Molecular genetic variability in coenopopulations of Caragana jubata (Pall.) Poir. (Fabaceae) in the mountains of Central Asia and Southern Siberia revealed using ISSR-markers

The genetic structure was studied using five ISSR markers in 44 individuals of samples obtained from eight coenopopulations (CPs) of Caragana jubata (Pall.) Poir. in the mountainous conditions of Central Asia – in the Western Pamirs and Inner Tien Shan (Kyrgyzstan) and in Southern Siberia – in Altai (Republic of Altai), Western (Republic of Tyva) and Eastern (Republic of Buryatia) Sayan. We studied the species in a range of geographical distances of more than 2,500 km and in the range of absolute altitudes of 1,570–3,680 m. Caragana jubata is listed in the Red Data Books of eight subjects of the Russian Federation. The species population is declining, including due to anthropogenic impact. The aim of the current work is to identify genetic diversity and heterogeneity in C. jubata coenopopulations depending on their geographic and altitudinal confinement in the mountains of Central Asia and Southern Siberia. It was shown that in undisturbed locations, the studied CPs of this species were characterized by a high number of individuals and by the occupied area of more than 100 m2. Almost every sample from the C. jubata CP studied by us (except for representatives from CP7) contained genotypes possessing unique DNA fragments. The highest proportion of such genotypes (75 %) was found in the sample from CP3 (Inner Tien Shan, Teskey-Ala-Too Ridge, absolute altitude 2,550 m). We did not find unique fragments in the genotypes of individuals from the studied sample of CP7 (Western Sayan, Republic of Tuva). Anthropogenic impact on plants at this location is a possible reason for that. The revealed predominance of intrapopulation genetic variability over interpopulation genetic variability in samples from eight C. jubata CPs studied by us may indicate the stability of representatives of this species within the parts of the range studied by us.

1. Bhardwaj P.K., Kapoor R., Mala D., Bhagwat G., Acharya V., Singh A.K., Vats S.K., Ahuja P.S., Kumar S. Braving the attitude of altitude: Caragana jubata at work in cold desert of Himalaya. Sci Rep. 2013;3:1022. doi 10.1038/srep01022

2. Chung M.Y., Mmerila J., Li J., Mao K., López-Pujo J., Tsumura Y., Chung M.G. Neutral and adaptive genetic diversity in plants: an overview. Front Ecol Evol. 2023;11:1116814. doi 10.3389/fevo.2023.1116814

3. Churiulina A.G., Bocharnikov M.V. Caragana jubata (Pall.) Poir. (Fabaceae), distribution mapping of rare relict species. Bot Pacifica. 2019;8(2):111-114. doi 10.17581/bp.2019.08207

4. Churyulina A.G. Geography of rare species (Caragana jubata (Pall.) Poir., Betula lanata (Regel) V. Vassil.) and communities with their participation in the mountain biomes of the Baikal region: Cand. Sci. (Geogr.) Dissertation. Moscow, 2021 (in Russian)

5. Churyulina A.G., Bocharnikov M.V., Ogureeva G.N. Geography of Caragana jubata (Pall.) Poir. (Fabaceae) and its phytocenotic role in the mountain vegetation cover. Vestnik Moskovskogo Universiteta. Seriya 5. Geografiya = Moscow University Bulletin. Series 5. Geography. 2020;3:108-117 (in Russian)

6. de Lafontaine G., Napier J.D., Petit R.J., Hu F.S. Invoking adaptation to decipher the genetic legacy of past climate change. Ecology. 2018;99(7):1530-1546. doi 10.1002/ecy.2382

7. Dorogina O.V., Zhmud E.V. Molecular-genetic methods in plant ecology. Contemp Probl Ecol. 2020;13(4):333-345. doi 10.1134/S1995425520040058

8. Dorogina O.V., Kuban I.N., Achimova A.A., Williams N., Lashchinskiy N.N., Zhmud E.V. Morphometric characteristics and genetic ISSR marker variability in Rhodiola rosea L. (Crassulaceae) in different ecological and geographic conditions in the Altai Republic. Int J Molec Sci. 2023;24(10):15224. doi 10.3390/ijms242015224

