Abstract
Nicotiana, a member of the Solanaceae family, is one of the most important research model plants, and of high agricultural and economic value worldwide. To better understand the substantial and rapid research progress with Nicotiana in recent years, its genomics, genetics, and nicotine gene studies are summarized, with useful web links. Several important genetic maps, including a high-density map of N. tabacum consisting of ~2,000 markers published in 2012, provide tools for genetics research. Four whole genome sequences are from allotetraploid species, including N. benthamiana in 2012, and three N. tabacum cultivars (TN90, K326, and BX) in 2014. Three whole genome sequences are from diploids, including progenitors N. sylvestris and N. tomentosiformis in 2013 and N. otophora in 2014. These and additional studies provide numerous insights into genome evolution after polyploidization, including changes in gene composition and transcriptome expression in N. tabacum. The major genes involved in the nicotine biosynthetic pathway have been identified and the genetic basis of the differences in nicotine levels among Nicotiana species has been revealed. In addition, other progress on chloroplast, mitochondrial, and NCBI-registered projects on Nicotiana are discussed. The challenges and prospects for genomic, genetic and application research are addressed. Hence, this review provides important resources and guidance for current and future research and application in Nicotiana.
Similar content being viewed by others
References
Baldwin IT (1988) The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77:378–381
Baldwin IT (1999) Inducible nicotine production in native Nicotiana as an example of phenotypic plasticity. J Chem Ecol 25:3–30
Bennett MD, Leitch IJ (1995) Nuclear DNA amounts in Angiosperms. Ann Botany 76:113–176
Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye C-Y, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012) Reference genome sequence of the model plant Setaria. Nat Biotech 30:555–561
Bindler G, van der Hoeven R, Gunduz I, Plieske J, Ganal M, Rossi L, Gadani F, Donini P (2007) A Microsatellite marker based linkage map of tobacco. Theor Appl Genet 114:341–349
Bindler G, Plieske J, Bakaher N, Gunduz I, Ivanov N, Van der Hoeven R, Ganal M, Donini P (2011) A high density genetic map of tobacco Nicotiana tabacum L.) obtained from large scale microsatellite marker development. Theor Appl Genet 123:219–230
Bombarely A, Edwards K, Sanchez-Tamburrino J, Mueller L (2012a) Deciphering the complex leaf transcriptome of the allotetraploid species Nicotiana tabacum: a phylogenomic perspective. BMC Genom 13:406
Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller L, Martin G (2012b) A Draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25:1523–1530
Bortolotti C, Cordeiro A, Alcazar R, Borrell A, Culianez-Macia FA, Tiburcio AF, Altabella T (2004) Localization of arginine decarboxylase in tobacco plants. Physiol Plant 120:84–92
Buggs RJA, Renny-Byfield S, Chester M, Jordon-Thaden IE, Viccini LF, Chamala S, Leitch AR, Schnable PS, Barbazuk WB, Soltis PS, Soltis DE (2012) Next-generation sequencing and genome evolution in allopolyploids. Am J Bot 99:372–382
Chakrabarti M, Meekins KM, Gavilano LB, Siminszky B (2007) Inactivation of the cytochrome P450 gene CYP82E2 by degenerative mutations was a key event in the evolution of the alkaloid profile of modern tobacco. New Phytol 175:565–574
Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS (2003) Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Ann Botany 92:107–127
Chaudhary B, Flagel L, Stupar RM, Udall JA, Verma N, Springer NM, Wendel JF (2009) Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182:503–517
Chen Z, Ni Z (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays 28:240–252
Chintapakorn Y, Hamill JD (2003) Antisense-mediated down-regulation of putrescine N-methyltransferase activity in transgenic Nicotiana tabacum L. can lead to elevated levels of anatabine at the expense of nicotine. Plant Mol Biol 53:87–105
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 33:75–90
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510
De Sutter V, Vanderhaeghen R, Tilleman S, Lammertyn F, Vanhoutte I, Karimi M, Inze D, Goossens A, Hilson P (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J 44:1065–1076
