Agrobacterium rhizogenes-Mediated Transformation of Plants for Improvement of Yields of Secondary Metabolites

  • Tatiana V. MatveevaEmail author
  • Sophie V. Sokornova
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)


The transgenic hairy root culture has revolutionized the role of tissue culture of plants in the synthesis of secondary metabolites. It was shown that hairy roots in the most cases exhibit higher biosynthetic capacity for secondary metabolite production comparing to the non-transgenic roots. A big number of medicinal compounds have been produced using this approach. However, the mechanism of influence of T-DNA genes on secondary metabolite production is not completely understood. The stimulatory effect of single rol genes (rolA, rolB, rolC) on secondary metabolite production was demonstrated for a number of plant species that are widely used in pharmacology. It is interesting to note that these rol genes are present in naturally transgenic Linaria, Ipomoea, and Nicotiana plants. Many species from these genera are used as medicinal. Besides, naturally transgenic plants could be a good model for study of possible evolutionary function of rol genes in the control of secondary metabolites for plant protection.


Agrobacterium rhizogenes T-DNA rol genes Secondary metabolism Naturally transgenic plants Medicinal plants 



This work is performed with financial support of RSF, a project № 16-16-10010 “Genome organization in naturally transgenic Linaria and Nicotiana plants.”


  1. 1.
    Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Hussain MS, Fareed S, Ansari S et al (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4(1):10–20PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Eich E (2008) Solanaceae and convolvulaceae: secondary metabolites: biosynthesis, chemotaxonomy, biological and economic significance (a handbook). Springer, Berlin/Heidelberg, 582 pCrossRefGoogle Scholar
  4. 4.
    DiCosmo F, Misawa M (1995) Plant cell and tissue culture: alternatives for metabolite production. Biotechnol Adv 13:425–453. Scholar
  5. 5.
    Palazon J, Pinol MT, Cusido RM et al (1997) Application of transformed root technology to the production of bioactive metabolites. Recent Res Dev Plant Phys 1:125–143Google Scholar
  6. 6.
    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 WOS:000273767100010Google Scholar
  7. 7.
    Giri A, Narasu ML (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18:1–22PubMedCrossRefGoogle Scholar
  8. 8.
    Guillon S, Tremouillaux-Guiller J, Pati PK et al (2006) Curr Opin Plant Biol 9:341–346Google Scholar
  9. 9.
    Sevon N, Oksman-Caldentey KM (2002) Agrobacterium rhizogenes-mediated transformation: root cultures as a source of alkaloids. Planta Med 68:859–868PubMedCrossRefGoogle Scholar
  10. 10.
    Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25(643):671–673PubMedCrossRefGoogle Scholar
  11. 11.
    Chilton MD, Drummond MH, Merio DJ, Sciaky D, Montoya AL, Gordon MP, Nester EW (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11(2):26371. Scholar
  12. 12.
    Chilton MD, Tepfer D, Petit A, David C, Casse Delbart FT (1982) Agrobacterium rhizogenes insert T-DNA into the genome of the host plant root cells. Nature 295(5848):432–434. Scholar
  13. 13.
    Burr T, Otten L (1999) Crown gall of grape: biology and disease management. Annu Rev Phytopathol (1):53–80.
  14. 14.
    Young JM, Kuykendall LD, Martínez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int J Syst Evol Microbiol 51(Pt 1):89–103. Scholar
  15. 15.
    Zupan J, Muth TR, Draper O, Zambryski P (2000) The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J 23(1):11–28. Scholar
  16. 16.
    Akiyoshi DE, Klee H, Amasino RM, Nester EW, Gordon MP (1984) T-DNA of Agrobacterium tumefaciens encodes an enzyme of cytokinin biosynthesis. Proc Natl Acad Sci U S A 81(19):5994–5998 PMCID: PMC391845PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Ozyigit II, Dogan I, Tarhan EA Agrobacterium rhizogenes-mediated transformation and its biotechnological applications in crops. Available from: Accessed 12 Aug 2016
  18. 18.
    Christey MC (2001) Use of Ri-mediated transformation for production of transgenic plants. In Vitro Cell Dev Biol Plant 37:687–700. Scholar
  19. 19.
    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. Scholar
  20. 20.
    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 PMCID: PMC553866PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Schmülling T, Schell J, Spena А (1988) Single genes from Agrobacterium rhizogenes influence plant development. ЕМВО J 7:2621–2629 PMCID: PMC457048Google Scholar
  22. 22.
    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. Scholar
  23. 23.
    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. Scholar
  24. 24.
    White FF, Taylor BH, Huffman GA, Gordon MP, Nester EW (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164(1):33–44 PubMed ID: 4044524PubMedPubMedCentralGoogle Scholar
  25. 25.
    Cardarelli M, Spano L, Mariotti D, Mauro ML, Van Sluys MA, Costantino P (1987) The role of auxin in hairy root induction. Mol Gen Genet 208:457–463. Scholar
  26. 26.
    Hansen G, Larribe M, Vaubert D, Tempe J, Biermann BJ, Montoya AL, Chilton MD, Brevet J (1991) Agrobacterium rhizogenes pRi8196 T-DNA: mapping and DNA sequence of functions involved in mannopine synthesis and hairy root differentiation (Ri plasmid). Proc Natl Acad Sci 88:7763–7767 PMCID: PMC52383PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    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. Scholar
  28. 28.
    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. Scholar
  29. 29.
    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. Scholar
  30. 30.
    Meyer A, Tempй J, Costantino P (2000) Hairy root: a molecular overview. Functional analysis of Agrobacterium rhizogenes T-DNA genes. In: Stacey G, Keen NT (eds) Plant Microbe Interactions. APS Press, St. Paul, pp 93–139Google Scholar
  31. 31.
    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. Scholar
  32. 32.
    Estruch JJ, Parets-Soler A, Schmulling T, Spena A (1991) Cytosolic localization in transgenic plants of the RolC peptide from Agrobacterium rhizogenes. Plant Mol Biol 17:547–550. Scholar
  33. 33.
    Faiss M, Strnad M, Redig P, Dolezal K, Hanus J, Van Onckelen H, Schmulling T (1996) Chemically induced expression of the rolC-encoded beta-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. Scholar
  34. 34.
    Trovato M, Maras B, Linhares F, Costantino P (2001) The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proc Natl Acad Sci U S A 98(23):13449–13453PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Lemcke K, Prinsen E, van Onckelen H, Schmulling T (2000) The ORF8 gene product of Agrobacterium rhizogenes TL-DNA has tryptophan 2-monooxygenase activity. MPMI 13(7): 787–790. Scholar
  36. 36.
    Stieger PA, Meyer AD, Kathmann P, Frundt C, Niederhauser I, Barone M, Kuhlemeier C (2004) The orf13 T-DNA gene of Agrobacterium rhizogenes confers meristematic competence to differentiated cells. Plant Physiol 135:1798–1808. Scholar
  37. 37.
    Lemcke K, Schmulling 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. Scholar
  38. 38.
    Capone I, Spano L, Cardarelli M, Bellincampi D, Petit A, Costantino P (1989) Induction and growth properties of carrot roots with different complements of Agrobacterium rhizogenes T-DNA. Plant Mol Biol 13:43–52. Scholar
  39. 39.
    Aoki S, Syono 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 WOS:000078719400017CrossRefGoogle Scholar
  40. 40.
    Comai L, Kosuge T (1982) Cloning and characterization of iaaM, a virulence determinant of Pseudomonas savastanoi. J Bacteriol 149:40–46 WOS:A1982MX09200006PubMedPubMedCentralGoogle Scholar
  41. 41.
    Van Onckelen H, Prinsen E, Inze D, Rudelsheim P, van Lijsebettens M, Follin A, Schell J, van Montagu M, De Greef J (1986) Agrobacterium T-DNA gene codes for tryptophan 2-monooxy-genase activity in tobacco crown gall cells. FEBS Lett 198:357–360. Scholar
  42. 42.
    Jouanin L, Vilaine F, Tourneur J, Tourneur C, Pautot V, Muller JF, Caboche M (1987) Transfer of a 4.3-kb fragment of the TL-DNA of Agrobacterium rhizogenes strain A4 confers the pRi-transformed phenotype to regenerated tobacco plants. Plant Sci 53:53–63. Scholar
  43. 43.
