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Influence of Agrobacterium oncogenes on secondary metabolism of plants

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Abstract

The transgenic hairy root cultures have revolutionized the role of tissue culture of plants in the production of secondary metabolites. It was shown that hairy roots often exhibit about the same or higher biosynthetic capacity for secondary metabolite production comparing to their normal roots. Using this methodology, a big number of chemical compounds has been synthesized. The role of single rol genes in secondary metabolite production was studied. Stimulatory effect on the production of secondary metabolites has been shown for genes rolA, rolB, rolC. These genes are present in naturally trasgenic Linaria and Nicotiana plants that are discussed as a model for study of possible evolutionary function of rol genes in the control of secondary metabolites.

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Abbreviations

T-DNA:

Transferred DNA

cT-DNA:

Cellular T-DNA

orf :

Open reading frame

References

  • Adler LS, Schmitt J, Bowers MD (1995) Genetic viation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85

    Google Scholar 

  • Ahmad VU, Kousar F, Zubair M et al (2006) A new iridoid glycoside from Linaria genestifolia. Fitoterapia 77:12–14

    CAS  PubMed  Google Scholar 

  • Akkol EK, Ercil D (2009) Antinociceptive and anti-inflammatory activities of some Linaria species from Turkey. Pharm Biol 47(3):188–194

    CAS  Google Scholar 

  • Al-Rehaily AJ, Abdel-Kader MS, Ahmad MS et al (2006) Iridoid glucosides from Kickxia abhaica D.A. Sutton from Scrophulariaceae. Phytochemistry 67(5):429–432

    CAS  PubMed  Google Scholar 

  • Aoki S, Syōno K (1999) Synergistic function of rolB, rolC, ORF13 and ORF14 of TL-DNA of Agrobacterium rhizogenes in hairy root induction in Nicotiana tabacum. Plant Cell Physiol 40:252–256

    CAS  Google Scholar 

  • Banerjee S, Zehra M, Kukreja AK et al (1995) Hairy roots in medicinal plants. Curr Res Med Arom Plants 17(3–4):348–377

    Google Scholar 

  • Beninger CW, Cloutier RR (2009) A comparison of antirrhinoside distribution in the organs of two related Plantaginaceae species with different reproductive strategies. J Chem Ecol 35:1363–1372

    CAS  PubMed  Google Scholar 

  • Beninger CW, Cloutier RR, Monteiro MA, Grodzinski B (2007) The distribution of two major iridoids in different organs of Antirrhinum majus L. at selected stages of development. J Chem Ecol 33:731–747

    CAS  PubMed  Google Scholar 

  • Beninger CW, Cloutier RR, Grodzinski B (2008) The iridoid glucoside, antirrhinoside, from Antirrhinum majus L. has differential effects on two generalist insect herbivores. J Chem Ecol 34:591–600

    CAS  PubMed  Google Scholar 

  • Benrezzouk R, Terencio MC, Ferrandiz ML et al (1999) Inhibition of human Spla2 and 5-lipoxygenase activitie by two neo-clerodane diterpenoids. Life Sci 64:205–211

    Google Scholar 

  • Bianco A, Esposito P, Guiso M et al (1971) Iridoids 10. Procumbide, a diastereoisomer of antirrinoside. Gazz Chim Ital 101(10):764

    CAS  Google Scholar 

  • Bianco A, Guiso M, Martino M et al (1996a) Iridoids from endemic Sardinian Linaria species. Phytochemistry 42(1):89–91

    CAS  Google Scholar 

  • Bianco A, Guiso M, Procaccio C et al (1996b) Iridoids in the Flora of Italy. Part 17. A new methyl-cyclopentanoid monoterpene from Linaria purpurea. Gazz Chim Ital 127(8):407–409

    Google Scholar 

  • Bianco A, Guiso M, Ballero M et al (1997) Muralioside, an iridoid from Cymbalaria muralis. Phytochemistry 44:1515–1517

