eISSN: 2221-6197 DOI: 10.31301/2221-6197

Features of phenotypic manifestation of rol-genes from Agrobacterim rhizogenes in plants

Year: 2017

Pages: 304-317

Number: Volume 9, issue 4

Type: scientific article

Summary:

Ri plasmids are transferred by Agrobacterium rhizogenes into plant cells and causing the appearance hairy roots. The rol-genes play a key role of such roots formation, and locate in the T-DNA of Ri plasmid. Bacteria interact with plants and transfer the rolA, B, C and D genes into the plant genome. Expression products of rol-genes are regulators of the phytohormones activity and change the physiological and morphological characteristics of plants. For example, rolB induces roots and stochastic buds formation, the increase of flowers size, and stimulates the production of auxin-binding proteins. The rolB-transgenic plants have resistance to salt stress, low and high temperatures, excessive light and to active forms of oxygen. The rol-genes products can influence growth processes, enhance the protective functions of plants, and promote the synthesis of valuable primary and secondary metabolites in hairy roots. Therefore, the technology of hairy roots cultivation is promising for use in the pharmaceutical, food and perfume industries. Rol-genes are studied for a long time but today their functions are not sufficiently explored. In this review article, we attempted to generalize the results of studies on the phenotypic manifestation of rol genes in growing plants and hairy roots.

Keywords:

rol-genes, Ri plasmid, hairy roots, Agrobacterium rhizogenes, T-DNA, transgenic plants, phenotypic characteristics, secondary metabolites, stress resistance

References:

  1. Авраменко Т.В. Активность и продукция пероксидаз III класса в клеточных культурах растений, трансформированных генами rolB и rolC: автореф. дис. канд. биол. наук / Т. В. Авраменко; Биол.-почв. ин-т ДВО РАН. Владивосток, 2015. 24 с. [Avramenko T.V Activity and production of Class III peroxidases in cell cultures of plants transformed with rolB and rolC genes: Abstract. dis. cand. biol. sciences / T.V Avramenko; Biol.-soil. institute of Far Eastern Branch of RAS. Vladivostok, 2015. 24 p. In Russian].
  2. Кулаева О.А., Матвеева Т.В., Лутова Л.А. Горизонтальный перенос генов от агрообактерий к растениям // Экологическая генетика. 2006. Т. IV. № 4. С. 10–19. [Kulaeva O.A., Matveeva T.V., Lutova L.A Horizontal transfer of genes from agroobacteria to plants // Ecological genetics. 2006. V. IV. № 4. P. 10–19. In Russian].
  3. Кулуев Б.Р. Каулимовирусы и их полногеномные промоторы // Биомика. Т. 4. С. 1-19. [Kuluev B.R. Caulimoviruses and their promoters // Biomics. 2012. V. 4. P. 1-19. In Russian].
  4. Кулуев Б.Р., Вершинина З.Р., Князев А.В., Чемерис Д.А., Баймиев Ан.Х., Чумаков М.И., Баймиев Ал.Х., Чемерис А.В. «Косматые» корни растений – важный инструментарий для исследователей и мощная фитохимбиофабрика для производственников // Биомика. 2015. Т. 7. С. 70–120. [Kuluev B.R., Vershinina Z.R., Knyazev A.V., Chemeris D.A., Baimiev A.N., Chumakov M.I., Baimiev A.L., Chemeris A.V. Plant hairy roots are important instrumentation for researchers and powerful phytochembiofactory for manufacturers // Biomics. 2015. V. 7. P. 70–120. In Russian].
