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Pollen morphology in Rubus (Rosaceae) and its taxonomic implications

  • Xian-Hua Xiong
  • Xin-Mao Zhou
  • Meng Li
  • Bo Xu
  • Heng-Ning Deng
  • Qi Yu
  • Xin-Fen GaoEmail author
Original Article
  • 23 Downloads

Abstract

Rubus is one of the most species-rich and most taxonomically challenging genera in Rosaceae. Pollen morphology of Rubus species has been described by many researchers but never in a comprehensive study. In this study, pollen morphology of 155 species and 13 varieties representing all 12 subgenera of Rubus was examined using scanning electron microscope to investigate whether pollen characters can help elucidate the challenging taxonomy in this genus. The results showed that the pollen grains of studied Rubus species are tricolporate, and pollen shape varies from suboblate, spheroidal, subprolate and prolate to perprolate. Exine ornamentation of examined pollen grains can be divided into six types and three subtypes. The pollen cluster analysis tree, which was performed using nine pollen characters, does not agree well with the traditional macromorphological classification and molecular phylogenetic trees based on DNA fragments. Except for subg. Chamaemorus and subg. Comaropsis, pollen morphology seems difficult to distinguish at subgeneric or sectional level, and consequently it lacks significant taxonomic value at these levels. Pollen morphology may not be considered a diagnostic feature for the division of subgenera and sections in Rubus. Though pollen morphology alone is not sufficient to elucidate or reconstruct the taxonomic relationships within Rubus, it can provide some useful information for the taxonomic treatment at specific level.

Keywords

Palynology Rosaceae Rubus SEM Taxonomy 

Notes

Acknowledgements

This work was funded by the National Natural Science Foundation of China (Grant No. 31670192) and China Science and Technology Basic Work (Grant No. 2013FY112100). We are grateful to Tian-Fang Huang (CDBI) for technical assistance with SEM, to Li-Bing Zhang (MO), Bao-Cai Han (PE) and herbaria KUN, MO and PE for providing some pollen materials, to the anonymous reviewers and the editor for the valuable comments and suggestions on the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2019_1600_MOESM1_ESM.pdf (152 kb)
Supplementary material 1 (PDF 151 kb)
606_2019_1600_MOESM2_ESM.pdf (253.6 mb)
Supplementary material 2 (PDF 259734 kb)

