Alkaloid production and capacity for methyljasmonate induction by hairy roots of two species in Tribe Anthocercideae, family Solanaceae
Suzanne M. Ryan A , Kathleen D. DeBoer A C and John D. Hamill B D
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, Monash University, Building 18, Clayton, Vic. 3800, Australia.
B Centre for Regional and Rural Futures (CeRRF), Deakin University, Locked Bag 20000, Geelong, Vic. 3220, Australia.
C Present address: The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA 6009, Australia.
D Corresponding author. Email: john.hamill@deakin.edu.au
Functional Plant Biology 42(8) 792-801 https://doi.org/10.1071/FP15045
Submitted: 20 February 2015 Accepted: 27 April 2015 Published: 5 June 2015
Abstract
In addition to producing medicinally important tropane alkaloids, some species in the mainly Australian Solanaceous tribe Anthocercideae, sister to genus Nicotiana, are known to also contain substantial levels of the pyridine alkaloids nicotine and nornicotine. Here, we demonstrate that axenic hairy root cultures of two tribe Anthocercideae species, Cyphanthera tasmanica Miers and Anthocercis ilicifolia ssp. ilicifolia Hook, contain considerable amounts of both nicotine and nornicotine (~0.5–1% DW), together with lower levels of the tropane alkaloid hyoscyamine (<0.2% DW). Treatment of growing hairy roots of both species with micromolar levels of the wound stress hormone methyl-jasmonate (MeJa) led to significant increases (P < 0.05) in pyridine alkaloid concentrations but not of hyoscyamine. Consistent with previous studies involving Nicotiana species, we also observed that transcript levels of key genes required for pyridine alkaloid synthesis increased in hairy roots of both Anthocercideae species following MeJa treatment. We hypothesise that wound-associated induction of pyridine alkaloid synthesis in extant species of tribe Anthocercideae and genus Nicotiana was a feature of common ancestral stock that existed before the separation of both lineages ~15 million years ago.
Additional keywords: gene expression, hairy roots, methyl-jasmonate induction, pyridine alkaloid, Solanaceae, tropane alkaloid.
References
Baldwin IT (1996) Methyl jasmonate-induced nicotine production in Nicotiana attenuata: inducing defenses in the field without wounding. Entomologia Experimentalis et Applicata 80, 213–220.| Methyl jasmonate-induced nicotine production in Nicotiana attenuata: inducing defenses in the field without wounding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xlslyitbs%3D&md5=d45a1af7db9493a9d59936852ec49e58CAS |
Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of the National Academy of Sciences of the United States of America 95, 8113–8118.
| Jasmonate-induced responses are costly but benefit plants under attack in native populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXks1Skurw%3D&md5=45419a267979ff90fa2e3a5899ceeafcCAS | 9653149PubMed |
Baldwin IT, Zhang Z, Diab N, Ohnmeiss TE, McCloud ES, Lynds GY, Schmelz EA (1997) Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris. Planta 201, 397–404.
| Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVeiu7g%3D&md5=51f0254af3c1135224877c46fa3743a2CAS |
Biastoff S, Brandt W, Dräger B (2009) Putrescine N-methyltransferase – the start for alkaloids. Phytochemistry 70, 1708–1718.
| Putrescine N-methyltransferase – the start for alkaloids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVWls7fJ&md5=47174c77af12fe94f08715bf4152adc4CAS | 19651420PubMed |
Bick JR, Bremner JB, Gillard JW, Winzenberg KN (1974) Alkaloids of Anthocercis tasmanica (Solanaceae). Australian Journal of Chemistry 27, 2515–2518.
| Alkaloids of Anthocercis tasmanica (Solanaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhsVSgtw%3D%3D&md5=5d632c74d3dae22034b7ea3b679be951CAS |
Biondi S, Fornalé S, Oksman-Caldentey KM, Eeva M, Agostani S, Bagni N (2000) Jasmonates induce over-accumulation of methylputrescine and conjugate polyamines in Hyoscyamus muticus L. root cultures. Plant Cell Reports 19, 691–697.
| Jasmonates induce over-accumulation of methylputrescine and conjugate polyamines in Hyoscyamus muticus L. root cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvVamt7g%3D&md5=dc194e1d018021354f58f22bfd529271CAS |
Bottomly W, White D (1950) The chemistry of Western Australian plants. IV. Duboisia hopwoodii. Australian Journal of Scientific Research, Series A: Physical Sciences 4, 107–111.