  5. Кулуев Б.Р., Геращенков Г.А., Рожнова Н.А., Баймиев Ан.Х., Вершинина З.Р., Князев А.В., Матниязов Р.Т., Ясыбаева Г.Р., Никоноров Ю.М., Чемерис Д.А., Баймиев Ал.Х., Чемерис А.В. CRISPR/Cas редактирование геномов растений // Биомика. 2017. Т. 9. С. 155–182. [Kuluev B.R., Gerashchenkov G.A., Rozhnova N.A., Baymiev An.Kh., Vershinina Z.R., Knyazev A.V., Matniyazov R.T., Gumerova G.R., Mikhailova E.V., Nikonorov Yu.M., Chemeris D.A., Baymiev Al.Kh., Chemeris A.V. CRISPR/Cas genome editing of plants // Biomics. 2017. V. 9. P. 155–182. In Russian].
  6. Кузовкина И.Н., Вдовитченко М.Ю. Генетически трансформированные корни как модельная система для изучения физиологических и биохимических процессов корневой системы целого растения / В кн.: Молекулярно-генетические и биохимические методы в современной биологии растений. Под ред. Кузнецова Вл. В., Кузнецова В.В., Романова Г.А. Москва, 2012. БИНОМ, Лаборатория знаний, C. 137–153. [Kuzovkina I.N., Vdovitchenko M.Yu. Genetically transformed roots as a model system for studying the physiological and biochemical processes of the root system of an entire plant / In: Molecular genetic and biochemical methods in modern plant biology. Kuznetsova Vl.V., Kuznetsova V.V., Romanova G.A. Moscow, 2012. BINOM, Laboratory of Knowledge, P. 137–153. In Russian].
  7. Михайлова Е.В., Кулуев Б.Р., Ясыбаева Г.Р., Чемерис А.В. Создание культур бородатых корней Withania somnifera и оценка параметров их роста при выращивании на твердых и жидких питательных средах // Вестник биотехнологии и физико-химической биологии им. Ю.А. Овчинникова. 2017. Т. 13. С. 40–45. [Mikhailova E.V., Kuluev B.R., Yasibaeva G.R., Chemeris A.V. Creation of cultures of hairy roots Withania somnifera and assessment of parameters of their growth at cultivation on firm and liquid nutritious environments // Journal “Yu.A. Ovchinnikov Bulletin of Biotechnology and Physical and Chemical Biology”. V. 13. P. 40-45. In Russian].
  8. Мусин Х.Г., Якупова А.Б., Михайлова Е.В., Кулуев Б.Р. Особенности роста культур генетически трансформированных (бородатых) корней табака и витании при изменении объема питательной среды // Вестник биотехнологии и физико-химической биологии им. Ю.А. Овчинникова. 2017. Т. 13. С. 46–50. [Musin Kh.G., Yakupova A.B, Mikhailova E.V., Kuluyev B.R. Peculiarities of the growth of cultures of genetically transformed (hairy) roots of tobacco and vitania with a change in the volume of nutrient medium // Journal “Yu.A. Ovchinnikov Bulletin  of Biotechnology and Physical and Chemical Biology”. V. 13. P. 46–50. In Russian].
  9. Павлова О.А., Матвеева Т.В., Лутова Л.А. Rol-гены Agrobacterium rhizogenes // Экологическая генетика. 2013. Т. XI. С. 59–68. [Pavlova O.A., Matveeva Т.V., Lutova L.A. Rol-genes of Agrobacterium rhizogenes // Ecological genetics. 2013. V. XI. P. 59–68. In Russian].
  10. Чемерис А.В., Бикбулатова С.М., Чемерис Д.А., Баймиев Ал.Х., Князев А.В., Кулуев Б.Р., Максимов И.В. Надо ли опасаться ГМО? Взгляд несторонних наблюдателей на истерию вокруг // Биомика. 2014. Т.6. С. 77–138. [Chemeris A.V., Bikbulatova S.M., Chemeris D.A., Baymiev A.L., Knyazev A.V., Kuluev B.R., Maksimov I.V. Should beware of the GMOs? On-site observers view on the hysteria around // Biomics. 2014. V.6. P. 77–138. In Russian].
