Abstract
Large variations in genome size are observed in angiosperms as a result of whole-genome duplications and the balance between amplification and deletion of repetitive DNA, together explaining the observed variation in plant genome size. In the genus Nicotiana, there are 42 cytogenetically diploid species that have been classified into eight sections. There are also six allopolyploid Nicotiana sections that have evolved from species in different diploid sections. The phylogenetic relationships among these Nicotiana species, along with recurrent polyploidization events, permits the divergence of repetitive content in both diploid and allopolyploid genomes to be compared through evolutionary time. In this chapter, we review genome size variation in Nicotiana that reveals both genome upsizing and genome downsizing in different polyploid species. We discuss the divergence of specific repetitive elements, including tandemly repeated satellite DNAs, retroelements, and intergenic spacers as well as the sub-repeats contained in 35S rDNA. The lag-phase hypothesis, which describes post-polyploid radiations, is posed as a potentially important mechanism of evolution in Nicotiana section Suaveolentes, the largest polyploid section that consists of over half the current species diversity.
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References
Bejarano ER, Khashoggi A, Witty M, Lichtenstein C (1996) Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proc Natl Acad Sci 93(2):759–764
Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25(12):1523–1530
Borisjuk NV, Davidjuk YM, Kostishin SS, Miroshnichenco GP, Velasco R, Hemleben V, Volkov RA (1997) Structural analysis of rDNA in the genus Nicotiana. Plant Mol Biol 35(5):655–660
Burk LG (1973) Partial self fertility in a theoretical amphiploid progenitor of N. tabacum. J Hered 64(6):348–350
Chase MW, Christenhusz MJ, Conran JG, Dodsworth S, Medeiros de Assis FN, Felix LP, Fay MF (2018) Unexpected diversity of Australian tobacco species (Nicotiana section Suaveolentes, Solanaceae) Curtis’s Bot Mag 35(3):212–227
Chen ZJ, Pikaard CS (1997) Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proc Natl Acad Sci 94(7):3442–3447
Clarkson JJ, Dodsworth S, Chase MW (2017) Time-calibrated phylogenetic trees establish a lag between polyploidisation and diversification in Nicotiana (Solanaceae). Plant Syst Evol 303:1001–1012
Clarkson JJ, Kelly LJ, Leitch AR, Knapp S, Chase MW (2010) Nuclear glutamine synthetase evolution in Nicotiana: phylogenetics and the origins of allotetraploid and homoploid (diploid) hybrids. Mol Phylogenet Evol 55(1):99–112
Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AR, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Mol Phylogenet Evol 33(1):75–90
Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168(1):241–252
Dadejová M, Lim KY, Soucková-Skalická K, Matyášek R, Grandbastien M-A, Leitch A, Kovařík A (2007) Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytol 174(3):658–668
Dodsworth S, Chase MW, Leitch AR (2016) Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? Bot J Linn Soc 180(1):1–5
Dodsworth S, Jang T-S, Struebig M, Chase MW, Weiss-Schneeweiss H, Leitch AR (2017) Genome-wide repeat dynamics reflect phylogenetic distance in closely related allotetraploid Nicotiana (Solanaceae). Plant Syst Evol 303(8):1013–1020
Dvořáčková M, Fojtová M, Fajkus J (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J 83(1):18–37
El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 5(5):954–965
Fajkus J, Kovařík A, mKrálovics R, Bezděk M (1995a) Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet MGG 247(5):633–638
Fajkus J, Královics R, Kovařík A, Fajkusová L (1995b) The telomeric sequence is directly attached to the HRS60 subtelomeric tandem repeat in tobacco chromosomes. FEBS Lett 364(1):33–35
Fulnec̆ek J, Lim KY, Leitch AR, Kovar̆ík A, Matyás̆ek R (2002) Evolution and structure of 5S rDNA loci in allotetraploid Nicotiana tabacum and its putative parental species. Heredity 88:19–25
Gazdová B, Široký J, Fajkus J, Brzobohatý B, Kenton A, Parokonny A, Heslop-Harrison JS, Palme K, Bezděk M (1995) Characterization of a new family of tobacco highly repetitive DNA, GRS, specific for the Nicotiana tomentosiformis genomic component. Chromosom Res 3(4):245–254
