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Composite potato plants with transgenic roots on non-transgenic shoots: a model system for studying gene silencing in roots

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Abstract

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Composite potato plants offer an extremely fast, effective and reliable system for studies on gene functions in roots using antisense or inverted-repeat but not sense constructs for gene inactivation.

Abstract

Composite plants, with transgenic roots on a non-transgenic shoot, can be obtained by shoot explant transformation with Agrobacterium rhizogenes. The aim of this study was to generate composite potato plants (Solanum tuberosum) to be used as a model system in future studies on root-pathogen interactions and gene silencing in the roots. The proportion of transgenic roots among the roots induced was high (80–100 %) in the four potato cultivars tested (Albatros, Desirée, Sabina and Saturna). No wild-type adventitious roots were formed at mock inoculation site. All strains of A. rhizogenes tested induced phenotypically normal roots which, however, showed a reduced response to cytokinin as compared with non-transgenic roots. Nevertheless, both types of roots were infected to a similar high rate with the zoospores of Spongospora subterranea, a soilborne potato pathogen. The transgenic roots of composite potato plants expressed significantly higher amounts of β-glucuronidase (GUS) than the roots of a GUS-transgenic potato line event. Silencing of the uidA transgene (GUS) was tested by inducing roots on the GUS-transgenic cv. Albatros event with strains of A. rhizogenes over-expressing either the uidA sense or antisense transcripts, or inverted-repeat or hairpin uidA RNA. The three last mentioned constructs caused 2.5–4.0 fold reduction in the uidA mRNA expression. In contrast, over-expression of uidA resulted in over 3-fold increase in the uidA mRNA and GUS expression, indicating that sense-mediated silencing (co-suppression) was not functional in roots. The results suggest that composite plants offer a useful experimental system for potato research, which has gained little previous attention.

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References

  • Alpizar E, Dechamp E, Espeout S, Royer M, Lecouls AC, Nicole M, Bertrand B, Lashermes P, Etienne H (2006) Efficient production of Agrobacterium rhizogenes transformed roots and composite plants for studying gene expression in coffee roots. Plant Cell Rep 25(9):959–967

    Article  CAS  PubMed  Google Scholar 

  • Alpizar E, Dechamp E, Lapeyre-Montes F, Guilhaumon C, Bertrand B, Jourdan C, Lashermes P, Etienne H (2008) Agrobacterium rhizogenes-transformed roots of coffee (Coffea arabica): conditions for long-term proliferation, and morphological and molecular characterization. Ann Bot 101(7):929–940. doi:10.1093/aob/mcn027

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Andersen B, Nicolaisen M, Nielsen S (2002) Alternative hosts for potato mop-top virus, genus Pomovirus and its vector Spongospora subterranea f. sp. subterranea. Potato Res 45(1):37–43. doi:10.1007/bf02732217

    Article  Google Scholar 

  • Andika IB, Kondo H, Tamada T (2005) Evidence that RNA silencing-mediated resistance to Beet necrotic yellow vein virus is less effective in roots than in leaves. Mol Plant Microbe Interact 18(3):194–204. doi:10.1094/MPMI-18-0194

    Article  CAS  PubMed  Google Scholar 

  • Bais HP, Sudha G, George J, Ravishankar GA (2001) Influence of exogenous hormones on growth and secondary metabolite production in hairy root cultures of Cichorium intybus L. cv. Lucknow local. In Vitro Cell Develop Biol Plant 37(2):293–299. doi:10.1007/s11627-001-0052-8

    Article  CAS  Google Scholar 

  • Batra J, Dutta A, Singh D, Kumar S, Sen J (2004) Growth and terpenoid indole alkaloid production in Catharanthus roseus hairy root clones in relation to left- and right-termini-linked RiT-DNA gene integration. Plant Cell Rep 23(3):148–154. doi:10.1007/s00299-004-0815-x

    Article  CAS  PubMed  Google Scholar 

  • Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. The. J Bacteriol 62(3):293–300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14(6):695–700

    Article  CAS  PubMed  Google Scholar 

  • Boisson-Dernier A, Andriankaja A, Chabaud M, Niebel A, Journet EP, Barker DG, de Carvalho-Niebel F (2005) MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol Plant Microbe Interact 18(12):1269–1276

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Caldo RA, Nettleton D, Wise RP (2004) Interaction-dependent gene expression in Mla-specified response to barley powdery mildew. Plant Cell 16(9):2514–2528. doi:10.1105/tpc.104.023382

