Hostname: page-component-669899f699-7tmb6 Total loading time: 0 Render date: 2025-04-26T06:12:03.367Z Has data issue: false hasContentIssue false

Genetic diversity and population structure of wild Salvia miltiorrhiza in China revealed by microsatellite markers and implication for conservation

Published online by Cambridge University Press:  12 September 2024

Xiaoguo Wang
Affiliation:
College of Applied Engineering, Henan University of Science and Technology, Sanmenxia 472000, China Sanmenxia Polytechnic, Sanmenxia 472000, China
Dongfeng Yan*
Affiliation:
College of Forestry, Henan Agricultural University, Zhengzhou 450002, China
Jine Quan
Affiliation:
College of Forestry, Henan Agricultural University, Zhengzhou 450002, China
Sanning Hu
Affiliation:
College of Applied Engineering, Henan University of Science and Technology, Sanmenxia 472000, China Sanmenxia Polytechnic, Sanmenxia 472000, China
Hongyan Liang
Affiliation:
College of Applied Engineering, Henan University of Science and Technology, Sanmenxia 472000, China Sanmenxia Polytechnic, Sanmenxia 472000, China
Xitian Yang*
Affiliation:
College of Forestry, Henan Agricultural University, Zhengzhou 450002, China
*
Corresponding author: Xitian Yang; Email: [email protected]
Corresponding author: Xitian Yang; Email: [email protected]

Abstract

Salvia miltiorrhiza is an outcrossing and perennial herb native to China. Although well-known for its medicinal value, there is a lack of knowledge regarding its natural population genetics. Here, we used 12 microsatellite markers to investigated population genetic diversity and structure of 215 samples from populations naturally distributed in central eastern China. A moderate level of genetic diversity was detected probably due to the over-mining of its roots. The allelic richness (AR) ranged from 3.034 to 4.889 with an average of 3.891. Moreover, pairwise estimates of FST among the populations of S. miltiorrhiza varied from 0.036 to 0.312 and two clusters were obtained by STRUCTURE and discriminant analysis of principal components. It is likely that the genetic differentiation of these two clusters was formed during glacial periods. Our result provides insights into the conservation of this valuable medicinal plant.

Type
Research Article
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of National Institute of Agricultural Botany

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

*

Both authors contributed equally to this work.

