Beyond Mendel and Morgan to the dynamic genome
https://doi.org/10.30901/2658-3860-2024-3-o1
Abstract
The conceptional shifts on genome organization and hereditary variability occurred during transition from classical mendelian to current mobile or dynamic genetics. The main changed premises of this transition are firstly presented in detail. Mendelian genetics mainly conceived genome as the set of chromosomes with of all genes. Now genome semantics is changed. It comprises entire hereditary constitution of the cell, including both structural and dynamic aspects of coding, storage and transfer of species-specific information. There are three kinds of heritable changes: mutations, variations and epigenetic alterations. It is reasonable to discriminate in the genome two subsystems: Obligate genetic elements (OGE) and Facultative genetic elements (FGE). FGEs comprise various kinds of repeated DNA, mobile elements, amplicons, inserted viral and foreign DNA, B-chromosomes and cytobionts. FGEs are predominant genome content of many plants. The number and cell topography of FGEs are different in different cells/tissues and most eukaryote individuals. Changes in the structure or order of OGEs correspond to classical mutations. Various changes in FGEs it is reasonable to call variations. Facultative elements and their variations are the first genomic reaction on biotic and environmental challenges. Together with epigenetic alterations they implement the operational genomic memory. Three template genome processes Replication, Transcription, Translation and three basic genetic processes – Repair, Recombination and Segregation are capable to facultative expression according to principle: the unity of the whole and freedom of the parts. This is the essence of the presented generalized concept of the genome organization and hereditary variations.
About the Author
M. D. GolubovskyRussian Federation
Mikhail D. Golubovsky, Dr. Sci (Biol.), St. Petersburg branch of the S. I. Vavilov Institute of History of Science and Technology of the Russian Academy of Sciences, S.I. Vavilov Institute for the History of Science and Technology of the Russian Academy of Sciences
5, Universitetskaya embankment, St. Petersburg, 199034 Russia
References
1. Arteaga-Vazquez M.A., Chandler V.L. Paramutation in maize: trans-generation gene silencing. Current Opinion in Genetics and Development. 2010;20(2):156-163. DOI: 10.1016/j.gde.2010.01.008
2. Berg R.L., Engels W.R., Kreber R.A. Site-specific X-chromosome rearrangements from hybrid dysgenesis in Drosophila melanogaster. Science. 1980;210(4468):427-429. DOI: 10.1126/science.6776625
3. Beurton P.J., Falk R., Rheinberger H.-J. (eds.). The Concept of the Gene in Development and Evolution. Cambridge: Cambridge University Press; 2000. DOI: 10.1017/CBO9780511527296
4. Blattner F.R.; Plunkett G., Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D. The complete genome sequence of Escherichia coli K-12. Science. 1997;277(5331):1453-1462. DOI: 10.1126/science.277.5331.1453
5. Brockhurst M.A, Harrison E., Hall J.P.J., Richards T., McNally A., MacLean C. The ecology and evolution of pangenomes. Current Biology. 2019;29(20):1094-1103. DOI: 10.1016/j.cub.2019.08.012
6. Chandler V.L. Paramutation: from maize to mice. Cell. 2007;128(4):641-645. DOI: 10.1016/j.cell.2007.02.007
7. Chandler V.L. Paramutation's properties and puzzles. Science. 2010;330(6004):628-629. DOI: 10.1126/science.1191044
8. Crick F. Split genes and RNA splicing. Science. 1979;204(4390):264-271. DOI: 10.1126/science.373120
9. Cullis C.A. Mechanisms and control of rapid genome changes in flax. Annals of botany. 2005;95(1):201-206. DOI: 10.1093/aob/mci013
10. Fedoroff N., Botstein D. (eds.). The Dynamic Genome: Barbara McClintock’s ideas in the century of genetics. New York: Cold Spring Harbor Laboratory Press; 1992.