    Article  CAS  PubMed Central  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(2):155–162

    Article  CAS  PubMed  Google Scholar 

  • Christey MC (2001) Use of ri-mediated transformation for production of transgenic plants. In Vitro Cell Dev Biol Plant 37(6):687–700. doi:10.1007/s11627-001-0120-0

    Article  CAS  Google Scholar 

  • Collier R, Fuchs B, Walter N, Kevin Lutke W, Taylor CG (2005) Ex vitro composite plants: an inexpensive, rapid method for root biology. Plant J 43(3):449–457. doi:10.1111/j.1365-313X.2005.02454.x

    Article  CAS  PubMed  Google Scholar 

  • Dalton DA, Boniface C, Turner Z, Lindahl A, Kim HJ, Jelinek L, Govindarajulu M, Finger RE, Taylor CG (2009) Physiological roles of glutathione S-transferases in soybean root nodules. Plant Physiol 150(1):521–530

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ding YL, Kalo P, Yendrek C, Sun JH, Liang Y, Marsh JF, Harris JM, Oldroyd GED (2008) Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20(10):2681–2695

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Düring K, Porsch P, Fladung M, Lörz H (1993) Transgenic potato plants resistant to the phytopathogenic bacterium Erwinia carotovora. Plant J 3(4):587–598

    Article  Google Scholar 

  • Eckes P, Rosahl S, Schell J, Willmitzer L (1986) Isolation and characterization of a light-inducible, organ-specific gene from potato and analysis of its expression after tagging and transfer into tobacco and potato shoots. Mol Gen Genet 205(1):14–22. doi:10.1007/bf02428027

    Article  CAS  Google Scholar 

  • Estrada-Navarrete G, Alvarado-Affantranger X, Olivares JE, Díaz-Camino C, Santana O, Murillo E, Guillén G, Sánchez-Guevara N, Acosta J, Quinto C, Li D, Gresshoff PM, Sánchez F (2006) Agrobacterium rhizogenes transformation of the Phaseolus spp.: a tool for functional genomics. Mol Plant Microbe Interact 19(12):1385–1393

    Article  CAS  PubMed  Google Scholar 

  • Furner IJ, Huffman GA, Amasino RM, Garfinkel DJ, Gordon MP, Nester EW (1986) An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature 319(6052):422–427

    Article  CAS  Google Scholar 

  • Gangopadhyay M, Dewanjee S, Chakraborty D, Bhattacharya S (2011) Role of exogenous phytohormones on growth and plumbagin accumulation in Plumbago indica hairy roots and conservation of elite root clones via synthetic seeds. Ind Crops Prod 33(2):445–450. doi:10.1016/j.indcrop.2010.10.030

  • Germundsson A, Sandgren M, Barker H, Savenkov EI, Valkonen JP (2002) Initial infection of roots and leaves reveals different resistance phenotypes associated with coat protein gene-mediated resistance to Potato mop-top virus. J Gen Virol 83(Pt 5):1201–1209

    CAS  PubMed  Google Scholar 

  • Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008a) SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105(12):4928–4932

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gherbi H, Nambiar-Veetil M, Zhong C, Felix J, Autran D, Girardin R, Vaissayre V, Auguy F, Bogusz D, Franche C (2008b) Post-transcriptional gene silencing in the root system of the actinorhizal tree Allocasuarina verticillata. Mol Plant Microbe Interact 21(5):518–524

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18(10):2680–2693

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hansen J, Jorgensen JE, Stougaard J, Marcker KA (1989) Hairy roots—a short cut to transgenic root nodules. Plant Cell Rep 8(1):12–15

    Article  CAS  PubMed  Google Scholar 

  • Hashem EA (2009) Estimation of the endogenous auxins and cytokinins in hairy roots incited on Solanum dulcamara plants by Ri plasmid of Agrobacterium rhizogenes. Aust J Basic Appl Sci 3(1):142–147

    CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:1–32

    Google Scholar 

  • Hoekema A, Hirsch PR, Hooykaas PJJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir-region and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303(5913):179–180

    Article  CAS  Google Scholar 

  • Holmström KO (1998) Engineering plant adaptation to water stress. Acta Universitatis Agriculturae Sueciae, Agraria Ph.D. thesis 84

  • Horn P, Schlichting A, Hammesfahr U, Thiele-Bruhn S, Kriete G, Baum C, Leinweber P, Broer I (2014) Influence of transgenic plants on soil: fast and sensitive in vivo studies under controlled environmental conditions to substitute long-term field trials. J Biotechnol (submitted)