    Schröder G, Waffenschmidt S, Weiler E, Schröder J (1984) The NOC region of Ti plasmid codes for an enzyme synthesizing indole-3-acetic acid. Eur J Biochem 138:387–391. Scholar
  44. 44.
    Thomashow LS, Reeves S, Thomashow MF (1984) Crown gall oncogenesis: evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyzes synthesis of indoleacetic acid. Proc Natl Acad Sci 81:5071–5075. Scholar
  45. 45.
    Jung G, Tepfer D (1987) Use of genetic transformation by the Ri T-DNA of Agrobacterium rhizogenes to stimulate biomass and tropane alkaloid production in Atropa belladonna and Calystegia sepium roots grown in vitro. Plant Sci 50:145–151. Scholar
  46. 46.
    Kim YJ, Weathers PJ, Wyslouzil BE (2002) Growth of Artemisia annua hairy roots in liquid and gas phase reactors. Biotechnol Bioeng 80:454–464. Scholar
  47. 47.
    Kim YJ, Wyslouzil BE, Weathers PJ (2002) Invited review: secondary metabolism of hairy root cultures in bioreactors. In Vitro Cell Dev Biol Plant 38:1–10. Scholar
  48. 48.
    Balandrin MF, Klocke JA, Wurtele ES, Bollinger WH (1985) Natural plant chemicals: sources of industrial and medicinal materials. Science 228:1154–1160. Scholar
  49. 49.
    Berlin J, Wray V, Forche E, Reng HG, Schuler H, Luckinger R, Muhlbach HP (1985) Production of potato spindle tuber viroid (pstv) by large-scale fermentation of pstv-infected potato cell-suspension cultures. J Exp Bot 36(173):1985–1995. Scholar
  50. 50.
    Mukundan U, Carvalho EB, Curtis WR (1998) Growth and pigment production by hairy root cultures of Beta vulgaris L. in a bubble column reactor. Biotechnol Lett 20(5):469–474. Scholar
  51. 51.
    Rokem JS, Goldberg I (1985) Secondary metabolites from plant cell suspension cultures: methods for yield improvement. In: Advances in biotechnological processes. Alan R. Liss Inc, New York, pp 241–274Google Scholar
  52. 52.
    Charlwood BV, Charlwood KA (1991) Terpenoid production in plant cell culture. In: Harborne JB, Tomas-Barberan F (eds) Ecological chemistry and biochemistry of plant terpenoids. Clarendon Press, Oxford, pp 95–132Google Scholar
  53. 53.
    Tian L (2015) Using hairy roots for production of valuable plant secondary metabolites. Adv Biochem Eng Biotechnol 149:275–324. Scholar
  54. 54.
    Stuessy TF (2010) Paraphyly and the origin and classification of angiosperms. Taxon 59(3):689–693 wos:000278744000001Google Scholar
  55. 55.
    Bonhomme V, Laurain-Mattar D, Fliniaux MA (2004) Hairy root induction of Papaver somniferum var. album, a difficult-to-transform plant, by A. rhizogenes LBA 9402. Planta 218:890–893. Scholar
  56. 56.
    Rostampour S, Sohi H, Jourabchi E, Ansari E (2009) Influence of Agrobacterium rhizogenes on induction of hairy roots and benzylisoquinoline alkaloids production in Persian poppy (Papaver bracteatum Lindl.): preliminary report. World J Microbiol Biotechnol 25:1807–1814. Scholar
  57. 57.
    Giri A, Banerjee S, Ahuja PS, Giri CC (1997) Production of hairy roots in Aconitum heterophyllum wall. using Agrobacterium rhizogenes. In Vitro Cell Dev Biol Plant 33:280–284 WOS:000071401800006CrossRefGoogle Scholar
  58. 58.
    Thiruvengadam M, Rekha K, Chung I-M (2016) Induction of hairy roots by Agrobacterium rhizogenes-mediated transformation of spine gourd (Momordica dioica Roxb. ex. willd) for the assessment of phenolic compounds and biological activities. Sci Hortic 198:132–141. Scholar
  59. 59.
    Ju H-J, Jeyakumar J, Kamaraj M, Praveen N, Chung IM, Kim SH, Thiruvengadam M (2014) High frequency somatic embryogenesis and plant regeneration from hypocotyl and leaf explants of gherkin (Cucumis anguria L.). Sci Hortic 169:161–168. Scholar
  60. 60.
    Abhyankar G, Suprasanna P, Pandey BN, Mishra KP, Rao KV, Reddy VD (2010) Hairy root extract of Phyllanthus amarus induces apoptotic cell death in human breast cancer cells. Innov Food Sci Emerg Technol 11:526–532. Scholar
  61. 61.
    Bhattacharyya R, Bhattacharya S (2004) Development of a potent in vitro source of Phyllanthus amarus roots with pronounced activity against surface antigen of the hepatitis B virus. In Vitro Cell Dev Biol Plant 40:504–508. Scholar
  62. 62.
    Chang C, Chang K, Lin Y, Liu S, Chen C (2005) Hairy root cultures of Gynostemma pentaphyllum (Thunb.) Makino: a promising approach for the production of gypenosides as an alternative of ginseng saponins. Biotechnol Lett 27:1165–1169. Scholar
  63. 63.
    Takeda T, Kondo T, Mizukami H, Ogihara Y (1994) Bryonolic acid production in hairy roots of Trichosanthes kirilowii Max. var Japonica Kitam. transformed with Agrobacterium rhizogenes and its cytotoxic activity. Chem Pharm Bull(Tokyo) 42:730–732 WOS:A1994ND46600058CrossRefGoogle Scholar
  64. 64.
    Wahby I, Arráez-Román D, Segura-Carretero A, Ligero F, Caba JM, Fernández-Gutiérrez A (2006) Analysis of choline and atropine in hairy root cultures of Cannabis sativa L. by capillary electrophoresis-electrospray mass spectrometry. Electrophoresis 27:2208–2215. Scholar
  65. 65.
    Motomori Y, Shimomura K, Mori K, Kunitake H, Nakashima T, Tanaka M, Miyazaki S, Ishimaru K (1995) Polyphenol production in hairy root cultures of Fragaria x ananassa. Phytochemistry 40:1425–1428. Scholar
  66. 66.
    Asada Y, Li W, Yoshikawa T (1998) Isoprenylated flavonoids from hairy root cultures of Glycyrrhiza glabra. Phytochemistry 47:389–392. Scholar
  67. 67.
    Babaoglu M, Davey MR, Power JB, Sporer F, Wink M (2004) Transformed roots of Lupinus mutabilis: induction, culture and isoflavone biosynthesis. Plant Cell Tiss Org Cult 78:29–36. Scholar
  68. 68.
    Bourgaud F, Bouque V, Guckert A (1999) Production of flavonoids by Psoralea hairy root cultures. Plant Cell Tiss Org Cult 56:96–103 WOS:000082531600005CrossRefGoogle Scholar
  69. 69.
    Carron TR, Robbins MP, Morris P (1994) Genetic modification of condensed tannin biosynthesis in Lotus corniculatus. 1. Heterologous antisense dihydroflavonol reductase downregulates tannin accumulation in “hairy root” cultures. Theor Appl Genet 87:1006–1015 WOS:A1994NE95700015PubMedCrossRefGoogle Scholar
  70. 70.
    Ionkova I, Kartnig T, Alfermann W (1997) Cycloartane saponin production in hairy root cultures of Astragalus mongholicus. Phytochemistry 45:1597–1600. Scholar
  71. 71.
    Karwasara V, Dixit V (2009) Agrobacterium rhizogenes mediated genetic transformation of Abrus precatorius L. Pharmacognosy Mag 5:336–342 WOS:000276214100012CrossRefGoogle Scholar
  72. 72.
    Kim S, Cha M, Lee E, Kim I, Kwon J, Kang S, Park T (2012) In vitro induction of hairy root from isoflavones-producing Korean wild arrowroot Pueraria lobata. J Plant Biotechnol 39:205–211CrossRefGoogle Scholar
  73. 73.
    Ko K, Ebizuka Y, Noguchi H, Sankawa U (1995) Production of polypeptide pigments in hairy root cultures of Cassia plants. Chem Pharm Bull(Tokyo) 43:274–278CrossRefGoogle Scholar
  74. 74.
    Medina-Bolivar F, Condori J, Rimando A, Hubstenberger J, Shelton K, O’Keefe S, Bennett S, Dolan M (2007) Production and secretion of resveratrol in hairy root cultures of peanut. Phytochemistry 68:1992–2003. Scholar
  75. 75.
