Abstract
It is commonly accepted that the plant pathogens Agrobacterium rhizogenes and Agrobacterium tumefaciens, acting via their T-DNA oncogenes, disturb hormone metabolism or hormone perception pathways in plants, thereby attaining their aim of successful pathogenesis. In this work, we summarize recent data on the A. rhizogenes rolC and rolB oncogenes in comparison to the A. tumefaciens 6b oncogene with respect to their effects on the physiology of transformed cells. The newly discovered functions of the rol genes include the modulation of secondary metabolism, the modulation of levels of intracellular ROS and stress resistance of transformed cells, changed sucrose metabolism, and the inhibition of programmed cell death. We show that the rol genes do not have suppressive effects on plant innate immunity; rather, these genes activate plant defense reactions. The existence of not only the hormone-related mechanism of pathogenicity but also the defense-related mechanism of pathogenicity during plant-Agrobacterium interactions is suggested.
Graphical Abstract
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- ROS:
-
Reactive oxygen species
- siRNA:
-
Small interfering RNA
- miRNA:
-
MicroRNA
- RISC:
-
RNA-induced silencing complex
- dsDNA:
-
Double-stranded DNA
- H2DCF-DA:
-
2,7-dichlorofluorescein diacetate
References
Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedren MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390
Baulcombe D (2004) RNA silencing in plants. Nature 431(7006):356–363
Bretz JR, Mock NM, Charity JC, Zeyad S, Baker CJ, Hutcheson SW (2003) A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol Microbiol 49:389–400
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
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
Bulgakov VP, Tchernoded GK, Mischenko NP, Khodakovskaya MV, Glazunov VP, 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
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
Bulgakov VP, Tchernoded GK, Mischenko NP, Shkryl YN, Fedoreyev SA, 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
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
Bulgakov VP (2008) Functions of rol genes in plant secondary metabolism. Biotechnol Adv 26:318–324
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
Bulgakov VP, Shkryl YN, Veremeichik GN (2010) Engineering high yields of secondary metabolites in Rubia cell cultures through transformation with rol genes. Methods Mol Biol 643:229–242
Bulgakov VP, Shkryl YN, Veremeichik GN, Gorpenchenko TY, Inyushkina YV (2011) Application of Agrobacterium rol genes in plant biotechnology: a natural phenomenon of secondary metabolism regulation. In: Alvarez M (ed) Genetic transformation. InTech, Rijeka, pp. 261–271. http://www.intechopen.com/articles/show/title/application-of-agrobacterium-rol-genes-in-plant-biotechnology-a-natural-phenomenon-of-secondary-meta
Bulgakov VP, Gorpenchenko TY, Veremeichik GN, Shkryl YN, Tchernoded GK, Bulgakov DV, Aminin DL, Zhuravlev YN (2012a) The rolB gene suppresses reactive oxygen species in transformed plant cells through the sustained activation of antioxidant defense. Plant Physiol 158:1371–1381
Bulgakov VP, Inyushkina YV, Fedoreyev SA (2012b) Rosmarinic acid and its derivatives: biotechnology and applications. Crit Rev Biotechnol 32:203–217
Casanova E, Trillas MI, Moysset L, Vainstein A (2005) Influence of rol genes in floriculture. Biotechnol Adv 23:3–39
Christensen B, Müller R (2009) The use of Agrobacterium rhizogenes and its rol-genes for quality improvement in ornamentals. Eur J Hort Sci 74:275–287
Clément B, Pollmann S, Weiler E, Urbanczyk-Wochniak E, Otten L (2006) The Agrobacterium vitis T-6b oncoprotein induces auxin-independent cell expansion in tobacco. Plant J 45:1017–1027
Clément B, Perot J, Geoffroy P, Legrand M, Zon J, Otten L (2007) Abnormal accumulation of sugars and phenolics in tobacco roots expressing the Agrobacterium T-6b oncogene and the role of these compounds in 6b-induced growth. Mol. Plant-Microbe Interact 20:53–62
Doran PM (2009) Application of plant tissue cultures in phytoremediation research: incentives and limitations. Biotechnol Bioeng 103:60–76
