Ген rolC агробактерий: на пути к пониманию функции

В процессе агротрансформации в растение попадает фрагмент плазмиды почвенной бактерии Agrobacterium rhizogenes Conn в результате чего под действием генов, входящих в состав данного фрагмента, у растения разрастается корневая система. Основные гены, контролирующие разрастание корней, объединяют в «корневой локус». Самым хорошо изученным геном “корневого локуса” является ген rolC. За более чем 30-летнюю историю исследований, посвященных гену rolC, были получены данные по его экспрессии, локализации и предполагаемых функциях белка, а также о его влиянии на морфологические и биохимические особенности растений. Так известно, что трансформация геном rolC приводит к множественным морфологическим эффектам, среди которых чаще всего встречаются карликовость, кустистость и изменение формы листовой пластинки. Подобные реакции растений связывают с изменением баланса гормонов, происходящим под влиянием rolC. Показано, что у трансформированных растений действительно изменяется количество ауксинов, цитокининов, а также абсцизовой кислоты, однако эти данные не складываются в единую картину. Также не установлены сигнальные пути, по которым rolC может воздействовать на гормональную систему растений. Морфогенетические эффекты могут проявляться в различной степени в зависимости от того, под контролем какого промотора работает rolC. Использование конститутивного промотора обычно приводит к более выраженному проявлению признаков, чем при работе гена под нативным промотором. Также показано влияние rolC на вторичный метаболизм растений. У трансформантов происходит активация синтеза различных метаболитов и, в отличие от морфогенетических эффектов, данный биохимический эффект не зависит от промотора, под которым экспрессируется ген. Некоторые вторичные метаболиты связаны с защитной системой растений. Таким образом, rolC способен опосредованно влиять и на этот аспект физиологии растений. В данном обзоре собраны результаты исследований, посвященных гену rolC в растениях, авторы попытались сформулировать основные гипотезы, связанные с механизмами работы гена, с целью приблизить читателей к пониманию его функции в растениях.

1. Bell R.L., Scorza R., Srinivasan C., Webb K. Transformation of Beurre Bosc Pear with the rolC gene. Journal of the American Society for Horticultural Science. 1999;124(6):570-574.

2. Bettini P., Baraldi R., Rapparini F., Melani L., Mauro M. L., Bindi D., Buiatti M. The insertion of the Agrobacterium rhizogenes rolC gene in tomato (Solanum lycopersicum L.) affects plant architecture and endogenous auxin and abscisic acid levels. Scientia Horticulturae. 2010;123(3):323-328. DOI: 10.1016/j.scienta.2009.09.013

3. Boase M.R., Winefield C.S., Lill T.A., Bendall M.J. Transgenic regal pelargoniums that express the rolC gene from Agrobacterium rhizogenes exhibit a dwarf floral and vegetative phenotype. In Vitro Cellular and Developmental Biology – Plant. 2004;40(1):46-50. DOI: 10.1079/IVP2003476

4. Bonhomme V., Laurain Mattar D., Fliniaux M.A. Effects of the rolC gene on hairy root: induction development and tropane alkaloid production by Atropa belladonna. Journal of Natural Products. 2000;63(9):1249-1252. DOI: 10.1021/np990614l

5. Bulgakov V.P., Khodakovskaya M.V., Labetskaya N.V., Chernoded G.K., Zhuravlev Y.N. The impact of plant rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochemistry. 1998;49:1929-1934. DOI: 10.1016/S0031-9422(98)00351-3

6. Bulgakov V.P., Tchernoded G.K., Mischenko N.P., Khodakovskaya M.V., Glazunov V.P., Zvereva E.V., Fedoreyev S.A., Zhuravlev Y.N. Effects of salicylic acid, methyl jasmonate, etephone and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with rolB and rolC genes. Journal of Biotechnology. 2002;97(3):213-221. DOI: 10.1016/S0168-1656(02)00067-6