References

  1. Aalders LE, Hall IV (1966) A cytotaxonomic survey of the native blackberries of Nova Scotia. Canad J Genet Cytol 8:528–532.  https://doi.org/10.1139/g66-063 CrossRefGoogle Scholar
  2. Alice LA, Campbell CS (1999) Phylogeny of Rubus (rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Amer J Bot 86:81–97.  https://doi.org/10.2307/2656957 CrossRefGoogle Scholar
  3. Alice LA, Dodson TM, Sutherland BL (2008) Diversity and relationships of Bhutanese Rubus. Acta Hort 777:63–69.  https://doi.org/10.17660/ActaHortic.2008.777.5 CrossRefGoogle Scholar
  4. Alice LA, Goldman DH, Macklin JA, Moore G (2014) Rubus. In: Flora of North America Editorial Committee (ed) Flora of North America north of Mexico, vol. 9. Oxford University Press, New York, pp 28–56Google Scholar
  5. Asok G, Ishita S (2017) Pollen morphological study of some selected Indian taxa of Rosaceae. Indian J Appl Pure Biol 32:121–130Google Scholar
  6. Bailey LH (1941–1945) Rubus in North America. Gentes Herbarum 5:1–932Google Scholar
  7. Chen SF, Ye JX, Zhu XL, Yu YF (1996) Pollen morphology of some Rubus species. Bull Bot Res 16:463–469Google Scholar
  8. Eide F (1981a) Key for northwest European rosaceae pollen. Grana 20:101–118.  https://doi.org/10.1080/00173138109427651 CrossRefGoogle Scholar
  9. Eide F (1981b) On the pollen morphology of Rubus chamaemorus L. (Rosaceae). Grana 20:25–27.  https://doi.org/10.1080/00173138109436733 CrossRefGoogle Scholar
  10. Erdtman G (1952) Pollen morphology and plant taxonomy. Angiosperms. Almqvist and Wiksell, StockholmGoogle Scholar
  11. Erdtman G (1969) Handbook of palynology—an introduction to the study of pollen grains and spores. Munksgaard, CopenhagenGoogle Scholar
  12. Fischer HE, Darrow GM, Perlmutter F (1943) Raspberry and blackberry breeding: production of tetraploid raspberries. Proc Amer Soc Hort Sci 42:447–456Google Scholar
  13. Focke WO (1910) Species Ruborum monographiae generis Rubi prodromus, Pars I. Biblioth Bot 17:1–120Google Scholar
  14. Focke WO (1911) Species Ruborum, Monographiae generis Rubi Prodromus, Pars II. Biblioth Bot 17:121–223Google Scholar
  15. Focke WO (1914) Species Ruborum, Monographiae generis Rubi Prodromus, Pars III. Biblioth Bot 19:224–498Google Scholar
  16. Gonzalez-Romano ML, Candau P (1989) Contribution to palynological studies in the Rosaceae. Acta Bot Malac 14:105–116Google Scholar
  17. Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–871.  https://doi.org/10.2307/2528823 CrossRefGoogle Scholar
  18. Gustafsson A (1943) The genesis of the European blackberry flora. Lunds Univ Arsskr 39:1–200Google Scholar
  19. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:1–9Google Scholar
  20. Hebda RJ, Chinnappa CC (1990) Studies on pollen morphology of Rosaceae in Canada. Rev Palaeobot Palynol 64:103–108.  https://doi.org/10.1016/0034-6667(90)90123-Z CrossRefGoogle Scholar
  21. Hebda RJ, Chinnappa CC (1994) Studies on pollen morphology of Rosaceae. Acta Bot Gallica 141:183–193.  https://doi.org/10.1080/12538078.1994.10515150 CrossRefGoogle Scholar
  22. Heslop-Harrison Y (1968) Rubus. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol. 2. Cambridge University Press, Cambridge, pp 7–25Google Scholar
  23. Huber H (1961) Rubus. In: Hegi G (ed) Illustrierte Flora von Mittel-Europa 4 (2A). Carl Hanser Verlag, Munchen, pp 274–411Google Scholar
  24. Jibran R, Dzierzon H, Bassil N, Bushakra JM, Edger PP, Sullivan S, Finn CE, Dossett M, Vining KJ, VanBuren R, Mockler TC, Liachko I, Davies KM, Foster TM, Chagne D (2018) Chromosome-scale scaffolding of the black raspberry (Rubus occidentalis L.) genome based on chromatin interaction data. Hort Res 5:1–11.  https://doi.org/10.1038/s41438-017-0013-y CrossRefGoogle Scholar