  11. Чемерис А.В., Чемерис Д.А., Баймиев А.Х., Князев А.В., Кулуев Б.Р., Максимов И.В. Борьба с ГМО как неолысенковщина // Биомика. 2015. Т. 7. С. 1–39. [Chemeris A.V., Chemeris D.A., Baymiev A.Kh., Knyazev A.V., Kuluev B.R., Maksimov I.V. The fight against GMO is neolysenkoism // Biomics. V. 7. P. 1–39. In Russian].
  12. Черпаков В.В. Дендрофильные насекомые - переносчики и симбионты возбудителей болезней древесных растений // VII Чтения памяти О. А. Катаева. Вредители и болезни древесных растений России / Материалы междунар. конференции, Санкт- Петербург, 25–27 ноября 2013 г. СПб.: СПб ГЛТУ, 2013. С. 97–98. [Cherpakov V.V. Dendrophilous insects - carriers and symbionts of pathogens of diseases of wood plants // VII Readings in memory of OA Katayev. Pests and diseases of woody plants in Russia / Intern. Conference, St. Petersburg, November 25–27, 2013 SPb.: St. Petersburg State Technical University, 2013. P. 97-98. In Russian].
  13. Чуб В.В. Растения-ГМО: как это делается // Потенциал. Химия. Биология. Медицина. №11. [Chub V.V. Plants-GMOs: how it's done // Potential. Chemistry. Biology. Medicine 2011. № 11. In Russian].
  14. Чумаков М.И. Механизм агробактериальной трансформации растений. Саратов: Слово, 2001. 256 с. [Chumakov M.I. The mechanism of agrobacterial transformation of plants. Saratov: The Word, 2001. 256 pp. In Russian].
  15. Чумаков М.И. Белковый аппарат, реализующий горизонтальный перенос Т-ДНК из агробактерий в эукариотические клетки (обзор) // Биохимия. Т. 78. С. 1670–1683. [Chumakov M.I. The protein complex realizes the horizontal transfer of T-DNA from agrobacterium to eukaryotic cells (review) // Biochemistry. 2013. V. 78. P. 1670–1683. In Russian].
  16. Эрст А.А., Зибарева Л.Н., Железниченко Т.В., Ковзунова О.В. Культура генетически трансформированных корней (hairy roots) Silene roemeri Friv. – источник получения фитоэкдистероидов // Вестник Томского государственного университета. Биология. 2017. № 37. С. 17–30. [Erst A.A., Zibareva L.N., Zheleznichenko T.V., Kovzunova O.V. Culture of genetically transformed roots (hairy roots) Silene roemeri Friv is source of phytoecdysteroids production // Tomsk State University Journal of Biology. 2017. №. 37. P. 17–30. In Russian].
  17. Ясыбаева Г.Р., Вершинина З.Р., Кулуев Б.Р., Чемерис А.В. Безбактериальное получение косматых корней // Вестник защиты растений. Т. 89. С. 187–188. [Yasibaeva G.R., Vershinina Z.R., Kuluev B.R., Chemeris A.V. Induction of hairy roots without Agrobacterium transformation // Plant Protection News. 2016. V. 89. P. 187–188. In Russian]
  18. Aggarwal B.B., Bhardwaj A., Aggarwal R.S., Seeram N.P., Shishodia S., Takada Y. Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies //Anticancer Res. 2004 V. 24. P. 2783–2840.