References

Benitez-Vieyra, S, Fornoni, J, Perez-Alquicira, J, Boege, K and Dominguez, CA (2014) The evolution of signal-reward correlations in bee- and hummingbird-pollinated species of Salvia. Proceedings of the Royal Society B: Biological Sciences 281, 20132934.CrossRefGoogle ScholarPubMed
Benitez-Vieyra, S, Perez-Alquicira, J, Sazatornil, FD, Dominguez, CA, Boege, K, Perez-Ishiwara, R and Fornoni, J (2019) Evolutionary transition between bee pollination and hummingbird pollination in Salvia: comparing means, variances and covariances of corolla traits. Journal of Evolutionary Biology 32, 783793.CrossRefGoogle ScholarPubMed
Cairampoma, L, Tello, JA and Claßen-Bockhoff, R (2020) Pollination in the desert: adaptation to bees and birds in Salvia rhombifolia. International Journal of Plant Sciences 181, 857870.CrossRefGoogle Scholar
Celep, F, Atalay, Z, Dikmen, F, Dogan, M and Classen-Bockhoff, R (2014) Flies as pollinators of melittophilous Salvia species (Lamiaceae). American Journal of Botany 101, 21482159.CrossRefGoogle Scholar
Celep, F, Atalay, Z, Dikmen, F, Doǧan, M, Sytsma, KJ and Claßen-Bockhoff, R (2020) Pollination ecology, specialization, and genetic isolation in sympatric bee-pollinated Salvia (Lamiaceae). International Journal of Plant Sciences 181, 800811.CrossRefGoogle Scholar
Chapuis, MP and Estoup, A (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621631.CrossRefGoogle ScholarPubMed
Clasenbockhoff, R, Speck, T, Tweraser, E, Wester, P, Thimm, S and Reith, M (2004) The staminal lever mechanism in Salvia L. (Lamiaceae): a key innovation for adaptive radiation? Organisms Diversity & Evolution 4, 189205.CrossRefGoogle Scholar
Erbano, M, Schuhli, GS and Santos, EP (2015) Genetic variability and population structure of Salvia lachnostachys: implications for breeding and conservation programs. International Journal of Molecular Sciences 16, 78397850.CrossRefGoogle ScholarPubMed
Evanno, G, Regnaut, S and Goudet, J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 26112620.CrossRefGoogle ScholarPubMed
Excoffier, L and Lischer, HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.CrossRefGoogle ScholarPubMed
Feng, X, Zhou, H, Zulfiqar, S, Luo, X, Hu, Y, Feng, L, Malvolti, ME, Woeste, K and Zhao, P (2018) The phytogeographic history of common walnut in China. Frontiers in Plant Science 9, 1399.CrossRefGoogle ScholarPubMed
Fragoso-Martínez, I, Martínez-Gordillo, M, Salazar, GA, Sazatornil, F, Jenks, AA, García Peña, M, Barrera-Aveleida, G, Benitez-Vieyra, S, Magallón, S, Cornejo-Tenorio, G and Granados Mendoza, C (2018) Phylogeny of the Neotropical sages (Salvia subg. Calosphace; Lamiaceae) and insights into pollinator and area shifts. Plant Systematics and Evolution 304, 4355.CrossRefGoogle Scholar
Gao, W, Jia, W, Gao, X, Wang, R and Xiao, P (2005) In vitro culture and cultivation of Chinese medicinal plants for industrial utilization and genetic resource conservation. Plant Genetic Resources 3, 116126.CrossRefGoogle Scholar
Gathmann, A and Tscharntke, T (2002) Foraging ranges of solitary bees. Journal of Animal Ecology 71, 757764.Google Scholar
Gerling, DHHWV, Velthuis, HHW and Hefetz, A (1989) Bionomics of the large carpenter bees of the genus Xylocopa. Annual Review of Entomology 34, 163190.CrossRefGoogle Scholar
Goslee, SC and Urban, DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22, 119.CrossRefGoogle Scholar
Goudet, J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485486.CrossRefGoogle Scholar
Hu, GX, Takano, A, Drew, BT, Liu, ED, Soltis, DE, Soltis, PS, Peng, H and Xiang, CL (2018) Phylogeny and staminal evolution of Salvia (Lamiaceae, Nepetoideae) in East Asia. Annals of Botany 122, 649668.CrossRefGoogle ScholarPubMed
Huang, ZH, Liu, HL and Huang, SQ (2015) Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body. Journal of Plant Ecology 8, 109115.CrossRefGoogle Scholar
