Abstract
Nicotiana attenuata (coyote tobacco) has been developed into a model plant system to understand the molecular basis of traits important for the Darwinian fitness of plants in nature. Twenty years of releases of transgenic N. attenuata plants into a nature preserve in the plant’s native habitat have greatly advanced our understanding of the traits related to herbivore resistance. We provide an account of the genome sequencing of this wild tobacco species, as well as of another sympatric diploid tobacco, N. obtusifolia, which has different responses to herbivore attack. N. attenuata is a post-fire annual with a long-lived seed bank and exhibits an impressive array of plastic responses to the environmental challenges it faces, including unpredictable herbivore and pathogen attacks, by reprogramming the expression of thousands of genes. Regulatory small RNAs, including microRNAs, along with their biogenesis and regulating machinery, are thought to tailor the much needed specificity in modulating these large-scale changes in gene expression. Here, we provide a detailed genome-informed account of the small RNA machinery and its evolution in N. attenuata.
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References
Abrouk M, Zhang R, Murat F, Li A, Pont C, Mao L, Salse J (2012) Grass MicroRNA gene paleohistory unveils new insights into gene dosage balance in subgenome partitioning after whole-genome duplication. Plant Cell 24:1776–1792
Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science 329:1075–10758
Anssour S, Baldwin IT (2010) Variation in antiherbivore defense responses in synthetic Nicotiana allopolyploids correlates with changes in uniparental patterns of gene expression. Plant Physiol 153:1907–19018
Baldwin IT (2001) An ecologically motivated analysis of plant-herbivore interactions in native tobacco. Plant Physiol 127:1449–1458
Bernstein KA, Shor E, Sunjevaric I, Fumasoni M, Burgess RC, Foiani M, Branzei D, Rothstein R (2009) Sgs1 function in the repair of DNA replication intermediates is separable from its role in homologous recombinational repair. EMBO J 28:915–925
Blevins T, Rajeswaran R, Shivaprasad PV, Beknazariants D, Si-Ammour A, Park HS, Vazquez F, Robertson D, Meins F Jr, Hohn T, Pooggin MM (2006) Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res 34:6233–6246
Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741
Bozorov TA, Baldwin IT, Kim S-G (2012a) Identification and profiling of miRNAs during herbivory reveals jasmonate-dependent and-independent patterns of accumulation in Nicotiana attenuata. BMC Plant Biol 12:209
Bozorov TA, Pandey SP, Dinh ST, Kim SG, Heinrich M, Gase K, Baldwin IT (2012b) DICER-like proteins and their role in plant-herbivore interactions in Nicotiana attenuata. J Integr Plant Biol 54
Brockmoller T, Ling Z, Li D, Gaquerel E, Baldwin IT, Xu S (2017) Nicotiana attenuata Data Hub (NaDH): an integrative platform for exploring genomic, transcriptomic and metabolomic data in wild tobacco. BMC Genom 18:79
Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280
Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, Holt C, Sanchez Alvarado A, Yandell M (2008) MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18
Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896
Chen K, Durand D, Farach-Colton M (2000) NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 7
Chen X, Liu J, Cheng Y, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129:1085–1094
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 55:99–112
Dalmay T, Horsefield R, Braunstein TH, Baulcombe DC (2001) SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J 20:2069–2078
Gaquerel E, Heiling S, Schoettner M, Zurek G, Baldwin IT (2010) Development and validation of a liquid chromatography-electrospray ionization-time-of-flight mass spectrometry method for induced changes in Nicotiana attenuata leaves during simulated herbivory. J Agric Food Chem 58:9418–9427
Gaquerel E, Stitz M, Kallenbach M, Baldwin IT (2013) Jasmonate Signaling in the Field, Part I: Elicited Changes in Jasmonate Pools of Transgenic Nicotiana attenuata Populations. In: Goossens A, Pauwels L (eds) Jasmonate signaling. Humana Press, Totowa, NJ, pp 83–95
Gase K, Baldwin IT (2012) Transformational tools for next-generation plant ecology: manipulation of gene expression for the functional analysis of genes. Plant Ecol Divers 5:485–490
Glawe GA, Zavala JA, Kessler A, Van Dam NM, Baldwin IT (2003) Ecological costs and benefits correlated with trypsin protease inhibitor production in Nicotiana attenuata. Ecology 84:79–90
Gulati J, Baldwin IT, Gaquerel E (2013a) An integrative statistical method to explore herbivory-specific responses in plants. Plant Signal Behav 8. https://doi.org/10.4161/psb.25638
