite- riontwo speciesrequires involved access in the to transfer.genomic It consists data of establishingthe two spec that geneies involved homologs between in the twotransf specieser. It exhibit consists a sequence of estab- identity that is significantly higher than the average of the other homologs in the genome, therefore not originating from lishingvertical transmission.that gene Inhomologs order to circumvent between the possibletwo species effect of strongexhibit selection a sequence (that could identity lead to high that sequence is significantly identity), highersynonymous than substitutions the average are of used the to measureother homologs sequence divergence. in the genome, The PI criterion therefore is based not on theoriginating incongruence from between vertical transmission.the topologies of In the order phylogenetic to circumvent tree of the species the andpossible that of theeffect horizontally of strong transferred selection genes. (that This requirescould lead sequence to high sequenceinformation identity), for a large phylogenetic synonymous panel, substitutions as well as to identify are the used presence to measure of the transferred sequence gene in divergence. a large enough The species PI cri- terionsample. is The based PD criterion on the is based incongruen on the presencece between of a given sequencethe topologies in only a subset of the of species phylogenetic across a phylogenetic tree of tree.the Thespecies presence of a sequence thus shared by phylogenetically distant species, albeit not by more closely related taxa, could suggest and that of the horizontally transferred genes. This requires sequence information for a large phy- the occurrence of an HGT. This third criterion must, however, be taken with caution since patchy distribution in phylogenies logeneticmay also be panel, caused by as gene well losses. as to Both identify PI and PD the criteria presence require access of the to genomictransferred information gene on in a phylogenetically a large enough relevant species sample. The PD criterion
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