Gill BS, Friebe B (2013) Nucleocytoplasmic interaction hypothesis of genome evolution and speciation in polyploid plants revisited: polyploid species-specific chromosomal polymorphisms in wheat. In: Chen AJ, Birchler JA (eds) Polyploid and hybrid genomics, pp 213–221
Gregor W, Mette MF, Staginnus C, Matzke MA, Matzke AJM (2004) A distinct endogenous pararetrovirus family in Nicotiana tomentosiformis, a diploid progenitor of polyploid tobacco. Plant Physiol 134(3):1191–1199
Greilhuber J, Leitch IJ (2013) Genome size and the phenotype. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF (eds) Plant genome diversity, vol 2, Physical structure, behaviour and evolution of plant genomes. Springer, Wien, pp 323–344
Guignard MS, Nichols RA, Knell RJ, Macdonald A, Romila C-A, Trimmer M, Leitch IJ, Leitch AR (2016) Genome size and ploidy influence angiosperm species’ biomass under nitrogen and phosphorus limitation. New Phytol 210:1195–1206
Horakova M, Fajkus J (2000) TAS49-a dispersed repetitive sequence isolated from subtelomeric regions of Nicotiana tomentosiformis chromosomes. Genome 43(2):273–284
Ibarra-Laclette E, Lyons E, Hernandez-Guzman G, Perez-Torres CA, Carretero-Paulet L, Chang T-H, Lan T, Welch AJ, Juarez MJA, Simpson J et al (2013) Architecture and evolution of a minute plant genome. Nature 498(7452):94–98
Kejnovsky E, Hawkins JS, Feschotte C (2012) Plant transposable elements: biology and evolution. In: Wendel JF, Greilhuber J, Doležel J, Leitch IJ (eds) Plant genome diversity, vol 1, Plant genomes, their residents, and their evolutionary dynamics. Springer-Verlag, Wien, pp 17–34
Kelly LJ, Leitch AR, Clarkson JJ, Hunter RB, Knapp S, Chase MW (2010) Intragenic recombination events and evidence for hybrid speciation in Nicotiana (Solanaceae). Mol Biol Evol 27(4):781–799
Kenton A, Parokonny AS, Gleba YY, Bennett MD (1993) Characterization of the Nicotiana tabacum L. genome by molecular cytogenetics. Mol Gen Genet 240(2):159–169
Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53(1):73–82
Koukalova B, Moraes AP, Renny-Byfield S, Matyasek R, Leitch AR, Kovarik A (2010) Fall and rise of satellite repeats in allopolyploids of Nicotiana over c. 5 million years. New Phytol 186(1):148–160
Koukalova B, Reich J, Bezdek M (1990) A BamHI family of tobacco highly repeated DNA—a study about its species-specificity. Biol Plant 32(6):445–449
Kovarik A, Dadejova M, Lim YK, Chase MW, Clarkson JJ, Knapp S, Leitch AR (2008) Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot 101(6):815–823
Kovarik A, Koukalova B, Lim KY, Matyasek R, Lichtenstein CP, Leitch AR, Bezdek M (2000) Comparative analysis of DNA methylation in tobacco heterochromatic sequences. Chromosom Res 8(6):527–541
Kovarik A, Matyasek R, Lim KY, Skalicka K, Koukalova B, Knapp S, Chase M, Leitch AR (2004) Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biol J Linn Soc 82(4):615–625
Kuhrova V, Bezdek M, Vyskot B, Koukalova B, Fajkus J (1991) Isolation and characterization of two middle repetitive DNA sequences of nuclear tobacco genome. Theor Appl Genet 81:740–744
Landis JB, Soltis DE, Li Z, Marx HE, Barker MS, Tank DC, Soltis PS (2018) Impact of whole-genome duplication events on diversification rates in angiosperms. Am J Bot 105(3):348–363
Leitch AR, Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol 194(3):629–646
Leitch AR, Lim KY, Skalicka K, Kovarik A (2006) Nuclear cytoplasmic interaction hypothesis and the role of translocations in Nicotiana allopolyploids. NATO Security through Science Series 319–326
Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Lin Soc 82:651–663
Leitch IJ, Hanson L, Lim KY, Kovarik A, Chase MW, Clarkson JJ, Leitch AR (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann Bot 101(6):805–814
Li W, Zhang P, Fellers JP, Friebe B, Gill BS (2004) Sequence composition, organization, and evolution of the core Triticeae genome. Plant J 40(4):500–511
Lim KY, Kovarik A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR (2000a) Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109(3):161–172
