The mechanisms underpinning lateral gene transfer between grasses

Lateral gene transfer (LGT) refers to the transmission of genetic material without sexual reproduction. LGT is widespread in a number plant species, including grasses. But how these genes foreign origin got there presently unknown. In this review, we show that transformation techniques used genetically modify organisms could occur wild and be responsible for frequently observed grass-to-grass LGTs. The distinction between natural evolutionary processes engineering might arbitrary, its validity will further debated as agricultural biotechnology becomes more widely examples “natural engineering” through increase. among species was initially thought restricted prokaryotes, but it has since been reported wide range eukaryotes, plants. Grasses seem particularly prone exchange species. However, mechanism(s) facilitating transfers economically ecologically important group plants are debated. Here, review vector-mediated, direct tissue-to-tissue contact, wide-crossing reproductive contamination mechanisms discuss likelihood each light recent studies. Of particular relevance approaches require minimal human intervention DNA grasses lab mimic wild. These include relatively simple techniques, such pollen tube pathway-mediated transformation, take advantage permeability process introduce alien from third individual into an embryo. This easily mirrored where one lands on stigma another, acting source can ultimately contaminate process. likely prevalent wind pollinated grasses, rates illegitimate pollination high. conclusion, methods requiring paralleled they act mechanism underpinning distantly related grass La transferencia lateral de se refiere la transmisión genético sin reproducción sexual. Se ha demostrado que está muy extendida en varias especies plantas, incluidas las gramíneas. Pero actualmente desconoce cómo han llegado estos origen foráneo. En esta revisión mostramos técnicas transformación utilizadas para modificar genéticamente los organismos podrían ocurrir naturaleza y ser responsables gramínea observados con frecuencia. distinción entre procesos evolutivos naturales ingeniería genética podría arbitraria, su validez seguirá debatiendo medida biotecnología agrícola generalice aumenten ejemplos “ingeniería natural” mediante genes. Le transfert latéral gènes désigne matériel génétique sans reproduction sexuée. Il été démontré le est très répandu chez certaines plantes, compris les graminées. On ignore actuellement comment ces d'origine étrangère sont passés d'une espèce à l'autre. Dans cette revue, nous montrons utilisées pour modifier génétiquement des organismes pourraient produire dans nature et être l'origine transferts latéraux graminées fréquemment observés. processus évolutifs naturels génie pourrait donc vue comme arbitraire. validité susceptible d'être plus débattue au fur mesure biotechnologie agricole répand exemples “génie naturel” par multiplient. by which acquired facilitates exchanges over much broader distances (even prokaryotes eukaryotes) than hybridization introgression. extensively studied both (transformation, conjugation, transduction) consequences well known (Hall al., 2020). rapid spread have drastic adaptive impacts. For example, allows antibiotic resistance plasmid (Ochman 2000). More generally, novel material, encoded proteins may optimized or unique functions. even unlock routes develop phenotypes outside those readily achievable descent with modification alone. evolution specific traits unlikely lineages do not possess required precursors (Blount 2012). potential bypass problem expanding pool beyond boundaries. While existence eukaryotes originally controversial, now question “how much” rather “if” occurs (Van Etten & Bhattacharya, advent high-throughput sequencing advances phylogenomics led ever accumulating LGTs broad eukaryotes. typically detected phylogenetic incongruences tree topologies. some unicellular about 1% predicted were laterally, most them being bacterial (Fan 2020; Matriano 2021). multicellular organisms, unequivocal animals (Bryon 2017; Undheim Jenner, 2021), fungi (Duarte Huynen, 2019; Murphy Szöllősi 2015), (Wickell Li, Among plants, seems especially parasites their hosts, tissue contact via feeding structures haustoria facilitate movements (Vogel 2018; Xi 2012; Yang Yoshida 2019). non-parasitic ferns (Li 2014) numerous members family (Christin Dunning Hibdige 2021; Mahelka 2021, Park Prentice 2015; Vallenback 2008; Wu 2022). transferred functions associated disease resistance, abiotic stress tolerance, photosynthesis Biochemical assays confirmed (Phansopa 2020), population genomics shows rapidly under positive selection (Olofsson Successful requires only acquisition also assimilation germ line so it. any ovules, pollen, embryo would easiest route mirror certain techniques. addition, meristematic cells give rise inflorescences gametes inherited progeny. Unlike animals, germline soma clearly separated many able reproduce vegetatively (Su Individuals