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The A and B Loci in Tobacco Regulate a Network of Stress Response Genes, Few of which are Associated with Nicotine Biosynthesis

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Abstract

Nicotine biosynthesis in Nicotiana tabacum is under genetic control by the A and B loci. Plants containing semi-dominant mutations at both the A and B loci (i.e. aabb genotype) have lower nicotine levels, reduced nicotine biosynthetic enzyme activities, and reduced mRNA levels of the corresponding biosynthetic genes. The A and B loci therefore appear to be coordinate regulators of several nicotine biosynthetic genes and define a group of co-regulated genes called the A–B regulon. To investigate the composition of genes in the A–B regulon, a fluorescent differential display (FDD) screen was used to randomly sample the transcriptomes of wild type and mutant aabb roots. This resulted in the isolation of 64 FDD clones, representing 49 unique genes or gene families. Four genes associated with nicotine biosynthesis were identified, whereas most of the other FDD clones were homologous with an assortment of stress response genes. Thirty-three genes or gene families showed reproducible aabb genotype effects, representing seven distinct mRNA expression patterns in response media treatments that increase the mRNA levels of known alkaloid biosynthetic genes. Thus, the A and B loci regulate the mRNA levels of some target genes differently than others. Eleven genes or gene families showed only treatment-specific effects, representing four mRNA accumulation patterns. These results indicate the A–B regulon is complex network of differentially expressed stress response genes, only a small subset of which are involved in nicotine biosynthesis.

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Abbreviations

ADC:

arginine decarboxylase

B21:

Burley 21

dAO:

Diamine oxidase

FDD:

fluorescent differential display

LA21:

low alkaloid Burley 21

IBA:

indolebutyric acid

ODC:

ornithine decarboxylase

MJA:

methyljasmonic acid

PMT:

putrescine methyltransferase

QS:

quinolinate synthetase

QPT:

quinolinate phosphoribosyltransferase

SAMS:

S-adenosylmethionine synthetase

STR:

strictosidine synthase

TIA:

terpene indole alkaloids

References

  • F.A. Ausubel R. Brent R.E. Kingston D.D. Moore J.G. Seidman J.A. Smith K. Struhl (2005) Current Protocols in Molecular Biology John Wiley & Sons New York

    Google Scholar 

  • I.T. Baldwin (2001) ArticleTitleAn ecologically motivated analysis of plant–herbivore interactions in native tobacco Plant Physiol. 127 1449–1458 Occurrence Handle10.1104/pp.127.4.1449 Occurrence Handle1:CAS:528:DC%2BD38XjtVWgsw%3D%3D Occurrence Handle11743088

    Article  CAS  PubMed  Google Scholar 

  • I.T. Baldwin D. Gorham E.A. Schmelz C.A. Lewandowski G.Y. Lynds (1998) ArticleTitleAllocation of nitrogen to an inducible defense and seed production in Nicotiana attenuata Oecologia 115 541–552 Occurrence Handle10.1007/s004420050552

    Article  Google Scholar 

  • I.T. Baldwin R. Halitschke A. Kessler U. Schittko (2001) ArticleTitleMerging molecular and ecological approaches in plant–insect interactions Curr. Opin. Plant Biol. 4 351–358 Occurrence Handle10.1016/S1369-5266(00)00184-9 Occurrence Handle1:CAS:528:DC%2BD3MXksVyktLg%3D Occurrence Handle11418346

    Article  CAS  PubMed  Google Scholar 

  • I.T. Baldwin E.A. Schmelz T.E. Ohnmeiss (1994) ArticleTitleWound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris Spegazzini and Comes J. Chem. Ecol. 20 2139–2157 Occurrence Handle10.1007/BF02066250 Occurrence Handle1:CAS:528:DyaK2cXlslGgu7c%3D

    Article  CAS  Google Scholar 

  • I.T. Baldwin Z.P. Zhang N. Diab T.E. Ohnmeiss E.S. McCloud G.Y. Lynds E.A. Schmelz (1997) ArticleTitleQuantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris Planta 201 397–404 Occurrence Handle10.1007/s004250050082 Occurrence Handle1:CAS:528:DyaK2sXjtVeiu7g%3D

    Article  CAS  Google Scholar 

  • K.A. Cane M. Mayer A.J. Lidgett A.J. Michael J.D. Hamill (2005) ArticleTitleMolecular analysis of alkaloid metabolism in AABB v. aabb genotype Nicotiana tabacum in response to wounding of aerial tissues and methyl jasmonate treatment of cultured roots Func. Plant Biol. 32 305–320 Occurrence Handle10.1071/FP04008 Occurrence Handle1:CAS:528:DC%2BD2MXjsFyktro%3D