  • Hühns M, Neumann K, Hausmann T, Ziegler K, Klemke F, Kahmann U, Staiger D, Lockau W, Pistorius EK, Broer I (2008) Plastid targeting strategies for cyanophycin synthetase to achieve high-level polymer accumulation in Nicotiana tabacum. Plant Biotechnol J 6(4):321–336

    Article  PubMed  Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139(3):1401–1410

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) Beta-Glucuronidase (GUS) as a sensitive and versatile gene fusion marker in plants. J Cell Biochem:57–57

  • Kawazu Y, Fujiyama R, Sugiyama K, Sasaya T (2006) A transgenic lettuce line with resistance to both lettuce big-vein associated virus and Mirafiori lettuce virus. J Am Soc Hortic Sci 131(6):760–763

    CAS  Google Scholar 

  • Kawazu Y, Fujiyama R, Noguchi Y (2009) Transgenic resistance to Mirafiori lettuce virus in lettuce carrying inverted repeats of the viral coat protein gene. Transgenic Res 18(1):113–120. doi:10.1007/s11248-008-9200-9

    Article  CAS  Google Scholar 

  • Kim YS, Li X, Park WT, Uddin MR, Park NI, Kim YB, Lee MY, Park SU (2012) Influence of media and auxins on growth and falvone production in hairy root cultures of baikal skullcap, Scutellaria baicalensis. Plant OMICS 5(1):24–27

    CAS  Google Scholar 

  • Kole AP (1954) A contribution to the knowledge of Spongospora subterranean, the cause of powdery scab of potatoes. Tijdschrift over Plantenziekten 60:65

    Google Scholar 

  • Konieczny R, Obert B, Bleho J, Novák O, Heym C, Tuleja M, Müller J, Strnad M, Menzel D, Šamaj J (2011) Stable transformation of Mesembryanthemum crystallinum (L.) with Agrobacterium rhizogenes harboring the green fluorescent protein targeted to the endoplasmic reticulum. J Plant Physiol 168(7):722–729. doi:10.1016/j.jplph.2010.10.013

    Article  CAS  PubMed  Google Scholar 

  • Kreuze JF, Savenkov EI, Cuellar W, Li X, Valkonen JPT (2005) Viral class 1 RNase III involved in suppression of RNA silencing. J Virol 79(11):7227–7238. doi:10.1128/jvi.79.11.7227-7238.2005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar GBS, Ganapathi TR, Srinivas L, Revathi CJ, Bapat VA (2006) Expression of hepatitis B surface antigen in potato hairy roots. Plant Sci 170(5):918–925

    Article  CAS  Google Scholar 

  • Küster H, Quandt HJ, Broer I, Perlick AM, Pühler A (1995) The promoter of the Vicia faba L. VfENOD-GRP3 gene encoding a glycine-rich early nodulin mediates a predominant gene expression in the interzone II-III region of transgenic Vicia hirsuta root nodules. Plant Mol Biol 29(4):759–772

    Article  PubMed  Google Scholar 

  • Larson RL, Wintermantel WM, Hill A, Fortis L, Nunez A (2001) Proteome changes in sugar beet in response to Beet necrotic yellow vein virus. Physiol Mol Plant Pathol 72(1–3):62–72

    Google Scholar 

  • Lennefors B-L, Savenkov EI, Bensefelt J, Wremerth-Weich E, Roggen P, Tuvesson S, Valkonen JPT, Gielen J (2006) dsRNA-mediated resistance to Beet necrotic yellow vein virus infections in sugar beet (Beta vulgaris L. ssp. vulgaris). Mol Breed 18(4):313–325. doi:10.1007/s11032-006-9030-5

    Article  CAS  Google Scholar 

  • Lennefors BL, van Roggen PM, Yndgaard F, Savenkov EI, Valkonen JP (2008) Efficient dsRNA-mediated transgenic resistance to Beet necrotic yellow vein virus in sugar beets is not affected by other soilborne and aphid-transmitted viruses. Transgenic Res 17(2):219–228. doi:10.1007/s11248-007-9092-0

    Article  CAS  PubMed  Google Scholar 

  • Limpens E, Ramos J, Franken C, Raz V, Compaan B, Franssen H, Bisseling T, Geurts R (2004) RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 55(399):983–992

    Article  CAS  PubMed  Google Scholar 

  • Maurel C, Barbier-Brygoo H, Spena A, Tempé J, Guern J (1991) Single rol genes from the Agrobacterium rhizogenes TL-DNA alter some of the cellular responses to auxin in Nicotiana tabacum. Plant Physiol 97(1):212–216

