Skip to main content

Plastid DNA diversity and genetic divergence within Rhododendron dauricum s.l. (R. dauricum s.s., R. ledebourii, R. sichotense and R. mucronulatum; Ericaceae)

Abstract

Genetic variation in 45 populations (267 plants) of Rhododendron dauricum s.l. across its range in Northeast Asia was assessed with four regions of plastid DNA (ptDNA). A total of 14 haplotypes were detected. The highest diversity was observed in the south of West Siberia (the Altai and Western Sayan Mountains) and the southern Russian Far East (the Sikhote-Alin Mountains). In contrast, only one haplotype occurred in populations from East Siberia located from Baikal to the Sikhote-Alin Mountains. In general, distribution of haplotypes showed a strong phylogeographical structure (GST = 0.897; NST = 0.985) and evidence of isolation by distance, supporting the independence of four species: R. ledebourii Pojark. and R. dauricum L. s.s. in Siberia, and R. sichotense Pojark. and R. mucronulatum Turcz. in the southern part of the Far East.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Aleksandrova MS (1975) Rododendrony prirodnoi flory SSSR. Nauka Press, Moscow (in Russian)

    Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molec Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Article  PubMed  CAS  Google Scholar 

  • Baranova TV, Kalendar RN, Kalaev VN (2014) K voprosu filogenii roda Rhododendron L. na osnove posledovatelnosti speisera ITS1–ITS2. Sibirsk Lesn Zhur 6:29–45 (in Russian)

    Google Scholar 

  • Belousov MV, Basova EV, Yusubov MS, Berezovskaya TP, Pokrovskii LM, Tkachyov AV (2000) Efirnye masla nekotoryh vidov Rhododendron L. Khim Rast Syrya 3:45–64 (in Russian)

    Google Scholar 

  • Binney HA, Willis KJ, Edwards ME, Bhagwat SA, Anderson PM, Andreev AA, Blaauw M, Damblon F, Haesaerts P, Kienast F (2009) The distribution of late-quaternary woody taxa in northern Eurasia: evidence from a new macrofossil database. Quatern Sci Rev 28:2445–2464. https://doi.org/10.1016/j.quascirev.2009.04.016

    Article  Google Scholar 

  • Boyarskaya TD (1989) Sopostavlenie amplitudy izmenchivosti paleoklimatov pozdnego pleistotsena i golotsena razlichnyh raionov SSSR. In: Hotinskii NA (ed) Paleoklimaty pozdnelednikovya i golotsena. Nauka Press, Moscow, pp 85–90 (in Russian)

    Google Scholar 

  • Bruchmann I, Hobohm C (2014) Factors that create and increase endemism. In: Hobohm C (ed) Endemism in vascular plants. Springer, Dordrecht, pp 51–68

    Chapter  Google Scholar 

  • Chamberlain DF, Hyam R, Argent G, Fairweather G, Walter KS (1996) The genus Rhododendron—its classification and synonymy. Royal Botanical Garden of Edinburgh Press, Edinburgh

    Google Scholar 

  • Chang CS, Kim H, Chang KS (2014) Provisional checklist of vascular plants for the Korea peninsula flora (KPF). Designpost Press, Seoul

    Google Scholar 

  • Cherepnin LM (1959) Flora yuzhnoi chasti Krasnoyarskogo kraya. KGPI Press, Krasnoyarsk (in Russian)

    Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Molec Ecol 4:129–134. https://doi.org/10.1111/j.1365-294X.1995.tb00201.x

    Article  CAS  Google Scholar 

  • Devey ME, Bell JS, Smith DN, Neale DB, Motan GF (1996) A genetic linkage map for Pinus radiata based on RFLP, RAPD and microsatellite markers. Theor Appl Genet 92:673–679. https://doi.org/10.1007/BF00226088

    Article  PubMed  CAS  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molec Ecol 11:2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molec Ecol Resources 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial-DNA restriction data. Genetics 131:479–491

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98. https://doi.org/10.1111/jbi.12867

    CAS  Article  Google Scholar 

  • Hantemiova EV, Heinze B, Knyazeva SG, Musaev AM, Lascoux M, Semerikov VL (2016) A new Eurasian phylogeographical paradigm? Limited contribution of southern populations to the recolonization of high latitude populations in Juniperus communis L. (Cupressaceae). J Biogeogr 44:271–282. https://doi.org/10.1111/jbi.12867