Gulati J, Kim SG, Baldwin IT, Gaquerel E (2013b) Deciphering herbivory-induced gene-to-metabolite dynamics in Nicotiana attenuata tissues using a multifactorial approach. Plant Physiol 162:1042–1059
Gulati J, Baldwin IT, Gaquerel E (2014) The roots of plant defenses: integrative multivariate analyses uncover dynamic behaviors of gene and metabolic networks of roots elicited by leaf herbivory. Plant J 77:880–892
Heiling S, Schuman MC, Schoettner M, Mukerjee P, Berger B, Schneider B, Jassbi AR, Baldwin IT (2010) Jasmonate and ppHsystemin regulate key Malonylation steps in the biosynthesis of 17-Hydroxygeranyllinalool Diterpene Glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. Plant Cell 22:273–292
Hernandez-Pinzon I, Yelina NE, Schwach F, Studholme DJ, Baulcombe D, Dalmay T (2007) SDE5, the putative homologue of a human mRNA export factor, is required for transgene silencing and accumulation of trans-acting endogenous siRNA. Plant J 50:140–148
Huang Y, Ji LJ, Huang QC, Vassylyev DG, Chen XM, Ma JB (2009) Structural insights into mechanisms of the small RNA methyltransferase HEN1. Nature 461:823–U86
Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32
Kahl J, Siemens DH, Aerts RJ, Gabler R, Kuhnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342
Kallenbach M, Bonaventure G, Gilardoni PA, Wissgott A, Baldwin IT (2012) Empoasca leafhoppers attack wild tobacco plants in a jasmonate-dependent manner and identify jasmonate mutants in natural populations. Proc Natl Acad Sci USA 109:E1548–E1557
Kessler D, Bhattacharya S, Diezel C, Rothe E, Gase K, Schottner M, Baldwin IT (2012) Unpredictability of nectar nicotine promotes outcrossing by hummingbirds in Nicotiana attenuata. Plant J 71:529–38
Kim SG, Yon F, Gaquerel E, Gulati J, Baldwin IT (2011) Tissue specific diurnal rhythms of metabolites and their regulation during herbivore attack in a native tobacco, Nicotiana attenuata. PloS One 6:e26214
Kuang H, Padmanabhan C, Li F, Kamei A, Bhaskar PB, Ouyang S, Jiang J, Buell CR, Baker B (2009) Identification of miniature inverted-repeat transposable elements (MITEs) and biogenesis of their siRNAs in the Solanaceae: new functional implications for MITEs. Genome Res 19:42–56
Kumar P, Pandit SS, Baldwin IT (2012) Tobacco rattle virus vector: A rapid and transient means of silencing Manduca sexta genes by plant mediated RNA interference. PLoS ONE 7:e31347
Kurzynska-Kokorniak A, Koralewska N, Pokornowska M, Urbanowicz A, Tworak A, Mickiewicz A, Figlerowicz M (2015) The many faces of Dicer: the complexity of the mechanisms regulating Dicer gene expression and enzyme activities. Nucleic Acids Res 43:4365–4380
Lee E, Helt GA, Reese JT, Munoz-Torres MC, Childers CP, Buels RM, Stein L, Holmes IH, Elsik CG, Lewis SE (2013) Web Apollo: a web-based genomic annotation editing platform. Genome Biol 14:R93
Lesburg CA, Cable MB, Ferrari E, Hong Z, Mannarino AF, Weber PC (1999) Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site. Nat Struct Biol 6:937–943
Li D, Baldwin IT, Gaquerel E (2015) Navigating natural variation in herbivory-induced secondary metabolism in coyote tobacco populations using MS/MS structural analysis. Proc Natl Acad Sci USA 112:E4147–E4155
Lou Y, Baldwin IT (2003) Manduca sexta recognition and resistance among allopolyploid Nicotiana host plants. Proc Natl Acad Sci USA 100:14581–14586
McCarthy EW, Arnold SE, Chittka L, Le Comber SC, Verity R, Dodsworth S, Knapp S, Kelly LJ, Chase MW, Baldwin IT, Kovarik A, Mhiri C, Taylor L, Leitch AR (2015) The effect of polyploidy and hybridization on the evolution of floral colour in Nicotiana (Solanaceae). Ann Bot 115:1117–1131
Mickiewicz A, Sarzynska J, Milostan M, Kurzynska-Kokorniak A, Rybarczyk A, Lukasiak P, Kulinski T, Figlerowicz M, Blazewicz J (2017) Modeling of the catalytic core of Arabidopsis thaliana Dicer-like 4 protein and its complex with double-stranded RNA. Comput Biol Chem 66:44–56
Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Remoue K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542
Mukherjee K, Campos H, Kolaczkowski B (2013) Evolution of animal and plant dicers: early parallel duplications and recurrent adaptation of antiviral RNA binding in plants. Mol Biol Evol 30:627–641
Onkokesung N, Galis I, von Dahl CC, Matsuoka K, Saluz HP, Baldwin IT (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Plant Physiol 153:785–798
Pandey SP, Baldwin IT (2007) RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. Plant J 50:40–53
Pandey SP, Baldwin IT (2008) Silencing RNA-directed RNA polymerase 2 increases the susceptibility of Nicotiana attenuata to UV in the field and in the glasshouse. Plant J 54:845–862
Pandey SP, Shahi P, Gase K, Baldwin IT (2008) Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proc Natl Acad Sci USA 105:4559–4564