Jombart, T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics (Oxford, England) 24, 14031405.Google Scholar
Jug-Dujaković, M, Ninčević, T, Liber, Z, Grdiša, M and Šatović, Z (2020) Salvia officinalis survived in situ Pleistocene glaciation in ‘refugia within refugia’ as inferred from AFLP markers. Plant Systematics and Evolution 306, 38.CrossRefGoogle Scholar
Liu, C, Berry, PM, Dawson, TP and Pearson, RG (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28, 385393.CrossRefGoogle Scholar
Liu, L, Hao, ZZ, Liu, YY, Wei, XX, Cun, YZ and Wang, XQ (2014) Phylogeography of Pinus armandii and its relatives: heterogeneous contributions of geography and climate changes to the genetic differentiation and diversification of Chinese white pines. PLoS ONE 9, e85920.CrossRefGoogle Scholar
Liu, SB, Wang, LL, He, CL, Ning, XF and Guo, YL (2015) Research of foraging behaviors of Xylocopa appendiculata on Savia miltiorrhiza in Luoyang. Journal of Environmental Entomology 37, 623626.Google Scholar
Ohashi, K (2002) Consequences of floral complexity for bumblebee-mediated geitonogamous self-pollination in Salvia nipponica Miq.(Labiatae). Evolution 56, 24142423.Google ScholarPubMed
Pasquet, RS, Peltier, A, Hufford, MB, Oudin, E, Saulnier, J, Paul, L, Knudsen, JT, Herren, HR and Gepts, P (2008) Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proceedings of the National Academy of Sciences 105, 1345613461.CrossRefGoogle ScholarPubMed
Peng, L, Ru, M, Wang, B, Wang, Y, Li, B, Yu, J and Liang, Z (2014) Genetic diversity assessment of a germplasm collection of Salvia miltiorrhiza Bunge. based on morphology, ISSR and SRAP markers. Biochemical Systematics and Ecology 55, 8492.CrossRefGoogle Scholar
Phillips, SJ, Anderson, RP and Schapire, RE (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231259.CrossRefGoogle Scholar
Radosavljević, I, Jakse, J, Javornik, B, Satovic, Z and Liber, Z (2011) New microsatellite markers for Salvia officinalis (Lamiaceae) and cross-amplification in closely related species. American Journal of Botany 98, 316318.CrossRefGoogle ScholarPubMed
Radosavljević, I, Satovic, Z, Jakse, J, Javornik, B, Greguraš, D, Jug-Dujaković, M and Liber, Z (2012) Development of new microsatellite markers for Salvia officinalis L. and its potential use in conservation-genetic studies of narrow endemic Salvia brachyodon Vandas. International Journal of Molecular Sciences 13, 1208212093.CrossRefGoogle ScholarPubMed
Rešetnik, I, Baričevič, D, Batîr Rusu, D, Carović-Stanko, K, Chatzopoulou, P, Dajić-Stevanović, Z, Gonceariuc, M, Grdiša, M, Greguraš, D, Ibraliu, A, Jug-Dujaković, M, Krasniqi, E, Liber, Z, Murtić, S, Pećanac, D, Radosavljević, I, Stefkov, G, Stešević, D, Šoštarić, I and Šatović, Z (2016) Genetic diversity and demographic history of wild and cultivated/naturalised plant populations: evidence from Dalmatian sage (Salvia officinalis L., Lamiaceae). PLoS ONE 11, e0159545.CrossRefGoogle ScholarPubMed
Rosenberg, NA (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137138.CrossRefGoogle Scholar
Rost, KT (2000) Pleistocene paleoenvironmental changes in the high mountain ranges of central China and adjacent regions. Quaternary International 65–66, 147160.CrossRefGoogle Scholar
Sarrou, E, Ganopoulos, I, Xanthopoulou, A, Masuero, D, Martens, S, Madesis, P, Mavromatis, A and Chatzopoulou, P (2017) Genetic diversity and metabolic profile of Salvia officinalis populations: implications for advanced breeding strategies. Planta 246, 201215.CrossRefGoogle ScholarPubMed
Song, Z, Li, X, Wang, H and Wang, J (2010) Genetic diversity and population structure of Salvia miltiorrhiza Bge in China revealed by ISSR and SRAP. Genetica 138, 241249.CrossRefGoogle Scholar
Stojanović, D, Aleksić, JM, Jančić, I and Jančić, R (2015) A Mediterranean medicinal plant in the continental Balkans: a plastid DNA-based phylogeographic survey of Salvia officinalis (Lamiaceae) and its conservation implications. Willdenowia 45, 103118.CrossRefGoogle Scholar
