Genetic diversity and population structure of Pyrus regelii in South Kazakhstan based on ISSR markers
Article Sidebar
Abstract Views: 400
File Views: 188
Main Article Content
Abstract
Abstract. Sitpayeva GT, Abdukhadyr A, Shmakov AI, Zverev NE, Koltunova AM, Yeszhanova AS, Shadmanova SH, Osmonali BB. 2025. Genetic diversity and population structure of Pyrus regelii in South Kazakhstan based on ISSR Markers. Biodiversitas 26: 4714-4729. Pyrus regelii is a relic wild pear species with a restricted distribution in the mountainous regions of South Kazakhstan. Despite its ecological and breeding importance, its genetic structure has never been systematically studied. This study provides the first comprehensive assessment of the genetic and morphological diversity of 5 natural populations from the Karatau and Kyrgyz Alatau ranges. A total of 12 ISSR primers were screened, with 6 highly polymorphic primers selected; these generated 113 loci, of which 112 were polymorphic (98.9%). The number of alleles per locus ranged from 3 to 7 (mean Na = 1.78 per locus). Expected Heterozygosity (He) varied between 0.24-0.31, while Observed Heterozygosity (Ho) was consistently lower, indicating slight inbreeding. Shannon's information index ranged from 0.36-0.47. Pairwise Fst values reached 0.3451 between populations from different mountain systems, reflecting strong differentiation and limited gene flow across orographic barriers. STRUCTURE analysis (K = 3) and PCA confirmed three major genetic clusters, with signs of admixture in several populations. Morphological assessment showed variation in plant height (0.2-3.5 m), crown diameter (0.1-4.4 m), and leaf forms. Heterophyllous populations occurred only in the Kyrgyz Alatau, while Karatau populations were uniform with dissected leaves. The combined genetic and phenotypic evidence indicates adaptive variation that helps survival in arid and cold environments. However, fragmented distribution and isolation make the species vulnerable. Populations with unique alleles (Almalysay) and genetically isolated groups (Bozturgai, Berkara) should be prioritized for in situ conservation and monitoring. Ex situ measures, including seed banks and living collections, are necessary to capture the full spectrum of genetic diversity. Beyond conservation, the adaptive traits of P. regelii offer valuable genetic resources for breeding climate-resilient pear cultivars. Overall, this study establishes the first molecular baseline for P. regelii in Kazakhstan and offers a scientific basis for integrated strategies in conservation and sustainable utilization.
Article Details
Issue
Section
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
References
Abdel-Sattar M, Al-Obeed RS, Rihan HZ, El-Badan GE. 2024. Genetic diversity and relationships among Indian jujube (Ziziphus mauritiana Lamk.) cultivars using morphometric characteristics, matK barcoding, and ISSR markers. Diversity 16 (6): 313. DOI: 10.3390/d16060313.
Abdukhadyr A, Sitpayeva GT, Ivaschenko AA, Zverev NE. 2024. Population assessment of Pyrus regelii Rehder in the Berikkara tract. Spiraeanthus 2024 (1): 120-124. DOI: 10.71130/spir-2024-1-120-124. [Russian]
Abouseada HH, Mohamed A-SH, Teleb SS, Badr A, Tantawy ME, Ibrahim SD, Ellmouni FY, Ibrahim M. 2023. Genetic diversity analysis in wheat cultivars using SCoT and ISSR markers, chloroplast DNA barcoding and grain SEM. BMC Plant Biol 23 (1): 193. DOI: 10.1186/s12870-023-04196-w.
Ali N, Nisa Z-U, Afrasiab H, Latif Z, Erinle KO, Hakimi SS. 2024. Assessment of genetic diversity of grapevine (Vitis vinifera L.) cultivars grown in Pakistan using ISSR markers. Intl J Appl Exp Biol 1 (1): 131. DOI: 10.56612/ijaaeb.v1i1.131.
