The evolution of land plants: a perspective from horizontal gene transfer

Qia Wang, Hang Sun, Jinling Huang

Abstract


Recent studies suggest that horizontal gene transfer (HGT) played a significant role in the evolution of eukaryotic lineages. We here review the mechanisms of HGT in plants and the importance of HGT in land plant evolution. In particular, we discuss the role of HGT in plant colonization of land, phototropic response, C4 photosynthesis, and mitochondrial genome evolution.

Keywords


mechanisms of HGT; plant evolution; mitochondrial genome; adaptation

Full Text:

PDF

References


Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000;405(6784):299–304. http://dx.doi.org/10.1038/35012500

Gogarten JP, Doolittle WF, Lawrence JG. Prokaryotic evolution in light of gene transfer. Mol Biol Evol. 2002;19(12):2226–2238.

Andersson JO. Lateral gene transfer in eukaryotes. Cell Mol Life Sci. 2005;62(11):1182–1197. http://dx.doi.org/10.1007/s00018-005-4539-z

Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 2008;9(8):605–618. http://dx.doi.org/10.1038/nrg2386

Andersson JO. Gene transfer and diversification of microbial eukaryotes. Annu Rev Microbiol. 2009;63:177–193. http://dx.doi.org/10.1146/annurev.micro.091208.073203

Richardson AO, Palmer JD. Horizontal gene transfer in plants. J Exp Bot. 2006;58(1):1–9. http://dx.doi.org/10.1093/jxb/erl148

Huang J. Horizontal gene transfer in eukaryotes: the weak-link model. Bioessays. 2013;35(10):868–875. http://dx.doi.org/10.1002/bies.201300007

Dunning Hotopp JC. Horizontal gene transfer between bacteria and animals. Trends Genet. 2011;27(4):157–163. http://dx.doi.org/10.1016/j.tig.2011.01.005

Boto L. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc Biol Sci. 2014;281(1777):20132450. http://dx.doi.org/10.1098/rspb.2013.2450

Gogarten JP, Townsend JP. Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol. 2005;3(9):679–687. http://dx.doi.org/10.1038/nrmicro1204

Huang J, Gogarten JP. Concerted gene recruitment in early plant evolution. Genome Biol. 2008;9(7):R109. http://dx.doi.org/10.1186/gb-2008-9-7-r109

Selosse MA, Albert B, Godelle B. Reducing the genome size of organelles favours gene transfer to the nucleus. Trends Ecol Evol. 2001;16(3):135–141. http://dx.doi.org/10.1016/S0169-5347(00)02084-X

Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 2004;5(2):123–135. http://dx.doi.org/10.1038/nrg1271

Kleine T, Maier UG, Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol. 2009;60(1):115–138. http://dx.doi.org/10.1146/annurev.arplant.043008.092119

Kurland CG, Canback B, Berg OG. Horizontal gene transfer: a critical view. Proc Natl Acad Sci USA. 2003;100(17):9658–9662. http://dx.doi.org/10.1073/pnas.1632870100

Bock R. The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci. 2010;15(1):11–22. http://dx.doi.org/10.1016/j.tplants.2009.10.001

Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA. 2004;101(51):17747–17752. http://dx.doi.org/10.1073/pnas.0408336102

Zhang D, Qi J, Yue J, Huang J, Sun T, Li S, et al. Root parasitic plant Orobanche aegyptiaca and shoot parasitic plant Cuscuta australis obtained Brassicaceae-specific strictosidine synthase-like genes by horizontal gene transfer. BMC Plant Biol. 2014;14(1):19. http://dx.doi.org/10.1186/1471-2229-14-19

Davis CC, Wurdack KJ. Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science. 2004;305(5684):676–678. http://dx.doi.org/10.1126/science.1100671

Xi Z, Bradley RK, Wurdack KJ, Wong K, Sugumaran M, Bomblies K, et al. Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genomics. 2012;13:227. http://dx.doi.org/10.1186/1471-2164-13-227

Xi Z, Wang Y, Bradley RK, Sugumaran M, Marx CJ, Rest JS, et al. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLoS Genet. 2013;9(2):e1003265. http://dx.doi.org/10.1371/journal.pgen.1003265

Mower JP, Stefanović S, Young GJ, Palmer JD. Plant genetics: gene transfer from parasitic to host plants. Nature. 2004;432(7014):165–166. http://dx.doi.org/10.1038/432165b