Sun, Z, Orozco-terWengel, P, Chen, G, Sun, R, Sun, L, Wang, H, Shi, W and Zhang, B (2021) Spatial dynamics of Chinese Muntjac related to past and future climate fluctuations. Current Zoology 67, 361370.CrossRefGoogle ScholarPubMed
Talebi, SM, Askary, M, Khalili, N, Matsyura, A, Ghorbanpour, M and Kariman, K (2021) Genetic structure and essential oil composition in wild populations of Salvia multicaulis Vahl. Biochemical Systematics and Ecology 96, 104269.CrossRefGoogle Scholar
Van Oosterhout, C, Hutchinson, WF, Wills, DP and Shipley, P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.CrossRefGoogle Scholar
Van Treuren, R, Bijlsma, R, Van Delden, W and Ouborg, NJ (1991) The significance of genetic erosion in the process of extinction. I. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size. Heredity 66, 181189.CrossRefGoogle Scholar
Wang, PX and Sun, XJ (1994) Last glacial maximum in China: comparison between land and sea. Catena 23, 341353.Google Scholar
Xu, G, Liu, C, Huang, L, Wang, X, Zhang, Y, Liu, S, Liao, C, Yuan, Q and Zhou, X (2013) Development of new EST-derived SSRs in Salvia miltiorrhiza (Labiatae) in China and preliminary analysis of genetic diversity and population structure. Biochemical Systematics and Ecology 51, 308313.CrossRefGoogle Scholar
Xu, XX, Cheng, FY, Peng, LP, Sun, YQ, Hu, XG, Li, SY, Xian, HL, Jia, KH, Abbott, RJ and Mao, JF (2019) Late Pleistocene speciation of three closely related tree peonies endemic to the Qinling–Daba Mountains, a major glacial refugium in Central China. Ecology and Evolution 9, 75287548.CrossRefGoogle Scholar
Yang, A, Dick, CW, Yao, X and Huang, H (2016) Impacts of biogeographic history and marginal population genetics on species range limits: a case study of Liriodendron chinense. Scientific Reports 6, 25632.CrossRefGoogle ScholarPubMed
Yeh, FC and Boyle, TJB (1999) POPGENE version 1.3.2: Microsoft window-based freeware for population genetic analysis. http://www.ualberta.ca/~fyeh/index.htmGoogle Scholar
Zhang, Y, Li, X and Wang, Z (2013) Diversity evaluation of Salvia miltiorrhiza using ISSR markers. Biochemical Genetics 51, 707721.CrossRefGoogle ScholarPubMed
Zhang, W, Liu, L, Chen, Y, Liu, B, Harbor, JM, Cui, Z, Liu, R, Liu, X and Zhao, X (2016) Late glacial 10Be ages for glacial landforms in the upper region of the Taibai glaciation in the Qinling Mountain range, China. Journal of Asian Earth Sciences 115, 383392.CrossRefGoogle Scholar
Zhang, XD, Yu, YG, Yang, DF, Qi, ZC, Liu, RZ, Deng, FT, Cai, ZX, Li, Y, Sun, YF and Liang, ZS (2018) Chemotaxonomic variation in secondary metabolites contents and their correlation between environmental factors in Salvia miltiorrhiza Bunge from natural habitat of China. Industrial Crops and Products 113, 335347.Google Scholar
Zhang, JL, Li, WX, Li, Y, Wong, MS, Wang, YJ and Zhang, Y (2021) Therapeutic options of TCM for organ injuries associated with COVID-19 and the underlying mechanism. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology 85, 153297.CrossRefGoogle ScholarPubMed
Zhou, X, Zhang, ZC, Huang, YB, Xiao, HW, Wu, JJ, Qi, ZC and Wei, YK (2021) Conservation genomics of wild red sage (Salvia miltiorrhiza) and its endangered relatives in China: population structure and interspecific relationships revealed from 2b-RAD data. Frontiers in Genetics 12, 707.Google Scholar
Zigene, ZD, Asfaw, BT and Bitima, TD (2021) Analysis of genetic diversity in rosemary (Salvia rosemarinus Schleid.) using SSR molecular marker for its management and sustainable use in Ethiopian genebank. Genetic Resources and Crop Evolution 68, 279293.CrossRefGoogle Scholar
Zona, S (2017) Fruit and seed dispersal of Salvia L. (Lamiaceae): a review of the evidence. The Botanical Review 83, 195212.Google Scholar
Supplementary material: File

Wang et al. supplementary material

Wang et al. supplementary material
Download Wang et al. supplementary material(File)
File 416.5 KB