    CAS  Google Scholar 

  • Bianco A, Guiso M, Ballero M et al (2004) Glycosidic monoterpenes from Linaria capraria. Nat Prod Res 18:241

    CAS  PubMed  Google Scholar 

  • Biere A, Marak HB, Van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441

    PubMed  Google Scholar 

  • Bonhomme V, Laurain-Mattar D, Fliniaux MA (2000) Effects of the rolC gene on hairy root: induction development and tropane alkaloid production by Atropa belladonna. J Nat Prod 63:1249–1252

    CAS  PubMed  Google Scholar 

  • Boros CA, Stermitz FR (1990) Iridoids. An updated review. Part II. J Nat Prod 53:1055–1147

    CAS  Google Scholar 

  • Bouchez D, Tourneur J (1991) Organization of the agropine synthesis region of the T-DNA of the Ri plasmid from Agrobacterium rhizogenes. Plasmid 25:27–39

    CAS  PubMed  Google Scholar 

  • Bowers MD, Stamp NE (1992) Chemical variation within and between individuals of Plantago lanceolata (Plantagin aceae). J Chem Ecol 18:985–995

    CAS  PubMed  Google Scholar 

  • Britton, MT, Escobar, MA, Dandekar, AM (2008) The oncogenes of Agrobacterium tumefaciens and Agrobacterium rhizogenes. In: Agrobacterium: from biology to biotechnology. Springer, New York, pp 523–563

  • Bulgakov VP, Khodakovskaya MV, Labetskaya NV et al (1998) The impact of plant rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochemistry 49:1929–1934

    CAS  Google Scholar 

  • Bulgakov VP, Tchernoded GK, Mischenko NP et al (2002) Effects of salicylic acid, methyl jasmonate, etephone and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with rolB and rolC genes. J Biotechnol 97:213–221

    CAS  PubMed  Google Scholar 

  • Bulgakov VP, Tchernoded GK, Mischenko NP et al (2003) Effects of Ca2+ channel blockers and protein kinase/phosphatase inhibitors on growth and anthraquinone production in Rubia cordifolia cultures transformed by the rolB and rolC genes. Planta 217:349–355

    CAS  PubMed  Google Scholar 

  • Bulgakov VP, Tchernoded GK, Mischenko NP et al (2004) The rolB and rolC genes activate synthesis of anthraquinones in Rubia cordifolia cells by mechanism independent of octadecanoid signaling pathway. Plant Sci 166:1069–1075

    CAS  Google Scholar 

  • Bulgakov VP, Veselova MV, Tchernoded GK et al (2005) Inhibitory effect of the Agrobacterium rhizogenes rolC gene on rabdosiin and rosmarinic acid production in Eritrichium sericeum and Lithospermum erythrorhizon transformed cell cultures. Planta 221:471–478

    CAS  PubMed  Google Scholar 

  • Bulgakov VP, Aminin DL, Shkryl YN et al (2008) Suppression of reactive oxygen species and enhanced stress tolerance in Rubia cordifolia cells expressing the rolC oncogene. Mol Plant Microbe Interact 21:1561–1570

    CAS  PubMed  Google Scholar 

  • Bulgakov VP, Shkryl YN, Veremeichik GN et al (2013) Recent advances in the understanding of Agrobacterium rhizogenes derived genes and their effects on stress resistance and plant metabolism. Adv Biochem Eng Biotechnol 134:1–22

    CAS  PubMed  Google Scholar 

  • Camilleri C, Jouanin L (1991) The TR-DNA region carrying the auxin synthesis genes of the Agrobacterium rhizogenes agropine-type plasmid pRiA4: nucleotide sequence analysis and introduction into tobacco plants. Mol Plant Microbe Interact 4:155–162

    CAS  PubMed  Google Scholar 

  • Capone I, Spanò L, Cardarelli M et al (1989) Induction and growth properties of carrot roots with different complements of Agrobacterium rhizogenes T-DNA. Plant Mol Biol 13:43–52