    Article  Google Scholar 

  • Hantemirova EV, Berkutenko AN, Semerikov VL (2012) Systematics and gene geography of Juniperus communis L. inferred from isoenzyme data. Russ J Genet 48:920–926. https://doi.org/10.1134/S1022795412090050

    Article  CAS  Google Scholar 

  • Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 40:393–412. https://doi.org/10.2307/1223218

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) Mr Bayers: Bayesian inference of phylogeny. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754

    Article  PubMed  CAS  Google Scholar 

  • Irving E, Hebda R (1993) Concerning the origin and distribution of rhododendrons. J Amer Rhododendron Soc 47:139–162

    Google Scholar 

  • Jiang N, Man L, Zhang W, Dong HX, Wang HY, Li MR, Shi FX, Sun MZ (2016) Chloroplast view of the population genetics and phylogeography of a widely distributed shrub species, Rhododendron dauricum (Ericaceae). Syst Bot 41:626–633. https://doi.org/10.1600/036364416X692343

    Article  Google Scholar 

  • Karpova EA, Karakulov AV (2011) Fenolnye soedineniya blizkorodstvennyh vidov roda Rhododendron L. (Ericaceae). Turczaninowia 14:145–149 (in Russian)

    Google Scholar 

  • Koksheeva I, Naryshkina N (2013) Morfologiya pyltsy I semyan nekotoryh dalnevostochnyh vidov roda Rhododendron subsect. Rhodorastrum (Ericaceae) na Dalnem Vostoke Rossii. Turczaninowia 16:164–172 (in Russian)

    Google Scholar 

  • Koksheeva I, Naryshkina N, Kislov D (2015) Seed morphology of Rhododendron sichotense (Ericaceae): systematic implications. Nordic J Bot 33:498–505. https://doi.org/10.1111/njb.00707

    Article  Google Scholar 

  • Koropachinskii IY, Vstovskaya TN (2002) Drevesnye rasteniya aziatskoi Rossii. Publisher House of SB RAS, Novosibirsk (in Russian)

    Google Scholar 

  • Korotkii AM, Volkova VG, Grebennikova TA et al (1999) Dalnii Vostok (The Far East). In: Velichko AA (ed) Izmeneniya klimata i landshaftov za poslednie 65 mln. let (Kainozoi: ot Pleistotsena do Golotsena). Geos Press, Moscow, pp 146–159 (in Russian)

    Google Scholar 

  • Krasnoborov IM (1976) Vysokogornaya flora Zapadnogo Sayana. Nauka Press, Novosibirsk (in Russian)

    Google Scholar 

  • Kremenetski CV, Tarasov PE, Cherkinsky AE (1997) The Latest Pleistocene in southwestern Siberia and Kazakhstan. Quatern Int 41:125–134. https://doi.org/10.1016/S1040-6182(96)00044-4

    Article  Google Scholar 

  • Kruklis MV, Milyutin LI (1977) Listvennitsa Chekanovskogo (Chekanovsky Larch). Nauka Press, Moscow (in Russian)

    Google Scholar 

  • Kutsev MG, Karakulov AV (2010) Rekonstruktsiya filogenii roda Rhododendron L. (Ericaceae) flory Rossii na osnove posledovatelnostei speiserov ITS1–ITS2. Turczaninowia 13:59–62 (in Russian)

    Google Scholar 

  • Lascoux M, Palme AE, Cheddadi R, Latta R (2004) Impact of the Ice Ages on the genetic structure of trees and shrubs. Philos Trans Roy Soc B Biol Sci 359:197–207. https://doi.org/10.1098/rstb.2003.1390

    Article  Google Scholar 

  • Maliouchenko O, Palme AE, Buonamici A, Vendramin GG, Lascoux M (2007) Comparative phylogeography and population structure of European Betula species, with particular focus on B. pendula and B. pubescens. J Biogeogr 34:1601–1610. https://doi.org/10.1111/j.1365-2699.2007.01729.x

    Article  Google Scholar 

  • Malyshev LI (1972) Floristicheskie spektry Sovetskogo Souza. In: Vasilchenko IT (ed) Istoriya flory I rastitelnosti Evrazii. Nauka Press, Leningrad, pp 17–40 (in Russian)