7. Bulgakov V.P., Tchernoded G.K., Mischenko N.P., Shkryl Y.N., Glazunov V.P., Fedoreyev S.A., Zhuravleva Y.N. Effects of Ca (2+) channel blockers and protein kinase/phosphatase inhibitors on growth and anthraquinone production in Rubia cordifolia callus cultures transformed by the rolB and rolC genes. Planta. 2003;217:349-355. DOI: 10.1007/s00425-003-0996-5

8. Bulgakov V.P., Tchernoded G.K., Mischenko N.P., Shkryl Y.N., Fedoreyev S.A., Zhuravlev Y.N. The rolB and rolC genes activate synthesis of anthraquinones in Rubia cordifolia cells by mechanism independent of octadecanoid signaling pathway. Plant Science. 2004;166:1069-1075. DOI: 10.1016/j.plantsci.2003.12.027

9. Bulgakov V.P., Aminin D.L., Shkryl Y.N., Gorpenchenko T.Y., Veremeichik G.N., Dmitrenok P.S., Zhuravlev Y.N. Suppression of reactive oxygen species and enhanced stress tolerance in Rubia cordifolia cells expressing the rolC oncogene. Molecular Plant-Microbe Interactions. 2008;21(12):1561-1570. DOI: 10.1094/mpmi-21-12-1561

10. Bulgakov V.P., Shkryl Y.N., Veremeichik G.N., Gorpenchenko T.Y., Vereshchagina Y.V. Recent Advances in the Understanding of Agrobacterium rhizogenes-Derived Genes and Their Effects on Stress Resistance and Plant Metabolism. In: P. Doran (ed). Biotechnology of Hairy Root Systems. Advances in Biochemical Engineering/Biotechnology. Vol. 134. Berlin, Heidelberg: Springer; 2013. p.1-22. DOI: 10.1007/10_2013_179

11. Bulgakov V.P., Veremeichik G.N., Grigorchuk V.P., Rybin V.G., Shkryl Y.N. The rolB gene activates secondary metabolism in Arabidopsis calli via selective activation of genes encoding MYB and bHLH transcription factors. Plant Physiology and Biochemistry. 2016;102:70-79. DOI: 10.1016/j.plaphy.2016.02.015

12. Cardarelli M., Mariotti D., Pomponi M., Spano L., Capone I., Costantino P. Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype. Molecular and General Genetics. 1987;209:475-480. DOI: 10.1007/bf00331152

13. Casanova E., Zuker A., Trillas M.I., Moysset L., Vainstein A. The rolC gene in carnation exhibits cytokinin- and auxin-like activities. Scientia Horticulturae. 2003;97(3-4):321-331. DOI: 10.1016/S0304-4238(02)00155-3

14. Casanova E., Valdés A.E., Zuker A., Fernández B., Vainstein A., Trillas M.I., Moysset L. rolC-transgenic carnation plants: adventitious organogenesis and levels of endogenous auxin and cytokinins. Plant Science. 2004;167(3):551-560. DOI: 10.1016/j.plantsci.2004.04.029

15. Casanova E., Trillas M.I., Moysset L., Vainstein A. Influence of rol genes in floriculture. Biotechnology Advances. 2005;23(1):3-39. DOI: 10.1016/j.biotechadv.2004.06.002

16. Chen K., Dorlhac de Borne F., Szegedi E., Otten L. 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. The Plant Journal. 2014;80(4):669-682. DOI: 10.1111/tpj.12661

17. Chen K., Otten L. Natural Agrobacterium transformants: recent results and some theoretical considerations. Frontiers in Plant Science. 2017;8:1600. DOI: 10.3389/fpls.2017.01600

18. Dilshad E., Cusido R.M., Estrada K.R., Bonfill M., Mirza B. Genetic transformation of Artemisia carvifolia Buch with rol genes enhances artemisinin accumulation. PLoS One. 2015;10(10):e0140266. DOI: 10.1371/journal.pone.0140266

19. Dubrovina A.S., Manyakhin A.Y., Zhuravlev Y.N., Kiselev K. Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in rolC transgenic cell cultures of Vitis amurensis. Applied Microbiology and Biotechnology. 2010;88:727-736. DOI: 10.1007/s00253-010-2792-z

20. Estruch J.J., Chriqui D., Grossmann K., Schell J., Spena A. The plant oncogene rolC is responsible for the release of cytokinins from glucoside conjugates. The EMBO Journal. 1991;10(10):2889-2895.