  19. Altamura M.M., Capitani F., Gazza L., Capone I., Costantino P. The plant oncogene rolB stimulates the formation of flower and root meristemoids in tobacco thin cell layers // New Phytol. 1994. V. 126. P. 283–293. doi: 10.1111/j.1469-8137.1994.tb03947.x
  20. Altamura M.M. Agrobacterium rhizogenes rolB and rolD genes: regulation and involvement in plant development // Plant Cell, Tissue and Organ Culture. 2004. V. 77. Р. 89–101. doi: 10.1023/B:T ICU.0000016609.22655.33
  21. Ayadi R., Tremouillaux-Guiller J. Root formation from transgenic calli of Ginkgo biloba // Tree Physiol. 2003. V. 23. P. 713–718. doi: 10.1093/treephys/23.10.713
  22. Barros L.M.G., Curtis R.H., Viana A.A.B., Campos L., Carneiro M. Fused RolA Protein enhances glucoronidase activity 50-fold: implication for rolA mechanism of action. protein pep // Lett. 2003. V. 10. P. 303–311. doi: 10.2174/0929866033478951
  23. Bellincampi D., Cardarelli M., Zaghi D., Serino G., Salvi G., Gatz C., Cervone F., Altamura M.M., Costantino P., De Lorenzo G. Oligogalacturonides prevent rhizogenesis in rolB transformed tobacco explants by inhibiting auxin-induced expression of the rolB gene // Plant Cell .1996. 8. P. 477–487. doi: 10.1105/tpc.8.3.477
  24. 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 // J Nat Prod. 2000. V. 63. P. 1249–1252. doi: 10.1021/np990614l
  25. Bulgakov V.P., Tchernoded G.K., Mischenko N.P., Khodakovskaya M.V., Glazunov V.P., Radchenko S.V., Zvereva E.V., Fedoreyev S.A., Zhuravlev Y.N., Effect of salicylic acid, methyl jasmonate, ethephon and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with the rolB and rolC genes // Biotechnol. 2002. V.97. P. 113–221. doi: 10.1016/S0168-1656(02)00067-6
  26. 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 // Adv. Biochem. Eng. Biotechnol. 2013. V.134. P.11–22. doi: 10.1007/10_2013_179
  27. Bulgakov V.P., Veremeichik G.N., Shkryl Y.N. The rolB gene activates the expression of genes encoding microRNA processing machinery // Biotechnol Lett. 2015. V. 37. P. 921–925. doi: 10.1007/s10529-014-1743-7
  28. Capone I., Frugis G., Costantino P., Cardarelli M. Expression in different populations of cells of the root meristem is controlled by different domains of the rolB promoter // Plant Mol. Biol. 1994. V. 25. P. 681–691. doi: 1007/BF00029606
  29. Cardarelli M., Mariotti D., Pomponi M., Spano L., Capone I., Costantino P. Agrobacterium rhizogenes T-DNA genes capable of inducing hairy root phenotype // Mol. Gen. Genet. 1987. V. 209. P. 475–480. doi: 10.1007/BF00331152
  30. Carneiro M., Vilaine F. Differential expression of the rolA plant oncogene and its effect on tobacco development // Plant J. 1993. V. 3. P. 785–792. doi: 10.1111/j.1365-313X.1993.00785.x
  31. Christey M.C. Use of Ri-mediated transformation for production of transgenic plants // In Vitro Cell Dev Biol. 2001. V. 37. P. 687–700. doi: 10.1079/IVP2001203
  32. Christensen B., Sriskandarajah S., Serek M., Müller R. Transformation of Kalanchoe blossfeldiana with rol-genes is useful in molecular breeding towards compact growth // Plant Cell Rep. 2008. V. 27. P. 1485–1495. doi: 10.1007/s00299-008-0575-0
  33. Costantino P., Capone I., Cardarelli M., De-Paolis A., Mauro M.L., Trovato M. Bacterial plant oncogenes: the rol genes’ saga // Genetica. 1994. V. 94. P. 203–211. doi: 10.1007/BF01443434
  34. De Paolis A., Sabatini S., De Pascalis L., Costantino P., Capone I. A rolB regulatory factor belongs to a new class of single zinc finger plant proteins // Plant J. 1996. V. 10. P. 215–223. doi: 10.1046/j.1365-313X.1996.10020215.x
  35. Dehio C., Schell J. Stable expression of a single-copy rolA gene in transgenic Arabidopsis thaliana plants allows an exhaustive mutagenic analysis of the transgene associated phenotype // Mol. Gen. Genet. 1993. V. 241. P. 359–366. doi: 10.1007/BF00284689
  36. Dehesh K., Bruce W.B., Quail P.H. A transacting factor that binds to a GT-motif in a phytochrome gene promoter // Science. 1990. V. 250. P. 1397–1399. doi: 10.1126/science.2255908
  37. Dilshad E., Cusido R.M., Palazon J., Estrada K.R., Bonfill M., Mirza B. Enhanced artemisinin yield by expression of rol genes in Artemisia annua // J. 2015. V. 14. P. 424. doi: 10.1186/s12936-015-0951-5
  38. Durand-Tardif M., Broglie R., Slightom J., Tepfer D. Structure and expression of Ri T-DNA from Agrobacterium rhizogenes in Nicotiana tabacum. Organ and phenotypic specificity // Mol. Biol. 1985. V. 186. P. 557–564. doi: 10.1016/0022-2836(85)90130-5
  39. 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 // EMBO J. 1991. V. 10. P. 2889–2895.