  25. Kalkman C (1987) The genus Rubus (Rosaceae) in Malesia 3. The subgenus Micranthobatus. Blumea 32:323–341Google Scholar
  26. Kosenko VN, Hiep NT, Yakovlev GP (1983) Palynomorphological study of the representatives of the genus Rubus (Rosaceae) in the flora of Viet-nam. Bot Zhur (St. Petersburg) 69:497–503Google Scholar
  27. Li WL, He SA, Chao WJ (2000) The geographical distribution and pollen morphology of the genus Rubus L. in Qinling Bashan mountain region. Bull Bot Res 20:221–230Google Scholar
  28. Li WL, He SA, Gu Y, Shu P, Pu ZM (2001) Pollen morphology of the genus Rubus from China. Acta Phytotax Sin 39:234–247Google Scholar
  29. Lu LT (1983) A study on the genus Rubus of China. Acta Phytotax Sin 21:13–25Google Scholar
  30. Lu LT, Boufford DE (2003) Rubus. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol. 9. Science Press, Beijing, pp 195–285Google Scholar
  31. Lu LT, Yu TT (1985) Rubus. In: Yu TT (ed) Flora Reipublicae Popularis Sinicae, vol. 37. Science Press, Beijing, pp 10–218Google Scholar
  32. Monasterio-Huelin E (1995) Taxonomy and distribution of the genus Rubus (Rosaceae) series Radula on the Iberian Peninsula. Nordic J Bot 15:365–373.  https://doi.org/10.1111/j.1756-1051.1995.tb00164.x CrossRefGoogle Scholar
  33. Monasterio-Huelin E, Pardo C (1995) Pollen morphology and wall stratification in Rubus L. (Rosaceae) in the Iberian Peninsula. Grana 34:229–236.  https://doi.org/10.1080/00173139509429050 CrossRefGoogle Scholar
  34. Perveen A, Qaiser M (2014) Pollen flora of Pakistan–LXXI. Rosaceae. Pakistan J Bot 46:1027–1037Google Scholar
  35. Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Pl Syst Evol 266:5–43.  https://doi.org/10.1007/s00606-007-0539-9 CrossRefGoogle Scholar
  36. Premathilake R, Epitawatta S, Nilsson S (1999) Pollen morphology of some selected plant species from Horton Plains, Sri Lanka. Grana 38:289–295.  https://doi.org/10.1080/001731300750044500 CrossRefGoogle Scholar
  37. Punt W, Hoen PP, Blackmore S, Nilsson S, Thomas AL (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143:1–81.  https://doi.org/10.1016/j.revpalbo.2006.06.008 CrossRefGoogle Scholar
  38. Reitsma TJ (1966) Pollen morphology of some European Rosaceae. Acta Bot Neerl 15:290–307.  https://doi.org/10.1111/j.1438-8677.1966.tb00234.x CrossRefGoogle Scholar
  39. Richards AJ, Kirschner J, Stepanek J, Marhold K (1996) Apomixis and taxonomy: an introduction. Folia Geobot Phytotaxon 31:281–282.  https://doi.org/10.1007/BF02815372 CrossRefGoogle Scholar
  40. Robertson KR (1974) The genera of Rosaceae in the southeastern United States. J Arnold Arbor 55:352–360Google Scholar
  41. Shi W, Wen J, Lutz S (2013) Pollen morphology of the Maddenia clade of Prunus and its taxonomic and phylogenetic implications. J Syst Evol 51:164–183.  https://doi.org/10.1111/j.1759-6831.2012.00233.x CrossRefGoogle Scholar
  42. Song JH, Moon HK, Hong SP (2016) Pollen morphology of the tribe Sorbarieae (Rosaceae). Pl Syst Evol 302:853–869.  https://doi.org/10.1007/s00606-016-1303-9 CrossRefGoogle Scholar
  43. Thiers B (2019) Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden, Bronx. Available at: http://sweetgum.nybg.org/science/ih/. Accessed 15 Feb 2019
  44. Thompson MM (1995) Chromosome numbers of Rubus species at the national clonal germplasm repository. HortScience 30:1447–1452CrossRefGoogle Scholar
  45. Tomlik-Wyremblewska A (1995) Pollen morphology of the genus Rubus L. I: introductory studies on the european representatives of the subgenus Rubus L. Acta Soc Bot Poloniae 64:187–203.  https://doi.org/10.5586/asbp.1995.027 CrossRefGoogle Scholar
  46. Tomlik-Wyremblewska A (2000) Pollen morphology of genus Rubus L. Part II: introductory studies on the Malesian species of subgenus Micranthobatus. Acta Soc Bot Poloniae 69:31–40.  https://doi.org/10.5586/asbp.2000.005 CrossRefGoogle Scholar