Lim KY, Kovarik A, Matyasek R, Chase MW, Clarkson JJ, Grandbastien MA, Leitch AR (2007) Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175(4):756–763
Lim KY, Kovarik A, Matyasek R, Chase MW, Knapp S, McCarthy E, Clarkson JJ, Leitch AR (2006) Comparative genomics and repetitive sequence divergence in the species of diploid Nicotiana section Alatae. Plant J 48(6):907–919
Lim KY, Matyasek R, Kovarik A, Fulnecek J, Leitch AR (2005) Molecular cytogenetics and tandem repeat sequence evolution in the allopolyploid Nicotiana rustica compared with diploid progenitors N. paniculata and N. undulata. Cytogenet Genome Res 109(1–3):298–309
Lim KY, Matyasek R, Kovarik A, Leitch AR (2004a) Genome evolution in allotetraploid Nicotiana. Biol J Lin Soc 82(4):599–606
Lim KY, Matyasek R, Lichtenstein CP, Leitch AR (2000b) Molecular cytogenetic analyses and phylogenetic studies in the Nicotiana section Tomentosae. Chromosoma 109(4):245–258
Lim KY, Skalicka K, Koukalova B, Volkov RA, Matyasek R, Hemleben V, Leitch AR, Kovarik A (2004b) Dynamic changes in the distribution of a satellite homologous to intergenic 26-18S rDNA spacer in the evolution of Nicotiana. Genetics 166(4):1935–1946
Lunerová J, Renny-Byfield S, Matyášek R, Leitch AR, Kovařík A (2017) Concerted evolution rapidly eliminates sequence variation in rDNA coding regions but not in intergenic spacers in Nicotiana tabacum allotetraploid. Plant Syst Evol 303(8):1043–1060
Ma JX, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14(5):860–869
Matyasek R, Fulnecek J, Leitch AR, Kovarik A (2011) Analysis of two abundant, highly related satellites in the allotetraploid Nicotiana arentsii using double-strand conformation polymorphism analysis and sequencing. New Phytol 192(3):747–759
Matyasek R, Fulnecek J, Y Lim K, Leitch A, Kovarik A (2002) Evolution of 5S rDNA unit arrays in the plant genus Nicotiana (Solanaceae)
Matyasek R, Gazdová B, Fajkus J, Bezdek M (1997) NTRS, a new family of highly repetitive DNAs specific for the T1 chromosome of tobacco. Chromosoma 106:369–379
Matzke M, Gregor W, Mette MF, Aufsatz W, Kanno T, Jakowitsch J, Matzke AJM (2004) Endogenous pararetroviruses of allotetraploid Nicotiana tabacum and its diploid progenitors, N. sylvestris and N. tomentosiformis. Biol J Linn Soc 82(4):627–638
Mayrose I, Zhan SH, Rothfels CJ, Arrigo N, Barker MS, Rieseberg LH, Otto SP (2015) Methods for studying polyploid diversification and the dead end hypothesis: a reply to Soltis et al. (2014). New Phytol 206(1):27–35
Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, Rieseberg LH, Otto SP (2011) Recently formed polyploid plants diversify at lower rates. Science 333(6047):1257
McClintock B (1984) The significance of responses of the genome to challenge. Science 226(4676):792–801
Melayah D, Lim KY, Bonnivard B, Chalhoub B, Dorlac de Borne F, Mhiri C, Leitch AR, Grandbastien MA (2004) Distribution of the Tnt1 retrotransposon family in the amphidiploid tobacco (Nicotiana tabacum) and its wild Nicotiana relatives. Biol J Linn Soc 82:639–649
Mhiri C, Morel J-B, Vernhettes S, Casacuberta JM, Lucas H, Grandbastien M-A (1997) The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol 33(2):257–266
Mhiri C, Parisod C, Daniel J, Petit M, Lim KY, Dorlhac de Borne F, Kovarik A, Leitch AR, Grandbastien M-A (2019) Parental transposable element loads influence their dynamics in young Nicotiana hybrids and allotetraploids. New Phytol 221(3):1619–1633
Moscone EA, Matzke MA, Matzke AJ (1996) The use of combined FISH/GISH in conjunction with DAPI counterstaining to identify chromosomes containing transgene inserts in amphidiploid tobacco. Chromosoma 105(5):231–236
Murad L, Bielawski JP, Matyasek R, Kovarik A, Nichols RA, Leitch AR, Lichtenstein CP (2004) The origin and evolution of geminivirus-related DNA sequences in Nicotiana. Heredity 92(4):352
Murad L, Lim KY, Christopodulou V, Matyasek R, Lichtenstein CP, Kovarik A, Leitch AR (2002) The origin of tobacco’s T genome is traced to a particular lineage within Nicotiana tomentosiformis (Solanaceae). Am J Bot 89(6):921–928