  40. 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 // Plant J. 1996. V. 10. P. 33–46. doi: 10.1046/j.1365-313X.1996.10010033.x
  41. Falasca G., Altamura M.M., D’Angeli S., Zaghi D., Costantino P., Mauro M.L. The rolD oncogene promotes axillary bud and adventitious root meristems in Arabidopsis // Plant Physiol Biochem. 2010. V. 48. P. 797–804. doi: 10.1016/j.plaphy.2010.06.002
  42. Gechev T.S., Van Breusegem F., Stone J.M., Denev I., Laloi C. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death // Bioessays. 2006. V. 28. P. 1091–1101. doi: 10.1002/bies.20493
  43. Guivarch A., Spena A., Noin M. The pleiotropic effects induced by the rolC gene in transgenic plants are caused by expression restricted to protophloem and companion cells // Transgen. Res. 1996. V. 5. P. 3–11. doi: 10.1007/BF01979917
  44. Ismail H., Dilshad E., Tahir Waheed M., Sajid M., Kayani K., Mirza B. Transformation of Lactuca sativa with rolC gene results in increased antioxidant potential and enhanced analgesic, anti-inflammatory and antidepressant activities in vivo // Biotech 2016. V. 6. P. 215. doi: 10.1007/s13205-016-0533-4
  45. Jill S. Gartland. Agrobacterium virulence// Methods in Molecular Biology. 1995. V. 44. P.15-28. doi: 10.1385/0-89603-302-3:15
  46. Kiselev K.V, Dubrovina A.S, Veselova M.V, Bulgakov V.P, Fedoreyev S.A., Zhuravlev Y.N. The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells // J Biotechnol. 2007. V. 128. P. 681–692. doi: 10.1016/j.jbiotec.2006.11.008
  47. Kuluev B.R., Knyazev A.V., Mikhaylova E.V., Ermoshin A.A., Nikonorov Y.M., Chemeris A.V. The poplar ARGOS-LIKE gene promotes leaf initiation and cell expansion, and controls organ size // Biologia Plantarum. 2016. V. 60. P. 513–522.
  48. Kuluev B.R., Knyazev A.V., Postrigan B.N., Chemeris A.V. The creation of transgenic tobacco plants expressing fragments of the ARGOS and NtEXPA4 genes in antisense orientation // Russian Journal of Genetics. 2014. V. 50. P. 37–44. doi: 10.1134/S1022795414010074
  49. Knyazev A.V., Kuluev B.R., Vershinina Z.R., Yasybaeva G.R., Chemeris A.V. Agrobacterium rhizogenes mediated hairy root induction in Parasponia andersonii Planch // Asian Journal of Plant Sciences. 2017. V. 16 (4). P. 227–234.
