The Botanical Review

, Volume 84, Issue 1, pp 79–98 | Cite as

Comparative Flower and Inflorescence Organogenesis among Genera of Betulaceae: Implications for Phylogenetic Relationships

  • Junyi Zhu
  • Lifan Zhang
  • Baoqing Ren
  • Min Chen
  • Ruiqi Li
  • You Zhou
  • Yu Liang
  • Jianhua Li
  • Zhiduan Chen


Betulaceae have simple flowers but complex inflorescences. Recent phylogenetic analyses using molecular data have produced robust phylogenetic trees of Betulaceae. In this study, we evaluated the phylogenetic value of comparative organogenetic data of reproductive organs in the context of molecular phylogenies. Flower and inflorescence developmental processes of 21 species from all six genera in Betulaceae were documented with scanning electron microscopy. In each pistillate cyme, there are one primary bract, two secondary bracts, and two or three flowers in the six genera; only in Alnus are there two tertiary bracts on the abaxial side. The pistillate flower of all genera but Alnus has tepal primordia. Two tepals stop developing early on, resulting in the lack of tepals in mature flowers of Betula; while the tepals are initiated from a common circular primordium at the base of pistil in Corylus, Ostryopsis, Carpinus, and Ostrya, and the developed tepals with irregular shape and unstable number of lobes are adnate to the top of the pistil. In staminate organogenesis, each cyme has one primary bract and three flowers in all genera; two secondary bracts are only present in Alnus, Betula, and Corylus. Staminate flowers have no tepals except in Alnus and Betula, and exhibit high variation in number of stamens among genera. The number of secondary and tertiary bracts in each pistillate and staminate cyme, as well as the presence of tepals in pistillate and staminate flowers was clarified in all genera. Micro-morphological characters were used to infer the phylogenetic relationships of genera and sections of Betulaceae. Our analyses support the division of two subfamilies: Betuloideae (Alnus and Betula) and Coryloideae (Corylus, Carpinus, Ostrya, and Ostryopsis), and three tribes: Betuleae (Alnus and Betula), Coryleae (Corylus), and Carpineae (Carpinus, Ostrya, and Ostryopsis). The results agree with those from molecular phylogenetic studies, and suggest that micro-morphological characters are phylogenetically informative in Betulaceae, and reproductive organs of Betulaceae have evolved in the direction of reduction in bracts and tepals.


Betulaceae Flower Cyme Inflorescence Organogenesis Primordia Secondary bract Tertiary bract Tepals SEM Phylogeny 



We thank Dr. Limin Lu for her morphological analyses and Professor Peter K. Endress for his critical review, in particular suggestions on the usage of flower and inflorescence terms that help improve the manuscript. This study was supported by the National Natural Science Foundation of China (NNSF 31170180 and NNSF 31270268), Field work was partially supported by CAS International Research & Education Development Program (Grant No. SAJC201315), and MOST Science and Technology Basic Work (2013FY112100).