Baitenov MS. 2001. Flora of Kazakhstan. Family Complex of Flora. Science Publishing, Almaty, Kazakhstan. [Russian]
Bandurko IA. 2016. Study and Breeding of Pear Varieties: A Textbook for Postgraduate Students in Agricultural Sciences. Maykop State Technological University Press, Maykop, Russia. [Russian]
Belousova LK, Ogar NP, Verzilov MA. 2016. The distribution area of Pyrus regelii in Kazakhstan. In: Proceedings of the Aksu-Jabagly Reserve. [Russian]
Bussmann RW, Paniagua-Zambrana NY, Kikvidze Z, Batsatsashvili K, Khutsishvili M, Maisaia I, Sikharulidze S, Tchelidze D, Fayvush G, Aleksanyan, A Muradalievich AA, Kamaludinovich GR, Mehdiyeva NP, Alizade VM, Mursal N. 2024. Pyrus caucasica Fed. Pyrus communis L. Pyrus pyraster (L.) Burgsd. Pyrus salicifolia Pall. Rosaceae. In: Bussmann RW (eds). Ethnobotany of the Caucasus. Ethnobotany of Mountain Regions. Springer, Cham. DOI: 10.1007/978-3-319-50009-6_63-2.
Cai K, Li X, Liu D, Bao S, Shi C, Zhu S, Xu K, Sun X, Li X. 2025. Function diversification of CONSTANS-like genes in Pyrus and regulatory mechanisms in response to different light quality. BMC Plant Biol 25: 303. DOI: 10.1186/s12870-025-06325-z.
Crowley D. 2021. Pyrus regelii. The IUCN Red List of Threatened Species. DOI: 10.2305/IUCN.UK.2021-1.RLTS.T61612002A61612005.en. [19 November 2024]
Dimeyeva L, Permitina V, Kurmantayeva A, Imanalinova A, Osmonali B, Kozybayeva F, Beiseyeva G, Ussen K, Iskakov R, Oyuntsetseg B, Friesen N. 2024. Habitats, plant diversity, and molecular phylogeny of endemic relic species Incarvillea semiretschenskia (Bignoniaceae). Plants 13 (23): 3299. DOI: 10.3390/plants13233299.
Dyussembekova D, Nurtaza A, Magzumova G, Zhenisbekuly G, Kakimzhanova A. 2025. Development of an in vitro conservation protocol for the endemic species Pyrus regelii. Plant Cell Tiss Organ Cult 162: 15. DOI: 10.1007/s11240-025-03127-x.
Earl DA, VonHoldt BM. 2012. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4: 359-361. DOI: 10.1007/s12686-011-9548-7.
Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol Ecol 14: 2611-2620. DOI: 10.1111/j.1365-294X.2005.02553.x.
GBIF Backbone Taxonomy. DOI: 10.15468/39omei. [20 February 2024]
Gu C, Xu Y, Wu L, Wang X, Qi K, Qiao X, Wang Z, Li Q, He M, Zhang S. 2025. Long-read genome sequencing reveals the sequence characteristics of pear self-incompatibility locus. Mol Hortic 5: 13. DOI: 10.1186/s43897-024-00132-0.
Guo G-L, Luo A-R, Tan Y-H, Yuan R-K, Luo T-Y, Ma P-P, Zhan J-Y, Han P, Liu L, Heng W, Ye Z, Yang S, Jia B. 2025. Integrative physiological and transcriptomic analysis provides insights on the molecular basis of ABA-enhanced drought tolerance in pear (Pyrus betulaefolia). BMC Plant Biol 25 (1): 496. DOI: 10.1186/s12870-025-06543-5.
Hammam WE, Gad AM, Gad MK, Kirollos FN, Yassin NA, El Tantawi ME, El Hawary SSE. 2023. Pyrus communis L. (pear) and Malus domestica Borkh. (apple) leaves lipoidal extracts as sources for beta-sitosterol rich formulae and their wound healing evaluation. Nat Prod Res 37 (15): 2613-2617. DOI: 10.1080/14786419.2022.2056181.