    Merkli A, Christen P, Kapetanidis I (1997) Production of diosgenin by hairy root cultures of Trigonella foenum-graecum L. Plant Cell Rep 16:632–636 WOS:A1997XG11400009CrossRefGoogle Scholar
  76. 76.
    Muji Ermayanti T, McComb JA, O’Brien PA (1994) Stimulation of synthesis and release of swainosonine from transformed roots of Swainsona galegifolia. Phytochemistry 36:313–317 WOS:A1994NQ30500011CrossRefGoogle Scholar
  77. 77.
    Shi H, Kintzios S (2003) Genetic transformation of Pueraria phaseoloides with Agrobacterium rhizogenes and puerarin production in hairy roots. Plant Cell Rep 21:1103–1107. Scholar
  78. 78.
    Shinde A, Malpathak N, Fulzele D (2009) Enhanced production of phytoestrogenic isoflavones from hairy root cultures of Psoralea corylifolia L. Using elicitation and precursor feeding. Biotechnol Bioprocess Eng 14:288–294.>CrossRefGoogle Scholar
  79. 79.
    Swain S, Rout K, Chand P (2012) Production of triterpenoid anti-cancer compound taraxerol in Agrobacterium-transformed root cultures of Butterfly Pea (Clitoria ternatea L.). Appl Biochem Biotechnol 168:487–503. Scholar
  80. 80.
    Udomsuk L, Jarukamjorn K, Tanaka H, Putalun W (2011) Improved isoflavonoid production in Pueraria candollei hairy root cultures using elicitation. Biotechnol Lett 33:369–374. Scholar
  81. 81.
    Zhang H, Liu J, Lu H, Gao S (2009) Enhanced flavonoid production in hairy root cultures of Glycyrrhiza uralensis Fisch by combining the over-expression of chalcone isomerase gene with the elicitation treatment. Plant Cell Rep 28:1205–1213. Scholar
  82. 82.
    Tusevski O, Stanoeva J, Stefova M, Kungulovski D, Pancevska N, Sekulovski N, Panov S, Simic S (2013) Hairy roots of Hypericum perforatum L.: a promising system for xanthone production. Cent Eur J Biol 8:1010–1022. Scholar
  83. 83.
    Tusevski O, Stanoeva JP, Stefova M, Pavokovic D, Simic SG (2014) Identification and quantification of phenolic compounds in Hypericum perforatum L. transgenic shoots. Acta physiologiae plantarum 36(10):2555–2569. Scholar
  84. 84.
    Lin HW, Kwok KH, Doran PM (2003) Development of Linum flavum hairy root cultures for production of coniferin. Biotechnol Lett 25:521–525. Scholar
  85. 85.
    Zhai B, Clark J, Ling T, Connelly M, Medina-Bolivar F, Rivas F (2014) Antimalarial evaluation of the chemical constituents of hairy root culture of Bixa orellana L. Molecules 19:756–766. Scholar
  86. 86.
    Triplett B, Moss S, Bland J, Dowd M (2008) Induction of hairy root cultures from Gossypium hirsutum and Gossypium barbadense to produce gossypol and related compounds. In Vitro Cell Dev Biol Plant 44:508–517. Scholar
  87. 87.
    Babakov A, Bartova L, Dridze I, Maisuryan A, Margulis G, Oganian R, Voblikova V, Muromtsev G (1995) Culture of transformed horseradish roots as a source of fusicoccin-like ligands. J Plant Growth Regul 14:163–167. Scholar
  88. 88.
    Głąb B, Furmanek T, Miklaszewska M, Banaś A, Królicka A (2013) Lipids in hairy roots and non-Agrobacterium induced roots of Crambe abyssinica. Acta Physiol Plant 35:2137–2145. Scholar
  89. 89.
    Wielanek M, Królicka A, Bergier K, Gajewska E, Skłodowska M (2009) Transformation of Nasturtium officinale, Barbarea verna and Arabis caucasica for hairy roots and glucosinolate-myrosinase system production. Biotechnol Lett 31:917–921. Scholar
  90. 90.
    Wielanek M, Urbanek H (1999) Glucotropaeolin and myrosinase production in hairy root cultures of Tropaeolum majus. Plant Cell Tiss Org Cult 57:39–45. Scholar
  91. 91.
    Srivastava S, Srivastava AK (2012) Azadirachtin production by hairy root cultivation of Azadirachta indica in a modified stirred tank reactor. Bioprocess Biosyst Eng 35:1549–1553. Scholar
  92. 92.
    Etsè KD, Aïdam AV, Melin C, Blanc N, Oudin A, Courdavault V, Creche J, Lanoue A (2014) Optimized genetic transformation of Zanthoxylum zanthoxyloides by Agrobacterium rhizogenes and the production of chelerythrine and skimmiamine in hairy root cultures. Eng Life Sci 14:95–99. Scholar
  93. 93.
    Sidwa-Gorycka M, Krolicka A, Orlita A, Malinski E, Golebiowski M, Kumirska J, Chromik A, Biskup E, Stepnowski P, Lojkowska E (2009) Genetic transformation of Ruta graveolens L. by Agrobacterium rhizogenes: hairy root cultures a promising approach for production of coumarins and furanocoumarins. Plant Cell Tiss Org Cult 97:59–69. Scholar
  94. 94.
    Bakkali AT, Jaziri M, Foriers A, Vander Heyden Y, Vanhaelen M, Homès J (1997) Lawsone accumulation in normal and transformed cultures of henna, Lawsonia inermis. Plant Cell Tiss Org Cult 51:83–87. Scholar
  95. 95.
    Ono N, Bandaranayake PCG, Tian L (2012) Establishment of pomegranate (Punica granatum) hairy root cultures for genetic interrogation of the hydrolyzable tannin biosynthetic pathway. Planta 236:931–94167. Scholar
  96. 96.
    Ishimaru K, Shimomura K (1991) Tannin production in hairy root culture of Geranium thunbergii. Phytochemistry 30:825–828. Scholar
  97. 97.
    Hamill J, Robins R, Rhodes M (1989) Alkaloid production by transformed root cultures of Cinchona ledgeriana. Planta Med 55:354–357 WOS:A1989AL50600005PubMedCrossRefGoogle Scholar
  98. 98.
    Lodhi AH, Bongaerts RJM, Verpoorte R, Coomber SA, Charlwood BV (1996) Expression of bacterial isochorismate synthase (EC in transgenic root cultures of Rubia peregrina. Plant Cell Rep 16:54–57 WOS:A1996VW96900012PubMedCrossRefGoogle Scholar
  99. 99.
    Park S, Kim Y, Lee S (2009) Establishment of hairy root culture of Rubia akane Nakai for alizarin and purpurin production. Sci Res Essays 4:94–97 WOS:000265885100008Google Scholar
  100. 100.
    Saito K, Sudo H, Yamazaki M, Koseki-Nakamura M, Kitajima M, Takayama H, Aimi N (2001) Feasible production of camptothecin by hairy root culture of Ophiorrhiza pumila. Plant Cell Rep 20:267–271 WOS:000168110200015CrossRefGoogle Scholar
  101. 101.
    Sato K, Yamazaki T, Okuyama E, Yoshihira K, Shimomura K (1991) Anthraquinone production by transformed root cultures of Rubia tinctorum: influence of phytohormones and sucrose concentration. Phytochemistry 30:1507–1509. Scholar
  102. 102.
    Krolicka A, Szpitter A, Stawujak K, Baranski R, Gwizdek-Wisniewska A, Skrzypczak A, Kaminski M, Lojkowska E (2010) Teratomas of Drosera capensis var. alba as a source of naphthoquinone: ramentaceone. Plant Cell Tiss Org Cult 103(3):285–292. Scholar
  103. 103.
    Taya M, Mine K, Kino-Oka M, Tone S, Ichi T (1992) Production and release of pigments by culture of transformed hairy root of red beet. J Ferment Bioeng 73:31–36. Scholar
  104. 104.
    Gangopadhyay M, Sircar D, Mitra A, Bhattacharya S (2008) Hairy root culture of Plumbago indica as a potential source for plumbagin. Biol Plant 52:533–537. Scholar
  105. 105.
    Verma PC, Singh D, Lu R, Gupta MM, Banerjee S (2002) In vitro-studies in Plumbago zeylanica: rapid micropropagation and establishment of higher plumbagin yielding hairy root cultures. J Plant Physiol 159:547–552. Scholar
  106. 106.