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Merz U (1989) Infectivity, inoculum density and germination of Spongospora subterranea resting spores: a solution-culture test system. EPPO Bulletin 19(3):585–592

    Article  Google Scholar 

  • Mohanpuria P, Kumar V, Ahuja PS, Yadav SK (2011) Agrobacterium-mediated silencing of caffeine synthesis through root transformation in Camellia sinensis L. Mol Biotechnol 48(3):235–243. doi:10.1007/s12033-010-9364-4

    Article  CAS  PubMed  Google Scholar 

  • Mrosk C, Forner S, Hause G, Küster H, Kopka J, Hause B (2009) Composite Medicago truncatula plants harbouring Agrobacterium rhizogenes-transformed roots reveal normal mycorrhization by Glomus intraradices. J Exp Bot 60(13):3797–3807

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    Article  CAS  Google Scholar 

  • Neumann K, Stephan DP, Ziegler K, Hühns M, Broer I, Lockau W, Pistorius EK (2005) Production of cyanophycin, a suitable source for the biodegradable polymer polyaspartate, in transgenic plants. Plant Biotechnol J 3(2):249–258. doi:10.1111/j.1467-7652.2005.00122.x

    Article  CAS  PubMed  Google Scholar 

  • Ooms G, Hooykaas PJ, Van Veen RJ, Van Beelen P, Regensburg-Tuink TJ, Schilperoort RA (1982) Octopine Ti-plasmid deletion mutants of Agrobacterium tumefaciens with emphasis on the right side of the T-region. Plasmid 7(1):15–29

    Article  CAS  PubMed  Google Scholar 

  • Palauqui J-C, Elmayan T, Pollien J-M, Vaucheret H (1997) Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16(15):4738–4745

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10(9):1571–1580

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Piron F, Nicolai M, Minoia S, Piednoir E, Moretti A, Salgues A, Zamir D, Caranta C, Bendahmane A (2010) An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PLoS One 5(6):e11313. doi:10.1371/journal.pone.0011313

    Article  PubMed Central  PubMed  Google Scholar 

  • Pistelli L, Giovannini A, Ruffoni B, Bertoli A, Pistelli L (2010) Hairy root cultures for secondary metabolites production. Adv Exp Med Biol 698:167–184

    Article  CAS  PubMed  Google Scholar 

  • Purcell MK, Hart SA, Kurath G, Winton JR (2006) Strand-specific, real-time RT-PCR assays for quantification of genomic and positive-sense RNAs of the fish rhabdovirus, Infectious hematopoietic necrosis virus. J Virol Methods 132(1–2):18–24. doi:10.1016/j.jviromet.2005.08.017

    Article  CAS  PubMed  Google Scholar 

  • Qu F, Ye X, Hou G, Sato S, Clemente TE, Morris TJ (2005) RDR6 has a broad-spectrum but temperature-dependent antiviral defense role in Nicotiana benthamiana. J Virol 79(24):15209–15217. doi:10.1128/JVI.79.24.15209-15217.2005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Quandt HJ (1994) Entwicklung eines Transformationssystems zur Analyse der Aktivität von Nodulinpromotoren in transgenen Wurzelknöllchen von Pflanzen der Gattung Vicia—analyse der expression des chimären pVfgLb3-gusA-int Gens. Dissertation (Dr. rer. nat.), Universität Bielefeld; Fakultät für Biologie

  • Quandt HJ, Pühler A, Broer I (1993) Transgenic root nodules of Vicia hirsuta : a fast and efficient system for the study of gene expression in indeterminate-type nodules. Mol Plant Microbe Interact 6(6):699–706

    Article  Google Scholar 

  • Rhodes MJC, Parr AJ, Giulietti A, Aird ELH (1994) Influence of exogenous hormones on the growth and secondary metabolite formation in transformed root cultures. Plant Cell Tissue Organ Cult 38(2):143–151

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics methods and protocols: methods in molecular biology, vol 132. Humana Press, Totowa