Hamrick JL, Godt MJW. 1996. Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B Biol Sci 351 (1345): 1291-1298.
Hayati R, Kasiamdari RS. 2024. Genetic diversity of Indonesian pineapple (Ananas comosus (L.) Merr.) cultivars based on ISSR markers. Pertanika J Trop Agric Sci 47: 1087-1100. DOI: 10.47836/pjtas.47.4.02.
Höfer M, Flachowsky H. 2023. Cryopreservation of Malus and Pyrus wild species in the 'Fruit Genebank' in Dresden-Pillnitz, Germany. Biology 12 (2): 200. DOI: 10.3390/biology12020200.
Imanbayeva A, Dinara Z, Nurzhaugan D, Orazov A, Nazerke T, Gulmira T. 2025. Unravelling the chloroplast genome of the Kazakh apricot (Prunus armeniaca L.) through MinION long-read sequencing. Plants 14 (5): 638. DOI: 10.3390/plants14050638.
Imanbayeva A, Duisenova N, Orazov A, Sagyndykova M, Belozerov I, Tuyakova A. 2024. Study of the floristic, morphological, and genetic (atpF-atpH, Internal Transcribed Spacer (ITS), matK, psbK-psbI, rbcL, and trnH-psbA) differences in Crataegus ambigua populations in Mangistau (Kazakhstan). Plants 13 (12): 1591. DOI: 10.3390/plants13121591.
Ivashchenko AA. 2015. On the distribution and status of populations of some rare plants in the Western Part of the Kyrgyz Alatau. In: Proceedings of the International Scientific Conference "Ecosystems of Central Asia under Conditions of Modern Socio-Economic Development", Ulan-Bator. [Russian]
Katayama H, Amo H, Wuyun T, Uematsu C, Iketani H. 2016. Genetic structure and diversity of the wild Ussurian pear in East Asia. Breed Sci 66 (1): 90-99. DOI: 10.1270/jsbbs.66.90.
Korotkova N, Parolly G, Khachatryan A, Ghulikyan L, Sargsyan H, Akopian J, Borsch T, Gruenstaeudl M. 2018. Towards resolving the evolutionary his-tory of Caucasian pears (Pyrus, Rosaceae) - Phylo-genetic relationships, divergence times and leaf trait evolution. J Syst Evol 56 (1): 35-47. DOI: 10.1111/jse.12276.
Kubentayev SA, Khapilina ON, Ishmuratova MY, Sarkytbayeva AK, Turzhanova AS, Imanbayeva AA, Alibekov DT, Zhumagul MZ. 2023. Current State of natural populations of Paeonia anomala (Paeoniaceae) in East Kazakhstan. Diversity 15: 1127. DOI: 10.3390/d15111127.
Li Y, Zhang J, Li L, Gao L, Xu J, Yang M. 2018. Structural and comparative analysis of the complete chloroplast genome of Pyrus hopeiensis—"wild plants with a tiny population"—and three other Pyrus species. Intl J Mol Sci 19: 3262. DOI: 10.3390/ijms19103262.
Li Y, Zhang J, Wang S, Zhang Y, Yang M. 2021. The distribution and origins of Pyrus hopeiensis-"wild plant with tiny population" using whole genome resequencing. Front Plant Sci 12: 668796. DOI: 10.3389/fpls.2021.668796.
Liu Q, Song Y, Liu, L, Zhang M, Sun J, Zhang S, Wu J. 2015. Genetic diversity and population structure of Pear (Pyrus spp.) collections revealed by a set of core genome-wide SSR markers. Tree Genet Genomes 11: 128. DOI: 10.1007/s11295-015-0953-z.
Liu S, Zhang L, Wang M, Liu W, Cui R, Du B, Song L. 2025. Effect of different pretreatment methods on soluble dietary fiber macromolecules extracted from Korla fragrant pear (Pyrus sinkiangensis Yü): Structure, physicochemical properties, and biological activity. Intl J Biol Macromol 302: 140901. DOI: 10.1016/j.ijbiomac.2025.140901.
