The diversity of genes for the synthesis of opines and their products in representatives of various taxa

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Opines are low molecular weight organic substances that occur in marine invertebrates, bacteria, some plants and fungi. Such an unusual range of organisms suggests the importance of studying and systematizing knowledge about the functions of these compounds and the genetic control of their metabolism. In recent years, new data have emerged on plants containing genes for the synthesis of opines as a result of horizontal gene transfer from agrobacteria. This review is devoted to systematization of information about opine synthase genes, their products and functions of the latter.

Full Text

Restricted Access

About the authors

Anton D. Shaposhnikov

Saint Petersburg State University

Author for correspondence.
Email: st096319@student.spbu.ru

student

Russian Federation, Saint Petersburg

Tatiana V. Matveeva

Saint Petersburg State University

Email: radishlet@gmail.com
ORCID iD: 0000-0001-8569-6665
SPIN-code: 3877-6598
Scopus Author ID: 7006494611

Dr. Sci. (Biol.), professor

Russian Federation, Saint Petersburg

References

  1. Dessaux Y, Petit A, Tempe J. Chemistry and biochemistry of opines, chemical mediators of parasitism. Phytochemistry. 1993;34(1):31–38. doi: 10.1016/S0031-9422(00)90778-7
  2. Vladimirov IA, Matveeva TV, Lutova LA. Opine biosynthesis and catabolism genes of Agrobacterium tumefaciens and Agrobacterium rhizogenes. Russian Journal of Genetics. 2015;51(2):137–146. (In Russ.) doi: 10.7868/S0016675815020162
  3. Matveeva T, Otten L. Opine biosynthesis in naturally transgenic plants: Genes and products. Phytochemistry. 2021;189:112813. doi: 10.1016/j.phytochem.2021.112813
  4. Hockachka PW, Hartline PH, Fields JHA. Octopine as an end product of anaerobic glycolysis in the chambered nautilus. Science. 1977;195(4273):72–74. doi: 10.1126/science.831256
  5. Harcet M, Perina D, Pleše B. Opine dehydrogenases in marine invertebrates. Biochem Genet. 2013;51(9–10):666–676. doi: 10.1007/s10528-013-9596-7
  6. Flores-Mireles AL, Eberhard A, Winans SC. Agrobacterium tumefaciens can obtain sulphur from an opine that is synthesized by octopine synthase using S-methylmethionine as a substrate: A sulphur-containing opine. Mol Microbiol. 2012;84(5):845–856. doi: 10.1111/j.1365-2958.2012.08061.x
  7. Hack E, Kemp JD. Purification and characterization of the crown gall-specific enzyme, octopine synthase. Plant Physiol. 1980;65(5):949–955.doi: 10.1104/pp.65.5.949
  8. Hall LM, Schrimsher JL, Taylor KB. A new opine derived from nopaline. J Biol Chem. 1983;258(12):7276–7279. doi: 10.1016/S0021-9258(18)32172-0
  9. Goldmann A. Octopine and nopaline dehydrogenases in crown-gall tumors. Plant Sci Lett. 1977;10(1):49–58. doi: 10.1016/0304-4211(77)90049-9
  10. Davioud E, Petit A, Tate ME, et al. Cucumopine — a new T-DNA-encoded opine in hairy root and crown gall. Phytochemistry. 1988;27(8):2429–2433. doi: 10.1016/0031-9422(88)87007-9
  11. Isogai A, Fukuchi N, Hayashi M, et al. Structure of a new opine, mikimopine, in hairy root induced by Agrobacterium rhizogenes. Agric Biol Chem. 1988;52(12):3235–3237. doi: 10.1080/00021369.1988.10869222
  12. Isogai A, Fukuchi N, Hayashi M, et al. Mikimopine, an opine in hairy roots of tobacco induced by Agrobacterium rhizogenes. Phytochemistry. 1990;29(10):3131–3134. doi: 10.1016/0031-9422(90)80171-C