  • Santala J, Samuilova O, Hannukkala A, Latvala S, Kortemaa H, Beuch U, Kvarnheden A, Persson P, Topp K, Ørstad K, Spetz C, Nielsen SL, Kirk HG, Budziszewska M, Wieczorek P, Obrępalska-Stęplowska A, Pospieszny H, Kryszczuk A, Sztangret-Wiśniewska J, Yin Z, Chrzanowska M, Zimnoch-Guzowska E, Jackeviciene E, Taluntytė L, Pūpola N, Mihailova J, Lielmane I, Järvekülg L, Kotkas K, Rogozina E, Sozonov A, Tikhonovich I, Horn P, Broer I, Kuusiene S, Staniulis J, Uth JG, Adam G, Valkonen JPT (2010) Detection, distribution and control of Potato mop-top virus, a soil-borne virus, in northern Europe. Ann Appl Biol 157(2):163–178

    Article  CAS  Google Scholar 

  • Sasaya T, Fujii H, Ishikawa K, Koganezawa H (2008) Further evidence of Mirafiori lettuce big-vein virus but not of Lettuce big-vein associated virus with big-vein disease in lettuce. Phytopathology 98(4):464–468. doi:10.1094/PHYTO-98-4-0464

    Article  CAS  PubMed  Google Scholar 

  • Sauerwein M, Wink M, Shimomura K (1992) Influence of light and phytohormones on alkaloid production in transformed root cultures of Hyoscyamus albus. J Plant Physiol 140(2):147–152. doi:10.1016/S0176-1617(11)80925-9

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18(5):1121–1133. doi:10.1105/tpc.105.039834

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen WH, Petit A, Guern J, Tempé J (1988) Hairy roots are more sensitive to auxin than normal roots. Proc Natl Acad Sci USA 85(10):3417–3421

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen WH, Davioud E, David C, Barbierbrygoo H, Tempé J, Guern J (1990) High sensitivity to auxin is a common feature of hairy root. Plant Physiol 94(2):554–560

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1(9):784–791

    Article  CAS  Google Scholar 

  • Simón-Mateo C, García JA (2011) Antiviral strategies in plants based on RNA silencing. Biochim Biophys Acta 1809(11–12):722–731. doi:10.1016/j.bbagrm.2011.05.011

    Article  PubMed  Google Scholar 

  • Slightom JL, Durand-Tardif M, Jouanin L, Tepfer D (1986) Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid—identification of open reading frames. J Biol Chem 261(1):108–121

    CAS  PubMed  Google Scholar 

  • Smith NA, Singh SP, Wang MB, Stoutjesdijk PA, Green AG, Waterhouse PM (2000) Gene expression: total silencing by intron-spliced hairpin RNAs. Nature 407(6802):319–320. doi:10.1038/35030305

    Article  CAS  PubMed  Google Scholar 

  • Sonoda S, Nishiguchi M (2000) Graft transmission of post-transcriptional gene silencing: target specificity for RNA degradation is transmissible between silenced and non-silenced plants, but not between silenced plants. Plant J 21(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Spanò L, Mariotti D, Cardarelli M, Branca C, Costantino P (1988) Morphogenesis and auxin sensitivity of transgenic tobacco with different complements of Ri T-DNA. Plant Physiol 87(2):479–483

    Article  PubMed Central  PubMed  Google Scholar 

  • Spena A (1993) Transgenic plants altered in phytohormone metabolism. Acta Bot Gallica 140(6):693–700

    Article  CAS  Google Scholar 

  • Stiller J, Martirani L, Tuppale S, Chian RJ, Chiurazzi M, Gresshoff PM (1997) High frequency transformation and regeneration of transgenic plants in the model legume Lotus japonicus. J Exp Bot 48(312):1357–1365

    Article  CAS  Google Scholar 

  • Stougaard J, Abildsten D, Marcker KA (1987) Agrobacterium rhizogenes pRi TL-DNA segment as a gene vector system for transformation of plants. Mol Gen Genet 207(2):251–255

    Article  CAS  Google Scholar 

  • Sun JH, Cardoza V, Mitchell DM, Bright L, Oldroyd G, Harris JM (2006) Crosstalk between jasmonic acid, ethylene and nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 46(6):961–970

    Article  CAS  PubMed  Google Scholar 

  • Thimmaraju R, Venkatachalam L, Bhagyalakshmi N (2008) Morphometric and biochemical characterization of red beet (Beta vulgaris L.) hairy roots obtained after single and double transformations. Plant Cell Rep 27(6):1039–1052

    Article  CAS  PubMed  Google Scholar 

  • Vancanneyt G, Schmidt R, O’Connor-Sanchez A, Willmitzer L, Rocha-Sosa M (1990) Construction of an intron-containing marker gene: splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation. Mol Gen Genet 220(2):245–250