    Google Scholar 

  • Mantel NA (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Mazurenko MT, Hohryakov AP (1991) Ericaceae Juss. In: Harkevich SS (ed) Sosudistye rasteniya sovetskogo Dalnego Vostoka. Nauka Press, St. Petersburg, pp 119–166 (in Russian)

    Google Scholar 

  • Mingyuan F, Ruizheng F, Mingyou H, Linzhen H, Hanbi Y, Chamberlain DF (2005) Rhododendron. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol. 14. Science Press, Beijing, pp 260–455

    Google Scholar 

  • National Museum of Nature and Science (2014) Database of National Museum of Nature and Science. Tokyo, Japan. Available at: http://science-net.kahaku.go.jp/specimen_en/collection/. Accessed 17 May 2017

  • Palme AE, Semerikov V, Lascoux M (2003) Absence of geographical structure of chloroplast DNA variation in sallow, Salix caprea L. Heredity 91:465–474. https://doi.org/10.1038/sj.hdy.6800307

    Article  PubMed  CAS  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palme A, Martın JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspot but not melting pots of genetic diversity. Science 300:1563–1565. https://doi.org/10.1126/science.1083264

    Article  PubMed  CAS  Google Scholar 

  • Pimenova EA (2016) Sosudistye rasteniya. In: Pimenova EA (ed) Rasteniya, griby i lishainiki Sihote-Alinskogo zapovednika. Dalnuka Press, Vladivostok, pp 172–355 (in Russian)

    Google Scholar 

  • Polezhaeva MA, Lascoux M, Semerikov VL (2010) Cytoplasmic DNA variation and biogeography of Larix Mill. in Northeast Asia. Molec Ecol 19:1239–1252. https://doi.org/10.1111/j.1365-294X.2010.04552.x

    Article  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    PubMed  PubMed Central  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Model test: testing the model of DNA substitution. Bioinformatics 14:817–818. https://doi.org/10.1093/bioinformatics/14.9.817

    Article  PubMed  CAS  Google Scholar 

  • Poyarkova AI (1952) Rod Rhododendron L. In: Shishkin BK, Bobrov EG (eds) Flora SSSR, vol. 18. AN SSSR Press, Moscow, pp 31–60 (in Russian)

    Google Scholar 

  • Probatova NS, Seledets VP (1999) Sosudistye rasteniya v kontaktnoy zone “continent-okean”. Vestn Dal’nevost Otd Russk Akad Nauk 3:80–92 (in Russian)

    Google Scholar 

  • Prost S, Guralnick RP, Waltari E, Fedorov VB, Kuzmina E, Smirnov N, Kolfschoten T, Hofreiter M, Vrieling K (2013) Losing ground: past history and future fate of Arctic small mammals in a changing climate. Global Change Biol 19:1854–1864. https://doi.org/10.1111/gcb.12157

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molec Biol Evol 9:552–569. https://doi.org/10.1093/oxfordjournals.molbev.a040727

    PubMed  CAS  Article  Google Scholar 

  • Rohlf FJ (1988) Numerical taxonomy and multivariate analysis system. Exeter Publishing, New York

    Google Scholar 

  • Semenyuk NB (1976) Ob areale i vidovyh otlichiyah Rhododendron ledebourii Pojark. Nauka Press, Moscow (in Russian)

    Google Scholar 

  • Semerikov VL, Semerikova SA, Polezhaeva MA, Kosintsev PA, Lascoux M (2013) Southern montane populations did not contribute to the recolonization of West Siberian Plain by Siberian larch (Larix sibirica): a range wide analysis of cytoplasmic markers. Molec Ecol 22:4958–4971. https://doi.org/10.1111/mec.12433

    Article  CAS  Google Scholar 

  • Semerikova SA, Semerikov VL, Lascoux M (2011) Post-glacial history and introgression in Abies (Pinaceae) species of the Russian Far East inferred from both nuclear and cytoplasmic markers. J Biogeogr 38:326–340. https://doi.org/10.1111/j.1365-2699.2010.02394.x

    Article  Google Scholar 

  • Taberlet PT, Geilly L, Patou G, Bouvet J (1991) Universal primers for amplification of three noncoding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152

    Article  CAS  Google Scholar 

  • Takahashi H (2015) An enumeration of the vascular plants of Hokkaido. The Hokkaido University Museum Press, Sapporo