    Article  CAS  Google Scholar 

  • Y. Chintapakorn J.D. Hamill (2003) ArticleTitleAntisense-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 Occurrence Handle10.1023/B:PLAN.0000009268.45851.95 Occurrence Handle1:CAS:528:DC%2BD3sXpvVGgtLY%3D Occurrence Handle14756309

    Article  CAS  PubMed  Google Scholar 

  • R.F. Dawson (1942a) ArticleTitleAccumulation of nicotine in reciprocal grafts of tomato and tobacco Am. J. Bot. 29 66–71 Occurrence Handle10.2307/2436544 Occurrence Handle1:CAS:528:DyaH38XhsV2msg%3D%3D

    Article  CAS  Google Scholar 

  • R.F. Dawson (1942b) ArticleTitleNicotine synthesis in excised tobacco roots Am. J. Bot. 29 813–815 Occurrence Handle10.2307/2437647 Occurrence Handle1:CAS:528:DyaH3sXht1elsA%3D%3D

    Article  CAS  Google Scholar 

  • R.F. Dawson M.L. Solt (1959) ArticleTitleEstimated contributions of root and shoot to the nicotine content of the tobacco plant Plant Physiol. 34 656–661 Occurrence Handle1:CAS:528:DyaF3cXitl2ktg%3D%3D Occurrence Handle16655293

    CAS  PubMed  Google Scholar 

  • J.B. Friesen E. Leete (1990) ArticleTitleNicotine synthase – an enzyme from Nicotiana species which catalyzes the formation of (S)-nicotine from nicotinic acid and 1-methyl-delta’-pyrrolinium chloride Tetrahedron Lett. 31 6295–6298 Occurrence Handle10.1016/S0040-4039(00)97046-1 Occurrence Handle1:CAS:528:DyaK3MXlsl2jsg%3D%3D

    Article  CAS  Google Scholar 

  • A. Goossens S.T. Hakkinen I. Laakso T. Seppanen-Laakso S. Biondi V. Sutter ParticleDe F. Lammertyn A.M. Nuutila H. Soderlund M. Zabeau D. Inze K.M. Oksman-Caldentey (2003) ArticleTitleA functional genomics approach toward the understanding of secondary metabolism in plant cells Proc. Natl. Acad. Sci. USA 100 8595–8600 Occurrence Handle10.1073/pnas.1032967100 Occurrence Handle1:CAS:528:DC%2BD3sXlsFGnu7g%3D Occurrence Handle12826618

    Article  CAS  PubMed  Google Scholar 

  • T. Hashimoto T. Shoji T. Mihara H. Oguri K. Tamaki K. Suzuki Y. Yamada (1998) ArticleTitleIntraspecific variability of the tandem repeats in Nicotiana putrescine N-methyltransferases Plant Mol. Biol. 37 25–37 Occurrence Handle10.1023/A:1005961122814 Occurrence Handle1:CAS:528:DyaK1cXjtlajt7s%3D Occurrence Handle9620262

    Article  CAS  PubMed  Google Scholar 

  • H.E. Heggestad (1966) ArticleTitleRegistration of Burley 1, Burley 2, Burley 11A, Burley 11B, Burley 21, Burley 37, and Burley 49 Tobaccos Crop Sci. 6 612 Occurrence Handle10.2135/cropsci1966.0011183X000600060043x

    Article  Google Scholar 

  • N. Hibi S. Higashiguchi T. Hashimoto Y. Yamada (1994) ArticleTitleGene expression in tobacco low-nicotine mutants Plant Cell 6 723–735 Occurrence Handle10.1105/tpc.6.5.723 Occurrence Handle1:CAS:528:DyaK2MXhsFCgsg%3D%3D Occurrence Handle8038607

    Article  CAS  PubMed  Google Scholar 

  • F.C. Huang T.M. Kutchan (2000) ArticleTitleDistribution of morphinan and benzo[c]phenanthridine alkaloid gene transcript accumulation in Papaver  somninferum Phytochemistry 53 555–564 Occurrence Handle10.1016/S0031-9422(99)00600-7 Occurrence Handle1:CAS:528:DC%2BD3cXhvFSgs7s%3D Occurrence Handle10724180