    Kim Y, Xu H, Park W, Park N, Lee S, Park S (2010) Genetic transformation of buckwheat (Fagopyrum esculentum M.) with Agrobacterium rhizogenes and production of rutin in transformed root cultures. Aust J Crop Sci 4:485–490 WOS:000282706300004Google Scholar
  107. 107.
    Thiruvengadam M, Praveen N, Kim E-H, Kim S-H, Chung I-M (2014) Production of anthraquinones, phenolic compounds and biological activities from hairy root cultures of Polygonum multiflorum Thunb. Protoplasma 251:555–566., 203CrossRefPubMedGoogle Scholar
  108. 108.
    Benjamin BD, Roja G, Heble MR (1994) Alkaloid synthesis by root cultures of Rauwolfia serpentina transformed by Agrobacterium rhizogenes. Phytochemistry 35:381–383. Scholar
  109. 109.
    Davioud E, Kan C, Hamon J, Tempé J, Husson H-P (1989) Production of indole alkaloids by in vitro root cultures from Catharanthus trichophyllus. Phytochemistry 28:2675–2680. Scholar
  110. 110.
    Sauerwein M, Ishimaru K, Shimomura K (1991) Indole alkaloids in hairy roots of Amsonia elliptica. Phytochemistry 30:1153–1155. Scholar
  111. 111.
    Shanks JV, Bhadra R, Morgan J, Rijhwani S, Vani S (1998) Quantification of metabolites in the indole alkaloid pathways of Catharanthus roseus: implications for metabolic engineering. Biotechnol Bioeng 58:333–338.–0290(19980420)58:2/3<333::AID-BIT35>3.0.CO;2-APubMedCrossRefGoogle Scholar
  112. 112.
    Sudha C, Obul Reddy B, Ravishankar G, Seeni S (2003) Production of ajmalicine and ajmaline in hairy root cultures of Rauvolfia micrantha Hook f., a rare and endemic medicinal plant. Biotechnol Lett 25(631–636):167. Scholar
  113. 113.
    Akhgari A, Laakso I, Seppanen-Laakso T, Yrjonen T, Vuorela H, Oksman-Caldentey KM, Rischer H (2015) Analysis of indole alkaloids from Rhazya stricta hairy roots by ultra-performance liquid chromatography-mass spectrometry. Molecules 20(12):22621–22634. Scholar
  114. 114.
    Ashraf MU, Muhammad G, Hussain MA, SNA B (2016) Cydonia oblonga M., A Medicinal Plant Rich in Phytonutrients for Pharmaceuticals. Front Pharmacol 7:163. 63CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Cui LJ, Ni XL, Ji Q, Teng XJ, Yang YR, Wu C, Zekria D, Zhang DS, Kai GY (2015) Co-overexpression of geraniol-10-hydroxylase and strictosidine synthase improves anti-cancer drug camptothecin accumulation in Ophiorrhiza pumila. Sci Rep 5:8227. Scholar
  116. 116.
    Huang SH, Vishwakarma RK, Lee TT, Chan HS, Tsay HS (2014) Establishment of hairy root lines and analysis of iridoids and secoiridoids in the medicinal plant Gentiana scabra. Bot Stud 55:17. Scholar
  117. 117.
    Ishimaru K, Sudo H, Satake M, Matsunaga Y, Hasegawa Y, Takemoto S, Shimomura K (1990) Amarogentin, amaroswerin and four xanthones from hairy root cultures of Swertia japonica. Phytochemistry 29:1563–1565. Scholar
  118. 118.
    Mencović N, Šavikin-Fodulović K, Vinterhalter B, Vinterhalter D, Jancović T, Krstić D (2000) Secoiridoid content in hairy roots of Gentiana punctata. Pharm Pharmacol Lett 10:73–75Google Scholar
  119. 119.
    Nagella P, Thiruvengadam M, Jung SJ, Murthy HN, Chung IM (2013) Establishment of Gymnema sylvestre hairy root cultures for the production of gymnemic acid. Acta Physiol Plant 35:3067–3073. Scholar
  120. 120.
    Tiwari RK, Trivedi M, Guang ZC, Guo GQ, Zheng GC (2007) Genetic transformation of Gentiana macrophylla with Agrobacterium rhizogenes: growth and production of secoiridoid glucoside gentiopicroside in transformed hairy root cultures. Plant Cell Rep 26:199–210. doi:10.1007/s00299-006-0236-0CrossRefPubMedGoogle Scholar
  121. 121.
    Bais HP, Walker TS, Schweizer HP, Vivanco JM (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995. Scholar
  122. 122.
    Dhakulkar S, Ganapathi TR, Bhargava S, Bapat VA (2005) Induction of hairy roots in Gmelina arborea Roxb. and production of verbascoside in hairy roots. Plant Sci 169:812–818. Scholar
  123. 123.
    Fraga BM, Díaz CE, Guadaño A, González-Coloma A (2005) Diterpenes from Salvia broussonetii transformed roots and their insecticidal activity. J Agric Food Chem 53:5200–5206. Scholar
  124. 124.
    Grzegorczyk I, Królicka A, Wysokińska H (2006) Establishment of Salvia officinalis L. hairy root cultures for the production of rosmarinic acid. Z Naturforsch C 61:351–356 WOS:000239444300009PubMedCrossRefGoogle Scholar
  125. 125.
    Kuźma Ł, Kisiel W, Królicka A, Wysokińska H (2011) Genetic transformation of Salvia austriaca by Agrobacterium rhizogenes and diterpenoid isolation. Pharmazie 66:904–907. Scholar
  126. 126.
    Kuźma Ł, Skrzypek Z, Wysokinska H (2006) Diterpenoids and triterpenoids in hairy roots of Salvia sclarea. Plant Cell Tiss Org Cult 84:152–160. Scholar
  127. 127.
    Lee S, Xu H, Kim Y, Park S (2008) Rosmarinic acid production in hairy root cultures of Agastache rugosa Kuntze. World J Microbiol Biotechnol 24:969–972. Scholar
  128. 128.
    Li F-X, Jin Z-P, Zhao D-X, Cheng L-Q, Fu C-X, Ma F (2006) Overexpression of the Saussurea medusa chalcone isomerase gene in S. involucrata hairy root cultures enhances their biosynthesis of apigenin. Phytochemistry 67:553–560. Scholar
  129. 129.
    Matsumoto T, Tanaka N (1991) Production of phytoecdysteroids by hairy root cultures of Ajuga reptans var. atropurpurea. Agric Biol Chem 55:1019–1025 WOS:A1991FL06900016Google Scholar
  130. 130.
    Sasaki K, Udagawa A, Ishimaru H, Hayashi T, Alfermann AW, Nakanishi F, Shimomura K (1998) High forskolin production in hairy roots of Coleus forskohlii. Plant Cell Rep 17:457–459 WOS:000073270200005CrossRefGoogle Scholar
  131. 131.
    Savona M, Mascarello C, Bisio A, Romussi G, Profumo P, Warchol M, Bach A, Ruffoni B (2003) S. cinnabarina Martens et Galeotti: optimisation of the extraction of a new compound, tissue culture and hairy root transformation. Agr Med 133:28–35Google Scholar
  132. 132.
    Zhi BH, Alfermann AW (1993) Diterpenoid production in hairy root cultures of Salvia miltiorrhiza. Phytochemistry 32:699–703 WOS:000259106300027CrossRefGoogle Scholar
  133. 133.
    Zhou Y, Hirotani M, Yoshikawa T, Furuya T (1997) Flavonoids and phenylethanoids from hairy root cultures of Scutellaria baicalensis. Phytochemistry 44:83–87. Scholar
  134. 134.
    Sauerwein M, Yamazaki T, Shimomura K (1991) Hernandulcin in hairy root cultures of Lippia dulcis. Plant Cell Rep 9:579–581 WOS:A1991FA20600012PubMedGoogle Scholar
  135. 135.
    Wysokiińska H, Rózga M (1998) Establishment of transformed root cultures of Paulownia tomentosa for verbascoside production. J Plant Physiol 152:78–83 WOS:000071824700012CrossRefGoogle Scholar
  136. 136.
    Georgiev MI (2011) Contemporary approaches towards production of phytopharmaceuticals: plant biotechnology meets medicinal chemistry. Mini-Rev Med Chem 11(10):822–822 WOS:000294691300001PubMedCrossRefGoogle Scholar
  137. 137.