clonal populations present high degrees variation them, indicates prevalence somatic variants (Haddadchi 2013; Yu Importantly, new mutations increase frequency during bottlenecks generated stolons rhizomes, becoming fixed subsequent clones (Yu Vegetative growth consider integrated transmitted next generations. Several hypothesized Roulin 2009; Soucy Sun Wickell Likewise, allowing established context hybridization. manuscript, mediate interspecific based experimental systems application LGT. We first suggested entry then briefly chromosomal integration. Our efforts help identify scenarios, demonstrate viable exist, removing obstacle acceptance biologists. Bacterial viral vectors often perceived behind eukaryotic transfers, perhaps because infection cycle (Figure 1). role eukaryote facilitated ubiquitous presence pathogens infect hosts (Feschotte Gilbert, Gilbert Cordaux, 2017). exchanged endogenization, retroviruses insert host genomes complete life (Weiss, 2006). retroviruses, endogenization pervasive variety viruses precise molecular happens known, although retrotransposons involved (Geuking Horie 2010). unidirectional, meaning integrate own genome, using either machinery (retroviruses) retrotransposon/host (Gilbert 2016). Some up 30% entire genome 2017), representing ~30–70 kb overall (Morissette Flamand, Therefore, possible virus acquires initial another part infection. Generalist potentially (Ingwell Bosque-Pérez, thereby passing fragments another. Virus-mediated approximately 1 regions documented real time (Catoni 2018). vector larger passed 400 times (Mahelka Genes found fact, bacteria successful transforming scientists laboratory decades (Horsch 1985). reliant Agrobacterium tumefaciens bacteria, pathogen Rhizobiaceae causes crown gall (Smith Townsend, 1907). A. integrates, expresses set infected plasmid, resulting formation (Hoekema 1984). ability manipulated replace loci encoding desired close relative rhizogenes naturally large (Intrieri Buiatti, 2001; Kyndt Matveeva Otten, Yet reciprocal, no (Wood 2001). thus less complex scenario moved intermediary. Furthermore, (Conner Dommisse, 1992; Lowe 2016), establishing lab-based transformations challenging (Nguyen Other capable unreported. It should noted symbiotic just pathogens, emergence land correlated tolerance soil (Cheng evidence Another arbuscular mycorrhizal fungi, mutualistic symbionts intimate long-term associations roots (Field 2015). Plants share molecules, sugars other nutrients mRNAs Wong-Bajracharya donors recipients (Sun Huang, Although association described yet, cannot rule out support refute involvement missing. There endophytic shown acquire transmit DNA. Epichloë endosymbiotic insect toxin gene, confers (Ambrose 2014), wheat (Wang Plant arthropods At simplest, involve contaminated mouthparts transferring tissues different interest insects directly feed seeds, offer recipient. Hemipterans belonging Lygaeidae commonly referred seed bugs needle-like piercing use extract (Burdfield-Steel Shuker, 2014). generalists, feed. this, Sap pathogens; maize streak leafhopper (Storey, 1924). insect-mediated convoluted incorporated herbivore before subsequently recipient contributes arthropod herbivory (Wybouw pests whitefly (Xia whether unknown, flanking (Dunning know viruses, host, bridge remains unclear. obvious signal vector-mediated moving “third party” temporary erode Olofsson large, makes explain Laterally length Hordeum bogdanii genomes. given lack recipient's unwieldy size, fact bacteria. No parasitic date (Nickrent, still contact. Inosculation spontaneous junction two individuals later continue whole, term generally applied trees. When performed artificially, inosculation named grafting. Grafting breeding applications usually increasing biotic (Melnyk Meyerowitz, Initially, stock (root system) scion (aerial portion plant) conserve integrity. data chloroplast, mitochondrial, nuclear asexually (Fuentes 2014; Gurdon 2016; Stegemann Bock, 2009). Subsequent detailed observation forming grafting revealed small, dedifferentiated chloroplasts cell wall pores (Hertle organelles carried plastid DNA, movement live imaging, ultimate proof monocotyledonous previously impossible due absence vascular cambium, promotes secondary groups (Rasool hypothesis embryonic essential grafting, Reeves al. (2022) developed method monocot embryos grafted several protective coat. Natural mature yet demonstrated. Previous studies investigating distribution producing rhizomes propagating themselves had significant (Hibdige increased mean takes place vegetative reproduction, example root-to-root dense multispecies clumps 2) Alternatively, correlation result reduced efficacy purge neutral deleterious asexual (Muller, 1964). propagate therefore rate retention acquisition. case, if demonstrated, recorded non-rhizomatous discordance infer actually driven rare events highly divergent subfamilies. diverse 11,000 diversified last 100 million years (Huang 2022; Soreng Distantly subfamilies diverged 80 Mya manually crossed obtain