21. Faiss M., Strnad M., Redig P., Doležal K., Hanuš J., Van Onckelen H., Schmülling T. Chemically induced expression of the rolC-encoded β-glucosidase in transgenic tobacco plants and analysis of cytokinin metabolism: rolC does not hydrolyze endogenous cytokinin glucosides in planta. The Plant Journal. 1996;10(1):33-46. DOI: 10.1046/J.1365-313X.1996.10010033.X

22. Fladung M. Transformation of diploid and tetraploid potato clones with the rolC gene of Agrobacterium rhizogenes and characterization of transgenic plants. Plant Breeding. 1990;104(4):295-304. DOI: 10.1111/j.1439-0523.1990.tb00439.x

23. Fladung M., Ballvora A. Further characterization of rolC transgenic tetraploid potato clones, and influence of daylength and level of rolC expression on yield parameters. Plant Breeding. 1992;109(1):18-27. DOI: 10.1111/j.1439-0523.1992.tb00145.x

24. Fladung M., Grossmann K., Ahuja M.R. Alterations in hormonal and developmental characteristics in transgenic Populus conditioned by the rolC gene from Agrobacterium rhizogenes, Journal of Plant Physiology. 1997;150:420-427. DOI: 10.1016/S0176-1617(97)80092-2

25. Fladung M., Gieffers W. Resistance reactions of leaves and tubers of rolC transgenic tetraploid potato to bacterial and fungal pathogens. Correlation with sugar, starch and chlorophyll content. Physiology and Molecular Plant Pathology. 1993;42:123-132. DOI: 10.1006/pmpp.1993.1010

26. Fujii N., Uchimiya H. Conditions favorable for the somatic embryogenesis in carrot cell culture enhance expression of the roIC promoter-GUS fusion gene. Plant Physiology. 1991;95(1):238-241. DOI: 10.1104/pp.95.1.238

27. Ganesan G., Sankararamasubramanian H.M., Harikrishnan M., Ashwin G., Parida A. A MYB transcription factor from the grey mangrove is induced by stress and confers NaCl tolerance in tobacco. Journal of Experimental Botany. 2012;63(12):4549-4561. DOI: 10.1093/jxb/ERS135

28. Gao Z., Liu G. Fu Y. A study on the glandular trichomes and their secretory cell in the leaves of aromatic tobacco plants. Acta Agriculturae Universitatis Henanensis. 1995;30:329-346.

29. Giovannini A., Zottini M., Morreale G., Spena A., Allavena A. Ornamental traits modification by rol genes in Osteospermum ecklonis transformed with Agrobacterium tumefaciens. In Vitro Cellular & Developmental Biology-Plant. 1999;35(1):70-75. DOI: 10.1007/s11627-999-0012-2

30. Graham M.W., Craig S., Waterhouse P.M. Expression patterns of vascular-specific promoters RolC and Sh in transgenic potatoes and their use in engineering PLRV-resistant plants. Plant Molecular Biology. 1997;33:729-735. DOI: 10.1023/A:1005726918110

31. Guivarch A., Spena A., Noin M., Besnard C., Chriqui D. The pleiotropic effects induced by the rolC gene in transgenic plants are caused by expression restricted to protophloem and companion cells. Transgenic Research. 1996;5(1):3-11. DOI: 10.1007/BF01979917