Dunoyer P, Himber C, Voinnet O (2006) Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections. Nat Genet 38:258–263
Espinosa A, Guo M, Tam VC, Fu ZQ, Alfano JR (2003) The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol Microbiol 49:377–387
Estruch JJ, Parets-Soler A, Schmülling T, Spena A (1991) Cytosolic localization in transgenic plants of the rolC peptide from Agrobacterium rhizogenes. Plant Mol Biol 17:547–550
Filippini F, Rossi R, Marin O, Trovato M, Costantino P, Downey PM, Lo Schiavo F, Terzi M (1996) A plant oncogene as a phosphatase. Nature 379:499–500
Gális I, Kakiuchi Y, Simek P, Wabiko H. (2004) Agrobacterium tumefaciens AK-6b gene modulates phenolic compound metabolism in tobacco. Phytochemistry 65:169–179
Gális I, Simek P, Van Onckelen HA, Kakiuchi Y, Wabiko H (2002) Resistance of transgenic tobacco seedlings expressing the Agrobacterium tumefaciens C58-6b gene, to growth-inhibitory levels of cytokinin is associated with elevated IAA levels and activation of phenylpropanoid metabolism. Plant Cell Physiol 43:939–950
Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101
Georgiev MI, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnological resource. Trends Biotechnol 30:528–537
Gorpenchenko TY, Kiselev KV, Bulgakov VP, Tchernoded GK, Bragina EA, Khodakovskaya MV, Koren OG, Batygina TB, Zhuravlev YN (2006) The Agrobacterium rhizogenes rolC-gene-induced somatic embryogenesis and shoot organogenesis in Panax ginseng transformed calluses. Planta 223:457–467
Gorpenchenko TY, Aminin DL, Vereshchagina YV, Shkry YN, Veremeichik GN, Tchernoded GK, Bulgakov VP (2012) Can plant oncogenes inhibit programmed cell death? The rolB oncogene reduces apoptosis-like symptoms in transformed plant cells. Plant Signal Behav 7(9):1058–1061
Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23:1512–1522
Guillon S, Trémouillaux-Guiller J, Pati PK, Rideau M, Gantet P (2006) Hairy root research: recent scenario and exciting prospects. Curr Opin Plant Biol 9:341–346
He P, Shan L, Lin N-C, Martin GB, Kemmerling B, Nürnberger T, Sheen J (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563–575
Helfer A, Pien S, Otten L (2002) Functional diversity and mutational analysis of Agrobacterium 6B oncoproteins. Mol Genet Genomics 267:577–586
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 (Moscow) 74:917–924
Kakiuchi Y, Gàlis I, Tamogami S, Wabiko H (2006) Reduction of polar auxin transport in tobacco by the tumorigenic Agrobacterium tumefaciens AK-6b gene. Planta 223:237–247
Kiselev KV, Kusaykin MI, Dubrovina AS, Bezverbny DA, Zvyagintseva TN, Bulgakov VP (2006) The rolC gene induces expression of a pathogenesis-related β-1,3-glucanase in transformed ginseng cells. Phytochemistry 67:2225–2231
Kitakura S, Fujita T, Ueno Y, Terakura S, Wabiko H, Machida Y (2002) The protein encoded by oncogene 6b from Agrobacterium tumefaciens interacts with a nuclear protein of tobacco. Plant Cell 14:451–463
Landi L, Capocasa F, Costantini E, Mezzetti B (2009) RolC strawberry plant adaptability, productivity, and tolerance to soil-borne disease and mycorrhizal interactions. Transgenic Res 18:933–942
Levesque H, Delepelaire P, Rousé P, Slightom J, Tepfer D (1988) Common evolutionary origin of the central portions of the Ri TL-DNA of Agrobacterium rhizogenes and the Ti T-DNAs of Agrobacterium tumefaciens. Plant Mol. Biol 11:731–744
Lütken H, Clarke JL, Müller R (2012) Genetic engineering and sustainable production of ornamentals: current status and future directions. Plant Cell Rep 31:1141–1157
Mohajjel-Shoja H, Clément B, Perot J, Alioua M, Otten L (2011) Biological activity of the Agrobacterium rhizogenes-derived trolC gene of Nicotiana tabacum and its functional relation to other plast genes. Mol Plant-Microbe Interact 24:44–53
Moriuchi H, Okamoto C, Nishihama R, Yamashita I, Machida Y, Tanaka N (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 38:260–275
Mullineaux P, Ball L, Escobar C, Karpinska B, Creissen G, Karpinski S (2000) Are diverse signaling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy? Phil Trans R Soc Lond B 355:1531–1540