    Article  CAS  PubMed  Google Scholar 

  • S. Imanishi K. Hashizume M. Nakakita H. Kojima Y. Matsubayashi T. Hashimoto Y. Sakagami Y. Yamada K. Nakamura (1998) ArticleTitleDifferential 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 Occurrence Handle10.1023/A:1006058700949 Occurrence Handle1:CAS:528:DyaK1MXksVCksQ%3D%3D Occurrence Handle9869416

    Article  CAS  PubMed  Google Scholar 

  • A. Katoh T. Hashimoto (2004) ArticleTitleMolecular biology of pyridine nucleotide and nicotine biosynthesis Front Biosci 9 1577–1586 Occurrence Handle1:CAS:528:DC%2BD2cXltl2ms7s%3D Occurrence Handle14977569

    CAS  PubMed  Google Scholar 

  • N. Kuno T. Muramatsu F. Hamazato M. Furuya (2000) ArticleTitleIdentification by large-scale screening of phytochrome-regulated genes in etiolated seedlings of Arabidopsis using a fluorescent differential display technique Plant Physiol. 122 15–24 Occurrence Handle10.1104/pp.122.1.15 Occurrence Handle1:CAS:528:DC%2BD3cXmvFansg%3D%3D Occurrence Handle10631245

    Article  CAS  PubMed  Google Scholar 

  • P.D. Legg J.F. Chaplin G.B. Collins (1969) ArticleTitleInheritance of percent total alkaloids in Nicotiana tabacum L.; populations derived from crosses of low alkaloid lines with burley and flue-cured varieties J. Hered. 60 213–217

    Google Scholar 

  • P.D. Legg G.B. Collins (1971) ArticleTitleInheritance of per cent total alkaloids in Nicotiana tabacum L. II. genetic effects of two loci in Burley 21 X LA Burley 21 populations Can. J. Cyto. 13 287–291

    Google Scholar 

  • P.D. Legg G.B. Collins C.C. Litton (1970) ArticleTitleRegistration of LA Burley 21 Tobacco Germplasm Crop Sci. 10 212 Occurrence Handle10.2135/cropsci1970.0011183X001000020041x

    Article  Google Scholar 

  • Y. Mano H. Ohkawa Y. Yamada (1989) ArticleTitleProduction of tropane alkaloids by hairy root cultures of Duboisia  leichhardtii transformed by Agrobacterium rhizogenes Plant Sci. 59 191–201 Occurrence Handle10.1016/0168-9452(89)90137-4 Occurrence Handle1:CAS:528:DyaL1MXhtlelsbc%3D

    Article  CAS  Google Scholar 

  • F.L. Menke A. Champion J.W. Kijne J. Memelink (1999) ArticleTitleA novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2 EMBO J. 18 4455–4463 Occurrence Handle10.1093/emboj/18.16.4455 Occurrence Handle1:CAS:528:DyaK1MXlslWnsr4%3D Occurrence Handle10449411

    Article  CAS  PubMed  Google Scholar 

  • A.G. Millgate B.J. Pogson I.W. Wilson T.M. Kutchan M.H. Zenk W.L. Gerlach A.J. Fist P.J. Larkin (2004) ArticleTitleAnalgesia: morphine-pathway block in top1 poppies Nature 431 413–414 Occurrence Handle10.1038/431413a Occurrence Handle1:CAS:528:DC%2BD2cXnslemu7w%3D Occurrence Handle15386001

    Article  CAS  PubMed  Google Scholar 

  • S. Mizusaki Y. Tanabe M. Noguchi E. Tamaki (1971) ArticleTitlePhytochemical studies on tobacco alkaloids XIV. The occurrence and properties of putrescine N-methyltransferase in tobacco roots Plant Cell Physiol. 12 633–640 Occurrence Handle1:CAS:528:DyaE38XlsFKqtQ%3D%3D

    CAS  Google Scholar 

  • S. Mizusaki Y. Tanabe M. Noguchi E. Tamaki (1972) ArticleTitleN-methylputrescine oxidase from tobacco roots Phytochemistry 11 2757–2762 Occurrence Handle10.1016/S0031-9422(00)86509-7 Occurrence Handle1:CAS:528:DyaE38XkvFyhsro%3D

    Article  CAS  Google Scholar 

  • S. Mizusaki Y. Tanabe M. Noguchi E. Tamaki (1973) ArticleTitleChanges in the activities of ornithine decarboxylase, putrescine N-methyltransferase and N-methylputrescine oxidase in tobacco roots in relation to nicotine biosynthesis Plant Cell Physiol. 14 103–110 Occurrence Handle1:CAS:528:DyaE3sXhtlelsrg%3D