DeBoer K, Lye J, Aitken C, Su AK, Hamill J (2009) The A622 gene in Nicotiana glauca (tree tobacco): evidence for a functional role in pyridine alkaloid synthesis. Plant Mol Biol 69:299–312
Dewey RE, Xie J (2013) Molecular genetics of alkaloid biosynthesis in Nicotiana tabacum. Phytochemistry 94:10–27
Edger P, Pires JC (2009) Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res 17:699–717
Estep MC, DeBarry JD, Bennetzen JL (2013) The dynamics of LTR retrotransposon accumulation across 25 million years of panicoid grass evolution. Heredity 110:194–204
Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred. II. error probabilities. Genome Res 8:186–194
Feldman M, Levi A, Fahima T, Korol A (2012) Genomic asymmetry in allopolyploid plants: wheat as a model. J Exp Bot 63:5045–5059
Flagel L, Udall J, Nettleton D, Wendel J (2008) Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6:16
Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453
Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant–pathogen interactions. MPMI 21:1015–1026
Goodspeed TH (1954) The genus nicotiana: Origins, relationships and evolution of its species in the light of their distribution, morphology and cytogenetics. Chronica Botanica Company, Waltham
Greuter W (2000) International Code of Botanical Nomenclature: Saint Louis Code : adopted by the Sixteenth International Botanical Congress. Koeltz Scientific Books, St Louis
Heim WG, Sykes KA, Hildreth SB, Sun J, Lu R-H, Jelesko JG (2007) Cloning and characterization of a Nicotiana tabacum methylputrescine oxidase transcript. Phytochemistry 68:454–463
Hibi N, Higashiguchi S, Hashimoto T, Yamada Y (1994) Gene expression in tobacco low-nicotine mutants. Plant cell 6:723–735
Hildreth SB, Gehman EA, Yang H, Lu R-H, Ritesh KC, Harich KC, Yu S, Lin J, Sandoe JL, Okumoto S, Murphy AS, Jelesko JG (2011) Tobacco nicotine uptake permease (NUP1) affects alkaloid metabolism. PNAS 108:18179–18184
Hirakawa H, Shirasawa K, Miyatake K, Nunome T, Negoro S, Ohyama A, Yamaguchi H, Sato S, Isobe S, Tabata S, Fukuoka H (2014) Draft genome sequence of eggplant (Solanum melongena L.): the representative solanum species indigenous to the old world. DNA Res
Huang X, Han B (2014) Natural variations and Genome-Wide Association Studies in crop plants. Annu Rev Plant Biol 65:531–551
Ilic K, SanMiguel PJ, Bennetzen JL (2003) A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes. PNAS 100:12265–12270
Imanishi S, Hashizume K, Nakakita M, Kojima H, Matsubayashi Y, Hashimoto T, Sakagami Y, Yamada Y, Nakamura K (1998) Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures. Plant Mol Biol 38:1101–1111
Kajikawa M, Hirai N, Hashimoto T (2009) A PIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Mol Biol 69:287–298
Kajikawa M, Shoji T, Kato A, Hashimoto T (2011) Vacuole-localized berberine bridge enzyme-like proteins are required for a late step of nicotine biosynthesis in tobacco. Plant Physiol 155:2010–2022
Katoh A, Uenohara K, Akita M, Hashimoto T (2006) Early steps in the biosynthesis of NAD in Arabidopsis start with Aspartate and occur in the plastid. Plant Physiol 141:851–857
Katoh A, Shoji T, Hashimoto T (2007) Molecular cloning of N-methylputrescine oxidase from tobacco. Plant Cell Physiol 48:550–554
Kim S, Park M, Yeom S-I, Kim Y-M, Lee JM, Lee H-A, Seo E, Choi J, Cheong K, Kim K-T, Jung K, Lee G-W, Oh S-K, Bae C, Kim S-B, Lee H-Y, Kim S-Y, Kim M-S, Kang B-C, Jo YD, Yang H-B, Jeong H-J, Kang W-H, Kwon J-K, Shin C, Lim JY, Park JH, Huh JH, Kim J-S, Kim B-D, Cohen O, Paran I, Suh MC, Lee SB, Kim Y-K, Shin Y, Noh S-J, Park J, Seo YS, Kwon S-Y, Kim HA, Park JM, Kim H-J, Choi S-B, Bosland PW, Reeves G, Jo S-H, Lee B-W, Cho H-T, Choi H-S, Lee M-S, Yu Y, Do Choi Y, Park B-S, van Deynze A, Ashrafi H, Hill T, Kim WT, Pai H-S, Ahn HK, Yeam I, Giovannoni JJ, Rose JKC, Sorensen I, Lee S-J, Kim RW, Choi I-Y, Choi B-S, Lim J-S, Lee Y-H, Choi D (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278
Klein RJ, Zeiss C, Chew EY, Tsai J-Y, Sackler RS, Haynes C, Henning AK, SanGiovanni JP, Mane SM, Mayne ST, Bracken MB, Ferris FL, Ott J, Barnstable C, Hoh J (2005) Complement factor H polymorphism in age-related macular degeneration. Science 308:385–389
Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73–82
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 186:148–160