    CAS  PubMed  Google Scholar 

  • Chen K, Dorlhac de Borne F, Szegedi E et al (2014) Deep sequencing of the ancestral tobacco species Nicotiana tomentosiformis reveals multiple T-DNA inserts and a complex evolutionary history of natural transformation in the genus Nicotiana. Plant J 80(4):669–682

    CAS  PubMed  Google Scholar 

  • Christey MC (2001) Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cell Dev Biol Plant 37:687–700

    CAS  Google Scholar 

  • DiCosmo F, Misawa M (1995) Plant cell and tissue culture: alternatives for metabolite production. Biotechnol Adv 13:425–453

    CAS  PubMed  Google Scholar 

  • El’kina OV, Shramm NI, Molokhova EI et al (2014) Optimization of the extraction of biologically active substances from yellow toadflax (Linaria vulgaris) herb. Pharm Chem J 48(4):273–275

    Google Scholar 

  • El-Naggar LJ, Beal JL (1980) Irodoids. An updated review. Part I. J Nat Prod 43:649–707

    CAS  PubMed  Google Scholar 

  • Ercil D, Sakar MK (2004) Chemical constituents of Linaria aucheri. Turk J Chem 28:133–139

    CAS  Google Scholar 

  • Estruch JJ, Parets-Soler A, Schmülling T et al (1991) Cytosolic localization in transgenic plants of the rolC peptide from Agrobacterium rhizogenes. Plant Mol Biol 17:547–550

    CAS  PubMed  Google Scholar 

  • Faiss M, Strnad M, Redig P et al (1996) Chemically induced expression of the rolC-encoded B-glucosidase in transgenic tobacco plants and analysis of cytokinin metabolism: rolC does not hydrolyze endogenous cytokinin glucosides in planta. Plant J 10(1):33–46

    CAS  Google Scholar 

  • Feliciano AS, Gordaliza M, Del Corral JMM et al (1993) Neo-clerodane diterpenoids from roots of Linaria saxatilis var glutinosa. Phytochemistry 33(3):631–633

    Google Scholar 

  • Franzyk H, Jensen SR, Thale Z et al (1999) Halohydrins and polyols derived from Antirrhinoside: structural revisions of muralioside and epimuralioside. J Nat Prod 62:275–278

    CAS  PubMed  Google Scholar 

  • Giri A, Narasu ML (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18:1–22

    CAS  PubMed  Google Scholar 

  • Gonuz A, Dulger B, Kargioglu M (2005) The morphological, anatomical properties and antimicrobial activity of endemic Linaria corifolia Desf. (Scrophulariaceae) in Turkey. Pak J Biol Sci 8:220–226

    Google Scholar 

  • Guillon S, Tremouillaux-Guiller J, Pati PK et al (2006) Curr Opin Plant Biol 9:341–346

    CAS  PubMed  Google Scholar 

  • Guiso M, Tassone G, Nicoletti M et al (2007) Chemotaxonomy of iridoids in Linaria vulgaris. Nat Prod Lett 21(13):1212–1216

    CAS  Google Scholar 

  • Handjieva NV, Ilieva EI, Spassov SL et al (1993) Iridoid glycosides from Linaria species. Tetrahedron 49(41):9261–9266

    CAS  Google Scholar 

  • Handjieva N, Tersieva L, Popov S et al (1995) Two iridoid glucosides, 5-O-menthiafoloylkickxioside and kickxin, from Kickxia Dum. species. Phytochemistry 39(4):925–927

    CAS  Google Scholar 

  • Hanson JR (1995) Diterpenoids. Nat Prod Rep 12(2):207–218

    CAS  Google Scholar 

  • Hanson JR (2015) Diterpenoids. Nat Prod Rep 32:76–87

    CAS  PubMed  Google Scholar 

  • Harborne JB, Valdés B (1971) Identification of scutellarein 4′-methyl ether in Linaria aeruginea. Phytochem Rev 10:2850–2851