    CAS  Google Scholar 

  • T.E. Ohnmeiss E.S. McCloud G.Y. Lynds I.T. Baldwin (1997) ArticleTitleWithin-plant relationships among wounding, jasmonic acid, and nicotine: implications for defence in Nicotiana sylvestris New Phytol. 137 441–452 Occurrence Handle10.1046/j.1469-8137.1997.00845.x Occurrence Handle1:CAS:528:DyaK1cXitVClsg%3D%3D

    Article  CAS  Google Scholar 

  • H.H. Pauli T.M. Kutchan (1998) ArticleTitleMolecular cloning and functional heterologous expression of two alleles encoding (S)-N-methylcoclaurine 3′-hydroxylase (CYP80B1), a new methyl jasmonate-inducible cytochrome P-450-dependent mono-oxygenase of benzylisoquinoline alkaloid biosynthesis Plant J. 13 793–801 Occurrence Handle10.1046/j.1365-313X.1998.00085.x Occurrence Handle1:CAS:528:DyaK1cXislejsLw%3D Occurrence Handle9681018

    Article  CAS  PubMed  Google Scholar 

  • B. Pauw F.A. Hilliou V.S. Martin G. Chatel C.J. Wolf Particlede A. Champion M. Pre B. Duijn Particlevan J.W. Kijne L. Fits Particlevan der J. Memelink (2004a) ArticleTitleZinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus  roseus J. Biol. Chem. 279 52940–52948 Occurrence Handle10.1074/jbc.M404391200 Occurrence Handle1:CAS:528:DC%2BD2cXhtVKqurrL

    Article  CAS  Google Scholar 

  • B. Pauw B. Duijn Particlevan J.W. Kijne J. Memelink (2004b) ArticleTitleActivation of the oxidative burst by yeast elicitor in Catharanthus  roseus cells occurs independently of the activation of genes involved in alkaloid biosynthesis Plant Mol. Biol. 55 797–805 Occurrence Handle1:CAS:528:DC%2BD2MXmtlGlsw%3D%3D

    CAS  Google Scholar 

  • D.G. Reed J.G. Jelesko (2004) ArticleTitleThe A and B loci of Nicotiana tabacum have non-equivalent effects on the mRNA levels of four alkaloid biosynthetic genes Plant Sci. 167 1123–1130 Occurrence Handle10.1016/j.plantsci.2004.06.006 Occurrence Handle1:CAS:528:DC%2BD2cXmsVGisL0%3D

    Article  CAS  Google Scholar 

  • D.E. Riechers M.P. Timko (1999) ArticleTitleStructure 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 Occurrence Handle10.1023/A:1006342018991 Occurrence Handle1:CAS:528:DyaK1MXnvVCltL4%3D Occurrence Handle10598105

    Article  CAS  PubMed  Google Scholar 

  • F. Saitoh M. Mona N. Kawashima (1985) ArticleTitleThe alkaloid contents of sixty Nicotiana species Phytochemistry 24 477–480 Occurrence Handle10.1016/S0031-9422(00)80751-7 Occurrence Handle1:CAS:528:DyaL2MXitFygu7w%3D

    Article  CAS  Google Scholar 

  • J.A. Saunders (1979) ArticleTitleInvestigations of vacuoles isolated from tobacco Plant Physiol. 64 74–78 Occurrence Handle1:CAS:528:DyaE1MXltVGgtr0%3D Occurrence Handle16660918

    CAS  PubMed  Google Scholar 

  • J.Q. Saunders L.P. Bush (1979) ArticleTitleNicotine biosynthetic enzyme activities in Nicotiana tabacum L. genotypes with different alkaloid levels Plant Physiol. 64 236–240 Occurrence Handle1:CAS:528:DyaE1MXlsFCnurg%3D Occurrence Handle16660940

    CAS  PubMed  Google Scholar 

  • T. Schmeller M. Wink (1998) Utilization of alkaloids in modern medicine M.F. Roberts M. Wink (Eds) Alkaloids: Biochemistry, Ecology, and Medicinal Applications Plenum Press New York 435–459

    Google Scholar 

  • T. Shoji K. Nakajima T. Hashimoto (2000a) ArticleTitleEthylene suppresses jasmonate-induced gene expression in nicotine biosynthesis Plant Cell Physiol. 41 1072–1076 Occurrence Handle10.1093/pcp/pcd027 Occurrence Handle1:CAS:528:DC%2BD3cXmvV2ktro%3D