Mamurova AT, Isakhanova AT, Tleuberlina OB, Akhtaeva NZ, Akhmetova AB, Kiekbayeva LN, Seilkhan AS, Osmonali B, Temirbay AZh. 2021. Botanical features of the medicinal plant Capparis spinosa L. (C. herbacea Willd.) found in the vegetation cover of the Kyrgyz Alatau. Farm Kaz 55: 83-87. DOI: 10.53511/pharmkaz.2021.55.62.023. [Russian]
Mantel N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res 27 (2): 209-220.
Metsalu T, Vilo J. 2015. ClustVis: A web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Res 43 (W1): W566-W570. DOI: 10.1093/nar/gkv468.
Mezhenskyj VM, Mezhenska LO, Mazur BM, Havryliuk OS. 2024. First blooming of a new intergeneric hybrid between Chaenomeles and Pyrus (Rosaceae). Regul Mech Biosyst 15 (4): 851-855. DOI: 10.15421/0224122.
Monte-Corvo L, Goula?o L, Oliveira C. 2001. ISSR analysis of cultivars of pear and suitability of molecular markers for clone discrimination. J Am Soc Hortic Sci 126 (5): 517-522. DOI: 10.21273/jashs.126.5.517.
Monte-Corvo L, Goulão L, Oliveira C. 2002. Discrimination of pear cultivars with RAPD, AFLPTM and ISSR. Acta Hortic 596: 187-191. DOI: 10.17660/actahortic.2002.596.25.
Mosca E, González-Martínez SC, Neale DB. 2014. Environmental versus geographical determinants of genetic structure in two subalpine conifers. New Phytol 201 (1): 180-192. DOI: 10.1111/nph.12476.
Nowicki M, Huff ML, Staton ME, Trigiano RN. 2022. Chloroplast genome of the invasive Pyrus calleryana underscores the high molecular diversity of the species. J Appl Genet 63 (3): 463-467. DOI: 10.1007/s13353-022-00699-8.
Osmonali BB, Vesselova PV, Kudabayeva GM, Skaptsov MV, Shmakov AI, Friesen N. 2023. Phylogeny and flow cytometry of the genus Kalidium Moq. (Amaranthaceae S.L.) in Kazakhstan. Plants 12 (14): 2619. DOI: 10.3390/plants12142619.
Paniagua-Zambrana NY, Bussmann RW, Kikvidze Z. 2024. Pyrus amygdaliformis Vill. Pyrus communis L. Pyrus elaeagnifolia Pall. Pyrus pyraster (L.) Burgsd. Rosaceae. In: Bussmann RW, Paniagua-Zambrana NY, Kikvidze Z (eds). Ethnobotany of the Mountain Regions of Eastern Europe. Ethnobotany of Mountain Regions. Springer, Cham. DOI: 10.1007/978-3-031-87802-2_240.
Peakall R, Smouse PE. 2006. GENALEX 6: Genetic Analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6 (1): 288-295. DOI: 10.1111/j.1471-8286.2005.01155.x.
Porras-Hurtado L, Ruiz Y, Santos C, Phillips C, Carracedo A, Lareu MV. 2013. An overview of STRUCTURE: Applications, parameter settings, and supporting software. Front Genet 4: 98. DOI: 10.3389/fgene.2013.00098.
Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155 (2): 945-959. DOI: 10.1093/genetics/155.2.945.
Raymond M, Rousset F. 1995. GENEPOP (Version 1.2): Population genetics software for exact tests and ecumenicism. J Hered 86 (3): 248-249. DOI: 10.1093/oxfordjournals.jhered.a111573.
Rohlf F. 2018. NTSYSpc: Numerical Taxonomy System, Ver. 2.21r. Applied Biostatistics 2018: 16-39.
Rousset F. 2008. Genepop'007: A complete reimplementation of the genepop software for Windows and Linux. Mol Ecol Resour 8 (1): 103-106. DOI: 10.1111/j.1471-8286.2007.01931.x.