Li X, Zhang TC, Qiao Q, Ren Z, Zhao J, Yonezawa T, et al. Complete chloroplast genome sequence of holoparasite Cistanche deserticola (Orobanchaceae) reveals gene loss and horizontal gene transfer from its host Haloxylon ammodendron (Chenopodiaceae). PLoS ONE. 2013;8(3):e58747. http://dx.doi.org/10.1371/journal.pone.0058747

Sanchez-Puerta MV, Cho Y, Mower JP, Alverson AJ, Palmer JD. Frequent, phylogenetically local horizontal transfer of the cox1 group I intron in flowering plant mitochondria. Mol Biol Evol. 2008;25(8):1762–1777. http://dx.doi.org/10.1093/molbev/msn129

Christin PA, Edwards EJ, Besnard G, Boxall SF, Gregory R, Kellogg EA, et al. Adaptive evolution of C4 photosynthesis through recurrent lateral gene transfer. Curr Biol. 2012;22(5):445–449. http://dx.doi.org/10.1016/j.cub.2012.01.054

Svab Z, Maliga P. Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc Natl Acad Sci USA. 2007;104(17):7003–7008. http://dx.doi.org/10.1073/pnas.0700063104

Diao X, Freeling M, Lisch D. Horizontal transfer of a plant transposon. PLoS Biol. 2006;4(1):e5. http://dx.doi.org/10.1371/journal.pbio.0040005

Vallenback P, Jaarola M, Ghatnekar L, Bengtsson BO. Origin and timing of the horizontal transfer of a PgiC gene from Poa to Festuca ovina. Mol Phylogenet Evol. 2008;46(3):890–896. http://dx.doi.org/10.1016/j.ympev.2007.11.031

Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, et al. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science. 2013;342(6165):1468–1473. http://dx.doi.org/10.1126/science.1246275

Park JM, Manen JF, Schneeweiss GM. Horizontal gene transfer of a plastid gene in the non-photosynthetic flowering plants Orobanche and Phelipanche (Orobanchaceae). Mol Phylogenet Evol. 2007;43(3):974–985. http://dx.doi.org/10.1016/j.ympev.2006.10.011

Sanderson MJ, Thorne JL, Wikström N, Bremer K. Molecular evidence on plant divergence times. Am J Bot. 2004;91(10):1656–1665. http://dx.doi.org/10.3732/ajb.91.10.1656

Emiliani G, Fondi M, Fani R, Gribaldo S. A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol Direct. 2009;4:7. http://dx.doi.org/10.1186/1745-6150-4-7

Yue J, Hu X, Sun H, Yang Y, Huang J. Widespread impact of horizontal gene transfer on plant colonization of land. Nat Commun. 2012;3:1152. http://dx.doi.org/10.1038/ncomms2148

Yue J, Hu X, Huang J. Horizontal gene transfer in the innovation and adaptation of land plants. Plant Signal Behav. 2013;8(5). http://dx.doi.org/10.4161/psb.24130

Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L. The phenylpropanoid pathway and plant defence – a genomics perspective. Mol Plant Pathol. 2002;3(5):371–390. http://dx.doi.org/10.1046/j.1364-3703.2002.00131.x

Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7(7):1085–1097. http://dx.doi.org/10.1105/tpc.7.7.1085

Yue J, Hu X, Huang J. Origin of plant auxin biosynthesis. Trends Plant Sci. 2014;19(12):764–770. http://dx.doi.org/10.1016/j.tplants.2014.07.004

Ligrone R, Duckett JG, Renzaglia KS. Major transitions in the evolution of early land plants: a bryological perspective. Ann Bot. 2012;109(5):851–871. http://dx.doi.org/10.1093/aob/mcs017

Jun JH, Ha CM, Nam HG. Involvement of the VEP1 gene in vascular strand development in Arabidopsis thaliana. Plant Cell Physiol. 2002;43(3):323–330. http://dx.doi.org/10.1093/pcp/pcf042

Yang Z, Zhou Y, Huang J, Hu Y, Zhang E, Xie Z, et al. Ancient horizontal transfer of transaldolase-like protein gene and its role in plant vascular development. New Phytol. 2014 (in press). http://dx.doi.org/10.1111/nph.13183

Cai C, Ouyang S, Wang Y, Fang Z, Rong J, Geng L, et al. An Early Silurian vascular plant. Nature. 1996;379(6566):592–592. http://dx.doi.org/10.1038/379592a0

Möglich A, Yang X, Ayers RA, Moffat K. Structure and function of plant photoreceptors. Annu Rev Plant Biol. 2010;61:21–47. http://dx.doi.org/10.1146/annurev-arplant-042809-112259

Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, et al. Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature. 2003;421(6920):287–290. http://dx.doi.org/10.1038/nature01310

Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R. Ferns diversified in the shadow of angiosperms. Nature. 2004;428(6982):553–557. http://dx.doi.org/10.1038/nature02361

Schuettpelz E, Pryer KM. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc Natl Acad Sci USA. 2009;106(27):11200–11205. http://dx.doi.org/10.1073/pnas.0811136106

Li FW, Villarreal JC, Kelly S, Rothfels CJ, Melkonian M, Frangedakis E, et al. Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. Proc Natl Acad Sci USA. 2014;111(18):6672–6677. http://dx.doi.org/10.1073/pnas.1319929111

Osborne CP, Beerling DJ. Nature’s green revolution: the remarkable evolutionary rise of C4 plants. Philos Trans R Soc Lond B Biol Sci. 2006;361(1465):173–194. http://dx.doi.org/10.1098/rstb.2005.1737

Ibrahim DG, Burke T, Ripley BS, Osborne CP. A molecular phylogeny of the genus Alloteropsis (Panicoideae, Poaceae) suggests an evolutionary reversion from C4 to C3 photosynthesis. Ann Bot. 2009;103(1):127–136. http://dx.doi.org/10.1093/aob/mcn204

Christin PA, Freckleton RP, Osborne CP. Can phylogenetics identify C4 origins and reversals? Trends Ecol Evol. 2010;25(7):403–409. http://dx.doi.org/10.1016/j.tree.2010.04.007

Rice DW, Palmer JD. An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol. 2006;4:31. http://dx.doi.org/10.1186/1741-7007-4-31

Moszczynski K, Mackiewicz P, Bodyl A. Evidence for horizontal gene transfer from bacteroidetes bacteria to dinoflagellate minicircles. Mol Biol Evol. 2012;29(3):887–892. http://dx.doi.org/10.1093/molbev/msr276

Bergthorsson U, Adams KL, Thomason B, Palmer JD. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature. 2003;424(6945):197–201. http://dx.doi.org/10.1038/nature01743

Mower JP, Stefanović S, Hao W, Gummow JS, Jain K, Ahmed D, et al. Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol. 2010;8(1):150. http://dx.doi.org/10.1186/1741-7007-8-150

Soltis PS, Soltis DE. Angiosperm phylogeny: a framework for studies of genome evolution. In: Greilhuber J, Dolezel J, Wendel JF, editors. Plant genome diversity. Vienna: Springer; 2013. p. 1–11. (vol 2). http://dx.doi.org/10.1007/978-3-7091-1160-4_1

Hao W, Palmer JD. Fine-scale mergers of chloroplast and mitochondrial genes create functional, transcompartmentally chimeric mitochondrial genes. Proc Natl Acad Sci USA. 2009;106(39):16728–16733. http://dx.doi.org/10.1073/pnas.0908766106

Hao W, Richardson AO, Zheng Y, Palmer JD. Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion. Proc Natl Acad Sci USA. 2010;107(50):21576–21581. http://dx.doi.org/10.1073/pnas.1016295107

Maumus F, Epert A, Nogué F, Blanc G. Plant genomes enclose footprints of past infections by giant virus relatives. Nat Commun. 2014;5:4268. http://dx.doi.org/10.1038/ncomms5268

Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ. Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell. 2009;21(7):1897–1911. http://dx.doi.org/10.1105/tpc.109.065805

Won H, Renner SS. Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA. 2003;100(19):10824–10829. http://dx.doi.org/10.1073/pnas.1833775100

Yoshida S, Maruyama S, Nozaki H, Shirasu K. Horizontal gene transfer by the parasitic plant Striga hermonthica. Science. 2010;328(5982):1128–1128. http://dx.doi.org/10.1126/science.1187145

Intrieri MC, Buiatti M. The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Mol Phylogenet Evol. 2001;20(1):100–110. http://dx.doi.org/10.1006/mpev.2001.0927

Nickrent DL, Blarer A, Qiu YL, Vidal-Russell R, Anderson FE. Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evol Biol. 2004;4(1):40. http://dx.doi.org/10.1186/1471-2148-4-40

Schönenberger J, Anderberg AA, Sytsma KJ. Molecular phylogenetics and patterns of floral evolution in the Ericales. Int J Plant Sci. 2005;166(2):265–288. http://dx.doi.org/10.1086/427198

Davis CC, Anderson WR, Wurdack KJ. Gene transfer from a parasitic flowering plant to a fern. Proc Biol Sci. 2005;272(1578):2237–2242. http://dx.doi.org/10.1098/rspb.2005.3226