Abstract
Horizontal gene transfer (HGT) describes the transmission of genetic material across species boundaries. HGT often occurs in microbic and eukaryotic genomes. However, the pathways by which HGTs occur in multicellular eukaryotes, especially in plants, are not well understood. We systematically summarized more than ten possible pathways for HGT. The intimate contact which frequently occurs in parasitism, symbiosis, pathogen, epiphyte, entophyte, and grafting interactions could promote HGTs between two species. Besides these direct transfer methods, genes can be exchanged with a vector as a bridge: possible vectors include pollen, fungi, bacteria, viruses, viroids, plasmids, transposons, and insects. HGT, especially when involving horizontal transfer of transposable elements, is recognized as a significant force propelling genomic variation and biological innovation, playing an important functional and evolutionary role in both eukaryotic and prokaryotic genomes. We proposed possible mechanisms by which HGTs can occur, which is useful in understanding the genetic information exchange among distant species or distant cellular components.
Similar content being viewed by others
Abbreviations
- HGT:
-
Horizontal gene transfer
- TE:
-
Transposable elements
References
Andersson JO (2005) Lateral gene transfer in eukaryotes. Cell Mol Life Sci 62(11):1182–1197
Archibald JM, Richards TA (2010) Gene transfer: anything goes in plant mitochondria. BMC Biol 8:147. doi:10.1186/1741-7007-8-147
Bansal AK, Meyer TE (2002) Evolutionary analysis by whole-genome comparisons. J Bacteriol 184(8):2260–2272
Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424(6945):197–201
Bird DM, Scholl EH (2011) Computational and phylogenetic validation of nematode horizontal gene transfer. BMC Biol 9:9. doi:10.1186/1741-7007-9-9
Bock R (2009) The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15(1):11–22
Boissinot S, Novick P, Smith J, Ray D (2010) Independent and parallel lateral transfer of DNA transposons in tetrapod genomes. Gene 449(1–2):85–94
Bonen L (2006) Mitochondrial genes leave home. New Phytol 172(3):379–381
Brennicke A, Grohmann L, Hiesel R, Knoop V, Schuster W (1993) The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Lett 325(1–2):140–145
Broothaerts W, Mitchell HJ, Weir B, Kaines S, Smith LMA, Yang W, Mayer JE, Roa-Rodriguez C, Jefferson RA (2005) Gene transfer to plants by diverse species of bacteria. Nature 433(7026):629–633. doi:10.1038/nature03309
Burger G, Lang BF (2003) Parallels in genome evolution in mitochondria and bacterial symbionts. IUBMB Life 55(4–5):205–212
Capy P, Loreto ELS, Carareto CMA (2008) Revisiting horizontal transfer of transposable elements in Drosophila. Heredity 100(6):545–554
Cullis CA, Vorster BJ, Van Der Vyver C, Kunert KJ (2009) Transfer of genetic material between the chloroplast and nucleus: how is it related to stress in plants? Ann Bot 103(4):625–633. doi:10.1093/Aob/Mcn173
Danchin EGJ, Haegeman A, Jones JT (2011) Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Mol Plant Microbe In 24(8):879–887
Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305(5684):676–678
Davis CC, Anderson WR, Wurdack KJ (2005) Gene transfer from a parasitic flowering plant to a fern. P Roy Soc B-Biol Sci 272(1578):2237–2242
de Wit PJGM, Mehrabi R, Bahkali AH, Abd-Elsalam KA, Moslem M, Ben M'Barek S, Gohari AM, Jashni MK, Stergiopoulos I, Kema GHJ (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. Fems Microbiol Rev 35(3):542–554
Deschavanne P, Mallet LV, Becq J (2010) Whole genome evaluation of horizontal transfers in the pathogenic fungus Aspergillus fumigatus. BMC Genomics 11:171
Diao XM, Freeling M, Lisch D (2006) Horizontal transfer of a plant transposon. Plos Biol 4(1):119–128
Diao YP, Qi YM, Ma YJ, Xia A, Sharakhov I, Chen XG, Biedler J, Ling E, Tu ZJ (2011) Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes. Plos One 6(2):e16743
