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Gynoecium structure in Sapindales and a case study of Trichilia pallens (Meliaceae)

Journal of Plant Research volume 135, pages 157–190 (2022)Cite this article

Abstract

Sapindales is a monophyletic order within the malvid clade of rosids. It represents an interesting group to address questions on floral structure and evolution due to a wide variation in reproductive traits. This review covers a detailed overview of gynoecium features, as well as a new structural study based on Trichilia pallens (Meliaceae), to provide characters to support systematic relationships and to recognize patterns of variations in gynoecium features in Sapindales. Several unique and shared characteristics are identified. Anacrostylous and basistylous carpels may have evolved multiple times in Sapindales, while ventrally bulging carpels are found in pseudomonomerous Anacardiaceae. Different from previous studies, similar gynoecium features, including degree of syncarpy, ontogenetic patterns, and PTTT structure, favors a closer phylogenetic proximity between Rutaceae and Simaroubaceae, or Rutaceae and Meliaceae. An apomorphic tendency for the order is that the floral apex is integrated in the syncarpous or apocarpous gynoecium, but with different length and shape among families. Nitrariaceae shares similar stigmatic features and PTTT structure with many Sapindaceae. As the current position of both families in Sapindales is uncertain, floral features should be investigated more extensively in future studies. Two different types of gynophore were identified in the order: either derived from intercalary growth below the gynoecium as a floral internode, or by extension of the base of the ovary locules as part of the gynoecium. Sapindales share a combination of gynoecial characters but variation is mostly caused by different degrees of development of the synascidiate part relative to the symplicate part of carpels, or the latter part is absent. Postgenital fusion of the upper part of the styles leads to a common stigma, while stylar lobes may be separate. Due to a wide variation in these features, a new terminology regarding fusion is proposed to describe the gynoecium of the order.

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Fig. 1

(modified from Bachelier and Endress (2009); i′ modified from Bachelier et al. (2011) and b modified from Bachelier and Endress (2008)). Asterisks: floral apex, indicated only in longitudinal schemes

Fig. 2

modified from Ramp (1988); ib, iii″ from Nair and Joshi (1958); iii‴ from Bachelier and Endress (2009). Asterisks: floral apex, indicated only in longitudinal schemes

Fig. 3

Modified from Pirani 1987 (a) and Devecchi and Pirani 2020 (b). Photographs, J.H.L.El Ottra

Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Modified from Pirani (1992) (a), Aubréville (1962) (b), and Acevedo-Rodriguez and Somner (2018) (c)

Notes

  1. In acrostylous carpel the style base overtops the ovary apex (i.e., the style base is “the apical continuation of the ovary”; Weberling 1989, Fig. 4a), while in anacrostylous carpels the style base (style “insertion”, Weberling, 1989) is at a more basal level than the ovary apex (e.g., Online Resource 4, a).

  2. Some Sapindaceae with one conspicuous main median dorsal bundle and a triangular-shaped ovary have a dorsal wing in the same region (Dodonaea, Paoli and Sarti 2008), or at least a dorsal rib in the anthetic gynoecium, that will develop later into the wings of fruitlets (many Paullinieae: Weckerle and Rutishauser 2005). Differently, other Sapindaceae with similar ovary shape (Koelreuteria), but with deep dehiscence lines (furrows) in the median region, dorsal bundles are absent (Avalos et al. 2019; Cao et al. 2018; Ronse De Craene et al. 2000).

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Acknowledgements

Thanks are due to the technicians of the Plant Anatomy Laboratory (IB-USP), Gisele R. O. Costa, Tássia C. Santos, and Irwandro R. Pires, for their assistance to the first author in the laboratory. We also thanks Klei Rodrigo Sousa for assistance with graphic work, Dr. W. Wayt Thomas for sharing an image of Picrolemma, and to the Class of BIB 434 (2016) from IB-USP course, for assisting the analysis of T. pallens. The first author thanks to the FLO-RE-S group, for fruitful conversations on floral structure and for joining plant scientists together in research to disentangle “the nature and causes behind the floral shape” (Bull-Hereñu et al. 2016; https://flores-network.com). This research was supported by grants from Fundação de Amparo à Pesquisa do Estado de São Paulo [FAPESP, grants numbers 14/18002-2, and 15/09776-7] awarded to J.R. Pirani and J.H.L. El Ottra; and Conselho Nacional de Desenvolvimento e Pesquisa [CNPq productivity Grant n. 307655/2015-6, awarded to J.R. Pirani, and CNPq grant n. 150634/2017-0 to J.H.L. El Ottra]. We appreciate the helpful review and comments of two anonymous reviewers.

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  1. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-090, Brazil

    Juliana Hanna Leite El Ottra, Gladys Flávia de Albuquerque Melo-de-Pinna, Diego Demarco & José Rubens Pirani

  2. Universidade Aberta Do Brasil, Universidade Federal Do ABC, Av. Dos Estados, 5001, Santo André, SP, 09210-580, Brazil

    Juliana Hanna Leite El Ottra

  3. Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, Scotland, UK

    Louis P. Ronse De Craene

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El Ottra, J.H.L., de Albuquerque Melo-de-Pinna, G.F., Demarco, D. et al. Gynoecium structure in Sapindales and a case study of Trichilia pallens (Meliaceae). J Plant Res 135, 157–190 (2022). https://doi.org/10.1007/s10265-022-01375-y

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Keywords

  • Apomorphic tendency
  • Carpellodes
  • Congenital fusion
  • Fruit
  • Gynoecium architecture
  • Postgenital fusion
  • Syncarpy
  • Vascularization