    CAS  Google Scholar 

  • Høgedal BD, Mølgaard P (2000) HPLC analysis of the seasonal and diurnal variation of iridoids in cultivars of Antirrhinum majus. Biochem Syst Ecol 28:949–962

    Google Scholar 

  • Hong S, Peebles C, Shanks JV et al (2006) Terpenoid indole alkaloid production by Catharanthus roseus hairy roots induced by Agrobacterium tumefaciens harboring rolABC genes. Biotechnol Bioeng 93:386–390

    CAS  PubMed  Google Scholar 

  • Hussain MdS, Fareed S, Ansari S et al (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4(1):10–20

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ilieva E, Handjieva N, Popov S (1992a) Iridoid glucosides from Linaria vulgaris. Phytochernistry 31(3):1040–1041

    CAS  Google Scholar 

  • Ilieva E, Handjieva N, Popov S (1992b) Genistifolin and other iridoid glucosides from Linaria genistifolia (L.) mill. Z Naturforsch C 47(11–12):791–793

    CAS  Google Scholar 

  • Ilieva EI, Handjieva NV, Spassov SL et al (1993) 5-O-allosylantirrinoside from Linaria species. Phytochem Rev 32:1068

    CAS  Google Scholar 

  • Inyushkina YV, Bulgakov VP, Veselova MV et al (2007) High rabdosiin and rosmarinic acid production in Eritrichium sericeum callus cultures and effect of the calli on Masugi-nephritis in rats. Biosci Biotecnol Biochem 71:1286–1293

    CAS  Google Scholar 

  • Inyushkina YV, Kiselev KV, Bulgakov VP et al (2009) Specific genes of cytochrome P450 monooxygenases are implicated in biosynthesis of caffeic acid metabolites in rolC-transgenic culture of Eritrichium sericeum. Biochemistry (Moscow) 74:917–924

    CAS  Google Scholar 

  • Jamieson MA, Bowers D (2010) Iridoid glycoside variation in the invasive plant dalmatian toadflax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent, Calophasia lunula. J Chem Ecol 36(1):70–79

    CAS  PubMed  Google Scholar 

  • Jamieson MA, Bowers D (2012) Soil nitrogen availability and herbivore attack influence the chemical defenses of an invasive plant (Linaria dalmatica; Plantaginaceae). Chemoecology 22:1–11

    CAS  Google Scholar 

  • Jamieson MA, Quintero C, Blumenthal DM (2013) Interactive effects of simulated nitrogen deposition and altered precipitation patterns on plant allelochemical concentrations. J Chem Ecol 39:1204–1208

    CAS  PubMed  Google Scholar 

  • Karuppusamy S (2009) A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plants Res 3:1222–1239

    CAS  Google Scholar 

  • Kiselev KV, Kusaykin MI, Dubrovina AS et al (2006) The rolC gene induces expression of a pathogenesis-related b-1,3-glucanase in transformed ginseng cells. Phytochemistry 67:2225–2231

    CAS  PubMed  Google Scholar 

  • Kiselev KV, Dubrovina AS, Veselova MV et al (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692

    CAS  PubMed  Google Scholar 

  • Kitagawa I, Yoshihara M, Tani T et al (1975) Linaridial, a new cis-clerodane-type diterpene dialdehyde, from Linaria japonica Miq. Tetrahedron Lett 1:23–26

    Google Scholar 

  • Kitagawa I, Yoshihara M, Tani T et al (1976) On the constituents of Linaria japonica Miq. II. The structure of linaridial, a new cis-clerodane-type diterpene dialdehyde. Chem Pharm Bull 24(2):294–302