Bremner JB, Cannon JR (1968) Isolation of (–)-hyoscyamine from Anthotroche pannosa Endl. Australian Journal of Chemistry 21, 1369–1370.
| Isolation of (–)-hyoscyamine from Anthotroche pannosa Endl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXksF2ntLw%3D&md5=8f79e48447287605d29f9c3ade102441CAS |
Cane KA, Mayer M, Lidgett AJ, Michael AJ, Hamill JD (2005) Molecular 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. Functional Plant Biology 32, 305–320.
| Molecular 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFyktro%3D&md5=3b6b3f80a0dd3596e09c22a1bd2b6350CAS |
Clarkson JJ, Knapp S, Garcia VF, Olmstead RG, Leitch AJ, Chase MW (2004) Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions. Molecular Phylogenetics and Evolution 33, 75–90.
| Phylogenetic relationships in Nicotiana (Solanaceae) inferred from multiple plastid DNA regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFCrsb8%3D&md5=2a1611d853cd1b53e2f3802acf138c5fCAS | 15324840PubMed |
Cordell GA (2013) Fifty years of alkaloid biosynthesis in Phytochemistry. Phytochemistry 91, 29–51.
| Fifty years of alkaloid biosynthesis in Phytochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFWrurk%3D&md5=f24d71f79056b1f4fda2b04be2ec44d7CAS | 22721782PubMed |
De Boer KD, Tilleman S, Pauwels L, Bossche RV, De Sutter V, Vanderhaeghen R, Hilson P, Hamill JD, Goossens A (2011) APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. The Plant Journal 66, 1053–1065.
| APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosFeru78%3D&md5=fe0aeda5519d9b4bea22657463dc3351CAS |
De Sutter V, Vanderhaeghen R, Tilleman S, Lammertyn F, Vanhoutte I, Karimi M, Inzé D, Goossens A, Hilson P (2005) Exploration of jasmonate signaling via automated and standardized transient expression assays in tobacco cells. The Plant Journal 44, 1065–1076.
| Exploration of jasmonate signaling via automated and standardized transient expression assays in tobacco cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslGksQ%3D%3D&md5=e5c31da476439ee47a565395901e05bcCAS | 16359398PubMed |
DeBoer KD, Lye JC, Aitken CD, Su AK, Hamill JD (2009) The A622 gene in Nicotiana glauca (tree tobacco): evidence for a functional role in pyridine alkaloid synthesis. Plant Molecular Biology 69, 299–312.
| The A622 gene in Nicotiana glauca (tree tobacco): evidence for a functional role in pyridine alkaloid synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVyjsg%3D%3D&md5=b23e04531f52e9c06951bd708edc2217CAS | 19011764PubMed |
DeBoer KD, Dalton HL, Edward FJ, Ryan SM, Hamill JD (2013) RNAi-mediated down-regulation of ornithine decarboxylase (ODC) impedes wound-stress stimulation of anabasine synthesis in Nicotiana glauca. Phytochemistry 86, 21–28.
| RNAi-mediated down-regulation of ornithine decarboxylase (ODC) impedes wound-stress stimulation of anabasine synthesis in Nicotiana glauca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWqur7N&md5=7023303af88b752c44397ddbfd23fcaeCAS | 23177980PubMed |
Dewey RE, Xie J (2013) Molecular genetics of alkaloid biosynthesis in Nicotiana tabacum. Phytochemistry 94, 10–27.
| Molecular genetics of alkaloid biosynthesis in Nicotiana tabacum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yhsrrN&md5=2b4c5dd5dcbe8c51b229d02766b7f8c1CAS | 23953973PubMed |
Dräger B (2006) Tropinone reductases, enzymes at the branch point of tropane alkaloid metabolism. Phytochemistry 67, 327–337.
| Tropinone reductases, enzymes at the branch point of tropane alkaloid metabolism.Crossref | GoogleScholarGoogle Scholar | 16426652PubMed |
El Imam Y, Evans W (1984) Tropane alkaloids of species Anthocercis, Cyphanthera and Crenidium. Planta Medica 50, 86–87.
| Tropane alkaloids of species Anthocercis, Cyphanthera and Crenidium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXks12gurs%3D&md5=4f59e8a7170d08ee60534babc3d1123cCAS | 17340258PubMed |
Endo T, Yamada Y (1985) Alkaloid production in cultured roots of three species of Duboisia. Phytochemistry 24, 1233–1236.
