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Ontogenesis in miniature. Pollen wall development in Campanula rapunculoides

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Our findings suggest a reconsideration of pollen wall ontogeny process, entailing examination of physical factors, which enable a new understanding of exine developmental processes as self-formation.

Abstract

The pollen wall, the most complex cell wall in plants, is especially interesting as a model of ontogeny in miniature. By a detailed study of each developmental stage of Campanula rapunculoides pollen wall, we aimed to understand the establishment of complex pollen walls and the underlying developmental mechanisms. Other aim was to compare our current observations with studies in other species to reveal the common principles. We also tried to analyse the reasons for commonalities in ontogenies of exines in remote species. TEM, SEM, comparative methods were used in this study. The sequence of events leading to exine emergence from early tetrad stage to maturity is as follows: the appearance of spherical micelles in the periplasmic space and de-mixing of the mixture in periplasm (condensed and depleted layers); appearance of plasma membrane invaginations and columns of spherical micelles inside condensed layer; appearance of rod-like units, pro-tectum and thin foot layer; the appearance of spiral substructure of procolumellae and of dendritic outgrowths on the tops of procolumellae, of vast depleted zone in aperture sites; formation of the endexine lamellae on the base of laminate micelles; gradual twisting of dendritic outgrowths (macromolecule chains) into clubs on the tops of columellae and into spines; final sporopollenin accumulation. Our observations are consistent with the sequence of self-assembling micellar mesophases. Complex organisation of the exine is established through processes of self-assembly operating together with another physical process—phase separation. After genomic determination of the exine building substances, purely physical processes which are not under direct genomic control play an important role after genomic control of constructive substances. The comparison of the underlying mechanisms of exine development in remote species occurred to be general and similar to crystallisation. Our ontogenetic experience has shown the commonality of pollen wall ontogenies in remote species.

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All data generated or analysed during this study are included in this published article.

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Acknowledgements

This work was carried out in the framework of the institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences ‘Pollen and spores of living and fossil plants: morphology and development’ no. AAAA-A19-119080790048-7 on the equipment of the Core Facility ‘Cellular and Molecular Technologies in Plant Science’ of the Komarov Botanical Institute (Saint Petersburg).

Funding

This study was supported by institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences.

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Correspondence to Nina I. Gabarayeva.

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The authors declare they have no financial interests.

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Communicated by Anastasios Melis.

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Gabarayeva, N.I., Grigorjeva, V.V., Polevova, S.V. et al. Ontogenesis in miniature. Pollen wall development in Campanula rapunculoides. Planta 258, 38 (2023). https://doi.org/10.1007/s00425-023-04198-w

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  • DOI: https://doi.org/10.1007/s00425-023-04198-w

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