Literature Cited

  1. Abbe, E. C. 1935. Studies in the phylogeny of the Betulaceae. 1. Floral and inflorescence anatomy. Botanical Gazette 97: 1–67.Google Scholar
  2. ———. 1938. Studies in the phylogeny of the Betulaceae. II. Extremes in the variation of floral and inflorescence morphology. Botanical Gazette 99: 431–469.CrossRefGoogle Scholar
  3. ———. 1974. Flowers and inflorescences of the “Amentiferae”. Botanical Review 40: 159–261.CrossRefGoogle Scholar
  4. Angiosperm Phylogeny Group III (APG III). 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105–121.Google Scholar
  5. Angiosperm Phylogeny Group IV (APG IV). 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1–20.Google Scholar
  6. Behnke, H. D. 1973. Sieve-tube plastids of Hamamelididae. Taxon 22: 205–210.CrossRefGoogle Scholar
  7. Bentham, G. & J. D. Hooker. 1883. Cupuliferae. Genera Plantarum 3: 402–410.Google Scholar
  8. Bousquet, J., S. H. Strauss & P. Li. 1992. Complete congruence between morphological and rbcL-based on molecular phylogenies in birches and related species (Betulaceae). Molecular Biology and Evolution 9: 1076–1088.PubMedGoogle Scholar
  9. Brunner, F. & D. E. Fairbrothers. 1979. Serological investigations of the Corylaceae. Bulletin of the Torrey Botanical Club 106: 97–108.CrossRefGoogle Scholar
  10. Chen, Z. D. 1991. Pollen morphology of the Betulaceae. Acta Phytotaxonomica Sinica 29(6): 494–503.Google Scholar
  11. ———. 1994a. Phylogeny and phytogeography of the Betulaceae. Acta Phytotaxonomica Sinica 32: 1–31.Google Scholar
  12. ———. 1994b. Phylogeny and phytogeography of the Betulaceae (cont.). Acta Phytotaxonomica Sinica 32: 101–153.Google Scholar
  13. ———, A. M. Lu & K. Y. Pan. 1990. The embryology of the genus Ostryopsis (Betulaceae). Cathaya 2: 53–62.Google Scholar
  14. ———, S. R. Manchester & H. Y. Sun. 1999. Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology, and paleobotany. American Journal of Botany 86: 1168–1181.Google Scholar
  15. ———, S. P, Xing, H. X, Liang & A. M. Lu. 2001. Morphogenesis of pistillate reproductive organs in Carpinus turczaninowii and Ostryopsis davidiana (Betulaceae). Acta Botanica Sinica 43: 1110–1114.Google Scholar
  16. ———, & Z. Y. Zhang. 1991. A study on foliar epidermis in Betulaceae. Acta Phytotaxonomica Sinica 29(2): 156–163.Google Scholar
  17. Crane, P. R. 1981. Betulaceous leaves and fruits from the British Upper Palaeocene. Botanical Journal of Linnean Society 83: 103–136.CrossRefGoogle Scholar
  18. ———. 1989. Early fossil history and evolution of the Betulaceae. Pp. 87–116. In: Crane, P. R. & S. Blackmore (eds.), Evolution, systematics, and fossil history of the Hamamelidae. Vol. 2: “Higher” Hamamelidae. Clarendon Press, Oxford.Google Scholar
  19. ———, S. R. Manchester & D. L. Dilcher. 1990. A preliminary survey of fossil leaves and well–preserved reproductive structures from the Sentinel Butte Formation (Paleocene) near Almont, North Dakota. Field Geology 20: 1–63.Google Scholar
  20. ———, & R. A. Stockey, 1987. Betula leaves and reproductive structures from the Middle Eocene of British Columbia, Canada. Canadian Journal of Botany 65: 2490–2500.Google Scholar
  21. Dahlgren, R. 1975. A system of classification of the angiosperms to be used to demonstrate the distribution of characters. Botaniska Notiser 128: 119–147.Google Scholar
  22. ———. 1980. A revised system of classification of the angiosperms. Botanical Journal of Linnean Society, 80: 91124.CrossRefGoogle Scholar
  23. ———. 1983. General aspects of angiosperm evolution and macrosystematics. Nordic Journal of Botany 3: 119–149.CrossRefGoogle Scholar
  24. Endress, P. K. 2008. The whole and the parts: relationships between floral architecture and floral organ shape, and their repercussions on the interpretation of fragmentary floral fossils. Annals of the Missouri Botanical Garden 95: 101–120.CrossRefGoogle Scholar