| Alkaloid production in cultured roots of three species of Duboisia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXksFWhsrk%3D&md5=17af3b613fe9749a52e4f4ba5bc7c98fCAS |
Evans W, Ramsey K (1981) Tropane alkaloids from Anthocercis and Anthotroche. Phytochemistry 20, 497–499.
| Tropane alkaloids from Anthocercis and Anthotroche.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltFGrs7o%3D&md5=413c1a37f8b5d91f344029803e2bf9ceCAS |
Evans W, Ramsey K (1983) Alkaloids of the Solanaceae tribe Anthocercideae. Phytochemistry 22, 2219–2225.
| Alkaloids of the Solanaceae tribe Anthocercideae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXmsV2qtA%3D%3D&md5=53b9b8bbca6d99153beeb22cd8e1f447CAS |
Feng F, Jelesko J, Hatzios KK (2006) Effects of glyphosate, chlorsulfuron and methyl jasmonate on growth and alkaloid biosynthesis of jimsonweel (Datura stramonium L). Pesticide Biochemistry and Physiology 82, 16–26.
Glenn WA, Runguphan W, O’Connor SE (2013) Recent progress in the metabolic engineering of alkaloids in plant systems. Current Opinion in Biotechnology 24, 354–365.
| Recent progress in the metabolic engineering of alkaloids in plant systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlSkt7%2FP&md5=dea9a4f55e4cfb825b60919ae2efa8b7CAS |
Goossens A, Häkkinen ST, Laakso I, Seppänen-Laakso T, Biondi S, Sutter VD, Lammertyn F, Nuutila AM, Söderlund H, Marc Zabeau DI, Oksman-Caldentey K (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proceedings of the National Academy of Sciences of the United States of America 100, 8595–8600.
| A functional genomics approach toward the understanding of secondary metabolism in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFGnu7g%3D&md5=9c52d6a81b9b1464540b8a4e51061c56CAS | 12826618PubMed |
Haegi L (1981) A conspectus of Solancaeae tribe Anthocercideae. Telopea 2, 173–180.
| A conspectus of Solancaeae tribe Anthocercideae.Crossref | GoogleScholarGoogle Scholar |
Häkkinen S, Rischer H, Laakso I, Maaheimo H, Seppänen-Laakso T, Oksman-Caldentey K (2004) Anatalline and other methyl jasmonate-inducible nicotine alkaloids from Nicotiana tabacum cv. BY-2 cell cultures. Planta Medica 70, 936–941.
| Anatalline and other methyl jasmonate-inducible nicotine alkaloids from Nicotiana tabacum cv. BY-2 cell cultures.Crossref | GoogleScholarGoogle Scholar | 15490322PubMed |
Häkkinen S, Tilleman S, Swiatek A, DeSutter V, Rischer H, Vanhoutte I, Onckelen HV, Hilson P, Inze D, Oksman-Caldentey K, Goossens A (2007) Functional characterisation of genes involved in pyridine alkaloid biosynthesis in tobacco. Phytochemistry 68, 2773–2785.
| Functional characterisation of genes involved in pyridine alkaloid biosynthesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 18001808PubMed |
Hamill JD, Lidgett AJ (1997) Hairy root cultures: opportunities and key protocols for studies in metabolic engineering. In ‘Hairy roots; culture and applications’. (Ed. PM Doran) pp. 1–29. (Harwood Academic Publishers: Amsterdam)
Hamill JD, Parr AJ, Robins RJ, Rhodes MJC (1986) Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed by Agrobacterium rhizogenes. Plant Cell Reports 5, 111–114.
| Secondary product formation by cultures of Beta vulgaris and Nicotiana rustica transformed by Agrobacterium rhizogenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xktl2nt7w%3D&md5=17ea14b5e6017318458e91d2d4d29dfeCAS | 24248047PubMed |
Hartmann T (2007) From waste products to ecochemicals: fifty years of plant secondary metabolism. Phytochemistry 68, 2831–2846.
| From waste products to ecochemicals: fifty years of plant secondary metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlykurbK&md5=d7e2a8c0dae04ed56be02a6d94f2b6f4CAS | 17980895PubMed |
Hashimoto T, Yukimune Y, Yamada Y (1989) Putresceine and putrescine N-methyltransferase in the biosynthesis of tropane alkaloids in cultured roots of Hyoscyamus albus: I. Biochemical studies. Planta 178, 123–130.
