Structural and functional organization of leaves and cellular metabolism of the hybridogenic taxon Echinops saksonovii (Asteraceae, Asterales) compared with the parental species

Hybridization is an important component of plant evolution and speciation. Interspecific and intraspecific crossings may lead to changes in the genome, thereby affecting the morphology, adaptation, growth and development of new plant species. The hybridogenic species Echinops saksonovii Vasjukov originates from the introgressive hybridization of E. ruthenicus M. Bieb. and E. sphaerocephalus L. At the morphological level, E. saksonovii differed from its parent species in smaller linear dimensions of the leaves and a longer length of the stomata. The content of green pigments and carotenoids in the leaves of the hybridogenic species was 2.0 and 2.5 times higher, respectively. However, in terms of the ratio of pigments, E. saksonovii is closer to its parent species E. ruthenicus. An increased content of lipids responsible for the formation of thylakoid and non-plastid membranes was found in the lipid complex of E. saksonovii. Among secondary compounds, E. saksonovii leaves accumulated more flavonoids and proline. In terms of the quantitative content of phenolic compounds and peroxidation products, E. saksonovii is closer to its parent shade-tolerant species E. sphaerocephalus. Thus, some features of the structural and functional organization and cellular metabolism in the leaves of the hybridogenic species E. saksonovii in comparison with its parent species have been revealed, which may contribute to better adaptability and viability of E. saksonovii and, as a consequence, to greater competitiveness. 

1. Ali M. A., Al-Hemaid F., Lee J., Hatamleh A.A., Gyulai G., Rahman M. O. Unraveling systematic inventory of Echinops (Asteraceae) with special reference to nrDNA ITS sequence-based molecular typing of Echinops abuzinadianus. Genetics and Molecular Research, 2015, vol. 14, no. 4, pp. 11752–11762. https://doi.org/10.4238/2015.October.2.9

2. Arinushkina E. V. Manual on Chemical Analysis of Soils. Moscow, Moscow University Press, 1970. 489 p. (in Russian).

3. Bates L. S., Waldren R. P., Teare I. D. Rapid determination of free proline for water-stress studies. Plant and Soil, 1973, vol. 39, pp. 205–207. https://doi.org/10.1007/BF00018060

4. Ben-Shem A., Frolow F., Nelson N. Crystal structure of plant photosystem I. Nature, 2003, vol. 426, pp. 630–635. https://doi.org/:10.1038/nature02200

5. Bitew H., Hymete A. The genus Echinops: Phytochemistry and biological activi-ties: A review. Frontiers in Pharmacology, 2019, vol. 10, article no. 1234. https://doi.org/10.3389/fphar.2019.01234

6. Bobowicz M. A., Stephan B. R., Prus-Gɫowacki W. Genetic variation of F1 hybrids from controlled crosses between Pinus montana var. rostrata and Pinus sylvestris in anatomical needle traits. Acta Societatis Botanicorum Poloniae, 2000, vol. 69, no. 3, pp. 207–214.

7. Bobrov E. G. Echinops L. In: Shishkin B. K., Bobrov E. G., eds. Flora of the USSR. Dehra Dun, Bishen Singh, Mahendra Pal Singh and Koelz Scientific Books, 1997, vol. 27, pp. 1–70.

8. Hedge I. C. Echinops L. In: Davis P. H., ed. Flora of Turkey and the East Aegean Islands.

9. Edinburgh, Edinburgh University Press, 1975, vol. 5, pp. 609–622.

10. Gross B. L., Rieseberg L. H. The ecological genetics of homoploid hybrid speciation. Journal Heredity, 2005, vol. 96, no. 3, pp. 241–252.

11. Gould K. S., Lister C. Flavonoid functions in plants. In: Andesen O. M., Markham K. R., eds. Flavonids. Chemistry, Biochemistry and Applications. Boca Raton, London, New York, CRC Press, 2006, pp. 397–443.