  50. Kunshi M., Shimomura K., Takida M., Kitanaka S. Growth and ginsenoside production of adventitious and hairy root cultures in an interspecific hybrid ginseng (Panax ginseng, quinquefolium) // Nat Med. 1998. V. 52. P. 1–4.
  51. Landi F., Capocasa E., Costantini B., Mezzetti M. RolC strawberry plant adaptability, productivity, and tolerance to soil-borne disease and mycorrhizal interactions // Transgenic Res. 2009. V. 18. P. 933–942. doi: 10.1007/s11248-009-9279-7
  52. Leach F., Aoyagi K. Promoter analysis of the highly expressed rolC and rolD root-inducing genes of Agrobacterium rhizogenes: enhancer and tissue-specific DNA determinants are dissociated // Plant Sci. 1991. V. 79. P. 69–76. doi: 10.1016/0168-9452(91)90071-F
  53. Magrelli A., Langenkemper K., Dehio C., Schell J., Spena A. Splicing of the rolA transcript of Agrobacterium rhizogenes in Arabidopsis // Science. 1994. V. 266. P. 1986–1988. doi: 10.1126/science.7528444
  54. Maurel S., Barbier-Bryqoo H., Spena A., Temp G., Guern G. Single rol genes from the Agrobacterium rhizogenes TL-DNA alter some of the cellular responses to auxin in Nicotiana tobacum // Plant Physiol. 1991. V. 97. P. 212–216. doi: 10.1104/pp97.1.212
  55. Mauro M.L., Trovato M., Paolis A.D., Gallelli A., Costantino P., Altamura M.M. The plant oncogene rolD stimulates flowering in transgenic tobacco plants // Dev. Biol. 1996. V. 180. P. 693–700. doi: 10.1006/dbio.1996.0338
  56. Mauro M.L., Costantino Р.P., Bettini P. The never ending story of rol genes: a century after // Plant Cell, Tissue and Organ Culture. 2017. V. 2. P. 201–212. doi: 10.1007/s11240-017-1277-5
  57. Mercuri A., Bruna S., De Benedetti L., Burchi G., Schiva T. Modification of plant architecture in Limonium induced by rol genes // Plant Cell Tiss Org Cult. 2001. V. 65. P. 247–253. doi: 10.1023/A:1010623309432
  58. Meyer A.D., Tempé J., Costantino P. Hairy root: a molecular overview. Functional analysis of Agrobacterium rhizogenes T-DNA genes // Plant microbe interaction. 2000. V 5. P. 93–139.
  59. Mohajjel-Shoja H. Contribution to the study of the Agrobacterium rhizogenes plast genes, rolB and rolC, and their homologs in Nicotiana tabacum. Thesis of University of Strasbourg. 2010.
  60. Moriuchi H., Okamoto C., Nishihama R., Yamashit I., Machida Y., Tanaka N. Nuclear localization and interaction of rolB with plant 14-3-3 proteins correlate with induction of adventitious roots by the oncogne rolB // Plant J. 2004. V. 38. P. 260–275. doi: 10.1111/j.1365-313X.2004.02041.x
  61. Nemhauser J.L., Feldman L.J., Zambryski P.C. Auxin and ETTIN in Arabidopsis gynoecium morphogenesis // Development. 2000. V. 127. P. 3877–3888.
  62. Nilsson O., Olsson O. Getting to the root: The role of the Agrobacterium 
    rhizogenes rol
    genes in the formation of hairy roots // Physiol Plant. 1997. V. 100. P. 463–473. doi: 10.1111/j.1399-3054.1997.tb03050.x
  63. Palazon J., Cusido R.M., Roig C., Piñol M.T. Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants // Plant Cell Rep. 1998. V. 17. P. 384–390. doi: 10.1007/s002990050411
  64. Shkryl Y.N., Veremeichik G.N., Bulgakov V.P., Tchernoded G.K., Mischenko N.P., Fedoreyev S.A., Zhuravle Y.N. Individual and combined effects of the rolA, B and C genes on anthraquinone production in Rubia cordifolia transformed calli // Biotechnol. Bioeng. 2008. V. 1. P. 118–125. doi: 10.1002/bit.21727
  65. Schmülling T., Schell J., Spena A. Single genes from Agrobacterium rhizogenes influence plant development // EMBO J. 1988. V. 7. P. 2621–2629.