| Putresceine and putrescine N-methyltransferase in the biosynthesis of tropane alkaloids in cultured roots of Hyoscyamus albus: I. Biochemical studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktVCgtro%3D&md5=e5280806edb3897a83ddec98b4eb5ce4CAS | 24212557PubMed |
Hashimoto T, Yun D-J, Yamada Y (1993) Production of tropane alkaloids in genetically engineered root cultures. Phytochemistry 32, 713–718.
| Production of tropane alkaloids in genetically engineered root cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitVKhsbc%3D&md5=a4e8dcbf82b2fbf602796c45ac5703afCAS |
Hibi N, Higashiguchi S, Hashimoto T, Yamada Y (1994) Gene expression in tobacco low-nicotine mutants. The Plant Cell 6, 723–735.
| Gene expression in tobacco low-nicotine mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhsFCgsg%3D%3D&md5=91f1f9845104b70ab5e07bfc25070a90CAS | 8038607PubMed |
Imanishi S, Hashizume K, Nakita M, Kojima H, Matsubayashi Y, Hashimoto T, 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 Molecular Biology 38, 1101–1111.
| Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksVCksQ%3D%3D&md5=8470ec61a4a589eb844f731bbf4bf96eCAS | 9869416PubMed |
Jouhikainen K, Lindgren L, Jokelainen T, Teeri TH, Oksman-Caldentey K-M (1999) Enhancement of scopolamine production in Hyoscyamus muticus L. hairy root cultures by genetic engineering. Planta 208, 545–551.
| Enhancement of scopolamine production in Hyoscyamus muticus L. hairy root cultures by genetic engineering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlSrt78%3D&md5=5e480d6ec08a00915228cf882b7c7c75CAS |
Kajikawa M, Hirai N, Hashimoto T (2009) A PIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Molecular Biology 69, 287–298.
| A PIP-family protein is required for biosynthesis of tobacco alkaloids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVOqug%3D%3D&md5=492eff3fae90e1cebc6e4dfb56e36e1fCAS | 19002761PubMed |
Mano Y, Ohkawa H, Yamada Y (1989) Production of tropane alkaloids by hairy roots cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes. Plant Science 59, 191–201.
| Production of tropane alkaloids by hairy roots cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtlelsbc%3D&md5=3d5b622cc325d600fea0dd711a003e80CAS |
Mizusaki S, Tanabe Y, Noguchi M, Tamaki E (1973) Changes in the activities of ornithine decarboxylase, putrescine N-methyltransferase and N-methylputrescine oxidase in tobacco roots in relation to nicotine biosynthesis. Plant & Cell Physiology 14, 103–110.
Moyano E, Fomalé S, Palazón J, Cusidó RM, Bagni N, Piñol MT (2002) Alkaloid production in Duboisia hybrid hairy root cultures overexpressing the pmt gene. Phytochemistry 59, 697–702.
| Alkaloid production in Duboisia hybrid hairy root cultures overexpressing the pmt gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitFWju7g%3D&md5=19c3ddfbf0fdc5ec75425c26798a17aeCAS | 11909625PubMed |
Moyano E, Jouhikainen K, Tammela P, Palazón P, Cusidó RM, Piñol MT, Teeri TH, Oksman-Caldentey K (2003) Effect of pmt gene overexpression on tropane alkaloid production in transformed root cultures of Datura metel and Hyoscyamus muticus. Journal of Experimental Botany 54, 203–211.
| Effect of pmt gene overexpression on tropane alkaloid production in transformed root cultures of Datura metel and Hyoscyamus muticus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlOiuro%3D&md5=9937ddf06fdb6e0251c083d41511a948CAS | 12493848PubMed |
Oksman-Caldentey K-M (2007) Tropane and nicotine alkaloid biosynthesis – novel approaches towards biotechnological production of plant-derived pharmaceuticals. Current Pharmaceutical Biotechnology 8, 203–210.
| Tropane and nicotine alkaloid biosynthesis – novel approaches towards biotechnological production of plant-derived pharmaceuticals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKqsLbP&md5=111b1672159962494050c35397e21e86CAS | 17691989PubMed |
Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57, 1159–1181.
Payne J, Hamill JD, Robins RJ, Rhodes MJC (1987) Production of hyoscyamine by hairy root cultures of Datura stramonium. Planta Medica 53, 474–478.
| Production of hyoscyamine by hairy root cultures of Datura stramonium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjs1eisw%3D%3D&md5=35fab629bb7f421a5436b9f92def3118CAS | 17269071PubMed |
Rhodes MJC, Robins RJ, Hamill JD, Parr AJ, Walton NJ (1987) Secondary product formation using Agrobacterium rhizogenes transformed hairy root cultures. IAPTC Newsletter 53, 2–15.