12. Jones M. R. Lipids in photosynthetic reaction centres: Structural roles and functional holes. Progress in Lipid Research, 2007, vol. 39, no. 1. pp. 56–87. https://doi.org/101016/j.plipres.2006.06.001

13. Kirk H., Choi Y. H., Kim H. K., Verpoorte R., Van Der Meijden E. Comparing metabolomes: The chemical consequences of hybridization in plants. New Phytologist, 2005, vol. 167, iss. 2, pp. 613–622. https://doi.org/10.1111/j.1469-8137.2005.01448.x

14. Kennedy D. O., Wightman E. L. Herbal extracts and phytochemicals: plant secondary metabolites and the enhancement of human brain function. American Society for Nutrition. Advances in Nutrition, 2011, vol. 2, iss. 1, pp. 32–50. https://doi.org/10.3945/an.110.000117

15. Knyazev M. S. A new species of Echinops (Asteraceae) from the Volga-Urals region. Novitates Systematicae Plantarum Vascularium, 2018, no. 49, pp. 133–138 (in Russian). https://doi.org/10.31111/novitates/2018.49.133

16. Kobayashi I. K., Endo K., Wada H. Roles of lipids in photosynthesis. In: Nakamura Y., LiBeisson Y., eds. Lipids in Plant and Algae Development. Cham, Springer, 2016, pp. 21–49. https://doi.org/10.1007/978-3-319-25979-6_2

17. Kolupaev Y. E., Karpets Y. V., Kabashnikova L. F. Antioxidative system of plants: Cellular compartmentalization, protective and signaling functions, mechanisms of regulation (Review). Applied Biochemistry and Microbiology, 2019, vol. 55, no. 5, pp. 441–459. https://doi.org/10.1134/S0003683819050089

18. Lichtenthaller H. K. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, 1987, vol. 148, pp. 350–382. https://doi.org/10.1016/00766879(87)48036-1

19. López-Caamal A., Tovar-Sánchez E. Genetic, morphological, and chemical patterns of plant hybridization. Revista Chilena de Historia Natural, 2014, vol. 87, article no. 16. https://doi.org/10.1186/s40693-014-0016-0

20. Mallet J. Hybridization as an invasion of the genome. Trends in Ecology Evolution, 2005, vol. 20, iss. 5, pp. 229–237. https://doi.org/10.1016/j.tree/2005.02.010

21. Martínez-Lüscher J., Torres N., Hilbert G., Richard T., Sànchez-Díaz M., Delrot S., Aguirreolea J., Pascual I., Gomѐs E. Ultraviolet-B radiation modifies the quantitative and qualitative profile of flavonoids and amino acids in grape berries. Phytochemistry, 2014, vol. 102, pp. 106–114. https://doi.org/10.1016/j.phytochem.2014.03.014

22. Maslova T. G., Markovskaya E. F., Slemnev N. N. Functions of carotenoids in leaves of higher plants (Review). Biology Bulletin Reviews, 2021, vol. 11, no. 5, pp. 476–487. https://doi.org/10.1134/s2079086421050078

23. Orians C. M. The effects of hybridization in plants on secondary chemistry: Implications for the ecology and evolution of plant-herbivore interactions. American Journal of Botany, 2000, vol. 87, iss. 12, pp. 1749–1756. https://doi.org/10.2307/2656824

24. Papuga G., Rossella F., Gauthier P., Gauthier P., Farris E. Variation in floral morphology in a hybrid complex of Cyclamen in Sardinia. Plant Ecology and Diversity, 2019, vol. 12, iss. 1, pp. 51–61. https://doi.org/10.1080/17550874.2019.1593545

25. Rakov N. S., Saksonov S. V., Senator S. A., Vasjukov V. M. Flora of the Volga River Basin. Vol. II. Vascular Plants of Ulyanovsk Region. Togliatti, Kassandra, 2014, pp. 39–40 (in Russian).