Kronenberger J, Lepingle A, Caboche M, Vaucheret H (1993) Cloning and expression of distinct nitrite reductases in tobacco leaves and roots. Mol Gen Genet 236:203–208
Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D, Balint-Kurti PJ, Holland JB (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nature Genet 43:163–168
Lackman P, Gonzalez-Guzman M, Tilleman S, Carqueijeiro I, Perez AC, Moses T, Seo M, Kanno Y, Hakkinen ST, Van Montagu MC, Thevelein JM, Maaheimo H, Oksman-Caldentey KM, Rodriguez PL, Rischer H, Goossens A (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. PNAS 108:5891–5896
Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linnean 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 Botany 101:805–814
Lewis RS, Bowen SW, Keogh MR, Dewey RE (2010) Three nicotine demethylase genes mediate nornicotine biosynthesis in Nicotiana tabacum L.: functional characterization of the CYP82E10 gene. Phytochemistry 71:1988–1998
Lim KY, Matyasek R, Kovarik A, Leitch AR (2004) Genome evolution in allotetraploid Nicotiana. Biol J Linnean Soc 82:599–606
Matassi G, Melis R, Macaya G, Bernardi G (1991) Compositional bimodality of the nuclear genome of tobacco. Nucleic Acids Res 19:5561–5567
Mauro-Herrera M, Wang X, Barbier H, Brutnell TP, Devos KM, Doust AN (2013) Genetic control and comparative genomic analysis of flowering time in Setaria (Poaceae). G3(3):283–295
Mochida K, Yamazaki Y, Ogihara Y (2004) Discrimination of homoeologous gene expression in hexaploid wheat by SNP analysis of contigs grouped from a large number of expressed sequence tags. Mol Genet Genomics 270:371–377
Morita M, Shitan N, Sawada K, Van Montagu MCE, Inze D, Rischer H, Goossens A, Oksman-Caldentey KM, Moriyama Y, Yazaki K (2009) Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. PNAS 106:2447–2452
Nakasugi K, Crowhurst RN, Bally J, Wood CC, Hellens RP, Waterhouse PM (2013) De Novo transcriptome sequence assembly and analysis of RNA silencing genes of Nicotiana benthamiana. PLoS ONE 8:e59534
Narayan RKJ (1987) Nuclear DNA changes, genome differentiation and evolution in Nicotiana (Solanaceae). Plant Syst Evol 157:161–180
Ow DW, De Wet JR, Helinski DR, Howell SH, Wood KV, Deluca M (1986) Transient and stable expression of the firefly Luciferase gene in plant cells and transgenic plants. Science 234:856–859
Parisod C, Mhiri C, Lim KY, Clarkson JJ, Chase MW, Leitch AR, Grandbastien MA (2012) Differential dynamics of transposable elements during long-term diploidization of Nicotiana Section Repandae (Solanaceae) allopolyploid genomes. PLoS ONE 7:e50352
Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudi H, Hvidsten TR, Consortium IWGS, Mayer KFX, Olsen O-A (2014) Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345
Poland JA, Bradbury PJ, Buckler ES, Nelson RJ, Goodman MM (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. In. National Academy of Sciences, p 6893
Renny-Byfield S, Chester M, Kovařík A, Le Comber SC, Grandbastien MA, Deloger M, Nichols RA, Macas J, Novák P, Chase MW, Leitch AR (2011) Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol Biol Evol 28:2843–2854
Renny-Byfield S, Kovařík A, Chester M, Nichols RA, Macas J, Novák P, Leitch AR (2012) Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS One 7:e36963
Renny-Byfield S, Kovarik A, Kelly LJ, Macas J, Novak P, Chase MW, Nichols RA, Pancholi MR, Grandbastien M-A, Leitch AR (2013) Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. Plant J 74:829–839
Riechers DE, Timko MP (1999) Structure and expression of the gene family encoding putrescine N-methyltransferase in Nicotiana tabacum: new clues to the evolutionary origin of cultivated tobacco. Plant Mol Biol 41:387–401
Schenke D, Sasabe M, Toyoda K, Inagaki YS, Shiraishi T, Ichinose Y (2003) Genomic structure of the NtPDR1 gene, harboring the two miniature inverted-repeat transposable elements, NtToya1 and NtStowaway101. Genes Genet Syst 78:409–418
Senthil-Kumar M, Mysore KS (2011) New dimensions for VIGS in plant functional genomics. Trends Plant Sci 16:656–665
Shi Q, Li C, Zhang F (2006) Nicotine synthesis in Nicotiana tabacum L. induced by mechanical wounding is regulated by auxin. J Exp Bot 57:2899–2907
Shoji T, Hashimoto T (2011) Nicotine biosynthesis In: Plant metabolism and biotechnology. John Wiley & Sons, Ltd, pp 191–216