9. Hamabata T., Kinoshita G., Kurita K., Cao P.-L., Ito M., Murata J., Komaki Y., Isagi Y., Makino T. Endangered island endemic plants have vulnerable genomes. Commun Biol. 2019;2:244. doi 10.1038/s42003-019-0490-7

10. Hantemirova E.V., Khoreva M.G., Bessonova V.A. Genetic and ecological differentiation of Caragana jubata (Pall.) Poir. Bot Pacifica. 2024;13(2):15-22. doi 10.17581/bp.2024.13204

11. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403-1405. doi 10.1093/bioinformatics/btn129

12. Kakorin P.A., Babenkova I.V., Teselkin Yu.O., Ramenskaya G.V., Demura T.A., Kukes V.G. Hepatoprotective activity of aqueous extract from Caragana jubata (Pall.) Poir. shoots in the model of acute hepatitis induced by acetaminophen in rats. Biomeditsinskaya Khimiya. 2018a;64(3):241-246. doi 10.18097/PBMC20186403241 (in Russian)

13. Kakorin P.A., Tereshkina O.I., Ramenskaya G.V. Potential biological activity and chemical composition of Caragana jubata (Pall.) Poir. (review). Pharm Chem J. 2018b;52(6):531-535. doi 10.1007/s11094-018-1854-x

14. Kakorin P.A., Fateeva T.V., Tereshkina O.I., Perova I.B., Ramenskaya G.V., Sologova S.S., Eller K.I. Antimicrobial activity of lyophilized aqueous extract from Caragana jubata (Pall.) Poir. Pharm Chem J. 2020;54(3):290-292. doi 10.1007/s11094-020-02193-z

15. Kassambara A. ggpubr: ‘ggplot2’ based publication ready plots. R package version 0.6.0. 2023. https://rpkgs.datanovia.com/ggpubr/

16. Koropachinsky I.Yu., Vstovskaya T.N. Woody Plants of Asian Russia. Novosibirsk: Geo Publ., 2012 (in Russian)

17. Liu C., Wang J., Ko Y.-Z., Shiao M.-S., Wang Y., Sun J., Yuan Q., Wang L., Chiang Y.-C., Guo L. Genetic diversities in wild and cultivated populations of the two closely-related medical plants species, Tripterygium wilfordii and T. hypoglaucum (Celastraceae). BMC Plant Biol. 2024;24(1):195. doi 10.1186/s12870-024-04826-x

18. Lysova N.V. Ecology of Caragana jubata (Pall.) Poir. in the Central Tien Shan. Byulleten Glavnogo Botanicheskogo Sada = Bulletin of the Moscow Botanical Garden of the Academy of Sciences. 1967; 64:64-67 (in Russian)

19. Magri D., Vendramin G.G., Comps B., Dupanloup I., Geburek T., Gömöry D., Latałowa M., Litt T., Paule L., Roure J.M., Tantau I., Van Der Knaap W.O., Petit R.J., De Beaulieu J.-L. A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol. 2006;171(1):199-221. doi 10.1111/j.1469-8137.2006.01740.x

20. Nabieva A.Yu., Zhmud E.V., Kuban I.N., Dorogina O.V. Morphometric and molecular analysis of Cypripedium × ventricosum (Orchidaceae) population in the Novosibirsk Region. Botanicheskii Zhurnal. 2020;105(6):597-603. doi 10.31857/S0006813620060058 (in Russian)

21. Nørgaard L.S., Mikkelsen D.M.G., Elmeros M., Chriél M., Madsen A.B., Nielsen J.L., Pertoldi C., Randi E., Fickel J., Brygida S., Ruiz-González A. Population genomics of the raccoon dog (Nyctereutes procyonoides) in Denmark: insights into invasion history and population development. Biol Invasions. 2017;19(5):1637-1652. doi 10.1007/s10530-017-1385-5