    Grąbkowska R, Królicka A, Mielicki W, Wielanek M, Wysokińska H (2010) Genetic transformation of Harpagophytum procumbens by Agrobacterium rhizogenes: iridoid and phenylethanoid glycoside accumulation in hairy root cultures. Acta Physiol Plant 32:665–673. Scholar
  138. 138.
    Ogasawara T, Chiba K, Tada M (1993) Production in high-yield of a naphthoquinone by a hairy root culture of Sesamum indicum. Phytochemistry 33:1095–1098. Scholar
  139. 139.
    Cheruvathur MK, Jose B, Thomas TD (2015) Rhinacanthin production from hairy root cultures of Rhinacanthus nasutus (L.). Kurz In vitro Cell Dev Biol Plant 51(4):420–427. Scholar
  140. 140.
    Piatczak E, Talar A, Kuzma L, Wysokinska H (2015) Iridoid and phenylethanoid glycoside production in multiple shoots and regenerated Rehmannia elata NE Brown ex Prain plants following micropropagation. Acta physiologiae plantarum 37(12):UNSP 255. Scholar
  141. 141.
    Majumdar S, Garai S, Jha S (2011) Genetic transformation of Bacopa monnieri by wild type strains of Agrobacterium rhizogenes stimulates production of bacopa saponins in transformed calli and plants. Plant Cell Rep 30:941–954. Scholar
  142. 142.
    Pradel H, Dumke-Lehmann U, Diettrich B, Luckner M (1997) Hairy root cultures of Digitalis lanata. Secondary metabolism and plant regeneration. J Plant Physiol 151:209–215 WOS:A1997XT59100011CrossRefGoogle Scholar
  143. 143.
    Saito K, Yamazaki M, Shimomura K, Yoshimatsu K, Murakoshi I (1990) Genetic transformation of foxglove (Digitalis purpurea) by chimeric foreign genes and production of cardioactive glycosides. Plant Cell Rep 9:121–124. Scholar
  144. 144.
    Verma P, ur Rahman L, Negi A, Jain D, Khanuja SPS, Banerjee S (2007) Agrobacterium rhizogenes-mediated transformation of Picrorhiza kurroa Royle ex Benth.: establishment and selection of superior hairy root clone. Plant Biotechnol Rep 1:169–174. Scholar
  145. 145.
    Tada H, Nakashima T, Kunitake H, Mori K, Tanaka M, Ishimaru K (1996) Polyacetylenes in hairy root cultures of Campanula medium L. J Plant Physiol 147:617–619 WOS:A1996TV52900022CrossRefGoogle Scholar
  146. 146.
    Bonhomme V, Laurain-Mattar D, Lacoux J, Fliniaux MA, Jacquin-Dubreuil A (2000) Tropane alkaloid production by hairy roots of Atropa belladonna obtained after transformation with Agrobacterium rhizogenes 15834 and Agrobacterium tumefaciens containing rol A, B, C genes only. J Biotechnol 81:151–158. Scholar
  147. 147.
    Carrizo CN, Pitta-Alvarez SI, Kogan MJ, Giulietti AM, Tomaro ML (2001) Occurrence of cadaverine in hairy roots of Brugmansia candida. Phytochemistry 57:759–763. Scholar
  148. 148.
    Caspeta L, Quintero R, Villarreal ML (2005) Novel airlift reactor fitting for hairy root cultures: developmental and performance studies. Biotechnol Prog 21:735–740. Scholar
  149. 149.
    Christen P, Roberts M, Phillipson JD, Evans W (1989) High-yield production of tropane alkaloids by hairy-root cultures of a Datura candida hybrid. Plant Cell Rep 8:75–77 WOS:A1989U876700006PubMedCrossRefGoogle Scholar
  150. 150.
    Deno H, Yamagata H, Emoto T, Yoshioka T, Yamada Y, Fujita Y (1987) Scopolamine production by root cultures of Duboisia myoporoides: II. Establishment of a hairy root culture by infection with Agrobacterium rhizogenes. J Plant Physiol 131:315–323 WOS:A1987L589900014CrossRefGoogle Scholar
  151. 151.
    Ikenaga T, Oyama T, Muranaka T (1995) Growth and steroidal saponin production in hairy root cultures of Solanum aculeatissimum. Plant Cell Rep 14:413–417 WOS:A1995QV24100003PubMedCrossRefGoogle Scholar
  152. 152.
    Jaziri M, Legros M, Homes J, Vanhaelen M (1988) Tropine alkaloids production by hairy root cultures of Datura stramonium and Hyoscyamus niger. Phytochemistry 27:419–420. Scholar
  153. 153.
    Kittipongpatana N, Hock R, Porter J (1998) Production of solasodine by hairy root, callus, and cell suspension cultures of Solanum aviculare Forst. Plant Cell Tiss Org Cult 52:133–143. Scholar
  154. 154.
    Knopp E, Strauss A, Wehrli W (1988) Root induction on several Solanaceae species by Agrobacterium rhizogenes and the determination of root tropane alkaloid content. Plant Cell Rep 7:590–593 WOS:A1988R565200033PubMedCrossRefGoogle Scholar
  155. 155.
    Mano Y, Nabeshima S, Matsui C, Ohkawa H (1987) Production of tropane alkaloids by hairy-root cultures of Scopolia japonica. Agric Biol Chem 50:2715–2722 WOS:A1986E987000003Google Scholar
  156. 156.
    Mano Y, Ohkawa H, Yamada Y (1989) Production of tropane alkaloids by hairy root cultures of Duboisia leichhardtii transformed by Agrobacterium rhizogenes. Plant Sci 59:191–201. Scholar
  157. 157.
    Murthy HN, Dijkstra C, Anthony P, White DA, Davey MR, Power JB, Hahn EJ, Paek KY (2008) Establishment of Withania somnifera hairy root cultures for the production of Withanolide A. J Integr Plant Biol 50:975–981. Scholar
  158. 158.
    Nussbaumer P, Kapétanidis I, Christen P (1998) Hairy roots of Datura candida×D. aurea: effect of culture medium composition on growth and alkaloid biosynthesis. Plant Cell Rep 17:405–409 WOS:000072596000015CrossRefGoogle Scholar
  159. 159.
    Okršlar V, Štrukelj B, Kreft S, Bohanec B, Zel J (2002) Micropropagation and hairy root culture of Solanum laciniatum Ait. In Vitro Cell Dev Biol Plant 38:352–357. Scholar
  160. 160.
    Parr A, Hamill J (1987) Relationship between Agrobacterium rhizogenes transformed hairy roots and intact, uninfected nicotiana plants. Phytochemistry 26:3241–3245 WOS:A1987L039000027CrossRefGoogle Scholar
  161. 161.
    Sauerwein M, Shimomura K (1991) Alkaloid production in hairy roots of Hyoscyamus albus transformed with Agrobacterium rhizogenes. Phytochemistry 30:3277–3280. Scholar
  162. 162.
    Cequier-Sanchez E, Rodriguez C, Dorta-Guerra R, Ravelo A, Zarate R (2011) Echium acanthocarpum hairy root cultures, a suitable system for polyunsaturated fatty acid studies and production. BMC Biotechnol 11:42. Scholar
  163. 163.
    Shimomura K, Sudo H, Saga H, Kamada H (1991) Shikonin production and secretion by hairy root cultures of Lithospermum erythrorhizon. Plant Cell Rep 10:282–285 WOS:A1991GG17000003PubMedCrossRefGoogle Scholar
  164. 164.
    Alikaridis F, Papadakis D, Pantelia K, Kephalas T (2000) Flavonolignan production from Silybum marianum transformed and untransformed root cultures. Fitoterapia 71:379–384. Scholar
  165. 165.
    Constabel CP, Towers GHN (1988) Thiarubrine accumulation in hairy root cultures of Chaenactis douglasii. J Plant Physiol 133:67–72 WOS:A1988Q000100012CrossRefGoogle Scholar
  166. 166.
    Delbeque J, Beydon P, Chapuis L (1995) In vitro incorporation of radio labelled cholesterol and mevalonic acid into ecdysterone by hairy root cultures of a plant Serratula tinctoria. Eur J Entomol 92:301–307 WOS:A1995QN05500037Google Scholar
  167. 167.