    Article  CAS  PubMed  Google Scholar 

  • Vanhala L, Eeva M, Lapinjoki S, Hiltunen R, Oksman-Caldentey K-M (1998) Effect of growth regulators on transformed root cultures of Hyoscyamus muticus. J Plant Physiol 153(3–4):475–481. doi:10.1016/S0176-1617(98)80177-6

  • Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16(1):69–79. doi:10.1016/j.molcel.2004.09.028

    Article  CAS  PubMed  Google Scholar 

  • Veena V, Taylor CG (2007) Agrobacterium rhizogenes : recent developments and promising applications. In Vitro Cell Dev Biol Plant 43(5):383–403

    Article  CAS  Google Scholar 

  • Vervliet G, Holsters M, Teuchy H, Vanmontagu M, Schell J (1975) Characterization of different plaque-forming and defective temperate Phages in Agrobacterium strains. J Gen Virol 26:33–48

    Article  CAS  PubMed  Google Scholar 

  • Vieweg MF, Frühling M, Quandt HJ, Heim U, Bäumlein H, Pühler A, Küster H, Andreas MP (2004) The promoter of the Vicia faba L. leghemoglobin gene VfLb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and nonlegume plants. Mol Plant Microbe Interact 17(1):62–69

    Article  CAS  PubMed  Google Scholar 

  • Vijn I, Christiansen H, Lauridsen P, Kardailsky I, Quandt HJ, Broer I, Drenth J, Jensen EO, vanKammen A, Bisseling T (1995) A 200 bp region of the Pea ENOD12 promoter is sufficient for nodule-specific and nod factor induced expression. Plant Mol Biol 28(6):1103–1110

    Article  CAS  PubMed  Google Scholar 

  • Vuorinen AL, Gammelgård E, Auvinen P, Somervuo P, Dere S, Valkonen JPT (2010) Factors underpinning the responsiveness and higher levels of virus resistance realised in potato genotypes carrying virus-specific R genes. Ann Appl Biol 157(2):229–241. doi:10.1111/j.1744-7348.2010.00424.x

    Article  CAS  Google Scholar 

  • Weathers PJ, Bunk G, McCoy MC (2005) The effect of phytohormones on growth and artemisinin production in Artemisia annua hairy roots. In Vitro Cell Dev Biol Plant 41(1):47–53. doi:10.1079/ivp2004604

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamada T (1993) The role of auxin in plant-disease development. Annu Rev Phytopathol 31(1):253–273. doi:10.1146/annurev.py.31.090193.001345

    Article  CAS  PubMed  Google Scholar 

  • Yang YK, Lee SY, Park WT, Park NI, Park SU (2010) Exogenous auxins and polyamines enhance growth and rosmarinic acid production in hairy root cultures of Nepeta cataria L. Plant OMICS 3(6):190–193

    CAS  Google Scholar 

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Acknowledgments

This project was carried out as part of the Baltic Sea Region MOP-TOP project supported by the Nordic Joint Committee for Agricultural Research (Project NKJ-122). Dr. Stuart Wale at the Scottish Agricultural College is thanked for providing potato tubers with powdery scab. Financial support from the Ministry of Agriculture and Forestry (Grant 1386/39/2005) and the Academy of Finland (Grants 1134579 and 1253126) to J.P.T.V., and from The Viikki Doctoral Programme of Molecular Biosiences to J.S. is gratefully acknowledged.

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There are no conflicts of interest.

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Authors and Affiliations

  1. Institute for Land Use, University of Rostock, Rostock, Germany

    Patricia Horn & Inge Broer

  2. Department of Agricultural Sciences, University of Helsinki, PO Box 27, 00014, Helsinki, Finland

    Johanna Santala & Jari P. T. Valkonen

  3. Department of Agroecology, Aarhus University, Flakkebjerg, Denmark

    Steen Lykke Nielsen

  4. Institute of Pathology, University of Rostock, Rostock, Germany

    Maja Hühns

Authors
  1. Patricia Horn
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  2. Johanna Santala
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  3. Steen Lykke Nielsen
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  4. Maja Hühns
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  5. Inge Broer
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  6. Jari P. T. Valkonen
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Corresponding author

Correspondence to Inge Broer.

Additional information

Communicated by Eugenio Benvenuto.

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Horn, P., Santala, J., Nielsen, S.L. et al. Composite potato plants with transgenic roots on non-transgenic shoots: a model system for studying gene silencing in roots. Plant Cell Rep 33, 1977–1992 (2014). https://doi.org/10.1007/s00299-014-1672-x

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  • DOI: https://doi.org/10.1007/s00299-014-1672-x

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