    Article  CAS  Google Scholar 

  • T. Shoji R. Winz T. Iwase K. Nakajima Y. Yamada T. Hashimoto (2002) ArticleTitleExpression patterns of two tobacco isoflavone reductase-like genes and their possible roles in secondary metabolism in tobacco Plant Mol. Biol. 50 427–440 Occurrence Handle10.1023/A:1019867732278 Occurrence Handle1:CAS:528:DC%2BD38Xmt12rsLg%3D Occurrence Handle12369619

    Article  CAS  PubMed  Google Scholar 

  • T. Shoji Y. Yamada T. Hashimoto (2000b) ArticleTitleJasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris Plant Cell Physiol. 41 831–839 Occurrence Handle10.1093/pcp/pcd001 Occurrence Handle1:CAS:528:DC%2BD3cXlt1Wlur4%3D

    Article  CAS  Google Scholar 

  • Y. Siberil S. Benhamron J. Memelink N. Giglioli-Guivarc’h M. Thiersault B. Boisson P. Doireau P. Gantet (2001) ArticleTitleCatharanthus  roseus G-box binding factors 1 and 2 act as repressors of strictosidine synthase gene expression in cell cultures Plant Mol. Biol. 45 477–488 Occurrence Handle10.1023/A:1010650906695 Occurrence Handle1:CAS:528:DC%2BD3MXjslWitr4%3D Occurrence Handle11352466

    Article  CAS  PubMed  Google Scholar 

  • S.J. Sinclair K.J. Murphy C.D. Birch J.D. Hamill (2000) ArticleTitleMolecular characterization of quinolinate phosphoribosyltransferase (QPRTase) in Nicotiana Plant Mol. Biol. 44 603–617 Occurrence Handle10.1023/A:1026590521318 Occurrence Handle1:CAS:528:DC%2BD3MXlslOntA%3D%3D Occurrence Handle11198422

    Article  CAS  PubMed  Google Scholar 

  • M.L. Solt (1957) ArticleTitleNicotine production and growth of excised tobacco root cultures Plant Physiol. 32 480–484 Occurrence Handle1:CAS:528:DyaG1cXitFKktA%3D%3D Occurrence Handle10.1104/pp.32.5.480 Occurrence Handle16655033

    Article  CAS  PubMed  Google Scholar 

  • A. Steppuhn K. Gase B. Krock R. Halitschke I.T. Baldwin (2004) ArticleTitleNicotine’s defensive function in nature PLoS Biol 2 E217 Occurrence Handle10.1371/journal.pbio.0020217 Occurrence Handle15314646 Occurrence Handle1:CAS:528:DC%2BD2cXntVemu7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • M. Tabata H. Yamamoto N. Hiraoka Y. Marumoto M. Konoshima (1971) ArticleTitleRegulation of nicotine production in tobacco tissue culture by plant growth regulators Phytochemistry 10 723–729 Occurrence Handle10.1016/S0031-9422(00)97139-5 Occurrence Handle1:CAS:528:DyaE3MXktlChu7c%3D

    Article  CAS  Google Scholar 

  • M. Takahashi Y. Yamada (1973) ArticleTitleRegulation of nicotine production by auxins in tobacco cultured cells in vitro Agr. Biol. Chem. 27 1755–1757

    Google Scholar 

  • L. Fits Particlevan der J. Memelink (2001) ArticleTitleThe jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element Plant J. 25 43–53 Occurrence Handle10.1046/j.1365-313x.2001.00932.x Occurrence Handle11169181

    Article  PubMed  Google Scholar 

  • L. Fits Particlevan der H. Zhang F.L. Menke M. Deneka J. Memelink (2000) ArticleTitleA Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway Plant Mol. Biol. 44 675–685 Occurrence Handle10.1023/A:1026526522555 Occurrence Handle11198427

    Article  PubMed  Google Scholar 

  • R. Wagner F. Feth K.G. Wagner (1986) ArticleTitleThe regulation of enzyme activities of the nicotine pathway in tobacco Physiol. Plant. 68 667–672 Occurrence Handle1:CAS:528:DyaL2sXpvFCrsw%3D%3D

