Plant Systematics and Evolution

, Volume 304, Issue 6, pp 763–774 | Cite as

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

  • Maria A. PolezhaevaEmail author
  • Elena A. Pimenova
  • Natalia A. Tikhonova
  • Olga S. Korchagina
Original Article


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.


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



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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2018_1508_MOESM1_ESM.pdf (927 kb)
Supplementary material 1 (PDF 927 kb)


  1. Aleksandrova MS (1975) Rododendrony prirodnoi flory SSSR. Nauka Press, Moscow (in Russian)Google Scholar
  2. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molec Biol Evol 16:37–48. CrossRefPubMedGoogle Scholar
  3. 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
  4. 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
  5. 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. CrossRefGoogle Scholar
  6. 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
  7. Bruchmann I, Hobohm C (2014) Factors that create and increase endemism. In: Hobohm C (ed) Endemism in vascular plants. Springer, Dordrecht, pp 51–68CrossRefGoogle Scholar
  8. Chamberlain DF, Hyam R, Argent G, Fairweather G, Walter KS (1996) The genus Rhododendron—its classification and synonymy. Royal Botanical Garden of Edinburgh Press, EdinburghGoogle Scholar
  9. Chang CS, Kim H, Chang KS (2014) Provisional checklist of vascular plants for the Korea peninsula flora (KPF). Designpost Press, SeoulGoogle Scholar
  10. Cherepnin LM (1959) Flora yuzhnoi chasti Krasnoyarskogo kraya. KGPI Press, Krasnoyarsk (in Russian)Google Scholar
  11. 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. CrossRefGoogle Scholar
  12. 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. CrossRefPubMedGoogle Scholar
  13. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molec Ecol 11:2571–2581. CrossRefGoogle Scholar
  14. 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. CrossRefGoogle Scholar
  15. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  16. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. 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. CrossRefGoogle Scholar
  19. 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. CrossRefGoogle Scholar
  20. Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 40:393–412. CrossRefGoogle Scholar
  21. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. CrossRefPubMedGoogle Scholar
  22. Huelsenbeck JP, Ronquist F (2001) Mr Bayers: Bayesian inference of phylogeny. Bioinformatics 17:754–755. CrossRefPubMedGoogle Scholar
  23. Irving E, Hebda R (1993) Concerning the origin and distribution of rhododendrons. J Amer Rhododendron Soc 47:139–162Google Scholar
  24. 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. CrossRefGoogle Scholar
  25. Karpova EA, Karakulov AV (2011) Fenolnye soedineniya blizkorodstvennyh vidov roda Rhododendron L. (Ericaceae). Turczaninowia 14:145–149 (in Russian)Google Scholar
  26. 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
  27. Koksheeva I, Naryshkina N, Kislov D (2015) Seed morphology of Rhododendron sichotense (Ericaceae): systematic implications. Nordic J Bot 33:498–505. CrossRefGoogle Scholar
  28. Koropachinskii IY, Vstovskaya TN (2002) Drevesnye rasteniya aziatskoi Rossii. Publisher House of SB RAS, Novosibirsk (in Russian)Google Scholar
  29. 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
  30. Krasnoborov IM (1976) Vysokogornaya flora Zapadnogo Sayana. Nauka Press, Novosibirsk (in Russian)Google Scholar
  31. Kremenetski CV, Tarasov PE, Cherkinsky AE (1997) The Latest Pleistocene in southwestern Siberia and Kazakhstan. Quatern Int 41:125–134. CrossRefGoogle Scholar
  32. Kruklis MV, Milyutin LI (1977) Listvennitsa Chekanovskogo (Chekanovsky Larch). Nauka Press, Moscow (in Russian)Google Scholar
  33. 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
  34. 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. CrossRefGoogle Scholar
  35. 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. CrossRefGoogle Scholar
  36. 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
  37. Mantel NA (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  38. 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
  39. 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 260–455Google Scholar
  40. National Museum of Nature and Science (2014) Database of National Museum of Nature and Science. Tokyo, Japan. Available at: Accessed 17 May 2017
  41. Palme AE, Semerikov V, Lascoux M (2003) Absence of geographical structure of chloroplast DNA variation in sallow, Salix caprea L. Heredity 91:465–474. CrossRefPubMedGoogle Scholar
  42. 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. CrossRefPubMedGoogle Scholar
  43. 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
  44. Polezhaeva MA, Lascoux M, Semerikov VL (2010) Cytoplasmic DNA variation and biogeography of Larix Mill. in Northeast Asia. Molec Ecol 19:1239–1252. CrossRefGoogle Scholar
  45. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245PubMedPubMedCentralGoogle Scholar
  46. Posada D, Crandall KA (1998) Model test: testing the model of DNA substitution. Bioinformatics 14:817–818. CrossRefPubMedGoogle Scholar
  47. 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
  48. 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
  49. 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. CrossRefGoogle Scholar
  50. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molec Biol Evol 9:552–569. PubMedCrossRefGoogle Scholar
  51. Rohlf FJ (1988) Numerical taxonomy and multivariate analysis system. Exeter Publishing, New YorkGoogle Scholar
  52. Semenyuk NB (1976) Ob areale i vidovyh otlichiyah Rhododendron ledebourii Pojark. Nauka Press, Moscow (in Russian)Google Scholar
  53. 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. CrossRefGoogle Scholar
  54. 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. CrossRefGoogle Scholar
  55. 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. CrossRefGoogle Scholar
  56. Takahashi H (2015) An enumeration of the vascular plants of Hokkaido. The Hokkaido University Museum Press, SapporoGoogle Scholar
  57. 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. CrossRefGoogle Scholar
  58. 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. CrossRefGoogle Scholar
  59. 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
  60. 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 173–174Google Scholar
  61. 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
  62. Vogelstein B, Gillespie D (1979) Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci USA 76:615–619CrossRefPubMedPubMedCentralGoogle Scholar
  63. Vologdina OS (2008) K ekologii tsveteniya daurskih rododendronov (Ericeceae). Sibirsk Ekol Zhur 2:353–358 (in Russian)Google Scholar
  64. Voroshilov VN (1982) Opredelitel rastenii sovetskogo Dalhego Vostoka. Nauka Press, Moscow (in Russian)Google Scholar
  65. 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. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Maria A. Polezhaeva
    • 1
    Email author
  • Elena A. Pimenova
    • 2
  • Natalia A. Tikhonova
    • 3
  • Olga S. Korchagina
    • 1
  1. 1.Institute of Plant and Animal Ecology UB RASEkaterinburgRussian Federation
  2. 2.Botanical Garden-Institute FEB RASVladivostokRussian Federation
  3. 3.Sukachev Institute of Forest SB RASKrasnoyarskRussian Federation

Personalised recommendations