    CAS  Google Scholar 

  • Kitagawa I, Yoshihara M, Kamigauchi T (1977) Linarienone, a new cis-clerodane-type diteppene from the subterranean part of Linaria japonica Miq. Tetrahedron Lett 14:1221–1224

    Google Scholar 

  • Kooiman P (1970) Occurrence of iridoid glycosides in Scrophulariaceae. Acta Bot Neer 19:329–340

    Google Scholar 

  • Kuptsova LP, Ban’kovskii AI (1970) A new flavonoid from some species of toadflax Khimiya Prirodnykh Soedinenii 6(1):128–129

    CAS  Google Scholar 

  • Lemcke K, Schmülling T (1998) Gain of function assays identify non-rol genes from Agrobacterium rhizogenes TL-DNA that alter plant morphogenesis or hormone sensitivity. Plant J 15:423–433

    CAS  PubMed  Google Scholar 

  • Lemcke K, Prinsen E, van Onckelen H et al (2000) The ORF8 gene product of Agrobacterium rhizogenes TL-DNA has tryptophan 2-monooxygenase activity. MPMI 13(7):787–790

    CAS  PubMed  Google Scholar 

  • Marak HB, Biere A, Van Damme JMM (2000) Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J Evol Biol 13:985–996

    CAS  Google Scholar 

  • Marak HB, Biere A, Van Damme JMM (2002a) Two herbivore-deterrent iridoid glycosides reduce the in vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L. Chemoecology 12:185–192

    CAS  Google Scholar 

  • Marak HB, Biere A, Van Damme JMM (2002b) Systemic, genotype-specific induction of two herbivore-deterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (Rob.) Niessel. J Chem Ecol 28(12):2429–2448

    CAS  PubMed  Google Scholar 

  • Marco JL (1985) Iridoid glucoside from Linaria clementei. Phytochemistry 24:1609–1610

    CAS  Google Scholar 

  • Mashcenko N, Kintia P, Gurev A et al (2008) Glycosides from Linaria vulgaris Mill. Chem J Moldova Gen Ind Ecol Chem 3(2):98–100

    Google Scholar 

  • Matveeva TV, Kosachev PA (2013) Sequences homologousto Agrobacterium rhizogenes rolC in the genome of Linaria acutiloba. In: Zheng D (ed) International conference on frontiers of environment, energy and bioscience (ICFEEB 2013). DES tech Publications, Inc., Lancaster, pp 541–546

  • Matveeva TV, Lutova LA (2014) Horizontal gene transfer from Agrobacterium to plants. Front Plant Sci 5:326

    PubMed Central  PubMed  Google Scholar 

  • Matveeva TV, Bogomaz DI, Pavlova OA et al (2012) Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. Mol Plant Microbe Interact 25:1542–1551

    CAS  PubMed  Google Scholar 

  • Maurizio T, Bruno M, Francisco L et al (2001) The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Plant Biol 98(23):13449–13453

    Google Scholar 

  • Meyer AD, Tempé J, Costantino G et al (2000) Stacy hairy root: a molecular overview. Functional analysis of Agrobacterium rhizogenes T-DNA genes. Plant Microbe Interactions. APS Press, St. Paul, pp 93–139

  • Mizuochi K, Tanaka T, Kouno I et al (2011) New iridoid diesters of glucopyranose from Linaria canadensis (L.) Dum. J Nat Med 65:172–175

    CAS  PubMed  Google Scholar 

  • Moriuchi H, Okamoto C, Nishihama R et al (2004) Nuclear localization and interaction of RolB with plant 14-3-3 proteins correlates with induction of adventitious roots by the oncogene rolB. Plant J 38(2):260–275

    CAS  PubMed  Google Scholar 

  • Moyano E, Fornale S, Palazon J et al (1999) Effect of Agrobacterium rhizogenes T-AND on alkaloid production in Solanaceae plants. Phytochemistry 52:1287–1292

