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Horizontal Gene Transfer Involving Chloroplasts International Journal of Molecular Sciences Review Horizontal Gene Transfer Involving Chloroplasts Ewa Filip 1,2,* and Lidia Skuza 1,2 1 Institute of Biology, University of Szczecin, 13 W ˛aska,71-415 Szczecin, Poland; [email protected] 2 The Centre for Molecular Biology and Biotechnology, University of Szczecin, 13 W ˛aska, 71-415 Szczecin, Poland * Correspondence: ewa.fi[email protected] Abstract: Horizontal gene transfer (HGT)- is defined as the acquisition of genetic material from another organism. However, recent findings indicate a possible role of HGT in the acquisition of traits with adaptive significance, suggesting that HGT is an important driving force in the evolution of eukaryotes as well as prokaryotes. It has been noted that, in eukaryotes, HGT is more prevalent than originally thought. Mitochondria and chloroplasts lost a large number of genes after their respective endosymbiotic events occurred. Even after this major content loss, organelle genomes still continue to lose their own genes. Many of these are subsequently acquired by intracellular gene transfer from the original plastid. The aim of our review was to elucidate the role of chloroplasts in the transfer of genes. This review also explores gene transfer involving mitochondrial and nuclear genomes, though recent studies indicate that chloroplast genomes are far more active in HGT as compared to these other two DNA-containing cellular compartments. Keywords: plants; cpDNA; HGT; chloroplast genes; endophytes 1. Introduction Citation: Filip, E.; Skuza, L. Horizontal gene transfer (HGT), also called lateral gene transfer (LGT), is the process Horizontal Gene Transfer Involving of transferring genetic material between organisms by routes other than parent-offspring Chloroplasts. Int. J. Mol. Sci. 2021, 22, (vertical gene transfer—VGT). HGT can involve the transfer of genetic material from one 4484. https://doi.org/10.3390/ cell to another: between different bacterial species by processes of conjugation, transduc- ijms22094484 tion, and transformation; between different single-celled organisms, e.g., bacteria and yeasts; or between even more distantly related organisms, e.g., bacteria and insects, fungi Academic Editor: Koichi Kobayashi and animals, or plants and fungi. In 1984, Syvanen introduced and gradually developed the concept of HGT as interspecies gene flow [1,2]. The phenomenon was first discovered Received: 26 February 2021 in 1951 in Klebs-Löffler bacillus (Corynebacterium diphtheriae). It was observed that the gene Accepted: 23 April 2021 Published: 25 April 2021 responsible for pathogenicity, tox, was of viral origin and could transfer from pathogenic to non-pathogenic bacteria. In 1959, it was shown that bacterial genes responsible for Publisher’s Note: MDPI stays neutral antibiotic resistance could also be transferred via this route. HGT has further been shown with regard to jurisdictional claims in to have a significant role in the evolution of eukaryotes. Above all, the role of this pro- published maps and institutional affil- cess in protists is to be highlighted. HGT can be considered a universal phenomenon iations. observed in the genomes of bacteria, fungi, plants, or animals [1,2]. HGT is commonplace in prokaryotes [3,4] as demonstrated by studies typing approximately 81% of genes in which transfer was noted [5]. In recent years, the readability of eukaryotic genomes in next generation sequencing (NGS) studies has facilitated the characterization of the occurrence and mechanism of HGT in eukaryotes [6]. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. Moreover, data on the entire genomes of prokaryotes revealed the presence of HGT This article is an open access article between distant species [7,8]. Extensive research on the participation of HGT in prokaryotic distributed under the terms and evolution (e.g., archaea and bacteria) has shown a possible mechanism to facilitate the conditions of the Creative Commons acquisition of new features [9]. However, this phenomenon has been speculated to be rare Attribution (CC BY) license (https:// in eukaryotes [10,11]. creativecommons.org/licenses/by/ Transmission and integration of transferred genes can provide several beneficial fea- 4.0/). tures, including prokaryotic adaptation during environmental changes [12,13], acquisition Int. J. Mol. Sci. 2021, 22, 4484. https://doi.org/10.3390/ijms22094484 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 16 Transmission and integration of transferred genes can provide several beneficial features, including prokaryotic adaptation during environmental changes [12,13], Int. J. Mol. Sci. 2021, 22, 4484 2 of 16 acquisition of new features/functionalities [14], and evolutionary adaptation in