  66. Shyamkumar Barampuram, Zhanyuan J. Zhang Recent Advances in Plant Transformation // Methods in Molecular Biology. 2011. V. 701. P. 1–35. doi: 10.1007/978-1-61737-957-4_1
  67. Sinkar P.S., Pythoud F., White F.F., Nester E.W., Gordon M.P. RolA locus of the Ri plasmid directs developmental abnormalities in transgenic tobacco plants // Genes Dev. 1988. V. 2. P. 688–697. doi: 10.1101/gad.2.6.688
  68. Spano L., Mariotti D., Cardarelli M., Branca C., Costantino P. Morphogenesis and auxin sensitivity of transgenic tobacco with different complements of Ri T-DNA // Plant Physiol. 1988. V. 87. P. 479–483.
  69. Spena A., Schmulling T., Koncz C., Shell J. Independent and synergistic activity of rolA, B and C loci in stimulating abnormal growth in plants // EMBO J. 1987. V. 6. P. 3891–3899.
  70. Ono N.N, Tian L. The multiplicity of hairy root cultures: prolific possibilities // Plant Sci. 2011. V. 180. Р. 439–446. doi: 10.1016/j.plantsci.2010.11.012.
  71. Palazon J., Cusido R.M., Roig C., Piñol M.T. Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants // Plant Cell Rep. 1998. V. 17. P. 384–390. doi: 10.1007/s002990050411
  72. Tobena-Santamaria R., Bliek K., Ljung G., Sandberg J.N.M. FLOOZYof petunia is a Flavin mono-oxygenaselike protein required for the specification of leaf and flower architecture // Gene Dev. 2002. V. 16. P. 753–763.
  73. Trovato M., Mauro M.L., Costantino P., Altamura, M.M. The rolD gene from Agrobacterium rhizogenes is developmentary regulated in transgenictobacco // Protoplasma. 1997. V. 197. P. 111–120. doi: 10.1007/BF01279889
  74. Trovato M., Maras B., Linhares F., Constantino P. The plant oncogene rolD encodes a functional ornithine cyclodeaminase // Proc. Natl. Acad. Sci. U.S.A 2001. V. 98. P. 13449–13453. doi: 10.1073/pnas.231320398
  75. Veremeichik G.N, Shkryl Y.N, Bulgakov V.P, Avramenko T.V, Zhuravlev Y.N. 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. 2012. V. 6. P. 1009–1019. doi: 10.1007/s00299-011-1219-3.
  76. White F.F., Taylor B.H., Huffman G.A., Gordon M.P., Nester E.W. Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes // J. Bacteriol. 1985. V. 164. P. 33–44.
  77. Yanagisawa S. Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants // Plant Cell Physiol. 2004. V. 45. P. 386–391.
  78. Yasybaeva G.R., Vershinina Z.R., Kuluev B.R., Mikhaylova E.V., Baymiev A.H., Chemeris A.V. Biolistic-mediated plasmid-free transformation for induction of hairy roots in tobacco plants // Plant Root. 2017. V. 11. P. 33–39. doi: 10.3117/plantroot.11.33
  79. Zuker A., Tzfira T., Scovel G., Ovadis M., Shklarman E., Itzhaki H. RolC-transgenic carnation with improved agronomic traits: Quantitative and qualitative analyses of greenhouse-grown plants // J. Am. Soc. Hortic. Sci. 2001. V. 126. P. 13–18.
Download pdf
up
eISSN: 2221-6197 DOI: 10.31301/2221-6197