Nagaki K, Shibata F, Suzuki G, Kanatani A, Ozaki S, Hironaka A, Kashihara K, Murata M (2011) Coexistence of NtCENH3 and two retrotransposons in tobacco centromeres. Chromosom Res 19(5):591–605
Neumann P, Novák P, Hoštáková N, Macas J (2019) Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mobile DNA 10(1):1
Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11(1):378
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29(6):792–793
Pellicer J, Fay MF, Leitch IJ (2010) The largest eukaryotic genome of them all? Bot J Linn Soc 164(1):10–15
Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ (2018) Genome size diversity and its impact on the evolution of land plants. Genes 9(2):88
Petit M, Guidat C, Daniel J, Denis E, Montoriol E, Bui QT, Lim KY, Kovarik A, Leitch AR, Grandbastien MA et al (2010) Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186(1):135–147
Petit M, Lim K, Julio E, Poncet C, de Borne Dorlhac, Fo Kovarik A, Leitch AR, Grandbastien M-Al, Mhiri C (2007) Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (Nicotiana tabacum). Mol Genet Genomics 278(1):1–15
Renny-Byfield S, Chester M, Kovařík A, Le Comber SC, Grandbastien M-A, Deloger M, Nichols RA, Macas J, Novák P, Chase MW et al (2011) Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol Biol Evol 28(10):2843–2854
Renny-Byfield S, Kovarik A, Chester M, Nichols RA, Macas J, Novak P, Leitch AR (2012) Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS ONE 7(5):e36963
Renny-Byfield S, Kovarik A, Kelly LJ, Macas J, Novak P, Chase MW, Nichols RA, Pancholi MR, Grandbastien MA, Leitch AR (2013) Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. Plant J 74(5):829–839
Särkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13(1):214
Schiavinato M, Marcet‐Houben M, Dohm JC, Gabaldón T, Himmelbauer H (2020) Parental origin of the allotetraploid tobacco. Plant J
Schranz EM, Mohammadin S, Edger PP (2012) Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Curr Opin Plant Biol 15(2):147–153
Shibata F, Nagaki K, Yokota E, Murata M (2013) Tobacco karyotyping by accurate centromere identification and novel repetitive DNA localization. Chromosom Res 21(4):375–381
Skalicka K, Lim KY, Matyasek R, Koukalova B, Leitch AR, Kovarik A (2003) Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. Am J Bot 90(7):988–996
Skalicka K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A (2005) Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytol 166(1):291–303
Šmarda P, Hejcman M, Březinová A, Horová L, Steigerová H, Zedek F, Bureš P, Hejcmanová P, Schellberg J (2013) Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilization experiment. New Phytol 200:911–921
Soltis DE, Segovia-Salcedo MC, Jordon-Thaden I, Majure L, Miles NM, Mavrodiev EV, Mei W, Cortez MB, Soltis PS, Gitzendanner MA (2014) Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytol 202(4):1105–1117
Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Natl Acad Sci (USA) 97(13):7051–7057
Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE, Hinchliff CE, Brown JW, Sessa EB, Harmon LJ (2015) Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol 207:454–467
Volkov RA, Borisjuk NV, Panchuk II, Schweizer D, Hemleben V (1999) Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol Biol Evol 16(3):311–320
Wendel JF (2015) The wondrous cycles of polyploidy in plants. Am J Bot 102(11):1753–1756
Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci (USA) 106(33):13875–13879
Xu S, Brockmöller T, Navarro-Quezada A, Kuhl H, Gase K, Ling Z, Zhou W, Kreitzer C, Stanke M, Tang H et al (2017) Wild tobacco genomes reveal the evolution of nicotine biosynthesis. Proc Natl Acad Sci 114(23):6133–6138
Yant L, Hollister Jesse D, Wright Kevin M, Arnold Brian J, Higgins James D, Franklin FChris H, Bomblies K (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol 23(21):2151–2156
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Dodsworth, S., Kovarik, A., Grandbastien, MA., Leitch, I.J., Leitch, A.R. (2020). Repetitive DNA Dynamics and Polyploidization in the Genus Nicotiana (Solanaceae). In: Ivanov, N.V., Sierro, N., Peitsch, M.C. (eds) The Tobacco Plant Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-29493-9_7
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