Sapkota S, Boggess SL, Trigiano RN, Klingeman WE, Hadziabdic D, Coyle DR, Nowicki M. 2022. Microsatellite loci reveal high genetic diversity, mutation, and migration rates as invasion drivers of callery pear (Pyrus calleryana) in the South-eastern United States. Front Genet 13: 861398. DOI: 10.3389/fgene.2022.861398.
Sedov EN, Dolmatov EA. 2022. Pomology: In 5 Volumes. Vol. II. Pear. Quince, Russian Academy of Sciences, Moscow. [Russian]
Sevindik E, Efe F, Murathan ZT. 2023. Molecular genetic diversity and phylogenetic investigation of Pyrus communis L. (Rosaceae) genotypes using cpDNA sequences with RAPD and ISSR analyses. Erwerbs-Obstbau 65: 231-240. DOI: 10.1007/s10341-022-00798-0.
Shadmanova L, Sitpayeva G, Mukanova G, Friesen N. 2019. Molecular-genetic analysis of Malus sieversii: Comparison of Dzungarian populations in situ and ex situ. Turczaninowia 22 (2): 187-198. DOI: 10.14258/turczaninowia.22.2.15.
Shi C, Wang D, Guan Y, Qu H. 2022. Dissection and ultramicroscopic observation of an apical pollen tube of Pyrus. Plant Reprod 35 (1): 1-8. DOI: 10.1007/s00497-021-00433-0.
Silva-Arias GA, Caballero-Villalobos L, Giudicelli GC, Freitas LB. 2021. Landscape and climatic features drive genetic differentiation processes in a South American coastal plant. BMC Ecol Evol 21 (1): 196. DOI: 10.1186/s12862-021-01916-4.
Sitpayeva GT, Veselova PV, Gemejiyeva NG, Grudzinskaya LM, Kerdyashkin AV, Kudabayev GM, Mukanova GS, Murzataeva TSh, Rakhimova EV, Sametova ES, Usen K. 2014. Comprehensive studies of wild relatives of cultivated plants of the Western Tien Shan. Institute of Botany and Phytointroduction, Almaty. [Russian]
Sitpayeva GT, Kudabayev? GM, Dimeyeva LA, Gemejiyeva NG, Vesselova PV. 2020. Crop wild relatives of Kazakhstani Tien Shan: Flora, vegetation, resources. Plant Divers 42 (1): 19-32. DOI: 10.1016/j.pld.2019.10.003.
Upadyshev M, Ivanova B, Motyleva S. 2023. Mass spectrometric identification of metabolites after magnetic-pulse treatment of infected Pyrus communis L. microplants. Intl J Mol Sci 24 (23): 16776. DOI: 10.3390/ijms242316776.
Vdovina TA, Isakova EA, Lagus OA, Sumbembayev AA. 2024. Selection assessment of promising forms of natural Hippophae rhamnoides (Elaeagnaceae) populations and their offspring in the Kazakhstan Altai Mountains. Biodiversitas 25 (4): 1809-1822. DOI: 10.13057/biodiv/d250451.
Velicevici G, Mado?? E, Ciulc? S, Ciulc? A, Camen D, Bein?an C, M?l?escu M, Imbrea I, Cre?escu I. 2023. Identification of genetic diversity among some pear cultivars with ISSR markers. Sci Pap Ser B Hortic 67 (1): 210-214.
Vesselova P, Makhmudova K, Kudabayeva G, Osmonali B, Mikhalev V. 2022. Current growth conditions of Populus diversifolia Schrenk and Populus pruinosa Schrenk in the Syr-Darya Valley. OnLine J Biol Sci 22 (4): 425-438. DOI: 10.3844/ojbsci.2022.425.438.
Waite JM, Gottschalk C, Reinhold LA, Bassil NV, Volk GM, Postman JD, Elkins RB, Bell RL. 2024. Vulnerability of pear (Pyrus) genetic resources in the U.S. Genet Resour Crop Evol 72: 815-843 DOI: 10.1007/s10722-024-01990-9.