Feschotte C, Gilbert C, Schaack S, Pace JK, Brindley PJ (2010) A role for host–parasite interactions in the horizontal transfer of transposons across phyla. Nature 464(7293):1347–1350
Finan TM (2002) Evolving insights: symbiosis islands and horizontal gene transfer. J Bacteriol 184(11):2855–2856
Fortune PM, Roulin A, Panaud O (2008) Horizontal transfer of transposable elements in plants. Commun Integr Biol 1(1):74–77
Fournier PE, Moliner C, Raoult D (2009) Evidence of horizontal gene transfer between amoeba and bacteria. Clin Microbiol Infec 15:178–180
Giulotto E, Nergadze SG, Lupotto M, Pellanda P, Santagostino M, Vitelli V (2010) Mitochondrial DNA insertions in the nuclear horse genome. Anim Genet 41:176–185
Gribaldo S, Emiliani G, Fondi M, Fani R (2009) A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol Direct 4(1):1–7
Hotopp JCD (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27(4):157–163
Jiang DH, Liu HQ, Fu YP, Li GQ, Xie JT, Cheng JS, Peng YL, Ghabrial SA, Yi XH (2010) Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol 84(22):11876–11887
Li B, Zhu B, Lou MM, Xie GL, Zhang GQ, Zhou XP, Jin GL (2011) Horizontal gene transfer in silkworm, Bombyx mori. BMC Genomics 12:248
Liang DC, White RG, Waterhouse PM (2012) Gene silencing in Arabidopsis Spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol 159(3):984–1000. doi:10.1104/pp. 112.197129
Liu H, Fu Y, Jiang D, Li G, Xie J, Cheng J, Peng Y, Ghabrial SA, Yi X (2010) Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol 84(22):11876–11887
Loria R, Bukhalid RA, Takeuchi T, Labeda D (2002) Horizontal transfer of the plant virulence gene, nec1, and flanking sequences among genetically distinct Streptomyces strains in the diastatochromogenes cluster. Appl Environ Microb 68(2):738–744
Lucas WJ, Ham LK, Kim JY (2009) Plasmodesmata—bridging the gap between neighboring plant cells. Trends Cell Biol 19(10):495–503. doi:10.1016/j.tcb.2009.07.003
Marienfeld J, Unseld M, Brennicke A (1999) The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci 4:495–502
Mc Ginty SE, Rankin DJ, Brown SP (2011) Horizontal gene transfer and the evolution of bacterial cooperation. Evolution 65(1):21–32
Mohr KI, Tebbe CC (2007) Field study results on the probability and risk of a horizontal gene transfer from transgenic herbicide-resistant oilseed rape pollen to gut bacteria of bees. Appl Microbiol Biotechnol 75(3):573–582
Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978):624–627
Mower JP, Stefanovic S, Young GJ, Palmer JD (2004) Plant genetics—gene transfer from parasitic to host plants. Nature 432(7014):165–166
Mower JP, Stefanovic S, Hao W, Gummow JS, Jain K, Ahmed D, Palmer JD (2010) Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 8:150
Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268(4):434–445
Ogata H, Monier A, Claverie JM (2007) Horizontal gene transfer and nucleotide compositional anomaly in large DNA viruses. BMC Genomics 8:456
Panaud O, Roulin A, Piegu B, Wing RA (2008) Evidence of multiple horizontal transfers of the long terminal repeat retrotransposon RIRE1 within the genus Oryza. Plant J 53(6):950–959
Panaud O, Roulin A, Piegu B, Fortune PM, Sabot F, D'Hont A, Manicacci D (2009) Whole genome surveys of rice, maize and sorghum reveal multiple horizontal transfers of the LTR-retrotransposon Route66 in Poaceae. BMC Evol Biol 9:58
Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, McLeod R, Roberts CW (2006) Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell 5(9):1517–1531. doi:10.1128/Ec.00106-06
Richards TA, Soanes DM, Foster PG, Leonard G, Thomton CR, Talbot NJ (2009) Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21(7):1897–1911
Rokas A, Slot JC (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Current Biol 21(2):134–139