  25. ———. 2010. Disentangling confusions in inflorescence morphology: Patterns and diversity of reproductive shoot ramification in angiosperms. Journal of Systematics and Evolution 48: 225–239.CrossRefGoogle Scholar
  26. ———, & E. M. Friis. 2006. Rosids-Reproductive structures, fossil and extant, and their bearing on deep relationships: Introduction. Plant Systematics and Evolution 260: 83–85.Google Scholar
  27. ———, & M. L. Matthews. 2006. First steps towards a floral structural characterization of the major rosid subclades. Plant Systematics and Evolution 260: 223–251.Google Scholar
  28. ———, & S. Stumpf. 1991. The diversity of stamen structures in “Lower” Rosidae ( Rosales, Fagales, Proteales, Sapindales). Botanical Journal of the Linnean Society 107: 217–293.Google Scholar
  29. Forest, F., V. Savolainen, M. W. Chase, R. Lupia, A. Bruneau & P. R. Crane. 2005. Teasing apart molecular-versus fossil-based error estimates when dating phylogenetic tree: a case study in the birch family (Betulaceae). Systematic Botany 30(1): 118–133.Google Scholar
  30. Furlow, J. J. 1979. The systematics of American species of Alnus (Betulaceae). Rhodora 81: 151–248. 1–121.Google Scholar
  31. ———. 1983. The phylogenetic relationships of the genera and infrageneric taxa of the Betulaceae (Abstract). American Journal of Botany 70 (Suppl.): 114.Google Scholar
  32. ———. 1990. The genera of Betulaceae in the southeastern United States. Journal of the Arnold Arboretum 71(1): 1–67.CrossRefGoogle Scholar
  33. Govaerts, R. & D. G. Frodin. 1998. World checklist and bibliography of Fagales. Royal Botanical Gardens, Kew. 17–35.Google Scholar
  34. Grimm, G. W. & S. S. Renner. 2013. Harvesting Betulaceae sequences from GenBank to generate a new chronogram for the family. Botanical Journal of the Linnean Society 172: 465–477.CrossRefGoogle Scholar
  35. Hall, J. W. 1952. The comparative anatomy and phylogeny of Betulaceae. Botanical Gazette 113: 235–270.CrossRefGoogle Scholar
  36. Hardin, J. W. & J. M. Bell. 1986. Atlas of foliar surface features in woody plants, IX. Betulaceae of eastern United States. Brittonia 38: 133–144.Google Scholar
  37. Hjelmqvist, H. 1948. Studies on the floral morphology and phylogeny of the Amentiferae. Botaniska Notiser Suppl. 2: 1–171.Google Scholar
  38. ———. 1957. Some notes on the endosperm and embryo development in Fagales and related orders. Botaniska Notiser 110: 173–195.Google Scholar
  39. ———. 1960. Notes on some names and combinations within the Amentiferae. Botaniska Notiser 113: 373–380.Google Scholar
  40. Hutchinson, J. 1967. The genera of flowering plants. Vol. 2. Oxford, England.Google Scholar
  41. ———. 1973. The families of flowering plants arranged according to a new system based on their probable phylogeny. Ed. 3. Oxford, England.Google Scholar
  42. Jury, S. 1978. Betulaceae. Flowering plants of the world. Oxford University Press, Oxford.Google Scholar
  43. Jussieu, A. L. D. 1789. Genera Plantarum. Apud Viduam Herissant, Paris. 407–411.Google Scholar
  44. Kato, H., K. Oginuma, Z. J. Gu, B. Hammel & H. Tobe. 1999. Phylogenetic relationships of Betulaceae based on matK sequences with particular reference to the position of Ostryopsis. Acta Phytotaxonomica et Geobotanica 49: 89–97.Google Scholar
  45. Kikuzawa, K. 1982. Leaf survival and evolution in Betulaceae. Annals of Botany 50: 345–354.CrossRefGoogle Scholar
  46. Koehne, E. 1893. Betulaceae. Deutsche Dendrologie. Verlag von Ferdinand Enke, Stuttgart. 106–120. Google Scholar
  47. Kuprianova, L. A. 1963. On a hitherto undescribed family belonging to the Amentiferae. Taxon 12: 12–13.CrossRefGoogle Scholar
  48. Laroche, J. & J. Bousquet. 1999. Evolution of the mitochondrial rps3 intron in perennial and annual angiosperms and homology to nad5 intron 1. Molecular Evolution and Biology 16(4): 441–452.Google Scholar
  49. Li, H. L. 1976. Betulaceae. Flora of Taiwan 2: 41–48.Google Scholar