11. Filipchenko Yu. A. The evolutionary idea in biology (Evolyutsionnaya ideya v biologii). 3nd ed. Moscow: Nauka; 1977. [in Russian]
12. Ghanim G.E., Rio D.C., Teixeira F.K. Mechanism and regulation of P element transposition. Open biology. 2020;10(12):200-244. DOI: 10.1098/rsob.200244
13. Gilbert W. Why genes in pieces? Nature. 1978;271:501-504. DOI: 10.1038/271501a0
14. Golubovsky M.D. Genome Inconstancy by Roman B. Khesin in terms of conceptual history of genetics. Molecular Biology. 2002;36(2):259-266. DOI: 10.1023/A:1015382209018
15. Golubovsky M.D. Genotype organization and forms of hereditary variations in eukaryotes. Advances in Current Biology. 1985;100(6):323-339. [in Russian]
16. Golubovsky M.D. The Century of Genetics: Evolution of ideas and concepts (Vek genetiki: evolyutsiya idey i ponyatiy). St. Petersburg; 2000. [in Russian]
17. Golubovsky M.D. The unity of the whole and freedom of parts: Facultativeness principle in the hereditary system. Russian Journal of Genetics: Applied Research. 2011;1(6):587-594. DOI: 10.1134/S2079059711060050
18. Golubovsky M.D., Churaev R.N. Dynamic heredity and epigenes. Priroda. 1997;4:16-25. [in Russian]
19. Golubovsky M.D., Ivanov Yu., Green M.M. Genetic instability in Drosophila melanogaster: Putative multiple insertional mutants of the singed bristle locus. Proceedings of the National Academy of Sciences of the United States of America. 1977;74(7):2973-2975. DOI: 10.1073/pnas.74.7.297
20. Golubovsky M.D., Manton K.G. Genome organization and three kinds of heritable changes: general description and stochastic factors (a review). Frontiers in Bioscience. 2005;10(1):335-344. DOI: 10.2741/1531
21. Green M.M. Annals of mobile DNA elements in Drosophila. In: The Dynamic Genome. Barbara McClintock’s ideas in the century of genetics. N. Fedoroff, D. Botstein (eds.). New York: Cold Spring Harbor Laboratory Press; 1992. p.117-122.
22. Green M.M. Controlling element mediated transposition of the white gene in Drosophila melanogaster. Genetics. 1969;61(2):429-441. DOI: 10.1093/genetics/61.2.429
23. Holliday R. The inheritance of epigenetic defects. Science. 1987;238(4824):163-170. DOI: 10.1126/science.3310230
24. Inge-Vechtomov S.G. Genetics in Retrospect. A Course of lectures. St. Petersburg: Publishing house N.-L.; 2015. [in Russian]
25. Ito H. Environmental stress and transpositions in plants. Genes & Genetic Systems. 2022;97(4):169-175. DOI: 10.1266/ggs.22-00045
26. Jablonka E., Lamb M. The epigenome in evolution: Beyond the modern synthesis. Vavilov Journal of Genetics and Breeding. 2008;12(1/2):242-254.
27. Jacob F., Monod J. Genetic regulatory mechanisms in the synthesis of proteins. Journal of Molecular Biology. 1961;3:318-356. DOI: 10.1016/s0022-2836(61)80072-7
28. Jacob F., Wollman E.L. Sexuality and genetics of bacteria. New York; London: Academic Press; 1961.
29. Johannsen W. The genotype conception of heredity. The American Naturalist. 1911;45(531):129-159. DOI: 10.1086/279202
30. Khesin R.B. Genome Inconstancy. Moscow: Nauka; 1984. [in Russian]
31. Kim E., Magen A., Ast G. Different levels of alternative splicing among eukaryotes. Nucleic Acids Research. 2007;35(1):125-131. DOI: 10.1093/nar/gkl924
32. King R.C., Stansfield W.D., Mulligan P.K. A dictionary of genetics. 7nd ed. Oxford University Press; 2006.
33. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., Devon K. et al. International Human Genome Sequencing Consortium: Initial sequencing and analysis of the human genome. Nature. 2001;409(6822):860-921. DOI: 10.1038/35057062. Erratum in: Nature. 2001;412(6846):565. Erratum in: Nature. 2001;411(6838):720.
34. Lisch D. Regulaton of transposable elements in maize. Current Opinion in Plant Biology. 2012;15(5):511-516. DOI: 10.1016/j.pbi.2012.07.001
35. Liu B., Wendel J.F. Non-Mendelian Phenomena in Allopolyploid Genome Evolution. Current Genomics. 2002;3(6):489-505. DOI: 10.2174/1389202023350255
36. McClintock B. Chromosome organization and genic expression. Cold Spring Harbor Symposia on Quantitative Biology. 1951;16:13-47. DOI: 10.1101/sqb.1951.016.01.004
37. McClintock B. Mechanisms that rapidly reorganize genome. Stadler Symposium. 1978;10:25-48.
38. McClintock. The significance of responses of the genome to challenge. Science. 1984;226(4676):792-801. DOI: 10.1126/science.15739260
39. Monod J.; Jacob F. General conclusion: Teleonomic mechanisms in cellular metabolism, growth and differentiation. Cold Spring Harbor Symposium Quantitative Biology. 1961;26:389-401. DOI: 10.1101/sqb.1961.026.01.048
40. Muyle A., Marais G., Bačovský V., Hobza R., Lenormand Th. Dosage compensation evolution in plants: theories, controversies and mechanisms. Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 2022;377(1850):20210222. DOI: 10.1098/rstb.2021.0222
41. Nanney D.J. Epigenetic control systems. Proceedings of the National Academy of Sciences of the United States of America. 1958;44(7):712-717. DOI: 10.1073/pnas.44.7.712
42. Olovnikov A.M. A theory of marginotomy. The incomplete copying of template margin in enzymatic synthesis of polynucleotides and biologicаl significance of the phenomenon. Journal of theoretical biology. 1973;41(1):181-190. DOI: 10.1016/0022-5193(73)90198-7
43. Polanyi M. Personal knowledge. Chicago: The University of Chicago Press; 1962.
44. Rodionov A.V. Tandem duplications, euploidy and secondarary diploidization-genetic mechanisms of plant speciation and progressive evolution. Turczaninowia. 2022;25(4):87-121. [in Russian]. DOI: 10.14258/turczaninowia.25.4.12
45. Saedler H., Starlinger P. Twenty-five years of transposable elements research in Koln. In: The Dynamic Genome. Barbara McClintock’s ideas in the century of genetics. N. Fedoroff, D. Botstein (eds.). New York: Cold Spring Harbor Laboratory Press; 1992. p.243-263.
46. Schimke R.T. The discovery of gene amplification in mammalian cells: To be in the right place at the right term. Bioessays. 1989;11(2-3):69-73. DOI: 10.1002/bies.950110208
47. Shapiro J. Genome organization and reorganization in evolution: formatting for computation and function. Annal New York Academy of Science. 2002;981:11-134. DOI: 10.1111/j.1749-6632.2002.tb04915.x
48. Shapiro J.A. Natural genetic engineering in evolution. Genetica. 1992;86(1-3):99-111. DOI: 10.1007/BF00133714
49. Stillman B. (ed.). Epigenetics: Cold Spring Harbor Symposia on Quantitative Biology. Vol. LXIX. 1nd ed. Cold Spring Harbor Laboratory Press; 2005.
50. Tchuraev R.N., Galimzyamov A.V. Gene and epigene network: two level of organizing of hereditary system. Journal Theoretical Biology. 2009;259(4):659-669. DOI: 10.1016/j.jtbi.2009.03.034
51. Tchuraev R.N., Stupak I.V., Tropinina, T.S., Stupak E.E. Epigene: design and construction of new hereditary units. FEBS Letters. 2000;486(3):200-202. DOI: 10.1016/s0014-5793(00)02300-0
52. Tikhodeyev O. The mechanisms of epigenetic inheritance: how diverse are they? Biological Review of the Cambridge Philosophical Society. 2018;93(4):1987-2005. DOI: 10.1111/brv.12429
53. Todd P.M. Plant genome size variation: bloating and purging DNA. Briefings in Functional Genomics. 2014;13(4):308-317. DOI: 10.1093/bfgp/elu005
54. Tyedmers J.; Madariaga M.L., Lindquist S. Prion switching in response to environmental stress. PLOS Biology. 2008;6(11):2605-2613. DOI: 10.1371/journal.pbio.0060294
55. Wendel J.F., Jackson S.A., Meyer B.C, Wing R.A. Evolution of Plant Genome Architecture. Genome Biology. 2016;17:37. DOI: 10.1186/s13059-016-0908-1
Review
For citations:
Golubovsky M.D. Beyond Mendel and Morgan to the dynamic genome. Vavilovia. 2024;7(3):37-54. https://doi.org/10.30901/2658-3860-2024-3-o1