  47. Tomlik-Wyremblewska A, Ham RWJM, Kosinski P (2004) Pollen morphology of genus Rubus L. Part III: studies on the Malesian species of subgenera Chamaebatus L. and Idaeobatus L. Acta Soc Bot Pol 73:207–227.  https://doi.org/10.5586/asbp.2004.028 CrossRefGoogle Scholar
  48. Ueda Y (1992) Pollen surface morphology in the genus Rosa and related genera. Jap J Palynol 38:94–105Google Scholar
  49. Ueda Y, Tomita H (1989) Morphometric analysis of pollen exine patterns in roses. J Jap Soc Hort Sci 58:211–220CrossRefGoogle Scholar
  50. VanBuren R, Bryant D, Bushakra JM, Vining KJ, Edger PP, Rowley ER, Priest HD, Michael TP, Lyons E, Filichkin SA, Dossett M, Finn CE, Bassil NV, Mockler TC (2016) The genome of black raspberry (Rubus occidentalis). Pl J 87:535–547.  https://doi.org/10.1111/tpj.13215 CrossRefGoogle Scholar
  51. VanBuren R, Wai CM, Colle M, Wang J, Sullivan S, Bushakra JM, Liachko I, Vining KJ, Dossett M, Finn CE, Jibran R, Chagne D, Childs K, Edger PP, Mockler TC, Bassil NV (2018) A near complete chromosome-scale assembly of the black raspberry (Rubus occidentalis) genome. GigaScience 7:1–9.  https://doi.org/10.1093/gigascience/giy094 CrossRefGoogle Scholar
  52. Wang YN (2011) Relationships among Rubus (Rosaceae) species used in traditional Chinese medicine. MSc Thesis, Western Kentucky University, KentuckyGoogle Scholar
  53. Wang Y, Chen Q, Chen T, Tang HR, Liu L, Wang XR (2016) Phylogenetic insights into Chinese Rubus (Rosaceae) from multiple chloroplast and nuclear DNAs. Frontiers Pl Sci 7:1–13.  https://doi.org/10.3389/fpls.2016.00968 Google Scholar
  54. Waugh R, Ven WTG, Phillips MS, Powell W (1990) Chloroplast DNA diversity in the genus Rubus (Rosaceae) revealed by Southern hybridization. Pl Syst Evol 172:65–75.  https://doi.org/10.1007/BF00937798 CrossRefGoogle Scholar
  55. Weber HE (1995) Rubus. In: Hegi G (ed) Illustrierte flora von Mittel-Europa 4(2A), 3rd edn. Blackwell Wissenschafts-Verlag, Berlin, pp 284–595Google Scholar
  56. Weber HE (1996) Former and modern taxonomic treatment of the apomictic Rubus complex. Folia Geobot Phytotaxon 31:373–380.  https://doi.org/10.1007/BF02815381 CrossRefGoogle Scholar
  57. Wronska-Pilarek D, Malinski T, Lira J (2006) Pollen morphology of Polish species of genus Rubus—Part I. Rubus gracilis. Dendrobiology 56:69–77Google Scholar
  58. Wronska-Pilarek D, Jagodzinski AM, Malinski T (2012) Morphological studies of pollen grains of the Polish endemic species of the genus Rubus (Rosaceae). Biologia 67:87–96.  https://doi.org/10.2478/s11756-011-0141-z CrossRefGoogle Scholar
  59. Xiang Y, Huang CH, Hu Y, Wen J, Li S, Yi T, Chen H, Xiang J, Ma H (2017) Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Molec Biol Evol 34:262–281.  https://doi.org/10.1093/molbev/msw242 Google Scholar
  60. Yang JY, Pak JH (2006) Phylogeny of Korean Rubus (Rosaceae) based on ITS (nrDNA) and trnL/F intergenic region (cpDNA). J Pl Biol 49:44–54.  https://doi.org/10.1007/BF03030787 CrossRefGoogle Scholar
  61. Zhou LH, Wei ZX, Wu ZY (1999) Pollen morphology of Rosoideae (Rosaceae) of China. Acta Bot Yunnan 21:455–460Google Scholar
  62. Zych CC, Otterbracher AG, Chu MC (1968) Pollen pore number and polyploidy in Rubus. Trans Illinois Acad Sci 61:421–424Google Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Chengdu Institute of Biology, Chinese Academy of SciencesChengduChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.School of Ecology and Environmental ScienceYunnan UniversityKunmingChina
  4. 4.Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the EnvironmentNanjing Forestry UniversityNanjingChina

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