    Flores H, Pickard J, Hoy M (1988) Production of polyacetylenes and thiophenes in heterotrophic and photosynthetic root cultures of Asteraceae. In: Lam J, Breheler H, Arnason T, Hansen L (eds) Chemistry and biology of naturally occurring acetylenes and related compounds (NOARC) bioactive molecules, vol 7. Elsevier, Amsterdam, pp 233–254Google Scholar
  168. 168.
    Fu C, Zhao D, Xue X, Jin Z, Ma F (2005) Transformation of Saussurea involucrata by Agrobacterium rhizogenes: hairy root induction and syringin production. Proc Biochem 40:3789–3794. Scholar
  169. 169.
    Gunjan S, Lutz J, Bushong A, Rogers D, Littleton J (2013) Hairy root cultures and plant regeneration in Solidago nemoralis transformed with Agrobacterium rhizogenes. Am J Plant Sci 4:1675–1678CrossRefGoogle Scholar
  170. 170.
    Hook I (1994) Secondary metabolites in hairy root cultures of Leontopodium alpinum Cass. (Edelweiss). Plant Cell Tiss Org Cult 38:321–326. Scholar
  171. 171.
    Inoguchi M, Ogawa S, Furukawa S, Kondo H (2003) Production of an allelopathic polyacetylene in hairy root cultures of goldenrod (Solidago altissima L.). Biosci Biotechnol Biochem 67:863–868 WOS:000182733600027PubMedCrossRefGoogle Scholar
  172. 172.
    Kisiel W, Stojakowska A (1997) A sesquiterpene coumarin ether from transformed roots of Tanacetum parthenium. Phytochemistry 46:515–516. Scholar
  173. 173.
    Kisiel W, Stojakowska A, Malarz J, Kohlmüzer S (1995) Sesquiterpene lactones in Agrobacterium rhizogenes—transformed hairy root culture of Lactuca virosa. Phytochemistry 40:1139–1140. Scholar
  174. 174.
    Kyo M, Miyauchi Y, Fujimoto T, Mayama S (1990) Production of nematocidal compounds by hairy root cultures of Tagetes patula L. Plant Cell Rep 9:393–397 WOS:A1990EH92500012PubMedCrossRefGoogle Scholar
  175. 175.
    Malarz J, Stojakowska A, Kisiel W (2002) Sesquiterpene lactones in a hairy root culture of Cichorium intybus. Z Naturforsch 57c:994–997 WOS:000181126300008CrossRefGoogle Scholar
  176. 176.
    Nin S, Bennici A, Roselli G, Mariotti D, Schiff S, Magherini R (1997) Agrobacterium mediated transformation of Artemisia absinthium L. (wormwood) and production of secondary metabolites. Plant Cell Rep 16:725–730 WOS:A1997XL61800013CrossRefGoogle Scholar
  177. 177.
    Romero F, Delate K, Kraus G, Solco A, Murphy P, Hannapel D (2009) Alkamide production from hairy root cultures of Echinacea. In Vitro Cell Dev Biol Plant 45:599–609. Scholar
  178. 178.
    Thron U, Maresch L, Beiderbeck R, Reichling J (1989) Accumulation of unusual phenylpropanoids in transformed and non-transformed root cultures of Coreopsis tinctoria. Z Naturforsch 44:573–577 WOS:A1989AL99700006CrossRefGoogle Scholar
  179. 179.
    Weathers PJ, Cheetham RD, Follansbee E, Teoh K (1994) Artemisinin production by transformed roots of Artemisia annua. Biotechnol Lett 16:1281–1286 WOS:A1994PY72500011Google Scholar
  180. 180.
    Zhao D, Fu C, Chen Y, Ma F (2004) Transformation of Saussurea medusa for hairy roots and jaceosidin production. Plant Cell Rep 23:468–474. Scholar
  181. 181.
    Jun Cheul A, Baik H, Tada H, Ishimaru K, Sasaki K, Shimomura K (1996) Polyacetylenes in hairy roots of Platycodon grandiflorum. Phytochemistry 42:69–72 WOS:A1996UF46700013CrossRefGoogle Scholar
  182. 182.
    Murakami Y, Shimomura K, Yoshihira K, Ishimaru K (1998) Polyacetylenes in hairy root cultures of Trachelium caeruleum L. J Plant Physiol 152:574–576 WOS:000073921400034CrossRefGoogle Scholar
  183. 183.
    Tada H, Shimomura K, Ishimaru K (1995) Polyacetylenes in hairy root cultures of Lobelia chinensis Lour. J Plant Physiol 146:199–202 WOS:A1995RJ37600002CrossRefGoogle Scholar
  184. 184.
    Tanaka N, Matsuura E, Terahara N, Ishimaru K (1999) Secondary metabolites in transformed root cultures of Campanula glomerata. J Plant Physiol 155:251–254 WOS:000081977000015CrossRefGoogle Scholar
  185. 185.
    Yamanaka M, Ishibashi K, Shimomura K, Ishimaru K (1996) Polyacetylene glucosides in hairy root cultures of Lobelia cardinalis. Phytochemistry 41:183–185. Scholar
  186. 186.
    Yonemitsu H, Shimomura K, Satake M, Mochida S, Tanaka M, Endo T, Kaji A (1990) Lobeline production by hairy root culture of Lobelia inflata. Plant Cell Rep 9(6):307–310 WOS:A1990EE64700004PubMedCrossRefGoogle Scholar
  187. 187.
    Bálványos I, Kursinszki L, Szoke E (2001) The effect of plant growth regulators on biomass formation and lobeline production of Lobelia inflata L. hairy root cultures. Plant Growth Regul 34(3):339–345. Scholar
  188. 188.
    Gränicher F, Christen P, Kapétanidis I (1995) Production of valepotriates by hairy root cultures of Centranthus ruber DC. Plant Cell Rep 14:294–298 WOS:A1995QG30000006PubMedCrossRefGoogle Scholar
  189. 189.
    Banerjee S, ur Rahman L, Uniyal GC, Ahuja PS (1998) Enhanced production of valepotriates by Agrobacterium rhizogenes induced hairy root cultures of Valeriana wallichii DC. Plant Sci 131:203–208. Scholar
  190. 190.
    Gränicher F, Christen P, Kapetanidis I (1992) High-yield production of valepotriates by hairy root cultures of Valeriana officinalis L. var. sambucifolia Mikan. Plant Cell Rep 11:339–342 WOS:A1992JD35800004PubMedCrossRefGoogle Scholar
  191. 191.
    Ahn J, Chong W, Kim Y, Hwang B (2006) Optimization of the sucrose and ion concentrations for saikosaponin production in hairy root culture of Bupleurum falcatum. Biotechnol Bioprocess Eng 11:121–126. Scholar
  192. 192.
    Arellano J, Vázquez F, Villegas T, Hernández G (1996) Establishment of transformed root cultures of Perezia cuernavacana producing the sesquiterpene quinone perezone. Plant Cell Rep 15:455–458 WOS:A1996UB44900001PubMedCrossRefGoogle Scholar
  193. 193.
    Kim O, Bang K, Shin Y, Lee M, Jung S, Hyun D, Kim Y, Seong N, Cha S, Hwang B (2007) Enhanced production of asiaticoside from hairy root cultures of Centella asiatica (L.) Urban elicited by methyl jasmonate. Plant Cell Rep 26:1941–1949. Scholar
  194. 194.
    Królicka A, Staniszewska I, Bielawski K, Maliński E, Szafranek J, Łojkowska E (2001) Establishment of hairy root cultures of Ammi majus. Plant Sci 160:259–264. Scholar
  195. 195.
    Kursinszki L, Troilina J, Szõke É (1998) Determination of visnagin in Ammi visnaga hairy root cultures using solid-phase extraction and high-performance liquid chromatography. Microchem J 59:392–398. Scholar
  196. 196.
    Santos PG, Figueiredo AC, Lourenço PL, Barroso J, Pedro L, Oliveira MM, Schripsema J, Deans S, Scheffer JC (2002) Hairy root cultures of Anethum graveolens (Dill): establishment, growth, time-course study of their essential oil and its comparison with parent plant oils. Biotechnol Lett 24:1031–1036. Scholar
  197. 197.
    Santos PAG, Figueiredo AC, Oliveira MM, Barroso JG, Pedro LG, Deans SG, Scheffer JJC (2005) Growth and essential oil composition of hairy root cultures of Levisticum officinale W. D.J. Koch (lovage). Plant Sci 168:1089–1096. Scholar
  198. 198.