22. Ohsawa T., Yuji I. Global patterns of genetic variation in plant species along vertical and horizontal gradients on mountains. Glob Ecol Biogeogr. 2008;17(2):152-163. doi 10.1111/j.1466-8238.2007.00357.x

23. Oorzhak U.S., Lopsan-Endan A.B., Dorzhu-ool Yu.N. Bioecological and chemical features of Caragana jubata (Pall.) Poir. Vestnik Tuvinskogo Gosudarstvennogo Universiteta. Estestvennye i Selskokhozyajstvennye Nauki – Vestnik of of Tuvan State University. Natural and Agricultural Sciences. 2024;1(5):16-24. doi 10.24411/2221-0458-2024-01-16-24 (in Russian)

24. Oyama K., Ito M., Yahara T., Ono M. Low genetic differentiation among populations of Arabis serrata (Brassicaceae) along an altitudinal gradient. J Plant Res. 1993;106(2):143-148. doi 10.1007/BF02344418

25. Parygin I.A., Khudonogova E.G. Plant communities of Caragana jubata (Pallas) Poiret of the southwestern regions of Buryatia. Vestnik Orenburgskogo Gosudarstvennogo Pedagogicheskogo Universiteta = Vestnik of Orenburg State Pedagogical University. 2017; 4(24):26-33 (in Russian)

26. R Core Team. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria, 2024. https://www.R-project.org/

27. Reisch C., Anke A., Röhl M. Molecular variation within and between ten populations of Primula farinose (Primulaceae) along an altitudinal gradient in the northern Alps. Basic Appl Ecol. 2005;6(1):35-45. doi 10.1016/j.baae.2004.09.004

28. Safaralikhonov A.B., Aknazarov O.A. The Effect of Environmental Factors of the Pamir Highlands on Plant Life. Dushanbe: Donish Publ., 2021 (in Russian)

29. Semenova G.P. Rare and Endangered Species of Siberian Flora: Biology, Conservation. Novosibirsk: Geo Publ., 2007 (in Russian)

30. Shi M.-M., Michalski S.G., Chen X.-Y., Durka W. Isolation by elevation: genetic structure at neutral and putatively non-neutral loci in a dominant tree of subtropical forests, Castanopsis eyrie. PLoS One. 2011;6(6):e21302. doi 10.1371/journal.pone.0021302

31. Smouse P.E., Banks S.C., Peakall R. Converting quadratic entropy to diversity: both animals and alleles are diverse, but some are more diverse than others. PLoS One. 2017;12(10):e0185499. doi 10.1371/journal.pone.0185499

32. Taberlet P., Fumagalli L., Wust-Saucy A.-G., Cosson J-F. Comparative phylogeography and postglacial colonization route in Europe. Mol Ecol. 1998;7(4):453-464. doi 10.1046/j.1365-294x.1998.00289.x

33. Talovina G.V. Crop Wild Relatives in the Magadan Province of Russia: Perspectives of Gene Pool Conservation. Vavilovia. 2019; 2(3):42-55. doi 10.30901/2658-3860-2019-3-42-55 (in Russian)

34. The Red Book of Altay Republic. Plants. Gorno-Altaysk: Gorno-Altayskaya Tipografia Publ., 2017 (in Russian)

35. The Red Book of Sakha Republic (Yakutia). Vol. 1. Rare and Endangered Species of Plants and Fungi. Moscow: Reart Publ., 2017 (in Russian)

36. The Red Book of Zabaykalskiy Kray. Novosibirsk: Dom Mira Publ., 2017 (in Russian)

37. The Red Book of Khabarovsk Kray. Rare and Endangered Species of Plants, Fungi, and Animals. Voronezh: Mir Publ., 2019 (in Russian)

38. The Red Book of Magadan Oblast. Rare and Endangered Species of Animals, Plants and Fungi. Magadan: Okhotnik Publ., 2019 (in Russian)

39. The Red Book of Irkutsk Oblast. Ulan-Ude, 2020 (in Russian)

40. The Red Book of Krasnoyarsk Kray. Vol. 2. Rare and Endangered Species of Plants and Fungi. Krasnoyarsk: Siberian Federal University, 2022 (in Russian)