Pandey P, Wang M, Baldwin IT, Pandey SP, Groten K (2018) Complex regulation of microRNAs in roots of competitively-grown isogenic Nicotiana attenuata plants with different capacities to interact with arbuscular mycorrhizal fungi. BMC Genom 19:937
Persson S, Wei H, Milne J, Page GP, Somerville CR (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102:8633–8638
Pradhan M, Pandey P, Gase K, Sharaff M, Singh RK, Sethi A, Baldwin IT, Pandey SP (2017) Argonaute 8 (AGO8) Mediates the elicitation of direct defenses against herbivory. Plant Physiol 175:927–946
Rensing SA (2014) Gene duplication as a driver of plant morphogenetic evolution. Curr Opin Plant Biol 17:43–48
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845–851
Self LS, Guthrie FE, Hodgson E (1964) Metabolism of nicotine by tobacco-feeding insects. Nature 204:300–301
Singh RK, Gase K, Baldwin IT, Pandey SP (2015) Molecular evolution and diversification of the Argonaute family of proteins in plants. BMC Plant Biol 15:23
Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000
Song JJ, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 34:W435–W439
Stanton MA, Prebetaler J, Paetz C, Boland W, Svatos A, Baldwin IT (2016) Plant-mediated pheromone emission by a hemipteran seed feeder increases the apparency of an unreliable but rewarding host. New Phytol 211:113–125
Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine’s defensive function in nature. PLoS Biol 2:E217
Steppuhn A, Schuman MC, Baldwin IT (2008) Silencing jasmonate signalling and jasmonate-mediated defences reveals different survival strategies between two Nicotiana attenuata accessions. Mol Ecol 17:3717–3732
Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302:249–255
Tang H (2009) Multiple collinearity scan—mcscan. In, 1.1 edn. Plant Genome Mapping Lab, University of Georgia, pp MCscan is a computer program that can simultaneously scan multiple genomes to identify homologous chromosomal regions and subsequently align these regions using genes as anchors. This is the toolset for generating the synteny correspondences in Plant Genome Duplication Database. It is intended as an easy-to-use and quick way to identify conserved gene arrays both within the same genome and across different genomes
Tonsor SJ, Alonso-Blanco C, Koornneef M (2005) Gene function beyond the single trait: natural variation, gene effects, and evolutionary ecology in Arabidopsis thaliana. Plant Cell Environ 28:2–20
Voelckel C, Schittko U, Baldwin IT (2001) Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced defenses in Nicotiana attenuata. Oecologia 127:274–280
Willmann MR, Endres MW, Cook RT, Gregory BD (2011) The functions of RNA-dependent RNA polymerases in Arabidopsis. Arab Book 9:e0146
Wink M, Theile V (2002) Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology 12:29–46
Wu J, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32:1161–1174
Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24
Wu J, Hettenhausen C, Baldwin IT (2006) Evolution of proteinase inhibitor defenses in North American allopolyploid species of Nicotiana. Planta 224:750–760
Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122
Wu J, Hettenhausen C, Schuman MC, Baldwin IT (2008) A comparison of two Nicotiana attenuata accessions reveals large differences in signaling induced by oral secretions of the specialist herbivore Manduca sexta. Plant Physiol 146:927–939
Xu S, Zhou W, Pottinger S, Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific among closely related Nicotiana species. BMC Plant Biol 15:2
Xu S, Brockmoller T, Navarro-Quezada A, Kuhl H, Gase K, Ling Z, Zhou W, Kreitzer C, Stanke M, Tang H, Lyons E, Pandey P, Pandey SP, Timmermann B, Gaquerel E, Baldwin IT (2017) Wild tobacco genomes reveal the evolution of nicotine biosynthesis. Proc Natl Acad Sci USA 114:6133–6138
Yang DH, Hettenhausen C, Baldwin IT, Wu J (2012) Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiol 159:1591–1607
Zhang H, Xia R, Meyers BC, Walbot V (2015) Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr Opin Plant Biol 27:84–90
Zhou W, Brockmoller T, Ling Z, Omdahl A, Baldwin IT, Xu S (2016) Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana. eLife 5:e19531
Zhou W, Kugler A, McGale E, Haverkamp A, Knaden M, Guo H, Beran F, Yon F, Li R, Lackus N, Kollner TG, Bing J, Schuman MC, Hansson BS, Kessler D, Baldwin IT, Xu S (2017) Tissue-specific emission of (E)-alpha-bergamotene helps resolve the dilemma when pollinators are also herbivores. Curr Biol 27:1336–1341
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Navarro-Quezada, A., Gase, K., Singh, R.K., Pandey, S.P., Baldwin, I.T. (2020). Nicotiana attenuata Genome Reveals Genes in the Molecular Machinery Behind Remarkable Adaptive Phenotypic Plasticity. 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_13
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