Rischer H, Häkkinen ST, Ritala A, Seppänen-Laakso T, Miralpeix B, Capell T, Christou P, Oksman-Caldentey K-M (2013) Plant cells as pharmaceutical factories. Current Pharmaceutical Design 19, 5640–5660.
| Plant cells as pharmaceutical factories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVylur7P&md5=4ad6eff10b46fda42ff4f199576701f9CAS | 23394561PubMed |
Robins RJ, Bent EG, Rhodes MJC (1991) Studies on the biosynthesis of tropane alkaloids in Datura stramonium L. transformed root cultures. Planta 185, 385–390.
| Studies on the biosynthesis of tropane alkaloids in Datura stramonium L. transformed root cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XotVGitg%3D%3D&md5=90bef87b1a5ac4339908e1d57b614deeCAS | 24186423PubMed |
Ryan SM (2012) Structure, expression and evolution of QPT genes in pyridine alkaloid producing species of the Solanaceae. PhD thesis, Monash University, Melbourne, Vic., Australia.
Ryan SM, Cane KA, DeBoer KD, Sinclair SJR, Brimblecombe R, Hamill JD (2012) Structure and expression of the quinolinate phosphoribosyltransferase (QPT) gene family in Nicotiana. Plant Science 188–189, 102–110.
| Structure and expression of the quinolinate phosphoribosyltransferase (QPT) gene family in Nicotiana.Crossref | GoogleScholarGoogle Scholar | 22525250PubMed |
Saitoh F, Noma M, Kawashima N (1985) The alkaloid contents of sixty Nicotiana species. Phytochemistry 24, 477–480.
| The alkaloid contents of sixty Nicotiana species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXitFygu7w%3D&md5=35bcf95e06891901a7396c5d571969abCAS |
Särkinen T, Bohn L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology 13, 214
| A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree.Crossref | GoogleScholarGoogle Scholar | 24283922PubMed |
Saunders JW, Bush LP (1979) Nicotine biosynthetic enzyme activities in Nicotiana tabacum L. genotypes with different alkaloid levels. Plant Physiology 64, 236–240.
| Nicotine biosynthetic enzyme activities in Nicotiana tabacum L. genotypes with different alkaloid levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXlsFCnurg%3D&md5=a9e782dc4b8dc415df4a46e1fc7222e2CAS | 16660940PubMed |
Sears MT, Zhang H, Rushton PJ, Wu M, Han S, Spano A, Timko MP (2014) NtERF32: a non-NIC2 locus AP2/ERF transcription factor required in jasmonate-inducible nicotine biosynthesis in tobacco. Plant Molecular Biology 84, 49–66.
| NtERF32: a non-NIC2 locus AP2/ERF transcription factor required in jasmonate-inducible nicotine biosynthesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Gjtr7E&md5=7b0ce7a67838698a15dbaf9c176a1db1CAS | 23934400PubMed |
Shoji T, Hashimoto T (2008) Why does anatabine, but not nicotine, accumulate in jasmonate-elicited cultured tobacco BY-2 cells? Plant & Cell Physiology 49, 1209–1216.
| Why does anatabine, but not nicotine, accumulate in jasmonate-elicited cultured tobacco BY-2 cells?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFSrsbnL&md5=d9fd701aa7932056fa8e682020d9d3eaCAS |
Shoji T, Hashimoto T (2011a) Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant & Cell Physiology 52, 1117–1130.
| Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWktrw%3D&md5=e3f5775d65a74b82bf827991b765a467CAS |
Shoji T, Hashimoto T (2011b) Recruitment of a duplicated primary metabolism gene into the nicotine biosynthesis regulon in tobacco. The Plant Journal 67, 949–959.
| Recruitment of a duplicated primary metabolism gene into the nicotine biosynthesis regulon in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1CgsL7N&md5=0bdc0cb103a6e47c60a313b943624ad5CAS | 21605206PubMed |
Shoji T, Hashimoto T (2012) DNA-binding and transcriptional activation properties of tobacco NIC2-locus ERF189 and related transcription factors. Plant Biotechnology 29, 35–42.
| DNA-binding and transcriptional activation properties of tobacco NIC2-locus ERF189 and related transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvFGmtr8%3D&md5=06fce04d20f5dc02556eab819f074d9cCAS |
Shoji T, Hashimoto T (2013) Smoking out the masters: transcriptional regulators for nicotine biosynthesis in tobacco. Plant Biotechnology 30, 217–224.