41. The Red Book of Republic of Buryatia. Rare and Endangered Species of Plants and Fungi. Belgorod: Konstanta Publ., 2023 (in Russian)

42. Wang Q., Wu X., Yang X., Zhang Y., Wang L., Li X., Qiu Y. Comprehensive quality evaluation of Lignum Caraganae and rapid discrimination of Caragana jubata and Caragana changduensis based on characteristic compound fingerprints by HPLC-UV and HPLC-MS/MS coupled with chemometrics analysis. Phytochem Anal. 2020; 31(6):846-860. doi 10.1002/pca.2950

43. Wickham H., Averick M., Bryan J., Chang W., McGowan L.D., François R., Grolemund G., … Takahashi K., Vaughan D., Wilke C., Woo K., Yutani H. Welcome to the Tidyverse. J Open Source Software. 2019;4(43):1686. doi 10.21105/joss.01686

44. Wright S. Breeding structure of populations in relation to speciation. Am Nat. 1940;74(752):232-248. doi 10.1086/280891

45. Xu S., Li L., Luo X., Chen M., Tang W., Zhan L., Dai Z., Lam T.T., Guan Y., Yu G. Ggtree: a serialized data object for visualization of a phylogenetic tree and annotation data. iMeta. 2022;1(4):e56. doi 10.1002/imt2.56

46. Yang X.-Z., Lyu J.-N., Xu C., Lin Q.-X., Yang J., Wang C., Song P. Cytotoxic chemical constituents from Caragana jubata (Pall.) Poir. J Yunnan Univ Nat Sci Ed. 2015;37(1):134-139. doi 10.7540/j.ynu.20140364

47. Yao N., Gao J., Wang L., Ma Z., Zhang J., Ma F., Xu T. Development of SSR molecular markers and analysis of genetic diversity in Caragana jubata (Pall.) Poir. Genet Resour Crop Evol. 2025;72(7): 8957-8972. doi 10.1007/s10722-025-02477-x

48. Yifru T., Hammer K., Huang X.Q., Röder M.S. Regional patterns of microsatellite diversity in Ethiopian tetraploid wheat accessions. Plant Breed. 2006;125(2):125-130. doi 10.1111/j.1439-0523.2006.01147.x

49. Zhang M.-L., Xiang X.-G., Xue J.-J., Sanderson S.C., Fritsch P.W. Himalayan uplift shaped biomes in Miocene temperate Asia: evidence from leguminous Caragana. Sci Rep. 2016;6:36528. doi 10.1038/srep36528

50. Zhang X., Korpelainen H., Li C. Microsatellite variation of Quercus aquifolioides populations at varying altitudes in the Wolong natural reserve of China. Silva Fenn. 2006;40(3):407-415. doi 10.14214/sf.326

51. Zhao D., Chen X., Wang R., Pang H., Wang J., Liu L. Determining the chemical profile of Caragana jubata (Pall.) Poir. by UPLC-QTOFMS analysis and evaluating its anti-ischemic stroke effects. J Ethnopharmacol. 2023;309:116275. doi 10.1016/j.jep.2023.116275

52. Zhmud E.V., Kuban I.N., Achimova A.A., Yamtyrov M.B., Dorogina O.V. Comparative analysis of genetic polymorphism in Rhaponticum carthamoides (Asteraceae) populations by ISSR markers in the Altai Republic. Trudy po Prikladnoy Botanike, Genetike i Selektsii = Proceedings on Applied Botany, Genetics, and Breeding. 2023;184(2):149-159. doi 10.30901/2227-8834-2023-2-149-159 (in Russian)

53. Zhmud E.V., Kuban I.N., Achimova A.A., Papina O.N., Dorogina O.V. Variability of morphometric parameters in Adonis villosa Ledeb. (Ranunculaceae) and its genetic differentiation based on ISSR markers in the Altai Republic. Contemp Probl Ecol. 2024;17(4):557-565. doi 10.1134/S1995425524700355