    CAS  Google Scholar 

  • Nicoletti M, Serafini M, Garbarino JA et al (1988) A chemosystematic study of Srophulariaceae iridoid glycosides. G Bot Ital 122(1–2):13–24

    Google Scholar 

  • Nikolova-Damyanova B, Ilieva E, Handjieva N et al (1994) Quantitative thin layer chromatography of iridoid and flavonoid glucosides in species of Linaria. Phytochem Anal 5:38–40

    CAS  Google Scholar 

  • Nilsson O, Moritz T, Imbault N et al (1993) Hormonal characterization of transgenic tobacco plants expressing the rolC gene of Agrobacterium rhizogenes TL-DNA. Plant Physiol 102:363–371

    PubMed Central  CAS  PubMed  Google Scholar 

  • Otsuka H (1993) Iridoid glucosides from Linaria japonica. Phytochem 33:617–622

    CAS  Google Scholar 

  • Otsuka H (1995) Iridoid mono- and diesters of d-glucopyranose from Linaria japonica. Phytochem 39:1111–1114

    CAS  Google Scholar 

  • Palazón J, Pinol MT, Cusido RM et al (1997) Application of transformed root technology to the production of bioactive metabolites. Recent Res Dev Plant Phys 1:125–143

    Google Scholar 

  • Palazón J, Cusidó RM, Roig C et al. (1998a) Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Rep 17(3):84–90

  • Palazón J, Cusidó RM, Gonzalo J et al (1998b) Relation between the amount the rolC gene product and indole alkaloid accumulation in Catharantus roseus transformed root cultures. J Plant Physiol 153:712–718

    Google Scholar 

  • Pandolfini T, Storlazzi A, Calabria E et al (2000) The spliceosomal intron of the rolA gene of Agrobacterium rhizogenes is a prokaryotic promoter. Mol Microbiol 35:1326–1334

    CAS  PubMed  Google Scholar 

  • Pandya P, Acharya R, Shukla VJ et al. (2013) Physico phyto-chemical evaluation of the root of kanoti (Linaria ramosissima Wall. Janch.). Ayurpharm Int J Ayur Alli Sci 2(9):259–264

  • Pavela R (2008) Larvicidal effects of various Euro-Asiatic plants against Culex quinquefasciatus Say larvae (Diptera: Culicidae). Parasitol Res 102:555–559

    PubMed  Google Scholar 

  • Pavlova OA, Matveeva TV, Lutova LA (2014) Genome of Linaria dalmatica contains Agrobacterium rhizogenes RolC Gene Homolog. Russ J Genet Appl Res 4(5):461–465

    Google Scholar 

  • Qi LS, Larson MH, Gilbert LA et al (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153

    CAS  PubMed  Google Scholar 

  • Robins RJ (1998) The application of root cultures to problems of biological chemistry. Nat Prod Rep 15:549–570

    CAS  Google Scholar 

  • Scherbakova OV, Petrichenko VM, Chekryshkina LA (2011) Spectrophotometric method of total flavonoid content determination in above-ground part of Linaria vulgaris (Scrophulariaceae). Rastitel’nye Resursy 47(4):141–147

  • Schmülling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629

  • Sevón N, Oksman-Caldentey KM (2002) Agrobacterium rhizogenes-mediated transformation: root cultures as a source of alkaloids. Planta Med 68:859–868

    PubMed  Google Scholar 

  • Shkryl YN, Veremeichik GN, Bulgakov VP et al (2008) Individual and combined effects of the rolA, B and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnol Bioeng 100:118–125

    CAS  PubMed  Google Scholar 

  • Smirnova IP, Zapesochnaya GG, Sheichenko VI, Ban’kovskii AI (1974) Structure of acetylpectolinarin, a new acylated flavonoid from plants of the genus Linaria. Chem Nat Comput 10(3):320

    Google Scholar 

  • Sokornova SV, Gasich EL, Matveeva TV et al (2015) Micromycetes of plants Linaria containing DNA sequences of Agrobacterial origin in their genomes. Mikologiya i Fitopatologiya 49(2):140–145

