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Pollen wall and tapetal development in Cymbalaria muralis: the role of physical processes, evidenced by in vitro modelling

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Abstract

Our aim was to unravel the underlying mechanisms of pollen wall development in Cymbalaria muralis. By determining the sequence of developing substructures with TEM, we intended to compare it with that of other taxa and clarify whether physical processes of self-assembly and phase separation were involved. In parallel, we tried to simulate in vitro the substructures observed in Cymbalaria muralis exine development, using colloidal mixtures, to determine whether purely physical self-assembly processes could replicate them. Exine ontogeny followed the main stages observed in many other species and was initiated by phase separation, resulting in heterogeneity of the homogeneous contents of the periplasmic space around the microspore which is filled with genome-determined substances. At every stage, phase separation and self-assembly come into force, gradually driving the substances through the sequence of mesophases: spherical micelles, columns of spherical micelles, cylindrical micelles arranged in a layer, laminate micelles. The final two of these mesophases define the structure of the columellate ectexine and lamellate endexine respectively. Structures obtained in vitro from colloidal mixtures simulated the developing exine structures. Striking columella-like surface of some abnormal tapetal cells and lamella-like structures in the anther medium confirm the conclusion that pattern generation is a feature of colloidal materials, after genomic control on material contents. Simulation experiments show the high pattern-generating capacity of colloidal interactions.

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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). Special thanks go to Stephen Blackmore for advices and help in the course of the preparation of the manuscript. We are grateful to our anonymous reviewers for their thoughtful and detailed reviews.

Funding

Institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences.

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Contributions

SVP: collecting and fixation of C. miralis material and preparing of ultrathin sections; VVG: fixations and embedding of models’ samples and preparing ultrathin sections, staining of all sections and taking a part of TEM pictures; NIG: design and performance of the modelling experiments, taking a part of TEM pictures, the principal analysis and writing the manuscript.

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Correspondence to Nina I. Gabarayeva.

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Polevova, S.V., Grigorjeva, V.V. & Gabarayeva, N.I. Pollen wall and tapetal development in Cymbalaria muralis: the role of physical processes, evidenced by in vitro modelling. Protoplasma 260, 281–298 (2023). https://doi.org/10.1007/s00709-022-01777-8

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  • DOI: https://doi.org/10.1007/s00709-022-01777-8

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