partial hybrids oat (Laurie Bennett, 1986; Riera-Lizarazu 1996). cases, rescue recover haploid crosses, yield hybrid low, around 3% all recovered (Riera-Lizarazu chromosomes mother incomplete donor pollen. Often, eliminated days development 1986), sometimes partially fertile, transmitting progenies (Kynast Wide crosses heterospecific tubes, grow extent grasses' styles (Heslop-Harrison, 1982; Lausser 2010; Reger James, 1982). Indeed, closely are, happen (Lausser trend mirrors pattern see amount relatedness, confounded biogeography non-syntenic insertion recipients' coexistence vertically copies argues straightforward recombination occurred transient cohabitation nucleus crosses. occurrence crops, possibly necessity greater taxonomic subfamilies, bridge. appears wide-crosses Reproductive Such effectively transgenic events, parallels requirement vitro culture. focus called repeated intervention. suggests barriers overcome wild, leading Repeated generate rice, aiming agronomic relatives (Liu 1999). chosen classify individual. procedure, emasculated rice cultivated treated same subfamily (Zizania latifolia) ~46 After 48 h, second cultivar 3a). Seedlings inspected very low percentage showed distinctive phenotypes. altered self-pollinated repeatedly recombinant inbred lines, stable. Surprisingly, vast majority cultivar, contained <0.1% genomic Z. latifolia (Shan 2005). Most identified sequences transposable elements (TE), caused rearrangements insertion. A similar study accession mobilization TEs after experiments, (Wu technique search situ (Silva Souza, 2013), cytological introgression, sensitive enough detect small fragments. Whole-genome obtained analyze TE mobilization, employed sequences. Since chromosome-level reference become recently available (Yan 2022), interesting evaluate whole-genome resequencing datasets contain Overall, experiments prove distant promote genome. clear where, when, happen, process, Pollen similarly approach. consists injecting at gynoecium order following nucellus pathway 3b) (Zhou 1979). effectiveness isotope tracing H3 labeled demonstrating heterologous entered (Gong 1988). Cotton transformed protocols specifically Zhang 2009), then, (Ali three pollen-tube technique: microinjection ovary, delivery onto stigma, 2013). exogenous ~0.5–1% seeds transformed. success demonstrates once pistil, deeper layers organ, Remarkably, itself does completely wind-pollinated indiscriminately receive co-occurring Depending compatibility, grains germinate extent. tubes fail point, proportion reach micropyle enter ovule. Once sperm released, succeed, giving (including crosses). when fails, already within ovule, offering opportunities integration segments experimentally 3c). unsuccessful, degenerative style lead tissue. inadvertently ovule transformation. discussed here reason why considered Getting half story, maintained future generations, needs easy part, proven methods. One particle bombardment (Klein 1987), mechanically introduced chance random position. happen. (TEs) major component genomes, comprising >80% (Lee Kim, repetitive overrepresented laterally (El Baidouri Fortune 2008, endogenous repair retrotransposon play mobilizing introgression evident consequence 2005; activated response environmental stresses (Alzohairy (Mirouze Vitte, situations. kind mobile element, “starships,” characterized (Gluck-Thaler Starships giant (>100 cases) containing specific, conserved allow cargo carrier content fungi. Starship investigated our knowledge. If excised exist stable intermediate prolonged period transfer, finally mechanism, stability against exonuclease degradation capacity reinsert extrachromosomal circular (eccDNA) good candidate (Cohen Koo molecules progeny chromosome tethering (Koo minicircles, composed mix sequences, sugar beet (Beta vulgaris) geminivirus BCTIV Fragments chimeric eccDNA, open reading frame present. circles four weeks inoculation, did tested eccDNA replicated Arabidopsis thaliana Nicotiana benthamiana B. vulgaris cells, event mediated eccDNA. To summarize, form (e.g., bombardment) properties mobility influence vector. As reports increase, skepticism waines (van argued well-characterized universal force (Martin, address demand, empirical underpin transfers. Multiple role, standout contamination. Repeated-pollination exact course lineage's remain existing exist. Finally, research reviewed beginning what class hybridization, discrete thought. Hybridization envisaged union sets female male gametes, whereas fraction ~400 kb. categories compared classical cases explicitly rely transformation? transgenesis analogous, artificial. again, culture naturally, case LGTs, point arbitrary. LP supported Environment Research Council (NERC) Standard Grant (NE/V000012/1), PAC funded Royal Society (grant URF\R\180022), LTD NERC Independent Fellowship (NE/T011025/1). thank Katie Greenin-Whitehead her work illustrations. authors declare conflict interest. L.P., P-A.C., L.T.D. literature wrote manuscript. Data sharing applicable article analyzed current study.