    CAS  Google Scholar 

  • J.M. Wang M. Sheehan H. Brookman M.P. Timko (2000) ArticleTitleCharacterization of cDNAs differentially expressed in roots of tobacco (Nicotiana tabacum cv Burley 21) during the early stages of alkaloid biosynthesis Plant Sci. 158 19–32 Occurrence Handle10.1016/S0168-9452(00)00293-4 Occurrence Handle1:CAS:528:DC%2BD3cXms1Sqs78%3D Occurrence Handle10996241

    Article  CAS  PubMed  Google Scholar 

  • M. Wink (1998) A short history of alkaloids M.F. Roberts M. Wink (Eds) Alkaloids: Biochemistry, Ecology, and Medicinal Applications Plenum Press New York 11–44

    Google Scholar 

  • R.A. Winz I.T Baldwin (2001) ArticleTitleMolecular interactions between the specialist herbivore Manduca  sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts Plant Physiol. 125 2189–2202 Occurrence Handle10.1104/pp.125.4.2189 Occurrence Handle1:CAS:528:DC%2BD3MXjtFOjsro%3D Occurrence Handle11299398

    Article  CAS  PubMed  Google Scholar 

  • J. Xie W. Song W. Maksymowicz W. Jin K. Cheah W. Chen C. Carnes J. Ke M.A. Conkling (2004) Biotechnology: a tool for reduced risk tobacco products – the nicotine experience from test tube to cigarette pack C. Johnson S. Wilson M. Zawadski (Eds) 58th Meeting Tobacco Science Research Conference Winston-Salem North Carolina 17–37

    Google Scholar 

  • B. Xu M. Timko (2004) ArticleTitleMethyl jasmonate induced expression of the tobacco putrescine N-methyltransferase genes requires both G-box and GCC-motif elements Plant Mol. Biol. 55 743–761 Occurrence Handle10.1007/s11103-004-1962-8 Occurrence Handle1:CAS:528:DC%2BD2MXks12htrg%3D Occurrence Handle15604714

    Article  CAS  PubMed  Google Scholar 

  • N. Yasumatsu (1967) ArticleTitleStudies on the chemical regulation of alkaloid biosynthesis in tobacco plants Agr. Biol. Chem. 31 1441–1447 Occurrence Handle1:CAS:528:DyaF1cXjvVeqsQ%3D%3D

    CAS  Google Scholar 

  • Y. Yoshikawa H. Mukai K. Asada F. Hino I. Kato (1998) ArticleTitleDifferential display with carboxy-X-rhodamine-labeled primers and the selection of differentially amplified cDNA fragments without cloning Anal. Biochem. 256 82–91 Occurrence Handle10.1006/abio.1997.2473 Occurrence Handle1:CAS:528:DyaK1cXosVyiug%3D%3D Occurrence Handle9466801

    Article  CAS  PubMed  Google Scholar 

  • Z.P. Zhang T. Krumm I.T. Baldwin (1997) ArticleTitleStructural requirements of jasmonates and mimics for nicotine induction in Nicotiana sylvestris J. Chem. Ecol. 23 2777–2789 Occurrence Handle10.1023/B:JOEC.0000006356.47959.ed Occurrence Handle1:CAS:528:DyaK1cXhtlektw%3D%3D

    Article  CAS  Google Scholar 

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  1. Plant Pathology, Physiology, and Weed Science Department, Virginia Polytechnic Institute and State University, Blacksburg, Virginia, 24061-0346, USA

    Sarah K. Kidd, Amanda A. Melillo, Rong-He Lu, Deborah G. Reed & John G. Jelesko

  2. Department of Molecular Cell Biology, Thomas Jefferson University, 1020 Locust St., 229 JAH, Philadelphia, PA, 19107-6799, USA

    Sarah K. Kidd

  3. Department of Microbiology Immunology, and Molecular Genetics, Albany Medical College, 47 New Scotland Ave., Albany, NY, 12208, USA

    Amanda A. Melillo

  4. Advanced Research Laboratories, Hitachi, Hatoyama, Saitama, 350-0395, Japan

    Norihito Kuno, Kenko Uchida & Masaki Furuya

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  1. Sarah K. Kidd
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  2. Amanda A. Melillo
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Correspondence to John G. Jelesko.

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Sarah K. Kidd and Amanda A. Melillo: These authors contributed equally.

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Kidd, S.K., Melillo, A.A., Lu, RH. et al. The A and B Loci in Tobacco Regulate a Network of Stress Response Genes, Few of which are Associated with Nicotine Biosynthesis. Plant Mol Biol 60, 699–716 (2006). https://doi.org/10.1007/s11103-005-5546-z

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