32. Hu Y., Chen B., Ni T., Li N., Lin Z. Promoter of the rolC gene of Agrobacterium rhizogenes can be strongly regulated in glandular cell of transgenic tobacco. Molecular Biotechnology. 2003;24(2):121-125. DOI: 10.1385/MB:24:2:121

33. Intrieri M.C., Buiatti M. The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Molecular Phylogenetics and Evolution. 2001;20(1):100-110. DOI: 10.1006/mpev.2001.0927

34. Inyushkina Y.V., Kiselev K.V., Bulgakov V.P., Zhuravlev Y.N. Specific genes of cytochrome P450 monooxygenases are implicated in biosynthesis of caffeic acid metabolites in rolC-transgenic culture of Eritrichium sericeum. Biochemistry (Moscow). 2009;74:917-924. DOI: 10.1134/S0006297909080148

35. Ismail H., Dilshad E., Waheed M.T., Sajid M., Kayani W.K., Mirza B. Transformation of Lactuca sativa L. with rolC gene results in increased antioxidant potential and enhanced analgesic, anti-inflammatory and antidepressant activities in vivo. 3 Biotech. 2016;6(2):215. DOI: 10.1007/s13205-016-0533-4

36. Jaglo K.R., Kleff S., Amundsen K.L., Zhang X., Haake V., Zhang J.Z, Deits T., Thomashow M.F. Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiology. 2001;127:910-917. DOI: 10.1104/pp.010548

37. Kaneyoshi J., Kobayashi S. Characteristics of transgenic trifoliate orange (Poncirus trifoliata Raf.) possessing the rolC gene of Agrobacterium rhizogenes Ri plasmid. Journal of Japanese Society of Horticultural Science. 1999;68:734-738. DOI 10.2503/jjshs.68.734

38. Kiselev K.V., Kusaykin M.I., Dubrovina A.S., Bezverbny D.A., Zvyagintseva T.N., Bulgakov V.P. The rolC gene induces expression of a pathogenesis-related β-1, 3-glucanase in transformed ginseng cells. Phytochemistry. 2006;67(20):2225-2231. DOI: 10.1016/j.phytochem.2006.07.019

39. Koshita Y., Nakamura Y., Kobayashi S., Morinaga K., Introduction of the rolC gene into the genome of the Japanese persimmon causes dwarfism. Journal of Japanese Society of Horticultural Science. 2002;71:529-531. DOI: 10.2503/jjshs.71.529

40. Kyndt T., Quispe D., Zhai H., Jarret R., Ghislain M., Liu Q., Gheysen G., Kreuze J.F. The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: an example of a naturally transgenic food crop. Proceedings of the National Academy of Sciences. 2015;112(18):5844-5849. DOI: 10.1073/pnas.1419685112

41. Kurioka Y., Suzuki Y., Kamada H., Harada H. Promotion of flowering and morphological alterations in Atropa belladonna transformed with a CaMV 35S-rolC chimeric gene of the Ri plasmid. Plant Cell Reports. 1992;12(1):1-6. DOI: 10.1007/BF00232412

42. Landi L., Capocasa F., Costantini E., Mezzetti B. ROLC strawberry plant adaptability, productivity, and tolerance to soil-borne disease and mycorrhizal interactions. Transgenic Research. 2009;18(6):933-942. DOI: 10.1007/s11248-009-9279-7

43. Lee C., Wang L., Ke S., Qin M., Cheng Z-M. Expression of the rolC gene in transgenic plants of Salpiglossis sinuata L. Horticultural Science. 1996;31:571. DOI: 10.21273/HORTSCI.31.4.571e

44. Martin-Tanguy J., Corbineau F., Burtin D., Ben-Hayyim G., Tepfer D. Genetic transformation with a derivative of rolC from Agrobacterium rhizogenes and treatment with α-aminoisobutyric acid produce similar phenotypes and reduce ethylene production and the accumulation of water-insoluble polyamine-hydroxycinnamic acid conjugates in tobacco flowers. Plant Science. 1993;93(1-2):63-76. DOI: 10.1016/0168-9452(93)90035-X