Nikravesh F, Khavari-Nejad RA, Rahimian H, Fahimi H (2011) Study of antioxidant enzymes activity and isozymes pattern in hairy roots and regenerated plants in Nicotiana tabacum. Acta Physiol Plant. doi:10.1007/s11738-011-0838-1
Nilsson O, Olsson O (1997) Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiol Plant 100:463–473
Ono NN, Tian L (2011) The multiplicity of hairy root cultures: prolific possibilities. Plant Sci 180:439–446
Otten L, Schmidt J (1998) A T-DNA from the Agrobacterium tumefaciens limited-host-range strain AB2/73 contains a single oncogene. Mol Plant-Microbe Interact 11:335–342
Palazón J, Cusidó RM, Roig C, Piñol MT (1998) Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Rep 17:384–390
Persiyanova EV, Kiselev KV, Bulgakov VP, Timchenko NF, Chernoded GK, Zhuravlev YN (2008) Defense response mechanisms of ginseng callus cultures induced by Yersinia pseudotuberculosis, a human pathogen. Russian J Plant Physiol 55:748–755
de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 130:698–708
Rigden D, Carneiro M (1999) A structural model for the RolA protein and its interaction with DNA. Proteins 37:697–708
Shadwick FS, Doran PM (2007) Propagation of plant viruses in hairy root cultures: a potential method for in vitro production of epitope vaccines and foreign proteins. Biotechnol Bioeng 96:570–583
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
Shkryl YN, Veremeichik GN, Bulgakov VP, Gorpenchenko TY, Aminin DL, Zhuravlev YN (2010) Decreased ROS level and activation of antioxidant gene expression in Agrobacterium rhizogenes pRiA4-transformed calli of Rubia cordifolia. Planta 232:1023–1032
Stieger PA, Meyer AD, Kathmann P, Fründt 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
Terakura S, Kitakura S, Ishikawa M, Ueno Y, Fujita T, Machida C, Wabiko H, Machida Y (2006) Oncogene 6b from Agrobacterium tumefaciens induces abaxial cell division at late stages of leaf development and modifies vascular development in petioles. Plant Cell Physiol 47:664–672
Terakura S, Ueno Y, Tagami H, Kitakura S, Machida C, Wabiko H, Aiba H, Otten L, Tsukagoshi H, Nakamura K, Machida Y (2007) An oncoprotein from the plant pathogen Agrobacterium has histone chaperone-like activity. Plant Cell 19:2855–2865
Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378
Underwood W, Zhang S, He SY (2007) The Pseudomonas syringae type III effector tyrosine phosphatase HopAO1 suppresses innate immunity in Arabidopsis thaliana. Plant J 52:658–672
Veremeichik GN, Shkryl YN, Bulgakov VP, Avramenko TV, Zhuravlev YN (2012) Molecular cloning and characterization of seven class III peroxidases induced by overexpression of the agrobacterial rolB gene in Rubia cordifolia transgenic callus cultures. Plant Cell Rep 110:183–188
Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220
Walmsley AM, Doran PM (2012) Foreign protein production using plant cells: opportunities and challenges. Biotechnol Adv 30:385–386
Wang M, Soyano T, Machida S, Yang J-Y, Jung C, Chua N-H, Yuan YA (2011) Molecular insights into plant cell proliferation disturbance by Agrobacterium protein 6b. Genes Dev 25:64–76
Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183
Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150
Acknowledgments
This work was supported by grants from the Russian Foundation for Basic Research and by the Grant Program “Molecular and Cell Biology” of the Russian Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Bulgakov, V.P., Shkryl, Y.N., Veremeichik, G.N., Gorpenchenko, T.Y., Vereshchagina, Y.V. (2013). Recent Advances in the Understanding of Agrobacterium rhizogenes-Derived Genes and Their Effects on Stress Resistance and Plant Metabolism. In: Doran, P. (eds) Biotechnology of Hairy Root Systems. Advances in Biochemical Engineering/Biotechnology, vol 134. Springer, Berlin, Heidelberg. https://doi.org/10.1007/10_2013_179
Download citation
DOI: https://doi.org/10.1007/10_2013_179
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-39018-0
Online ISBN: 978-3-642-39019-7
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)