  13. Suzuki K, Tanaka N, Kamada H, Yamashita I. Mikimopine synthase (mis) gene on pRi1724. Gene. 2001;263(1–2):49–58. doi: 10.1016/S0378-1119(00)00578-3
  14. Chang C-C, Chen C-M. Evidence for the presence of N2-(1,3-dicarboxypropyl)-L-amino acids in crown-gall tumors induced by Agrobacterium tumefaciens strains 181 and EU6. FEBS Letters. 1983;162(2):432–435. doi: 10.1016/0014-5793(83)80802-3
  15. Chilton WS, Tempé J, Matzke M, Chilton MD. Succinamopine: a new crown gall opine. J Bacteriol. 1984;157(2):357–362. doi: 10.1128/JB.157.2.357-362.1984
  16. Chilton WS, Rinehart KL, Chilton MD. Structure and stereochemistry of succinamopine. Biochemistry. 1984;23(14):3290–3297. doi: 10.1021/bi00309a027
  17. Blundy KS, White J, Firmin JL, Hepburn AG. Characterisation of the T-region of the SAP-type Ti-plasmid pTiAT181: identification of a gene involved in SAP synthesis. Mol Gen Genet. 1986;202(1):62–67. doi: 10.1007/BF00330518
  18. Chilton WS, Hood E, Rinehart KL Jr, Chilton M-D. L,L-Succinamopine: an epimeric crown gall opine. Phytochemistry. 1985;24(12):2945–2948. doi: 10.1016/0031-9422(85)80032-7
  19. Chang C-c, Chen C-m, Adams BR, Trost BM. Leucinopine, a characteristic compound of some crown-gall tumors. PNAS USA. 1983;80(12):3573–3576. doi: 10.1073/pnas.80.12.3573
  20. Chilton WS, Hood E, Chilton M-D. Absolute stereochemistry of leucinopine, a crown gall opine. Phytochemistry. 1985;24(2):221–224. doi: 10.1016/S0031-9422(00)83523-2
  21. Tate ME, Ellis JG, Kerr A, et al. Agropine: A revised structure. Carbohydr Res. 1982;104(1):105–120. doi: 10.1016/S0008-6215(00)82224-7
  22. Ellis JG, Ryder MH, Tate ME. Agrobacterium tumefaciens TR-DNA encodes a pathway for agropine biosynthesis. Mol Gen Genet. 1984;195(3):466–473. doi: 10.1007/BF00341448
  23. Dessaux Y, Guyon P, Farrand SK, et al. Agrobacterium Ti and Ri plasmids specify enzymic lactonization of mannopine to agropine. Microbiology. 1986;132(9):2549–2559. doi: 10.1099/00221287-132-9-2549
  24. Dransart V-V, Petit A, Poncet C, et al. Novel Ti plasmids in Agrobacterium strains isolated from fig tree and chrysanthemum tumors and their opinelike molecules. Mol Plant Microbe Interact. 1995;8(2):311–321. doi: 10.1094/mpmi-8-0311
  25. Shao S, Zhang X, van Heusden GPH, et al. Complete sequence of the tumor-inducing plasmid pTiChry5 from the hypervirulent Agrobacterium tumefaciens strain Chry5. Plasmid. 2018;96–97:1–6. doi: 10.1016/j.plasmid.2018.02.001
  26. Ellis JG, Murphy PJ. Four new opines from crown gall tumours — their detection and properties. Mol Gen Genet. 1981;181(1):36–43. doi: 10.1007/BF00339002
  27. Petit A, David C, Dahl GA, et al. Further extension of the opine concept: Plasmids in Agrobacterium rhizogenes cooperate for opine degradation. Mol Gen Genet. 1983;190(2):204–214. doi: 10.1007/BF00330641
  28. Ryder MH, Tate ME, Jones GP. Agrocinopine A, a tumor-inducing plasmid-coded enzyme product, is a phosphodiester of sucrose and L-arabinose. J Biol Chem. 1984;259(15):9704–9710. doi: 10.1016/S0021-9258(17)42757-8
  29. Dessaux Y, Petit A, Farrand SK, Murphy PJ. Opines and opine-like molecules involved in plant-rhizobiaceae interactions. In: Spaink HP, Kondorosi A, Hooykaas PJJ, editors. The Rhizobiaceae. Dordrecht: Springer Netherlands, 1998. P. 173–197. doi: 10.1007/978-94-011-5060-6_9
  30. www.pubchem.ncbi.nlm.nih.gov [Internet]. Explore chemistry [cited: 2023 Jun 10]. Available at: https://pubchem.ncbi.nlm.nih.gov
  31. Matveeva TV, Otten L. Widespread occurrence of natural genetic transformation of plants by Agrobacterium. Plant Mol Biol. 2019;101(4–5):415–437. doi: 10.1007/s11103-019-00913-y