45. Matsuki R., Onodera H., Yamauchi T., Uchimiya H. Tissue-specific expression of the rolC promoter of the Ri plasmid in transgenic rice plants. Molecular and General Genetics. 1989;220:12-16. DOI: 10.1007/BF00260849

46. Matveeva T.V., Bogomaz D.I., Pavlova O.A., Nester E.W., Lutova L.A. Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. Molecular Plant-Microbe Interactions. 2012;25(12):1542-1551. DOI: 10.1094/MPMI-07-12-0169-R

47. Matveeva T.V., Sokornova S.V. Agrobacterium rhizogenes-mediated Transformation of Plants for Improvement of Yields of Secondary Metabolites. In: A. Pavlov, T. Bley (eds). Bioprocessing of Plant In Vitro Systems. Reference Series in Phytochemistry. Cham (Switzerland): Springer; 2016. p.161-202. DOI: 10.1007/978-3-319-32004-5_18-1

48. Matveeva T.V., Otten L. Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Molecular Biology. 2019;101(4):415-437. DOI: 10.1007/s11103-019-00913-y

49. Mauro M.L., Costantino P., Bettini P.P. The never-ending story of rol genes: a century after. Plant Cell, Tissue and Organ Culture. 2017;131(2):201-212. DOI: 10.1007/s11240-017-1277-5

50. Michael T., Spena A. The plant oncogenes rolA, B, and C from Agrobacterium rhizogenes. In: K.M.A. Gartland, M.R. Davey (eds) Agrobacterium Protocols. Methods in Molecular Biology. 1995;44:207-222. DOI: 10.1385/0-89603-302-3:207

51. Mitiouchkina T.Y., Dolgov S.V. Modification of chrysanthemum plant and flower architecture by rolC gene from Agrobacterium rhizogenes introduction. Acta Horticulturae. 2000;508:163-172. DOI: 10.17660/ActaHortic.2000.508.21

52. Mohajjel-Shoja H., Clément B., Perot J. Alioua M., Otten L. Biological activity of the Agrobacterium rhizogenes-derived trolC gene of Nicotiana tabacum and its functional relation to other plast genes. Molесular Plant-Microbe Interactions. 2011;24(1):44-53. DOI: 10.1094/MPMI-06-10-0139

53. Nagata N., Kosono S., Sekine M., Shinmyo A., Syono K. The regulatory functions of the rolB and rolC genes of Agrobacterium rhizogenes are conserved in the homologous genes (Ngrol) of Nicotiana glauca in tobacco genetic tumors. Plant and Cell Physiology. 1995;36(6):1003-1012. DOI: 10.1093/oxfordjournals.pcp.a078842

54. Naseem M., Dandekar T. The role of auxin-cytokinin antagonism in plant-pathogen interactions. PLoS Pathogene. 2012;11:e1003026. DOI: 10.1371/journal.ppat.1003026

55. Nilsson O., Moritz T., Imbault N., Sandberg G., Olsson O. Hormonal characterization of transgenic tobacco plants expressing the rolC gene of Agrobacterium rhizogenes T L -DNA. Plant Physiology. 1993;102(2):363-371.

56. Nilsson O., Little C.H.A., Sandberg G., Olsson O. Expression of two heterologous promoters, Agrobacterium rhizogenes rolC and cauliflower mosaic virus 35S, in the stem of transgenic hybrid aspen plants during the annual cycle of growth and dormancy. Plant Molecular Biology. 1996;31(4):887-895. DOI: 10.1007/bf00019475

57. Nilsson O., Olssen O. Getting to the root: The role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiologia Plantarum. 1997;100:463-473. DOI: 10.1111/j.1399-3054.1997.tb03050.x