Rolland T, Neuveglise C, Sacerdot C, Dujon B (2009) Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes. Plos One 4(8):e6515
Roney JK, Khatibi PA, Westwood JH (2007) Cross-species translocation of mRNA from host plants into the parasitic plant dodder. Plant Physiol 143(2):1037–1043. doi:10.1104/pp. 106.088369
Schaack S, Choi EJ, Lynch M, Pritham EJ (2010) DNA transposons and the role of recombination in mutation accumulation in Daphnia pulex. Genome Biol 11(4):R46. doi:10.1186/Gb-2010-11-4-R46
Schluter K, Futterer J, Potrykus I (1995) Horizontal gene-transfer from a transgenic potato line to a bacterial pathogen (Erwinia chrysanthemi) occurs—if at all—at an extremely low frequency. Bio-Technol 13(10):1094–1098
Schneeweiss GM, Park JM, Manen JF (2007) Horizontal gene transfer of a plastid gene in the non-photosynthetic flowering plants Orobanche and Phelipanche (Orobanchaceae). Mol Phylogenet Evol 43(3):974–985
Seifert HS, Anderson MT (2011) Opportunity and means: horizontal gene transfer from the human host to a bacterial pathogen. Mbio 2(1):e00005–e00011. doi:10.1128/mBio.00005-11
Shirasu K, Yoshida S, Maruyama S, Nozaki H (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328(5982):1128–1128
Silva JC, Loreto EL, Clark JB (2004) Factors that affect the horizontal transfer of transposable elements. Curr Issues Mol Biol 6:57–71
Sommer RJ, Mayer WE, Schuster LN, Bartelmes G, Dieterich C (2011) Horizontal gene transfer of microbial cellulases into nematode genomes is associated with functional assimilation and gene turnover. BMC Evol Biol 11:13. doi:10.1186/1471-2148-11-13
Sormacheva I, Smyshlyaev G, Mayorov V, Blinov A, Novikov A, Novikovaz O (2012) Vertical evolution and horizontal transfer of CR1 non-LTR retrotransposons and Tc1/mariner DNA transposons in Lepidoptera species. Mol Biol Evol 29(12):3685–3702. doi:10.1093/molbev/mss181
Stegemann S, Bock R (2009) Exchange of genetic material between cells in plant tissue grafts. Science 324(5927):649–651
Stegemann S, Keuthe M, Greiner S, Bock R (2012) Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci U S A 109(7):2434–2438. doi:10.1073/pnas.1114076109
Thyssen G, Svab Z, Maliga P (2012) Cell-to-cell movement of plastids in plants. Proc Natl Acad Sci U S A 109(7):2439–2443
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135. doi:10.1038/Nrg1271
Trobridge GD (2009) Foamy virus vectors for gene transfer. Expert Opin Biol Th 9(11):1427–1436
van Elsas JD, Turner S, Bailey MJ (2003) Horizontal gene transfer in the phytosphere. New Phytol 157(3):525–537
Vogel TM, Pontiroli A, Rizzi A, Simonet P, Daffonchio D, Monier JM (2009) Visual evidence of horizontal gene transfer between plants and bacteria in the phytosphere of transplastomic tobacco. Appl Environ Microb 75(10):3314–3322
Wang D, Lloyd AH, Timmis JN (2011) Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants. Proc Natl Acad Sci U S A 109(7):2444–2448
Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9(5):383–395. doi:10.1038/Nrg2348
Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O'Neill SL (2009) An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 26(2):367–374
Zambryski P, Crawford K (2000) Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Bi 16:393–421
Acknowledgments
This work was supported financially by the National Natural Science Foundation of China (code 31260335) and the Research Fund for the Doctoral Program of Higher Education of China (code 20123603120002). A. Mason is supported by an Australian Research Council Discovery Early Career Researcher Award (DE120100668).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gao, C., Ren, X., Mason, A.S. et al. Horizontal gene transfer in plants. Funct Integr Genomics 14, 23–29 (2014). https://doi.org/10.1007/s10142-013-0345-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-013-0345-0