    Santos PM, Figueiredo AC, Oliveira MM, Barroso J, Pedro LG, Deans SG, Younus AKM, Scheffer JJC (1998) Essential oils from hairy root cultures and from fruits and roots of Pimpinella anisum. Phytochemistry 48:455–460. Scholar
  199. 199.
    Sircar D, Roychowdhury A, Mitra A (2007) Accumulation of p-hydroxybenzoic acid in hairy roots of Daucus carota. J Plant Physiol 164:1358–1366. Scholar
  200. 200.
    Xu H, Park J, Kim Y, Park N, Lee S, Park S (2009) Optimization of growth and pyranocoumarins production in hairy root culture of Angelica gigas Nakai. J Med Plant Res 3:978–981 WOS:000281784600023Google Scholar
  201. 201.
    Mathur A, Gangwar A, Mathur A, Verma P, Uniyal G, Lal R (2010) Growth kinetics and ginsenosides production in transformed hairy roots of American ginseng—Panax quinquefolium L. Biotechnol Lett 32:457–461. Scholar
  202. 202.
    Washida D, Shimomura K, Nakajima Y, Takido M, Kitanaka S (1998) Ginsenosides in hairy roots of a panax hybrid. Phytochemistry 49:2331–2335. Scholar
  203. 203.
    Yoshikawa T, Furuya T (1987) Saponin production by cultures of Panax ginseng transformed with Agrobacterium rhizogenes. Plant Cell Rep 6:449–453 WOS:A1987L335900013PubMedGoogle Scholar
  204. 204.
    Venditti A, Serrilli AM, Bianco A (2013) Iridoids from Bellardia trixago (L.) all. Nat Prod Res 27:1413–1416PubMedCrossRefGoogle Scholar
  205. 205.
    Venditti A, Ballero M, Serafini M, Bianco A (2014) Polar compounds from Parentucellia viscosa (L.) Caruel from Sardinia. Nat Prod Res 29:602–606. Scholar
  206. 206.
    Venditti A, Serafini M, Nicoletti M, Bianco A (2015) Terpenoids of Linaria alpina (L.) Mill. from Dolomites, Italy. Nat Prod Res 29(21):2041–2044. Scholar
  207. 207.
    Serafini M, Corazzi G, Poli F, Piccin A, Tomassini L, Foddai S (2005) Phenylpropanoid glycosides in Italian Orobanche spp., sect Orobanche. Nat Prod Res 19(6):547–550. Scholar
  208. 208.
    Venditti A, Frezza C, Serafini M, Bianco A (2016) Iridoids and phenylethanoid from Pedicularis kerneri Dalla Torre growing in Dolomites, Italy. Nat Prod Res 30(3):327–331 Scholar
  209. 209.
    Venditti A, Serrilli AM, Di Cecco M (2012) Phytochemical analysis of Plantago sempervirens from Majella National Park. Nat Prod Res 26(2):2035–2039. Scholar
  210. 210.
    Cheriet T, Baatouche S, Sarri D, Chalard P, Seghiri R, Mekkiou R, Boumaza O, Leon F, Benayache S, Benayache F (2015) Secondary Metabolites from Linaria tingitana. Nat Prod Res 51(6):1202–1203. Scholar
  211. 211.
    Begley TP (2009) Encyclopedia of chemical biology. Wiley, Hoboken. Scholar
  212. 212.
    Bálványos I, Szõke É, Kursinszki L (1998) Effect of magnesium on the growth and alkaloid production of Lobelia inflate L. hairy root cultures. In: Kiss SA (ed) Magnesium and interaction of magnesium with trace elements. Hung Chemical Society, Budapest, pp 358–361Google Scholar
  213. 213.
    Cavé A, Rigadère B, Laurens A, Cortes D (1996) Acetogenins from Annonaceae. In: Herz W (ed) Progress in the chemistry of organic natural products, vol 70. The Florida State University, Tallahassee, pp 81–288Google Scholar
  214. 214.
    Richardson LL, Adler LS, Leonard AS, Andicoechea JKH, Anthony WE, Manson JS, Irwin RE (2015) Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc Royal Soc B Biol Sci 282(1803):20142471. Scholar
  215. 215.
    Sampaio-Santos MI, Kaplan MAC (2001) Biosynthesis significance of iridoids in chemosystematics. J Braz Chem Soc 12(2):144–153 WOS:000168263300004CrossRefGoogle Scholar
  216. 216.
    Marak HB, Biere A, Van Damme JMM (2002) 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. Scholar
  217. 217.
    Marak HB, Biere A, Van Damme JMM (2002) 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. Scholar
  218. 218.
    Biere A, Marak HB, Van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441. Scholar
  219. 219.
    Meira M, da Silva EP, David JM, David JP Review of the genus Ipomoea: traditional uses, chemistry and biological activities. Rev Bras Farm 22(3):682–713. Scholar
  220. 220.
    Zhang P, Li X, Wang BG (2016) Secondary metabolites from the marine algal-derived endophytic fungi: chemical diversity and biological activity. Planta Med 82(9–10):832–842 SI Scholar
  221. 221.
    Sekulić T.D., Božin B., Smoliński A. (2016) Chemometric study of biological activites of 10 aromatic Lamiaceae species’ essential oils J Chemometr 30(4):188–196
  222. 222.
    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. Scholar
  223. 223.
    Robins RJ (1998) The application of root cultures to problems of biological chemistry. Nat Prod Rep 15:549–570 WOS:000077782100002CrossRefGoogle Scholar
  224. 224.
    Moyano E, Fornale S, Palazon J, Cusido RM, Bonfill M, Morales C, Pinol MT (1999) Effect of Agrobacterium rhizogenes T-AND on alkaloid production in Solanaceae plants. Phytochemistry 52:1287–1292. Scholar
  225. 225.
    Palazon J, Cusido RM, Gonzalo J, Bonfill M, Morales C, Pinol MT (1998) Relation between the amount the rolC gene product and indole alkaloid accumulation in Catharanthus roseus transformed root cultures. J Plant Physiol 153:712–718 WOS:000077320800027CrossRefGoogle Scholar
  226. 226.
    Shkryl YN, Veremeichik GN, Bulgakov VP, Tchernoded GK, Mischenko NP, Fedoreyev SA, Zhuravlev YN (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. Scholar
  227. 227.
    Kiselev KV, Dubrovina AS, Veselova MV, Bulgakov VP, Fedoreyev SA, Zhuravlev YN (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692. Scholar
  228. 228.
    Bulgakov VP, Veremeichik GN, Grigorchuk VP, Rybin VG, Shkryl YN (2016) The rolB gene activates secondary metabolism in Arabidopsis calli via selective activation of genes encoding MYB and bHLH transcription factors. Plant Physiol Biochem 102:70–79. Scholar
  229. 229.
    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. Scholar
  230. 230.
    Palazon J, Cusido RM, Roig C, Pinol MT (1998) Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Rep 17(3):84–90 WOS:000072596000011Google Scholar
  231. 231.
    Bulgakov VP, Khodakovskaya MV, Labetskaya NV, Chernoded GK, Zhuravlev YN (1998) The impact of plant rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochemistry 49:1929–1934. Scholar
  232. 232.
    Bulgakov VP, Tchernoded GK, Mischenko NP, Khodakovskaya M, Glazunov VP, Radchenko SV, Zvereva EV, Fedoreyev SA, Zhuravlev YN (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. Scholar
  233. 233.
    Bulgakov VP, Tchernoded GK, Mischenko NP, Shkryl YN, Glazunov VP, Fedoreyev SA, Zhuravlev YN (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. Scholar
  234. 234.
    Kayani WK, Palazòn J, Cusidòb RM, Mirza B (2016) The effect of rol genes on phytoecdysteroid biosynthesis in Ajuga bracteosa differs between transgenic plants and hairy roots. RSC Adv 6:22700–22708. Scholar
  235. 235.
    Bulgakov VP, Veselova MV, Tchernoded GK, Kiselev KV, Fedoreyev SA, Zhuravlev YN (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. Scholar
  236. 236.
    Bulgakov VP, Tchernoded GK, Mischenko NP, Fedoreyev SA, Shkryl YN, Zhuravlev YN (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. Scholar
  237. 237.
    Bulgakov VP, Aminin DL, Shkryl YN, Gorpenchenko TY, Veremeichik GN, Dmitrenok PS, Zhuravlev YN (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. Scholar
  238. 238.