Wang J-S, He J-H, Chen H-R, Chen Y-Y, Qiao F. 2017. Genetic diversity in various accessions of pineapple [Ananas comosus (L.) Merr.] using ISSR and SSR markers. Biochem Genet 55 (5-6): 347-366. DOI: 10.1007/s10528-017-9803-z.
Wang T, Wang Z, Xia F. 2016. Local adaptation to temperature and precipitation in naturally fragmented populations of Cephalotaxus oliveri, an endangered conifer endemic to China. Sci Rep 6: 25031. DOI: 10.1038/srep25031.
Wang X, Mingyang L, Lin T, Dongyun L. 2022. Clematis genetic diversity and hybrid identification using ISSR markers. Res Sq 2022: 1-19. DOI: 10.21203/rs.3.rs-1279637/v1.
Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38 (6): 1358-1370. DOI: 10.1111/j.1558-5646.1984.tb05657.x.
Wu Y, Yu X, Tang W, Yang W, Fu Q, Zheng Y, Zhang C. 2024. Morphological and molecular evidence for natural hybridization between Sorbus pohuashanensis and S. discolor (Rosaceae). J For Res 35: 25. DOI: 10.1007/s11676-023-01659-6.
Wu Z, Xu X, Zhang J, Wiegleb G, Hou H. 2019. Influence of environmental factors on the genetic variation of the aquatic macrophyte Ranunculus subrigidus on the Qinghai-Tibetan Plateau. BMC Evol Biol 19 (1): 228. DOI: 10.1186/s12862-019-1559-0.
Xu B, Sun G, Wang X. 2017. Population genetic structure is shaped by historical, geographic, and environmental factors in the leguminous shrub Caragana microphylla on the Inner Mongolia Plateau of China. BMC Plant Biol 17: 200. DOI: 10.1186/s12870-017-1147-7.
Xu Y, Li X, Yang X, Wassie M, Shi H. 2023. Genome-wide identification and molecular characterization of the AP2/ERF superfamily members in sand pear (Pyrus pyrifolia). BMC Genomics 24 (1): 32. DOI: 10.1186/s12864-022-09104-4.
Yang S, Bai M, Hao G, Guo H, Fu B. 2022. Transcriptomics analysis of field-droughted pear (Pyrus spp.) reveals potential drought stress genes and metabolic pathways. PeerJ 10: e12921. DOI: 10.7717/peerj.12921.
Yang X, Dong X, Li K, Zhang Y, Xu C, Huo H, Tian L, Xu J, Liu C, Qi D, Cao Y. 2025. The genetic diversity, population structure, and historical dynamics of wild Pyrus species on the Yunnan-Kweichow Plateau. Horticulturae 11: 106. DOI: 10.3390/horticulturae11010106.
Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX. 1999. POPGENE Version 1.32: The user-friendly software for population genetic analysis. University of Alberta and Centre for International Forestry Research, Edmonton. https://sites.ualberta.ca/~fyeh/popgene_download. html.
Yu Z, Wang Y, Zhang M, Liu Q, Pan Q, Li T, Wang S. 2025. An efficient leaf regeneration and genetic transformation system for Pyrus betulifolia. Hortic Adv 3: 6. DOI: 10.1007/s44281-024-00060-5.
Zhailybayeva T, Shalabayev K, Raimbekova B, Shapalov S, Berkinbayeva G. 2023. Systematic analysis of the flora of the western part of the Kyrgyz Alatau. Intl J Adv Sci Eng Inf Technol 13 (5): 1847-1853. DOI: 10.18517/ijaseit.13.5.18012.
Zheng X, Cai D, Potter D, Postman J, Liu J, Teng Y. 2014. Phylogeny and evolutionary histories of Pyrus L. revealed by phylogenetic trees and networks based on data from multiple DNA sequences. Mol Phylogenet Evol 80: 54-65. DOI: 10.1016/j.ympev.2014.07.009.