  32. Sokornova S, Matveeva T. Relationships of ascomycetes opine synthases. Selected abstracts of bioinformatics: from algorithms to applications 2021 conference. BMC Bioinformatics. 2021;22(S16):591 doi: 10.1186/s12859-021-04475-z
  33. Banta LM, Montenegro M. Agrobacterium and plant biotechnology. In: Tzfira T, Citovsky V, editors. Agrobacterium: from biology to biotechnology. New York: Springer New York, 2008. P. 73–147. doi: 10.1007/978-0-387-72290-0_3
  34. White FF, Ghidossi G, Gordon MP, Nester EW. Tumor induction by Agrobacterium rhizogenes involves the transfer of plasmid DNA to the plant genome. PNAS USA. 1982;79(10):3193–3197. doi: 10.1073/pnas.79.10.3193
  35. White FF, Garfinkel DJ, Huffman GA, et al. Sequences homologous to Agrobacterium rhizogenes T-DNA in the genomes of uninfected plants. Nature. 1983;301(5898):348–350. doi: 10.1038/301348a0
  36. Furner IJ, Huffman GA, Amasino RM, et al. An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature. 1986;319(6052):422–427. doi: 10.1038/319422a0
  37. Suzuki K, Yamashita I, Tanaka N. Tobacco plants were transformed by Agrobacterium rhizogenes infection during their evolution: Origin of cT-DNA in tobacco plants. Plant J. 2002;32(5):775–787. doi: 10.1046/j.1365-313X.2002.01468.x
  38. Pavlova OA, Matveeva TV, Lutova LA. Genome of Linaria dalmatica Contains Agrobacterium rhizogenes RolC gene homolog. Russ J Genet Appl Res. 2014;4(5):461–465. doi: 10.1134/S2079059714050116
  39. Matveeva TV, Bogomaz DI, Pavlova OA, et al. Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. MPMI. 2012;25(12):1542–1551. doi: 10.1094/MPMI-07-12-0169-R
  40. Kovacova V, Zluvova J, Janousek B, et al. The evolutionary fate of the horizontally transferred agrobacterial mikimopine synthase gene in the genera Nicotiana and Linaria. PLoS ONE. 2014;9(11):e113872. doi: 10.1371/journal.pone.0113872
  41. Matveeva TV, Lutova LA. Horizontal gene transfer from Agrobacterium to plants. Front Plant Sci. 2014;5:326. doi: 10.3389/fpls.2014.00326
  42. Chen K, de Borne FD, 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. Plant J. 2014;80(4):669–682. doi: 10.1111/tpj.12661
  43. Chen K, de Borne FD, Sierro N, et al. Organization of the TC and TE cellular T-DNA regions in Nicotiana otophora and functional analysis of three diverged TE-6b genes. Plant J. 2018;94(2):274–287. doi: 10.1111/tpj.13853
  44. Kyndt T, Quispe D, Zhai H, et al. The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: An example of a naturally transgenic food crop. PNAS USA. 2015;112(18):5844–5849. doi: 10.1073/pnas.1419685112
  45. Quispe-Huamanquispe DG, Gheysen G, Yang J, et al. The horizontal gene transfer of Agrobacterium T-DNAs into the series Batatas (Genus Ipomoea) genome is not confined to hexaploid sweetpotato. Sci Rep. 2019;9(1):12584. doi: 10.1038/s41598-019-48691-3
  46. Matveeva T. New naturally transgenic plants: 2020 update BioComm. 2021;66(1):36–46. doi: 10.21638/spbu03.2021.105
  47. Matveeva T.М. Natural GMOs: a history of research. Ecological genetics. 2022;20(1S):7–8. doi: 10.17816/ecogen112371
  48. Bogomaz FD, Matveeva TV. Expression sequences of opine synthase genes in natural GMOs based on analysis of their transcriptomes. Plant Biotechnology and Breeding. 2022;5(3):15–24. (In Russ.) doi: 10.30901/2658-6266-2022-3-o2
  49. Matveeva TV. Agrobacterium-mediated transformation in the evolution of plants. In: Gelvin SB, editor. Agrobacterium Biology. Vol. 418. Cham: Springer International Publishing, 2018. P. 421–441. doi: 10.1007/82_2018_80