    Google Scholar 

  • Spena A, Schmulling T, Koncz C et al (1987) Independent and synergistic activity of rolA, B, C loci in stimulating abnormal growth in plants. EMBO J 6:3891–3899

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sticher O (1971) Isolation of antirrinoside from Linaria vulgaris. Phytochemistry 10:1974–1975

    CAS  Google Scholar 

  • Sticher O (1977) Plant mono terpenoids di terpenoids and sesqui terpenoids with pharmacological or therapeutical activity. In: Wagner H, Wolff P (eds) New natural products and plant drugs with pharmacological, biological or therapeutical activity. Springer, Berlin, p 148

    Google Scholar 

  • Stieger PA, Meyer AD, Kathmann P et al (2004) The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells. Plant Physiol 135:1798–1808

    PubMed Central  CAS  PubMed  Google Scholar 

  • Suzuki K, Yamashita I, Tanaka N (2002) Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution. Plant J 32:775–787

    CAS  PubMed  Google Scholar 

  • Taneja J, Jaggi M, Wankhede DP et al (2010) Effect of loss of T-DNA genes on MIA biosynthetic pathway gene regulation and alkaloid accumulation in Catharanthus roseus hairy roots. Plant Cell Rep 29(10):1119–1129

    CAS  PubMed  Google Scholar 

  • Taskova R, Mitova M, Evstatieva L et al (1997) Iridoids, flavonoids and terpenoids as taxonomic markers in Lamiaceae, Scrophulariaceae, and Rubiaceae. Bocconea 5:631–636

    Google Scholar 

  • Tundis R, Deguin B, Dodaro D et al (2008) Iridoid glycosides from Linaria multicaulis (L.) Miller subsp. multicaulis (Scrophulariaceae). Biochem Syst Ecol 36:142

    CAS  Google Scholar 

  • Valdés B (1970) Flavonoid pigments in flower and leaf of the genus Linaria (Scrophulariaceae). Phytochemistry 9(6):1253–1260

    Google Scholar 

  • Van Der Sluis WG, Van Der Nat JM, Labadie RP (1983) Thin-layer chromatographic bioassay of iridoid and secoiridoid glucosides with a fungitoxic aglucone moiety using beta-glucosidase and the fungus Penicillium expansum as a test organism. J Chromatogr 259:522–526

    PubMed  Google Scholar 

  • Vansuyt G, Vilaine F, Tepfer M et al (1992) rolA modulates the sensitivity to auxin of the proton translocation catalyzed by the plasma membrane H+-ATPase in transformed tobacco. FEBS Lett 298(1):89–92

    CAS  PubMed  Google Scholar 

  • White FF, Garfinkel DJ, Huffman GA et al (1983) Sequence homologous to Agrobacterium rhizogenes TDNA in the genomes of uninfected plants. Nature 301:348–350

    CAS  Google Scholar 

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Acknowledgments

This paper was prepared within the framework of the thematic plan of St. Petersburg State University ## 0.37.526.2013; 1.39.315.2014 and supported by a grant to Tatiana V. Matveeva from the Russian Foundation for Basic Research #14-04-01480.

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  1. St. Petersburg State University, Universitetskaya emb, 7/9, St. Petersburg, Russia

    Tatiana V. Matveeva, Sophie V. Sokornova & Ludmila A. Lutova

  2. All Russian Institute of Plant Protection, St. Petersburg, Russia

    Sophie V. Sokornova

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  1. Tatiana V. Matveeva
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  3. Ludmila A. Lutova
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Correspondence to Tatiana V. Matveeva.

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Matveeva, T.V., Sokornova, S.V. & Lutova, L.A. Influence of Agrobacterium oncogenes on secondary metabolism of plants. Phytochem Rev 14, 541–554 (2015). https://doi.org/10.1007/s11101-015-9409-1

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