  50. Li, H. L., W. Wang, P. E. Mortimer, R. Q. Li, D. Z. Li, K. D. Hyde, J. C. Xu, D. E. Soltis & Z. D. Chen. 2015. Large-scale phylogenetic analyses reveal multiple gains of actinorhizal nitrogen-fixing symbioses in angiosperms associated with climate change. Scientific Reports 5: 14023.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Li, J. H. 2008. Sequences of low–copy nuclear gene support the monophyly of Ostrya and paraphyly of Carpinus (Betulaceae). Journal of Systematics and Evolution 46: 333–340.Google Scholar
  52. Li, P. C. & S. X. Cheng. 1979. Betulaceae. In: Kuang, K. Z. & P. C. Li (eds.), Flora Republicae Popularis Sinicae 21: 44–137. Science Press, Beijing.Google Scholar
  53. ——— & A. K. Skvortsov. 1999. Betulaceae. In: Wu, Z. Y. & P. H. Raven (eds.), Flora of China 4: 286–313. Science Press, Beijing; Missouri Botanical Garden Press, St. Louis.Google Scholar
  54. Li, R. Q., Z. D. Chen, A. M. Lu, D. E. Soltis, P. S. Soltis & P. S. Manos. 2004. Phylogenetic relationships in Fagales based on DNA sequences from three genomes. International Journal of Plant Sciences 165: 311–324.CrossRefGoogle Scholar
  55. Lin, R. Z., J. Zeng & Z. D. Chen. 2010. Organogenesis of reproductive structures in Betula alnoides (Betulaceae). International Journal of Plant Sciences 171: 586–594.CrossRefGoogle Scholar
  56. Ma, H., J. Lu, B. B. Liu, B. B. Duan, X. D. He & J. Q. Liu. 2015. Phylotranscriptomic analyses in plants using Betulaceae as an example. Journal of Systematics and Evolution 53: 403–410.CrossRefGoogle Scholar
  57. Maggia, L. & J. Bousquet. 1994. Molecular phylogeny of the actinorhizal Hamamelidae and relationships with host promiscuity towards Frankia. Molecular Ecology 3: 459–467.CrossRefGoogle Scholar
  58. Manchester, S. R. & Z. D. Chen. 1996. Palaeocarpinus aspinosa sp. nov. (Betulaceae) from the Paleocene of Wyoming, USA. International Journal of Plant Sciences 157: 644–655.CrossRefGoogle Scholar
  59. ———, & Z. D. Chen. 1998. A new genus of Coryloideae (Betulaceae) from the Paleocene of North America. International Journal of Plant Sciences 159: 522–532.Google Scholar
  60. ———, & P. R. Crane. 1987. A new genus of Betulaceae from the Oligocene of western North America. Botanical Gazette 148: 263–273.Google Scholar
  61. ———, K. B. Pigg & P. R. Crane. 2004. Palaeocarpinus dakotensis sp. n. (Betulaceae: Coryloideae) and associated staminate catkins, pollen, and leaves from the Paleocene of North Dakota. International Journal of Plant Sciences 165: 1135–1148.Google Scholar
  62. Manos, P. S. 1997. Systematics of Nothofagus (Nothofagaceae) based on rDNA spacer sequences (ITS): taxonomic congruence with morphology and plastid sequences. American Journal of Botany 84: 1137–1137.CrossRefPubMedGoogle Scholar
  63. ———, & K. P. Steele. 1997. Phylogenetic analyses of “higher” Hamamelididae based on plastid sequence data. American Journal of Botany 84: 1407–1407.Google Scholar
  64. ———, Z. K. Zhou & C. H. Cannon. 2001. Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. International Journal of Plant Sciences 162: 1361–1379.Google Scholar
  65. Melchior, H. 1964. Betulaceae. Pp. 47–49. In: Melchior, H. (ed.), A. Engler’s Syllabus der Pflanzenfamilien. Vol. 2. Ed. 12. Gebrüder Borntraeger, Berlin.Google Scholar
  66. Pigg, K. B., S. R. Manchester & W. C. Wehr. 2003. Corylus, Carpinus, and Palaeocarpinus (Betulaceae) from the middle Eocene Klondike Mountain and Allenby formations of northwestern North America. International Journal of Plant Sciences 164: 807–882.CrossRefGoogle Scholar
  67. Prantl, K. 1894. Betulaceae. In: Engler, A. & K. Prantl (eds.), Die Natürlichen Pflanzenfamilien 3(1): 38–46. Engelmann, Leipzig.Google Scholar
  68. Qiu, Y. L., M. W. Chase, S. B. Hoot, F. Conti, P. R. Crane, K. J. Sytsma & C. R. Parks. 1998. Phylogenetics of the Hamamelidae and their allies: parsimony analyses of nucleotide sequences of the plastid gene rbcL. International Journal of Plant Sciences 159: 891–905.CrossRefGoogle Scholar
  69. Regel, E. 1861. Monographische Bearbeitung der Betulaceen. Nouveaux Mémoires de la Société Impériale des Naturalistes de Moscou 13(2): 59–187.Google Scholar