26. Rieseberg L. H., Ellstrand N. C., Arnold Dr. M. What can molecular and morphological markers tell us about plant hybridization? Critical Reviews in Plant Sciences, 1993, vol. 12, iss. 3, pp. 213–241. https://doi.org/10.1080/07352689309701902

27. Rocha J., Nitenberg M., Girard-Egrot A., Jouhet J., Maréchal E., Block M. A., Breton C. Do galactolipid synthases play a key role in the biogenesis of chloroplast membranes of higher plants? Frontier Plant Science, 2018, vol. 9, article no. 126. https://doi.org/10.3389/fpls.2018.00126

28. Rodionov A. V., Amosova, A. V., Belyakov, E. A., Zhurbenko P. M, Mikhailova Yu. V., Punina E. O., Shneyer V. S., Loskutov I. G., Muravenko O. V. Genetic consequences of interspecific hybridization, its role in speciation and phenotypic diversity of plants. Russian Journal Genetics, 2019, vol. 55, iss. 3, pp. 278–294. https://doi.org/10.1134/S1022795419030141

29. Rozentsvet O. A., Nesterov V. N., Bogdanova E. S. Membrane-forming lipids of wild halophytes growing under the conditions of Prieltonie of South Russia. Phytochemistry, 2014, vol. 105, pp. 37–42. https://doi.org/10.1016/j.phytochem.2014.05.007

30. Soltis P. S., Soltis D. E. The role of hybridization in plant speciation. Annual Review Plant Biology, 2009, vol. 60, pp. 561–588. https://doi.org/10.1146/annurev.arplant.043008.092039

31. Somayeh M., Alfonso S., Juan Antonio C., Valiollah M., Mohammad Reza R. Molecular systematics and phylogeography of the genus Echinops (Compositae, Cardueae–Echinopsinae): Focus on the Iranian centre of diversification. Phytotaxa, 2017, vol. 997, no. 2, article no. 27. https://doi.org/10.1146/10.11646/phytotaxa.297.2.1

32. Sánchez-Jiménez I., Lazkov G. A., Hidalgo O., Garnatje T. Molecular systematics of Echinops L. (Asteraceae, Cynareae): A phylogeny based on ITS and trnL-trnF sequences with emphasis on sectional delimitation. Taxon, 2010, vol. 9, no. 3, pp. 698–708. https://doi.org/10.2307/25677662

33. Swain T., Hillis W. E. The phenolic constituents of Prunus domestica. I. The quantitative analysis of phenolic constituents. Journal Science of Food and Agriculture, 1959, vol. 10, no. 1, pp. 63–68. https://doi.org/10.1002/jsfa.2740100110

34. Thompson J. D., Gaudeul M., Debussche M. Conservation value of sites of hybridization in peripheral populations of rare plant species. Conservation Biology, 2010, vol. 24, iss. 1, pp. 236–245. https://doi.org/10.1111/j.1523-1739.2009.01304-x

35. Vasilyeva G. Light microscopic structure of needle in Pinus sibirica, P. pumila, and their hybrids. Flora, 2021, vol. 285, article no. 151964. https://doi.org/10.1016/j.flora.2021.151964

36. Vasjukov V. M., Bondarevа V. V. A new species of Echinops (Asteraceae) from Middle Volga region. Botanicheskii Zhurnal, 2021, vol. 106, no. 11, pp. 1127–1130 (in Russian). https://doi.org/10.31857/S0006813621110120

37. Wada H., Murata N. The essential role of phosphatidylglycerol in photosynthesis. Photosynthesis Research, 2007, vol. 92, no. 2, pp. 205–215. https://doi.org/10.1007/s11120-007-9203-z

38. Whitney K. D., Ahern J. R., Campbell L. G., Albert L. P., King M. S. Patterns of hybridization in plants. Perspectives in Plant Ecology, Evolution and Systematics, 2010, vol. 12, no. 3, pp. 175 –182. https://doi.org/10.1016/j.ppees.2010.02.002

39. Whitney K. D., Randell R. A., Rieseberg L. H. Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. American Naturalist, 2006, vol. 167, no. 6, pp. 794–807. https://doi.org/10.1086/504606

40. Wu S. Molybdenum induces alterations in the glycerolipidome that confer drought tolerance in wheat. Journal Experimental Botany, 2020, vol. 71, iss. 16, pp. 5074–5086. https://doi.org/10.1093/jxb/eraa215

41. Uchiyama M., Mihara M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Analytical Biochemistry, 1978. vol, 86, iss. 1, pp. 271–278. https://doi.org/10.1016/0003-2697(78)90342-1