58. Oono Y., Kanaya K., Uchimiya H. Early flowering in transgenic tobacco plants possessing the rolC gene of Agrobacterium rhizogenes Ri plasmid. The Japanese Journal of Genetics. 1990;65(1):7-16. DOI: 10.1266/jjg.65.7

59. Otten L. The Agrobacterium phenotypic plasticity (Plast) genes. Current Topics in Microbiology and Immunology. 2018;418:375-419. DOI: 10.1007/82_2018_93

60. Ovadis M., Zuker A., Tzfira T., Ahroni A., Shklarman E., Scovel G., Itzhaki H. Ben-Meir Vainstein A. Generation of transgenic carnation plants with novel characteristics by combining microprojectile bombardment with Agrobacterium tumefaciens transformation. Plant Biotechnology and In Vitro Biology in the 21st Century. 1999;36:189-192. DOI: 10.1007/978-94-011-4661-6_44

61. Palazón J., Cusidó R.M., Roig C., Piñol M.T. Effect of rol genes from Agrobacterium rhizogenes TL-DNA on nicotine production in tobacco root cultures. Plant Physiology and Biochemistry. 1997;35:155-62.

62. Palazón J., Cusidó R.M., Roig C., Piñol M.T. Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Reports. 1998a;17:384-390. DOI: 10.1007/s002990050411

63. Palazón J., Cusidó R.M., Gonzalo J., Bonfill M., Morales S., Piñol M.T. Relation between the amount of rolC gene product and indole alkaloid accumulation in Catharantus roseus transformed root cultures. Journal of Plant Physiology. 1998b;153:712-718. DOI: 10.1016/S0176-1617(98)80225-3

64. Pavlova O.A., Matveyeva T.V., Lutova L.A. Rol-GENES of Agrobacterium rhizogenes. Ecological genetics. 2013;11(1):59-68. [In Russian] (Павлова О.А., Матвеева Т.В., Лутова Л.А. Rol-гены Agrobacterium rhizogenes. Экологическая генетика. 2013;11(1):59-68). doi: 10.17816/ecogen11159-68

65. Pieterse C.M.J., Van der Does D., Zamioudis C., Leon-Reyes A., Van Wees S.C.M. Hormonal modulation of plant immunity. Annual Revew of Cell and Development Biology. 2012;28:489-521. DOI: 10.1146/annurev-cellbio-092910-154055

66. Riker A.J., Banfield W.M., Wright W.H., Keitt G.W., Sagen H.E. Studies on infectious hairy root of nursery apple trees. Journal of Agricultural Research. 1930;41(7):507-540.

67. Sawada H., Ieki H., Oyaizu H., Matsumoto S. Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes. International Journal of Systematic Bacteriology. 1993;43(4):694-702.

68. Schmülling T., Schell J., Spena A. Single genes from Agrobacterium rhizogenes influence plant development. The EMBO Journal. 1988;7:2621-2629. DOI: 10.1002/j.1460-2075.1988.tb03114.x

69. Schmülling T., Fladung M., Grossmann K., Schell J. Hormonal content and sensitivity of transgenic tobacco and potato plants expressing single rol genes of Agrobacterium rhizogenes T-DNA. The Plant Journal. 1993;3:371-382. DOI: 10.1046/j.1365-313X.1993.t01-20-00999.x

70. Shkryl Y.N., Veremeichik G.N., Bulgakov V.P., Tchernoded G.K., Mischenko N.P., Fedoreyev S.A., Zhuravlev Y.N. Individual and combined effects of the rolA, B and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnology and Bioengineering. 2008;100:118-125. DOI: 10.1002/bit.21727

71. Shkryl Y.N., Veremeichik G.N., Bulgakov V.P., Gorpechenko T.Y., Aminin D.L., Zhuravlev Y.N. Decreased ROS level and activation of antioxidant gene expression in Agrobacterium rhizogenes pRiA4-transformed calli of Rubia cordifolia. Planta. 2010;232:1023-1032. DOI: 10.1007/s00425-010-1237-3