Shoji T, Hashimoto T (2014) Stress-induced expression of NICOTINE2-locus genes and their homologs encoding Ethylene Response Factor transcription factors in tobacco. Phytochemistry. doi:10.1016/j.phytochem.2014.05.017
Shoji T, Nakajima K, Hashimoto T (2000) Ethylene suppresses Jasmonate-induced gene expression in nicotine biosynthesis. Plant Cell Physiol 41:1072–1076
Shoji T, Ogawa T, Hashimoto T (2008) Jasmonate-induced nicotine formation in tobacco is mediated by tobacco COI1 and JAZ genes. Plant Cell Physiol 49:1003–1012
Shoji T, Kajikawa M, Hashimoto T (2010) Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. Plant cell 22:3390–3409
Sierro N, Battey J, Ouadi S, Bovet L, Goepfert S, Bakaher N, Peitsch M, Ivanov N (2013) Reference genomes and transcriptomes of Nicotiana sylvestris and Nicotiana tomentosiformis. Genome Biol 14:R60
Sierro N, Battey JND, Ouadi S, Bakaher N, Bovet L, Willig A, Goepfert S, Peitsch MC, Ivanov NV (2014) The tobacco genome sequence and its comparison with those of tomato and potato. Nat Commun 5
Siminszky B, Gavilano L, Bowen SW, Dewey RE (2005) Conversion of nicotine to nornicotine in Nicotiana tabacum is mediated by CYP82E4, a cytochrome P450 monooxygenase. PNAS 102:14919–14924
Sinclair SJ, Murphy KJ, Birch CD, Hamill JD (2000) Molecular characterization of quinolinate phosphoribosyltransferase (QPRTase) in Nicotiana. Plant Mol Biol 44:603–617
Skalická 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 166:291–303
Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine’s defensive function in nature. PLoS Biol 2:1074–1080
Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272:603–615
The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195
The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Todd AT, Liu E, Polvi SL, Pammett RT, Page JE (2010) A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana. Plant J 62:589–600
Tong Z, Jiao T, Wang F, Li M, Leng X, Gao Y, Li Y, Xiao B, Wu W (2012a) Mapping of quantitative trait loci conferring resistance to brown spot in flue-cured tobacco (Nicotiana tabacum L.). Plant Breeding 131:335–339
Tong Z, Yang Z, Chen X, Jiao F, Li X, Wu X, Gao Y, Xiao B, Wu W (2012b) Large-scale development of microsatellite markers in Nicotiana tabacum and construction of a genetic map of flue-cured tobacco. Plant Breeding 131:674–680
Wang SS, Shi QM, Li WQ, Niu JF, Li CJ, Zhang FS (2008) Nicotine concentration in leaves of flue-cured tobacco plants as affected by removal of the shoot apex and lateral buds. J Integr Plant Biol 50:958–964
Welter D, MacArthur J, Morales J, Burdett T, Hall P, Junkins H, Klemm A, Flicek P, Manolio T, Hindorff L, Parkinson H (2014) The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res 42:D1001–D1006
Wu F, Eannetta N, Xu Y, Plieske J, Ganal M, Pozzi C, Bakaher N, Tanksley S (2010) COSII genetic maps of two diploid Nicotiana species provide a detailed picture of synteny with tomato and insights into chromosome evolution in tetraploid N. tabacum. Theor Appl Genet 120:809–827
Xu B, Sheehan MJ, Timko MP (2004) Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. bright yellow 2) cell suspensions by methyl-jasmonate treatment. Plant Growth Regul 44:101–116
Yukawa M, Tsudzuki T, Sugiura M (2006) The chloroplast genome of Nicotiana sylvestris and Nicotiana tomentosiformis: complete sequencing confirms that the Nicotiana sylvestris progenitor is the maternal genome donor of Nicotiana tabacum. Mol Genet Genomics 275:367–373
Acknowledgments
The authors thank Prof. Katrien M. Devos of the University of Georgia, USA for her efforts, suggestions, and assistance in editing during manuscript preparation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Graw.
Electronic supplementary material
Below is the link to the electronic supplementary material.
438_2015_989_MOESM1_ESM.xlsx
Supplemental File 1 Short read archive (SRA) resources of Nicotiana in the NCBI. File listed as Nicotiana short read archive resources in the NCBI on April 2nd 2014. (XLSX 46 kb)
Rights and permissions
About this article
Cite this article
Wang, X., Bennetzen, J.L. Current status and prospects for the study of Nicotiana genomics, genetics, and nicotine biosynthesis genes. Mol Genet Genomics 290, 11–21 (2015). https://doi.org/10.1007/s00438-015-0989-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-015-0989-7