| Smoking out the masters: transcriptional regulators for nicotine biosynthesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslyitL7E&md5=329a429ff0dac3b1d9dd5819f3f04f29CAS |
Shoji T, Yamada Y, Hashimoto T (2000) T jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris. Plant & Cell Physiology 41, 831–839.
| T jasmonate induction of putrescine N-methyltransferase genes in the root of Nicotiana sylvestris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Wlur4%3D&md5=1f4e6c47dcf2e09c32dd7c716d3b5348CAS |
Shoji T, Kajikawa M, Hashimoto T (2010) Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. The Plant Cell 22, 3390–3409.
| Clustered transcription factor genes regulate nicotine biosynthesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2msrfE&md5=db123dc3234e960513760653d01663beCAS | 20959558PubMed |
Siegmund B, Leitner E, Pfannhauser W (1999) Determination of the nicotine content of various edible nightshades (Solanaceae) and their products and estimation of the associated dietary nicotine intake. Journal of Agricultural and Food Chemistry 47, 3113–3120.
| Determination of the nicotine content of various edible nightshades (Solanaceae) and their products and estimation of the associated dietary nicotine intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksFGitrc%3D&md5=dbb367c875d32cf93af2f0b4946d637dCAS | 10552617PubMed |
Sinclair SJ, Johnson R, Hamill JD (2004) Analysis of wound-induced gene expression in Nicotiana species with contrasting alkaloid profiles. Functional Plant Biology 31, 721–729.
| Analysis of wound-induced gene expression in Nicotiana species with contrasting alkaloid profiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFGqsro%3D&md5=f959ecbd19d19963a42298adb6acf2f2CAS |
Subroto MA, Kwok KH, Hamill JD, Doran PM (1996) Co-culture of genetically transformed roots and shoots for synthesis, translocation, and biotransformation of secondary metabolites. Biotechnology and Bioengineering 49, 481–494.
| Co-culture of genetically transformed roots and shoots for synthesis, translocation, and biotransformation of secondary metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtFartbo%3D&md5=889d17b2843904265d6c7826eb605a35CAS | 18623610PubMed |
Suzuki K, Yamada Y, Hashimoto T (1999) Expression of Atropa belladonna putrescine N-methyltransferase gene in root pericycle. Plant & Cell Physiology 40, 289–297.
| Expression of Atropa belladonna putrescine N-methyltransferase gene in root pericycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVSltro%3D&md5=093c8ed8e48d5da208a28e5d01cf636aCAS |
Svensson J, Rane A, Säwe J, Sjöqvist F (1982) Determination of morphine, morphine-3-glucuronide and (tentatively) morphine-6-glucuronide in plasma and urine using ion-pair high-performance liquid chromatography. Journal of Chromatography 230, 427–432.
| Determination of morphine, morphine-3-glucuronide and (tentatively) morphine-6-glucuronide in plasma and urine using ion-pair high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XkvVCls74%3D&md5=2f9d1c129df8fc8932d1c9bdb4614a59CAS | 7107787PubMed |
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. The Plant Journal 62, 589–600.
| A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1GhsLY%3D&md5=4478b0e2d597c8a566552133b4188a20CAS | 20202168PubMed |
Walton NJ, Robins RJ, Peerless MJC (1990) Enzymes of N-methylputrescine biosynthesis in relation to hyoscyamine formation in transformed root cultures of Datura stramonium and Atropa belladonna. Planta 182, 136–141.
| Enzymes of N-methylputrescine biosynthesis in relation to hyoscyamine formation in transformed root cultures of Datura stramonium and Atropa belladonna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVynsbk%3D&md5=ecab0478061a05b3546b45b859779135CAS | 24197009PubMed |
Zabetakis I, Edwards R, O’Hagan D (1999) Elicitation of tropane alkaloid biosynthesis in transformed root cultures of Datura stramonium. Phytochemistry 50, 53–56.
| Elicitation of tropane alkaloid biosynthesis in transformed root cultures of Datura stramonium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVKnsQ%3D%3D&md5=80564c8b57787846176563dd147c2e07CAS |
Zenk MH, Juenger M (2007) Evolution and current status of the phytochemistry of nitrogenous compounds. Phytochemistry 68, 2757–2772.
| Evolution and current status of the phytochemistry of nitrogenous compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlykurbM&md5=ee9b09401e25a85106e385b0566a03caCAS | 17719615PubMed |