72. Scorza R., Zimmerman T.W., Cordts J.M., Footen K.J., Ravelonandro M. Horticultural characteristics of transgenic tobacco expressing the rolC gene from Agrobacterium rhizogenes. Journal of the American Society for Horticultural Science. 1994;119(5):1091-1098. DOI: 10.21273/JASHS.119.5.1091

73. Slightom J., Durand-Tardif M., Jouanin L., Tepfer D. Nucleotide sequence analysis of TL-DNA of Agrobacterium rhizogenes agropine type plasmid. Identification of open reading frames. Journal of Biological Chemistry. 1986;261:108-121. DOI: 10.1016/S0021-9258(17)42439-2

74. Souq F., Coutos-Thevenot P., Yean H., Delbard G., Maziere Y., Barbe J.P., Boulay M. Genetic transformation of roses, 2 examples: one on morphogenesis, the other on anthocyanin biosynthetic pathway. Second International Symposium on Roses. Acta Horticulturae. 1996;424:381-388. 10.17660/ActaHortic.1996.424.73

75. Spena A., Schmülling T., Koncz C., Schell J. Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants. The EMBO Journal. 1987;6:3891-3899. DOI: 10.1002/j.1460-2075.1987.tb02729.x

76. Spena A., Aalen R.B., Schulze S.C. Cell-autonomous behavior of the rolC gene of Agrobacterium rhizogenes during leaf development: a visual assay for transposon excision in transgenic plants. The Plant Cell. 1989;1(12):1157-1164. DOI: 10.105/tpc.1.12.1157

77. Sugaya S., Hayakawa K., Handa T., Uchimiya H. Cell-specific expression of the rolC gene of the T L -DNA of Ri plasmid in transgenic tobacco plants. Plant and Cell Physiology. 1989;30(5):649-653. DOI: 10.1093/oxfordjournals.pcp.a077789

78. Sugaya S., Uchimiya H. Deletion analysis of the 5′-upstream region of the Agrobacterium rhizogenes Ri plasmid rolC gene required for tissue-specific expression. Plant Physiology. 1992;99(2):464-467. DOI: 10.1104/pp.99.2.464

79. Tzfira T., Vainstein A. Altman A. rol-Gene expression in transgenic aspen (Populus tremula) plants results in accelerated growth and improved stem production index. Trees. 1999;14:49-54. DOI: 10.1007/PL00009753

80. White F.F., Garfinkel D.J., Huffman G.A., Gordon M.P., Nester E.W. Sequence homologous to Agrobacterium rhizogenes T-DNA in the genome of uninfected plants. Nature. 1983;301:348-350. doi.org/10.1038/301348a0

81. Winefield C., Lewis D., Arathoon S., Deroles D. Alteration of petunia plant form through the introduction of the rolC gene from Agrobacterium rhizogenes. Molecular Breeding. 1999;5:543-551. DOI: 10.1023/A:1009638401275

82. Yokoyama R., Hirose T., Fujii N., Aspuria E.T., Kato A., Uchimiya H. The rolC promoter of Agrobacterium rhizogenes Ri plasmid is activated by sucrose in transgenic tobacco plants. Molecular and General Genetics. 1994;244:15-22. DOI: 10.1007/BF00280182

83. Young J.M., Kuykendall L.D., Martínez-Romero E., Kerr A., Sawada H. 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. International Journal of Systematics and Evolutionary Microbiology. 2001;51(1):89-103. doi:10.1099/00207713-51-1-89.

84. Zuker A., Tzfira T., Scovel G., Ovadis M., Shklarman E., Itzhaki H., Vainstein A. RolC-transgenic carnation with improved horticultural traits: quantitative and qualitative analyses of green-house-grown plants. Journal of the American Society for Horticultural Science. 2001;126(1):13-18. DOI: 10.21273/JASHS.126.1.13