eukaryotes [15,16]. Most cases revealed one transfer of one gene in one species, but recent findings reported a case of massive transfer of at least tens, and probably hundreds, of foreignof new mitochondrial features/functionalities genes in Amborella [14], and trichopoda evolutionary. adaptation in eukaryotes [15,16]. MostThere cases are revealedalso other one mechanisms, transfer of onee.g., gene intracellular in one species, transfer but involving recent findings cell organelles, reported a suchcase as of the massive nucleus, transfer the of mitochondria, at least tens, and an probablyd the chloroplasts hundreds, of (intracellular foreign mitochondrial gene transfer—IGT)genes in Amborella [17], or trichopoda the transfer. of genetic material to a different location in the genomeThere of the are same also organism other mechanisms, (intragenomic e.g., transfer intracellular or transposition) transfer involving (Figure cell 1). organelles, Given thesuch endosymbiotic as the nucleus, origin the of mitochondria, mitochondria and and the chloroplasts, chloroplasts many (intracellular genes of gene eubacterial transfer— originIGT) migrated [17], or the from transfer these of geneticorganelles material to the to anucleus different via location IGT inas thewell genome as horizontal of the same transfer.organism Many (intragenomic recorded transfers transfer oroccurred transposition) relatively (Figure recently1). Given during the endosymbioticevolutionary historyorigin and of mitochondriawere limited to and a single chloroplasts, recipient, many or to genes a small of eubacterialnumber of originspecies migrated within the from genus.these However, organelles while to the the nucleus IGT rate via IGThas asdro wellpped as horizontalsignificantly transfer. since the Many appearance recorded trans-of eukaryotes,fers occurred it remains relatively a common recently process during evolutionarycharacteristic history of the andevolution were limitedof the tonuclear a single andrecipient, organelle or genomes to a small in number plants [18–23]. of species Am withinong the the three genus. types However, of genomes while in the a IGTplant rate cell,has there dropped are six significantly possible directions since the for appearance gene transfer. of eukaryotes, The most it prominent remains a common are from process the organellecharacteristic (mitochondrial) of the evolution genome ofto thethe nuclearnuclear andgenome organelle [22,23], genomes and from in plantsthe nuclear[18–23 ]. Among the three types of genomes in a plant cell, there are six possible directions for gene and plastid (chloroplast) genome to the mitochondrial genome [18]. Intracellular transfer transfer. The most prominent are from the organelle (mitochondrial) genome to the nuclear to the highly compact plastid genome appears to be quite rare; however, it is being genome [22,23], and from the nuclear and plastid (chloroplast) genome to the mitochon- reported increasingly frequently. More information can be found in the literature drial genome [18]. Intracellular transfer to the highly compact plastid genome appears indicating numerous cases of nuclear-to-mitochondrial IGT transfer than from to be quite rare; however, it is being reported increasingly frequently. More information chloroplast to mitochondrion or to cell nucleus [18]. can be found in the literature indicating numerous cases of nuclear-to-mitochondrial IGT transfer than from chloroplast to mitochondrion or to cell nucleus [18]. Figure 1. Intracellular gene transfer (IGT) and horizontal gene transfer (HGT) between two plant Figurespecies. 1. Intracellular Intergenomic gene gene transfer transfer (IGT) represent and horizo linesntal in the gene cell transfer from the (HGT) left. Solid between blue, two green, plant and red species.lines Intergenomic depict the number gene oftransfer reported represent HGT events lines in between the cell cellfrom compartments. the left. Solid Thickerblue, green, lines and indicate redmore lines frequentdepict the events number than of thinner reported lines. HGT Dashed events grey between lines cell depict comp putativeartments. transfers. Thicker cp: lines chloroplast; indicatemt: mitochondria; more frequent nu: events nucleus. than thinner lines. Dashed grey lines depict putative transfers. cp: chloroplast; mt: mitochondria; nu: nucleus. Recent studies have shown that plant mitochondrial genomes are more likely to transferRecent DNA studies to the have other shown two cellular that plant compartments mitochondrial mentioned genomes above. are The more ever-increasing likely to transfernumber DNA of plant to mitochondrialthe other two genomes cellular (mtDNA) compartments sequenced [mentioned20,24–27] reveals above. the The extent ever-increasingof transfer from
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