    Google Scholar 

  • Tarasov PE, Volkova OV, Webb T, Andreev AA, Bezusko LG, Bezusko TV, Bykova GV, Dorofeyuk NI, Kvavadze EV, Osipova IM, Panova NK, Sevastyanov DV (2000) Last glacial maximum biomes reconstructed from pollen and plant macrofossil data from northern Eurasia. J Biogeogr 27:609–620. https://doi.org/10.1046/j.1365-2699.2000.00429.x

    Article  Google Scholar 

  • Tikhonova NA, Polezhaeva MA, Pimenova EA (2012) AFLP analysis of the genetic diversity of closely related Rhododendron species of the section Rhodorastra (Ericaceae) from Siberia and the Far East of Russia. Russ J Genet 48:1153–1161. https://doi.org/10.1134/S1022795412100110

    Article  CAS  Google Scholar 

  • Tyulina LN (1954) Listvennichnye lesa severo-vostochnogo poberezhya Baikala I zapadnogo sklona Barguzinskogo hrebta. In: Lavrenko EM (ed) Trudy botanicheskogo instituta imeni V. L. Komarova, seria geobotanicheskaya, vol. 9. AN SSSR Press, Moscow, pp 150–209 (in Russian)

    Google Scholar 

  • Urgamal M, Oyuntsetseg B, Nyambayar D, Dulamsuren C (2014) Ericaceae. In: Sanchir C, Jamsran T (eds) Conspectus of the vascular plants of Mongolia. Admon Printing Press, Ulaanbaatar, pp 173–174

    Google Scholar 

  • Vipper VN (1962) Rhododendron dauricum v listvennichnyh I sosnovyh lesah yugo-vostochnoi chasti Buryatii. In: Zhukov AB (ed) Trydy instiuta lesa I drevesiny, vol. 54. AN SSSR Press, Moscow, pp 223–234 (in Russian)

    Google Scholar 

  • Vogelstein B, Gillespie D (1979) Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci USA 76:615–619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vologdina OS (2008) K ekologii tsveteniya daurskih rododendronov (Ericeceae). Sibirsk Ekol Zhur 2:353–358 (in Russian)

    Google Scholar 

  • Voroshilov VN (1982) Opredelitel rastenii sovetskogo Dalhego Vostoka. Nauka Press, Moscow (in Russian)

    Google Scholar 

  • Willis KJ, Van Andel TH (2004) Trees or not trees? The environments of central and eastern Europe during the Last Glaciation. Quatern Sci Rev 23:2269–2287. https://doi.org/10.1016/j.quascirev.2004.06.002

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to A. Berkutenko, A. Polezhaev, N. Badmayeva, I. Katz, S. Yalkovskii, D. Krivenko, E. Filippov, S. Kazanovskii, T.Polyakova, A. Belyaev, I. Tikhonova, I. Yamskikh, N. Molokova for the help with material collections. We also thank to Joyce Fingerut, director of NARGS Seed Exchange, for correction of the English grammar and two anonymous reviewers for helpful comments on the manuscript. The collection of samples (Altai and Sayan mountains) was supported by the State Contract of the Institute of Plant and Animal Ecology, UB RAS. The collection of samples (all other locations) and laboratory treatments were supported by the Russian Science Foundation for Basic Research (Project No. 15-04-01640).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria A. Polezhaeva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling editor: Pablo Vargas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 927 kb)

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Alignments of concatenated ptDNA sequences for 267 plants from 45 populations of Rhododendron dauricum s.l. that were used to produce Bayesian phylogenies with the Mr. Bayers 3.2.3. Each sequence composed of four ptDNA regions: part of trnT–trnF region with primers a, b (TabAB), and second part with primers c, d (TabCD) of Taberlet et al. (1991); the part of trnK–matK (matK) and psbC–trnS (CS) with primers according to Demesure et al. (1995).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Polezhaeva, M.A., Pimenova, E.A., Tikhonova, N.A. et al. Plastid DNA diversity and genetic divergence within Rhododendron dauricum s.l. (R. dauricum s.s., R. ledebourii, R. sichotense and R. mucronulatum; Ericaceae). Plant Syst Evol 304, 763–774 (2018). https://doi.org/10.1007/s00606-018-1508-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-018-1508-1

Keywords

  • Genetic diversity
  • Genetic structure
  • Glacial refugia
  • Northeast Asia
  • Phylogeography
  • Plastid DNA
  • Rhododendron dauricum s.l