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

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Abstract

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.

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Acknowledgments

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).

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Authors and Affiliations

  1. College of Life Science, Tonghua Normal University, Tonghua, 134002, China

    Junyi Zhu, Lifan Zhang, You Zhou, Yu Liang & Jianhua Li

  2. Constructional and Preparation Office of Taiyuan Taishan Botanical Garden, Taiyuan, 030025, China

    Baoqing Ren

  3. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 10093, China

    Min Chen, Ruiqi Li & Zhiduan Chen

  4. Biology Department, Hope College, Holland, MI, 49423, USA

    Jianhua Li

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  1. Junyi Zhu
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Correspondence to Junyi Zhu, Jianhua Li or Zhiduan Chen.

Appendices

Appendix 1

Morphological characters including floral developmental data used in phylogenetic analysis (Hall, 1952; Hjelmqvist, 1957, 1960; Hardin & Bell, 1986; Crane, 1989; Chen et al., 1990; Chen, 1991; Chen & Zhang, 1991; Manos, 1997; Manos et al., 2001; Chen et al., 1999; Chen et al., 2001; Zhu & Lu, 2008; Lin et al., 2010; Zhu et al., 2014a, b, c; and this study)

  1. 1.

    Inflorescence---bisexual (0), unisexual (1)

  2. 2.

    Female cyme---secondary bract laminar (0), leaf-shaped (1)

  3. 3.

    Female cyme---tertiary bract present (0), absent (1)

  4. 4.

    Female cyme---1 to 3 flowers (0), 1 or 2 flowers (1)

  5. 5.

    Female flower---pollen tube entering the stigma by papillae, absent (0), present (1)

  6. 6.

    Female flower--- pollen tube entering the stigma by stylar epidermal cells or intercellular spaces, present (0), absent (1)

  7. 7.

    Male cyme---secondary bracts 2 (0), none(1)

  8. 8.

    Male cyme---Tertiary bracts 2 (0), none (1)

  9. 9.

    Male flower---tepal present (0), absent (1)

  10. 10.

    Male flower—pistillode present (0), absent (1)

  11. 11.

    Male flower---thecae and filaments not or slightly divided longitudinally (0), thecae separated, filaments partly divided (1), thecae separated, filaments completely divided (2)

  12. 12.

    Wood---vessel perforations scalariform (0), simple (1)

  13. 13.

    Wood---vessel with spiral thickening absent (0), present (1)

  14. 14.

    Wood---tracheids present (0), absent (1)

  15. 15.

    Wood---rays heterocellular (0), homocellular (1)

  16. 16.

    Wood---tyloses absent (0), present (1)

  17. 17.

    Leaves---embedded glands present (0), absent (1)

  18. 18.

    Leaves---brachyparacytic stomatal apparatus absent (0), present (1)

  19. 19.

    Leaves—teeth absent (0), simple (1), compound (2)

  20. 20.

    Pollen---endexine thickening present (0), absent (1)

  21. 21.

    Pollen---operculum absent (0), present (1)

  22. 22.

    Pollen---arci present (0), absent (1)

  23. 23.

    Fruits---laterally winged nutlets present (0), absent (1)

  24. 24.

    Fruits---dispersal units with adnate persistent involucre absent (0), present (1)

  25. 25.

    Seeds---germination epigeal (0), hypogeal (1)

Appendix 2

Table 4 Data matrix for morphological characters used in this analysis (including the outgroup Nothofagus; “?” indicating not applicable
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Zhu, J., Zhang, L., Ren, B. et al. Comparative Flower and Inflorescence Organogenesis among Genera of Betulaceae: Implications for Phylogenetic Relationships. Bot. Rev. 84, 79–98 (2018). https://doi.org/10.1007/s12229-017-9195-0

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