  50. Matveeva TV. Why do plants need agrobacterial genes? Ecological genetics. 2021;19(4):365–375. (In Russ.) doi: 10.17816/ecogen89905
  51. Mansouri H, Petit A, Oger P, Dessaux Y. Engineered rhizosphere: the trophic bias generated by opine-producing plants is independent of the opine type, the soil origin, and the plant species. Appl Environ Microbiol. 2002;68(5):2562–2566. doi: 10.1128/aem.68.5.2562-2566.2002
  52. Geddes BA, Paramasivan P, Joffrin A, et al. Engineering transkingdom signalling in plants to control gene expression in rhizosphere bacteria. Nat Commun. 2019;10(1):3430. doi: 10.1038/s41467-019-10882-x
  53. Chen K, de Borne FD, Julio E, et al. Root-specific expression of opine genes and opine accumulation in some cultivars of the naturally occurring genetically modified organism Nicotiana tabacum. Plant J. 2016;87(3):258–269. doi: 10.1111/tpj.13196
  54. Zhang Y, Wang D, Wang Y, et al. Parasitic plant dodder (Cuscuta spp.): A new natural Agrobacterium-to-plant horizontal gene transfer species. Sci China Life Sci. 2020;63(2):312–316. doi: 10.1007/s11427-019-1588-x
  55. Otten LABM, Vreugdenhil D, Schilperoort RA. Properties of D(+)-lysopine dehydrogenase from crown gall tumour tissue. Biochimica et Biophysica Acta (BBA) — Enzymology. 1977;485(2):268–277. doi: 10.1016/0005-2744(77)90163-2
  56. Hack E, Kemp JD. Comparison of octopine, histopine, lysopine, and octopinic acid synthesizing activities in sunflower crown gall tissues. Biochem Biophys Res Commun. 1977;78(2):785–791. doi: 10.1016/0006-291x(77)90248-0
  57. Biemann K, Lioret C, Asselineau J, et al. On the structure of lysopine, a new amino acid isolated from crown gall tissue. Biochimica et Biophysica Acta. 1960;40:369–370. doi: 10.1016/0006-3002(60)91370-6
  58. Kemp JD. A new amino acid derivative present in crown gall tumor tissue. Biochem Biophys Res Commun. 1977;74(3):862–868. doi: 10.1016/0006-291x(77)91598-4
  59. Bates HA, Kaushal A, Deng PN, et al. Structure and synthesis of histopine, a histidine derivative produced by crown gall tumors. Biochemistry. 1984;23(14):3287–3290. doi: 10.1021/bi00309a026
  60. Szegedi E, Czakó M, Otten L, Koncz CS. Opines in crown gall tumours induced by biotype 3 isolates of Agrobacterium tumefaciens. Physiol Mol Plant Pathol. 1988;32(2):237–247. doi: 10.1016/S0885-5765(88)80020-1
  61. Chilton WS, Petit A, Chilton M-D, Dessaux Y. Structure and characterization of the crown gall opines heliopine, vitopine and ridéopine. Phytochemistry. 2001;58(1):137–142. doi: 10.1016/S0031-9422(01)00166-2

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Chemical reactions of the formation of opines [30, 31]

Download (109KB)
Indexing metadata
3. Fig. 2. Phylogenetic tree of angiosperms (APG IV) [31, 46], where the arrows indicate the orders in which nGMO were found. *Musa acuminata Colla and **Dioscorea alata L. are representatives of the class of monocotyledonous plants

Download (127KB)
Indexing metadata
4. Fig. 3. The number of nGMO genera with different cT-DNA structures [31, 46, 48]

Download (88KB)
Indexing metadata
5. Fig. 4. Distribution of three structural types of cT-DNA according to the orders of dicotyledonous plants [31, 46, 48]

Download (142KB)
Indexing metadata
6. Fig. 5. Structural formulas of opines [30]

Download (103KB)
Indexing metadata

Copyright (c) 2023 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 65617 от 04.05.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies