Izvestiya of Saratov University.

Chemistry. Biology. Ecology

ISSN 1816-9775 (Print)
ISSN 2541-8971 (Online)


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Yudakova O. I., Kaybeleva E. I. Evolutionary role of apomixis: S. S. Khokhlov’s hypothesis in the light of modern data. Izvestiya of Saratov University. Chemistry. Biology. Ecology, 2022, vol. 22, iss. 1, pp. 89-98. DOI: 10.18500/1816-9775-2022-22-1-89-98

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Evolutionary role of apomixis: S. S. Khokhlov’s hypothesis in the light of modern data

Autors: 
Yudakova Olga Ivanovna, Saratov State University
Kaybeleva Elmira I., Saratov State University
Abstract: 

In 1949 S. S. Khokhlov (one of the founders of the Russian scientifi c school on the problem of apomixes) proved the original conception of the progressive evolutionary role of apomixis. He contended that the basic direction of the reproductive system evolution in angiosperms is a gradual failure of sex reproduction and transition to apomixis. This hypothesis was heavily criticized and called a “scientist’s fantasy”. In the second half of the 20th century the discovery of recombination repair led to a reassessment of the role of meiosis in the evolution. Now meiosis is considered as the guarantor of genomic stability, and not only as a source of combinative variability. Various molecular-genetic mechanisms of genome transformation unrelated to the sexual process were described. There are gene duplications, horizontal gene transfers and mobile gene systems. All this creates grounds to assume that not only amphymixis but apomixis can solve the dilemma: (1) saving the genotypic structure of the species, (2) providing the genetic diversity of the progeny. Parthenogesis allows the copying of genotypes and the saving of the genotypic structure of the species. The dropping out of meiosis from the development cycle of apomicts, on the one hand, increases its mutability because there is no recombination repair, and, in the other hand, promotes polyploidyzation and consequently contributes to the evolution by gene duplication. The accumulated data about distribution and embryology features of apomicts indicate its signifi cant evolutionary potential. In the light of the modern data S. S. Khokhlov’s hypothesis of the beginning of “apomixis era” appears to be not so fantastic as before.

Reference: 
  1. Petrov D. F. Genetisheskie osnovy apomixisa [Genetic basis of apomixis]. Novosibirsk, Nauka, Sib. otd-nie Publ., 1979. 276 p. (in Russian).
  2. Petrov D. F. Apomixis v prirode i opyte [Apomixis in the nature and an experience]. Novosibirsk, Nauka, Sib. otd-nie Publ., 1988. 213 p. (in Russian).
  3. Nogler G. A. Gametophytic apomixis. In: Embryology of Angiosperms. Berlin, Springel-Verlag, 1984, pp. 476–518.
  4. Asker S. E., Jerling L. Apomixis in Plants. Boca Raton, USA, CRC Perss, 1992. 298 p.
  5. Koltunow A., Grossniklaus U., Lookeren C. M. van. A bright future for apomixis. Trends in Plant Science, 1998, vol. 3, no. 11, pp. 415–416. https://doi.org/10.1016/S1360-1385(98)01338
  6. Savidan Y. H. Apomixis in higher plants. In: Hörandl E., Grossniklaus U., Van Dijk P. J., Sharbel T., eds. Apomixis: Evolution, Mechanisms and Perspectives. Gantner, Ruggell; Liechtenstein, 2007, pp. 15–22.
  7. Tyrnov V. S. Applied aspects of gametophytic apomixis. In: Embryology of Flowering Plants: Terminology and Concepts. Reproductive Systems. USA, Science Publishers, 2009, pp. 144–147.
  8. Khokhlov S. S. Agamospermous plants. Historical background and evolutionary prospects. Uchenye zapiski Saratovskogo universiteta, 1946, no. 1, pp. 3–75 (in Russian).
  9. Khokhlov S. S. Prospects of the higher plant evolution. Uchenye zapiski Saratovskogo pedagogicheskogo instituta, 1949, no. 9, pp. 40–43 (in Russian).
  10. Khokhlov S. S. Apomixis: classifi cation and distribution in the angiosperms. In: Uspehi sovremennoi genetiki [Advances in modern genetics]. Moscow, Nauka Publ., 1967, pp. 43–105 (in Russian).
  11. Khokhlov S. S. Evolutionary-genetic problems of apomixis in the angiosperms. In: Apomixis i selekstiya [Apomixis and selection]. Moscow, Nauka Publ., 1970, pp. 7–21 (in Russian).
  12. Darlington C. D. Recent Advances in Cytology. London, Churchill, 1937. 671 p.
  13. Komarov V. L. Uchenie o vide u rastenii: stranitsa is istorii biologii [The doctrine of species in plants: the page of the biology history]. Moscow, Izd-vo AN SSSR Press, 1940. 212 p. (in Russian).
  14. Stebbins G. Z. Apomixis in the Angiosperms. Bot. Rev., 1941, vol. 7, pp. 507–552.
  15. Gustafsson A. Apomixis in higher plants. Parts I–III. Lunds Univ. Arsskr. N.F. 1946–1947, vol. 42, no. 3, pp. 1–67; vol. 43, no. 2, pp. 69–179; vol. 43, no. 12, pp. 181–370.
  16. Kozo-Polyanskii B. M. On the question of the phylogenetic signifi cance of apomixis. Botanicheskii Zhurnal, 1948, vol. 33, no. 1, pp. 123–127 (in Russian).
  17. Baranov P. A. The debate on the S. S. Khokhlov’s report. In: Problems of phylogeny and phylogenesis: Newsitems of the V conf. of plant physiology. Leningrad, 1960, pp. 27 (in Russian).
  18. Muller H. J. The relation between recombination to mutational advance. Mutational Research. 1964, vol. 106, no. 1, pp. 2–9. https://doi.org/10.1016/0027-5107(64)90047-8
  19. Khokhlov S. S., Zaitseva M. I., Kupriyanov P. G. Vyyavlenie apomiktichnyh form vo fl ore tsvetkovyh rastenii SSSR [Identification of apomictic forms in the fl owering plants fl ora of the USSR]. Saratov, Izd-vo Sarat. un-ta, 1978. 224 p. (in Russian).
  20. Shishkinskaya N. A., Yudakova O. I., Tyrnov V. S. Po pulyastionnaya embriologiya i apomixis u zlakov [Population embryology and apomixis in the grasses]. Saratov, Izd-vo Sarat. un-ta, 2004. 145 p. (in Russian).
  21. Yudakova O. I., Shishkinskaya N. A. Embiologicheskie osobennosti apomiktichnyh zlakov [Embryological features of apomictic grasses]. Saratov, Izd-vo Sarat. un-ta, 2008. 105 p. (in Russian).
  22. Kashin A. S., Yudakova O. I., Kohanova I. S., Polyanskaya M. V., Mindubaeva A. H. The distribution of gametophytic apomixis in Asteraceae и Poaceae (with species of Saratov region fl ora as an example). Botanicheskii Zhurnal, 2009, vol. 94, no. 5, pp. 120–132 (in Russian).
  23. Kashin A. S., Kochanova I. S., Lisitzkaya N. M., Berezutsky M. A. Gametophytic apomixis distribution in representatives of the Asteraceae family in the fl orae of the Lower-Volga region and Northwest Caucasus. Povolzhskiy Journal of Ecology, 2012, vol. 1, pp. 22–32 (in Russian).
  24. Yudakova O. I. Embryological features of seed reproductive system in the facultative apomictic grasses. Thesis Diss. Dr. Sci. (Biol.). Saratov, 2009. 240 p. (in Russian).
  25. Tsvelev N. N. Zlaki [Cereals]. Leningrad, Nauka, Leningr. otd-nye Publ., 1976. 788 p. (in Russian).
  26. Bayer R. J. Investigations into evolutionary history of Antennaria rosea (Asteraceae: Inuleae) polyploid complex. Plant Systematics and Evolution, 1990, vol. 69, pp. 97–110. https://doi.org/10.1007/BF00935988
  27. Soejima A., Yahara T., Watanabe K. Distribution and variation of sexual and agamospermous populations of Stevia (Asteraceae: Eupatorieae) in lower latitudes, Mexico. Plant Species Biology, 2001, vol. 16, pp. 91–105. https://doi.org/10.1046/j.1442-1984.2001.00055.x
  28. Urbani M. N. Cytogeography and reproduction of the Paspalum simplex polyploid complex. Plant Systematics and Evolution, 2002, vol. 236, no. 1, pp. 99–105. https://doi.org/10.1007/s00606-002-0237-6
  29. Van Dijk P. Ecological and evolutionary opportunities of apomixis: Insights from Taraxacum and Chondrilla. Philosophical transactions of the Royal society of London, 2003, vol. 358, pp. 1113–1121. https://doi.org/10.1098/rstb/2003/1302
  30. Cuellar O., Kluge A. G. Natural parthenogenesis in the gekkonid lizard Lepidodactylus lugubris. J. of Genet., 1972, vol. 6, pp. 14.
  31. Brown A. H. D., Marshall D. R. Evolutionary changes accompanying colonization in plants. In: Evolution Today. Proc. of 2nd Intern. cong. of systematic and evolutionary biol. Pittsburgh, 1981, pp. 351–363.
  32. Price S. C., Jain S. K. Are inbreeders better colonizers? Oecologia, 1981, vol. 49, pp. 283.
  33. Selander R. K. Evolutionary consequences of inbreeding. In: Genetics and Conservation. San-Francisco, USA, 1983, pp. 201–215.
  34. Husband B. C., Barrett S. C. H. Colonization history and population genetic structure of Eichhornia paniculata in Jamaica. Heredity, 1991, vol. 66, pp. 287–291. https://doi.org/10.1038/hdy.1991.36
  35. Doums C., Perdieu M.A., Jarne P. Resource allocation and stressful conditions in the aphallic snail. Bulinus truncates. Ecology, 1998, vol. 79, pp. 720–733. https://doi.org/10.1890/0012-9658(1998)079
  36. Viard F., Justy F., Jarne P. The infl uence of self-fertilization and population dynamics on the genetic structure of subdivided populations: A case study using microsatellite markers in the freshwater snail Bulinus truncates. Evolution, 1997, vol. 51, pp. 1322–1323. https://doi.org/10.1111/j.1558-5646.1997.tb01475.x
  37. Ostrowski M. F., Jarne P., David P. Quantitative genetics of sexual plasticity: the Environmental Threshold Model and genotype-by-environment interaction for phallus development in the snail Bulinus truncates. Evolution, 2000, vol. 4, pp. 1614–1625. https://doi.org/10.1111/j.0014-3820.2000.tb00706.x
  38. Carman J. G. Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory and polyembryony. Biol. J. Linn. Soc., 1997, vol. 61, no. 1, pp. 51–94. https://doi.org/10.1111/j.1095-8312.1997.tb01778.x 
  39. Hojsgaard D., Klatt S., Baier R., Carman J. G., Hörandl E. Taxonomy and biogeography of apomixis in angiosperms and associated biodiversity characteristics. Crit. Rev. Plant Sci., 2014, vol. 33, no. 5, pp. 414–427. https://doi.org/10.1080/07352689.2014.898488
  40. Hörandl E., Hojsgaard D. The evolution of apomixis in angiosperms: A reappraisal. Plant Biosystems, 2012, vol. 146, no. 3, pp. 681–693. https://doi.org/10.1080/11263504.2012.716795
  41. Albertini E., Barcaccia G., Mazzucato A., Sharbel T. F., Falcinelli M Apomixis in the era of biotechnology. Plant Developmental Biology – Biotechnological Perspectives, 2010, vol. 1, pp. 405–436. https://doi.org/10.1007/978-3-642-02301-9_20
  42. Sailer Сh., Schmid B., Stöcklin J., Grossniklaus U. Sexual Hieracium pilosella plants are better inter-specifi c, while apomictic plants are better intra-specifi c competitors. Perspectives in Plant Ecology Evolution and Systematics, 2014, vol. 16, no. 2, pp. 43–51.
  43. Ellstrand N. C., Roose M. L. Patterns of genotypic diversity in clonal plant species. Am. J. Bot., 1987, vol. 74, pp. 123–131. https://doi.org/10.2307/2444338
  44. Hamrick J. L., Godt M. J. W. Allozyme diversity in plant species. In: Plant Population Genetics, Breeding, and Genetic Resources. Sunderland, MA, Sinauer, 1990, pp. 43–63.
  45. Assienan B., Noirot M. Isozyme polymorphism and organization of the agamic complex of the Maximae (Panicum maximum Jacq., P. infestum Anders, and P. trichocladum K. Schum.) in Tanzania. Theor. Appl. Genet., 1995, vol. 91, pp. 672–680. https://doi.org/10.1007/BF00223296
  46. Schmelzer G. H., Renno J.-F. Genetic variation in the agamic species complex of Pennisetum section Brevivalvula (Poaceae) from West Africa: ploidy levels and isozyme polymorphism. Euphytica, 1997, vol. 96, pp. 23–29. https://doi.org/10.1023/A:1002974304592
  47. Akiyama T., Suzuki O., Matsuda J., Aoki F. Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genetics, 2011, vol. 7, pp. e1002279. https://doi.org/10.1371/journal.pgen.1002279.
  48. Van der Hulst R. G. M., Mes T. H., Falque M., Stam P., Den Nijs J. C., Bachmann K. Genetic structure of a population sample of apomictic dandelions. Heredity, 2003, vol. 90, pp. 326–335. https://doi.org/10.1038/sj.hdy.6800248
  49. Pellino M., Hojsgaard D., Schmutzer T., Scholz U., Hörandl E., Vogel H. Asexual genome evolution in the apomictic Ranunculus auricomus complex: Examining the effects of hybridization and mutation accumulation. Mol. Ecol., 2013, vol. 22, pp. 5908–5921. https://doi.org/10.1111/mec.12533
  50. Hojsgaard D., Hörandl E. A little bit of sex matters for genome evolution in asexual plants. Frontiers in Plant Science, 2015, vol. 6, pp. 1–6. https://doi.org/10.3389/fpls.2015/00082
  51. Tavva M. D., Rao Y. V., Bandaru V. R., Rao M. V. S. Apomixis in crop improvement. In: Plant Biology and Biotechnology: Vol. I: Plant Diversity, Organization, Function and Improvement. Andhra Pradesh, Springer India, 2015, pp. 39–47.
  52. Welch M. D., Meselson M. Evidence for the evolution of Bdelloid rotifers without sexual reproduction or genetic exchange. Science, 2000, vol. 288, no. 5469, pp. 1211– 1215. https://doi.org/10.1126/science.288.5469.1211
  53. Normark B. B. The evolution of alternative genetic systems in insects. Ann. Rev. Entomol., 2003, vol. 48, pp. 397–423. https://doi.org/10.1146/annurev.ento.48.091801.112703
  54. Popad’in K. Yu. The evolution of sex reproduction: The role of deleterious mutations and mobile elements. Zhurnal Obshchei Biologii, 2003, vol. 64, no. 6, pp. 463–478 (in Russian).
  55. Nazarov V. I. Evolutsiya ne po Darvinu: Smena evolutsionnoi modeli [Evolution is not by Darwin: Change of the evolutionary model]. Moscow, Izd-vo LKI, 2007. 520 p. (in Russian).
  56. Balloux F., Lehmann L., Meeûs T. de. The population genetics of clonal and partially clonal diploids. Genetics. 2003, vol. 164, pp. 1635–1644. https://doi.org/10.1093/genetics/164.4.1635
  57. Bengtsson B. O. Genetic variation in organisms with sexual and asexual reproduction. J. Evol. Biol., 2003, vol. 16, pp. 189–199.
  58. Loxdale H., Lushai D. G. Rapid Changes in clonal lines: the death of a “Sacred Cow”. Biol. J. Linn. Soc. London, 2003, no. 7, pp. 3–16. https://doi.org/10.1046/j.1095-8312.2003.00177.x
  59. Lushai G., Loxdale H. D., Allen J. A. The dynamic clonal genome and its adaptive potential. Biol. J. Linn.Soc. London, 2003, no. 79, pp. 193–208. https://doi. org/10.1046/j.1095-8312.2003.00189.x
  60. Adolfsson S., Bengtsson B. O. The spread of apomixis and its effect on resident genetic variation. J. Evol. Biol., 2007, vol. 20, no. 5, pp. 1933–1940. https://doi. org/10.1111/j.1420-9101.2007.0 1371.x
  61. Yadav C. B, Suresh Y. Q., Kumar M. G., Bhat G. V. Genetic linkage maps of the chromosomal regions associated with apomictic and sexual modes of reproduction in Cenchrus ciliaris. Mol. Breed., 2012, vol. 30, pp. 239–250. https://doi.org/10.1007/s11032-011-9614-6
  62. Leon-Martinez G., Vielle-Calzada J.-P. Apomixis in fl owering plants: Developmental and evolutionary considerations. Current Topics in Developmental Biology, 2019, vol. 131, pp. 565–604. https://doi.org/10.1016/bs.ctdb.2018.11.014
  63. Fiaz S., Wang X., Younas A., Alharthi B., Riaz A., Ali H. Apomixis and strategies to induce apomixis to preserve hybrid vigor for multiple generations. GM Crops and Food, 2021, vol. 12, no. 1, pp. 57–70. https://doi.org/10.1080/21645698.2020.1808423
  64. Hurst L. D., Peck J. R. Recent advances in understanding of the evolution and maintenance of sex. Trends Ecol. Evol., 1996, vol. 11, no. 2, pp. 46–52. https://doi.org/10.1016/0169-5347(96)81041-x
  65. Berthaud J. Apomixis and the Management of Genetic Diversity. In: The Flowering of Apomixis: From Mechanisms to Genetic Engineering. Houston, TX, CIMMYT Publications, 2001, pp. 8–23.
Received: 
10.10.2021
Accepted: 
25.11.2021
Published: 
31.03.2022