  70. ———. 1868. Betulaceae. In: de Candolle A. & C. de Candolle (eds.), Prodromous Systematis Naturalis Regni Vegetabilis Sumptibus Victoris Masson et Filii, Paris. 16: 181–189. Google Scholar
  71. Rehder, A. 1940. Manual of cultivated trees and shrubs. Ed. 2. The Macmillan Company, New York. Corylaceae, 124–126.Google Scholar
  72. Rendle, A. B. 1925. The classification of flowering plants. Vol. 2. Cambridge University Press, Cambridge. 23–30.Google Scholar
  73. Savard, L., M. Michaud & J. Bousquet. 1993. Genetic diversity and phylogenetic relationships between birches and alders using ITS, 18S rRNA, and rbcL gene sequences. Molecular Phylogenetics and Evolution 2: 112–118.Google Scholar
  74. Spach, A. E. 1841. Revisio Betulacearum. Annales des Sciences Naturelles, ser. 215: 182–212.Google Scholar
  75. Soltis, D. E., P. S. Soltis, D. R. Morgan, S. M. Swensen, B. C. Mullin, J. M. Dowd & P. G. Martin. 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences USA 92: 2647–2651.Google Scholar
  76. Sun, F. & R. A. Stockey. 1992. A new species of Palaeocarpinus (Betulaceae) based on infructescences, fruits, and associated staminate inflorescences and leaves from the Paleocene of Alberta, Canada. International Journal of Plant Sciences 153: 136–146.Google Scholar
  77. Takhtajan, A. 1969. Flowering plants: Origin and dispersal. Oliver & Boyd, Edinburgh. Google Scholar
  78. ———. 1980. Outline of the classification of flowering plants (Magnoliophyta). Botanical Review 46: 225–359.CrossRefGoogle Scholar
  79. Thorne, R. F. 1973. The Amentiferae or Hamamelidae as an artificial group: a summary statement. Brittonia 25: 395–405.CrossRefGoogle Scholar
  80. ———. 1983. Proposed new realignments in the angiosperms. Nordic Journal of Botany 3: 85–117.CrossRefGoogle Scholar
  81. Werner, G. D. A., W. K. Cornwell, J. I. Sprent, J. Kattge & E. T. Kiers. 2014. A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nature Communication 5: 4087.CrossRefGoogle Scholar
  82. Winkler, H. 1904. Betulaceae. In: Engler, A. (ed.), Das Pflanzenreich 19 (IV. 6.): 1–149. Engelmann, Leipzig.Google Scholar
  83. Yoo, K. O. & J. Wen. 2007. Phylogeny of Carpinus and subfamily Coryloideae (Betulaceae) based on chloroplast and nuclear ribosomal sequence data. Plant Systematics and Evolution 267: 25–35.CrossRefGoogle Scholar
  84. Zhang, L. F., J. Y. Zhu, P. Shen, B. Q. Ren & Y. Liang. 2013. The organogenesis of inflorescence and flower of Corylus heterophylla and C. avellana. Journal of Tonghua Normal University (Natural Science) 34(12): 61–63.Google Scholar
  85. Zhu, J. Y. & J. M. Lu. 2008. Morphogenesis of inflorescence and floret in Alnus (Betulaceae). Journal of Systematics and Evolution 46: 641–650.Google Scholar
  86. ———, L. F. Zhang, P. Shen, B. Q. Ren, Y. Liang & Z. D. Chen. 2014a. The morphogenesis of inflorescence and flower in Corylus (Betulaceae). Plant Diversity and Resources 36(4): 433–442.Google Scholar
  87. ———, L. F. Zhang, P. Shen, B. Q. Ren, Y. Liang & Z. D. Chen. 2014b. Wind pollination characteristics of styles in Betulaceae. Chinese Bulletin of Botany 49(5): 524–538.Google Scholar
  88. ———, L. F. Zhang, P. Shen, B. Q. Ren, Y. Liang & Z. D. Chen. 2014c. Inflorescence and floral organ development in Carpinus cordata. Bulletin of Botanical Research 34(2): 170–176.Google Scholar
  89. Swofford, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Ver. 4. Sinauer Associates, Sunderland, MA.Google Scholar

Copyright information

© The New York Botanical Garden 2017

Authors and Affiliations

  1. 1.College of Life ScienceTonghua Normal UniversityTonghuaChina
  2. 2.Constructional and Preparation Office of Taiyuan Taishan Botanical GardenTaiyuanChina
  3. 3.State Key Laboratory of Systematic and Evolutionary Botany, Institute of BotanyChinese Academy of SciencesBeijingChina
  4. 4.Biology DepartmentHope CollegeHollandUSA

Personalised recommendations