    Schmulling T, Schell J, Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7:2621–2629 WOS:A1988P845900001PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Kiselev KV, Kusaykin MI, Dubrovina AS, Bezverbny DA, Zvyagintseva TN, Bulgakov VP (2006) The rolC gene induces expression of a pathogenesis-related b-1,3glucanase in transformed ginseng cells. Phytochemistry 67:2225–2231. Scholar
  240. 240.
    Inyushkina YV, Bulgakov VP, Veselova MV, Bryukhanov VM, Zverev YF, Lampatov VV, Azarova OV, Tchernoded GK, Fedoreyev SA, Zhuravlev YN (2007) High rabdosiin and rosmarinic acid production in Eritrichium sericeum callus cultures and effect of the calli on Masugi nephritis in rats. Biosci Biotechnol Biochem 71:1286–1293. Scholar
  241. 241.
    Inyushkina YV, Kiselev KV, Bulgakov VP, Zhuravlev YN (2009) Specific genes of cytochrome P450 monooxygenases are implicated in biosynthesis of caffeic acid metabolites in rolC-transgenic culture of Eritrichium sericeum. Biochemistry (Mosc) 74:917–924. Scholar
  242. 242.
    Mukundan U, Dawda HG, Ratnaparkhi S (1997) Hairy root culture and secondary metabolite production. Agro Botanica, MumbaiGoogle Scholar
  243. 243.
    Wallaart TE, Pras N, Quax WJ (1999) Isolation and identification of dihydroartemisinic acid hydroperoxide from Artemisia annua: a novel biosynthetic precursor of artemisinin. J Nat Prod 62:1160–1162. Scholar
  244. 244.
    White FF, Garfinkel DJ, Huffman GA, Gordon MP, Nester EW (1983) Sequence homologous to Agrobacterium rhizogenes TDNA in the genomes of uninfected plants. Nature 301:348–350. Scholar
  245. 245.
    Matveeva TV, Bogomaz DI, Pavlova OA, Nester EW, Lutova LA (2012) Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. Mol Plant Microbe Interact 25:1542–1551. Scholar
  246. 246.
    Kyndt T, Quispe D, Zhai H, Jarret R, Ghislain M, Liu Q, Gheysen G, Kreuze JF (2015) The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: An example of a naturally transgenic food crop. Proc Natl Acad Sci U S A 112(18):5844–5849. Scholar
  247. 247.
    Suzuki K, Yamashita I, Tanaka N (2002) Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution. Plant J 32:775–787. Scholar
  248. 248.
    Matveeva TV, Kosachev PA (2013) Sequences homologous to 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 WOS:000337630200070Google Scholar
  249. 249.
    Pavlova OA, Matveeva TV, Lutova LA (2014) Genome of Linaria dalmatica contains Agrobacterium rhizogenes rolC Gene Homolog. Russ J Genet Appl Res 4(5):461–465CrossRefGoogle Scholar
  250. 250.
    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. Scholar
  251. 251.
    Matveeva TV, Lutova LA (2014) Horizontal gene transfer from Agrobacterium to plants. Front Plant Sci 5:326PubMedPubMedCentralCrossRefGoogle Scholar
  252. 252.
    Matveeva TV, Sokornova SV, Lutova LA (2015) Influence of Agrobacterium oncogenes on secondary metabolism of plants. Phytochem Rev 14:541. Scholar
  253. 253.
    Weeks WW (1999) Chapter 8D, Relationship between leaf chemistry and organoleptic properties of tobacco smoke. In: Davis DL, Nielsen MT (eds) Tobacco: production, chemistry, and technology. Iowa State Press/Blackwell Science, Inc., Malden, pp 304–312Google Scholar
  254. 254.
    Bush L, Hempflin WP, Burton H (1999) Biosynthesis of nicotine and related compounds. In: Gorrod JW, Jacob III P (eds) Analytical determination of nicotine and related compounds and their metabolites. Elsevier Science B.V, Amsterdam, pp 13–44CrossRefGoogle Scholar
  255. 255.
    Baldwin IT (1989) Mechanism of damage-induced alkaloid production in wild tabacco. J Chem Ecol 15:1661–1680PubMedCrossRefGoogle Scholar
  256. 256.
    Wei X, Sumithran SP, Deaciuc AG, Burton HR, Bush LP, Dwoskin LP, Crooks PA (2005) Identification and synthesis of novel alkaloids from the root system of Nicotiana tabacum: Affinity for neuronal nicotinic acetylcholine receptors. Life Sci 78:495–505PubMedCrossRefGoogle Scholar
  257. 257.
    Bailey JA, Burden RS, Vincent GG (1975) Capsidiol: an antifungal compound produced in Nicotiana tabacum and Nicotiana clevelandii following infection with tobacco necrosis virus. Phytochemistry 14:597–582CrossRefGoogle Scholar
  258. 258.
    Bailey JA, Vincent GG, Burden RS (1976) The antifungal activity of glutinosone and capsidiol and their accumulation in virus-infected tobacco species. Physiol Plant Pathol 8:35–41CrossRefGoogle Scholar
  259. 259.
    Gordon M, Stoessl A, Stothers JB (1973) Post-infectional inhibitors from plants .4. structure of capsidiol – antifungal sesquiterpene from sweet peppers. Can J Chem-revue canadienne de chimie 51(5):748–752 WOS:A1973P134800015CrossRefGoogle Scholar
  260. 260.
    El-Naggar LJ, Beal JL (1980) Iridoids. An updated review. Part I. J Nat Prod 43:649–707PubMedCrossRefGoogle Scholar
  261. 261.
    Boros CA, Stermitz FR (1990) Iridoids. An updated review. Part II. J Nat Prod 53:1055–1147. Scholar
  262. 262.
    Harborne JB, Valdés B (1971) Identification of scutellarein 40-methyl ether in Linaria aeruginea. Phytochem Rev 10:2850–2851. Scholar
  263. 263.
    Kuptsova LP, Ban’kovskii AI (1970) A new flavonoid from some species of toadflax. Khimiya Prirodnykh Soedinenii 6(1):128–129Google Scholar
  264. 264.
    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 WOS:A1974T923800009CrossRefGoogle Scholar
  265. 265.
    Ercil D, Sakar MK (2004) Chemical constituents of Linaria aucheri. Turk J Chem 28:133–139 WOS:000220680100015Google Scholar
  266. 266.
    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 WOS:A1975V063200006CrossRefGoogle Scholar
  267. 267.
    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 WOS:A1980KG51800017CrossRefGoogle Scholar
  268. 268.
    Kitagawa I, Yoshihara M, Kamigauchi T (1977) Linarienone, a newcis-clerodane-type diteppene from the subterranean part of Linaria japonica Miq. Tetrahedron Lett 14:1221–1224 WOS:A1977DB08900003CrossRefGoogle Scholar
  269. 269.
    Feliciano AS, Gordaliza M, Del Corral JMM et al (1993) Neoclerodane diterpenoids from roots of Linaria saxatilis var glutinosa. Phytochemistry 33(3):631–633. Scholar
  270. 270.
    Widhalm JR, Rhodes D (2016) Biosynthesis and molecular actions of specialized 1,4-naphthoquinone natural products produced by horticultural plants. Hortic Res 3:16046. Scholar
  271. 271.
    Hanson JR (2015) Diterpenoids of terrestrial origin. Nat Prod Rep 32:76–87. Scholar
  272. 272.
    Nicoletti M, Serafini M, Garbarino JA et al (1988) A chemosystematic study of Scrophulariaceae iridoid glycosides.G. Bot Ital 122(1–2):13–24. Scholar
  273. 273.
    Guiso M, Tassone G, Nicoletti M et al (2007) Chemotaxonomy of iridoids in Linaria vulgaris. Nat Prod Lett 21(13):1212–1216. Scholar
  274. 274.
    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. Scholar
  275. 275.
    Taskova R, Mitova M, Evstatieva L et al (1997) Iridoids, flavonoids and terpenoids as taxonomic markers in Lamiaceae, Scrophulariaceae, and Rubiaceae. Bocconea 5:631–636Google Scholar
  276. 276.
    Sticher O (1977) Plant mono terpenoids di terpenoids and sesquiterpenoids 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 148Google Scholar
  277. 277.
    Bulgakov VP, Shkryl YN, Veremeichik GN, Gorpenchenko TY, Vereshchagina YV (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. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.St. Petersburg State UniversitySt. PetersburgRussia
  2. 2.All Russian Institute of Plant ProtectionSt. PetersburgRussia

Personalised recommendations