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Comparative development of staminate and pistillate flowers in the dioecious cactus Opuntia robusta

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PCD role in unisexual flowers.

Abstract

The developmental processes underlying the transition from hermaphroditism to unisexuality are key to understanding variation and evolution of floral structure and function. A detailed examination of the cytological and histological patterns involved in pollen and ovule development of staminate and pistillate flowers in the dioecious Opuntia robusta was undertaken, and the potential involvement of programmed cell death in the abortion of the sex whorls was explored. Flowers initiated development as hermaphrodites and became functionally unisexual by anthesis. Female individuals have pistillate flowers with a conspicuous stigma, functional ovary, collapsed stamens and no pollen grains. Male individuals have staminate flowers, with large yellow anthers, abundant pollen grains, underdeveloped stigma, style and an ovary that rarely produced ovules. In pistillate flowers, anther abortion resulted from the premature degradation of the tapetum by PCD, followed by irregular deposition of callose wall around the microsporocytes, and finally by microspore degradation. In staminate flowers, the stigma could support pollen germination; however, the ovaries were reduced, with evidence of placental arrest and ovule abortion through PCD, when ovules were present. We demonstrate that PCD is recruited in both pistillate and staminate flower development; however, it occurs at different times of floral development. This study contributes to the understanding of the nature of the O. robusta breeding system and identifies developmental landmarks that contribute to sexual determination in Cactaceae.

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Acknowledgements

We are grateful to Silvia Espinosa for SEM work, to Gabriel Orozco for confocal microscopy, to Anabel Bieler for light microscopy, and Aldo Domínguez for illustration of Fig. 8. We particularly thank the anonymous reviewers for comments to the final version of the manuscript. This work was supported by Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica [IN226808 to S.V.S.] and Consejo Nacional de Ciencia y Tecnología [101771 to S.V.S.]. Fellowship from Consejo Nacional de Ciencia y Tecnología [to R.H.C. and F.G.C.]. Graduate Program in Biological Sciences of the National Autonomous University of Mexico (UNAM) for R.H.C.

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  1. Laboratorio de Desarrollo en Plantas, Departamento de Biología Comparada, Facultad de Ciencias, UNAM, 04510, Mexico City, Mexico

    Rocío Hernández-Cruz, Jesús Silva-Martínez, Gregorio Orozco-Arroyo, Isabel Alfaro & Sonia Vázquez-Santana

  2. Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, CENID-COMEF, 04010, Coyoacán, Mexico City, Mexico

    Florencia García-Campusano

  3. Departamento de Bioquímica, Facultad de Química, UNAM, Conjunto E, 04510, Mexico City, Mexico

    Felipe Cruz-García

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  1. Rocío Hernández-Cruz
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Correspondence to Sonia Vázquez-Santana.

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Supplementary Figure 1

DNA degradation in ovaries of pistillate flowers. (a-i) In the left column, light microscopy (a, d, g). In the central column, sections stained with DAPI (b, e, h, j, l). The right column corresponds to the TUNEL assays (c, f, i, k, m). a-c No signal of DNA fragmentation was detected in stigmatic lobes of pistillate flowers before anthesis. Autofluorescence of stigmatic papillae in c. d-f No signal of DNA fragmentation was detected in the transmission tissue of stylar canal. DNA fragmentation in some nuclei in the mucilage-producing cells (white arrows in f). g-i DNA fragmentation in the mucilage-producing cells in the style (white arrows in i). j-k Positive control of the TUNEL assay; the green fluorescence showing DNA fragmentation observed in all nuclei as expected (white arrows in k). l-m Negative control of the TUNEL assay shows no fluorescent nuclei (m). Scale bars = 200 μm (a-i), 50 μm (j-m). Mc mucilage-producing cells, P papilla, sc stylar channel, Tt transmitting tissue. (TIFF 14119 kb)

Supplementary Table 1

Main characteristics of developmental stages in staminate and pistillate flowers of Opuntia robusta. (DOCX 14 kb)

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Hernández-Cruz, R., Silva-Martínez, J., García-Campusano, F. et al. Comparative development of staminate and pistillate flowers in the dioecious cactus Opuntia robusta. Plant Reprod 32, 257–273 (2019). https://doi.org/10.1007/s00497-019-00365-w

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