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Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture

Although the evolution of spores was critical to the diversification of plants on land, sporogenesis is incompletely characterized for model plants such as Physcomitrium patens. In this study, the complete process of P. patens sporogenesis is detailed from capsule expansion to mature spore formation...

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Autores principales: Renzaglia, Karen S., Ashton, Neil W., Suh, Dae-Yeon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10133578/
https://www.ncbi.nlm.nih.gov/pubmed/37123413
http://dx.doi.org/10.3389/fcell.2023.1165293
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author Renzaglia, Karen S.
Ashton, Neil W.
Suh, Dae-Yeon
author_facet Renzaglia, Karen S.
Ashton, Neil W.
Suh, Dae-Yeon
author_sort Renzaglia, Karen S.
collection PubMed
description Although the evolution of spores was critical to the diversification of plants on land, sporogenesis is incompletely characterized for model plants such as Physcomitrium patens. In this study, the complete process of P. patens sporogenesis is detailed from capsule expansion to mature spore formation, with emphasis on the construction of the complex spore wall and proximal aperture. Both diploid (sporophytic) and haploid (spores) cells contribute to the development and maturation of spores. During capsule expansion, the diploid cells of the capsule, including spore mother cells (SMCs), inner capsule wall layer (spore sac), and columella, contribute a locular fibrillar matrix that contains the machinery and nutrients for spore ontogeny. Nascent spores are enclosed in a second matrix that is surrounded by a thin SMC wall and suspended in the locular material. As they expand and separate, a band of exine is produced external to a thin foundation layer of tripartite lamellae. Dense globules assemble evenly throughout the locule, and these are incorporated progressively onto the spore surface to form the perine external to the exine. On the distal spore surface, the intine forms internally, while the spiny perine ornamentation is assembled. The exine is at least partially extrasporal in origin, while the perine is derived exclusively from outside the spore. Across the proximal surface of the polar spores, an aperture begins formation at the onset of spore development and consists of an expanded intine, an annulus, and a central pad with radiating fibers. This complex aperture is elastic and enables the proximal spore surface to cycle between being compressed (concave) and expanded (rounded). In addition to providing a site for water intake and germination, the elastic aperture is likely involved in desiccation tolerance. Based on the current phylogenies, the ancestral plant spore contained an aperture, exine, intine, and perine. The reductive evolution of liverwort and hornwort spores entailed the loss of perine in both groups and the aperture in liverworts. This research serves as the foundation for comparisons with other plant groups and for future studies of the developmental genetics and evolution of spores across plants.
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spelling pubmed-101335782023-04-28 Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture Renzaglia, Karen S. Ashton, Neil W. Suh, Dae-Yeon Front Cell Dev Biol Cell and Developmental Biology Although the evolution of spores was critical to the diversification of plants on land, sporogenesis is incompletely characterized for model plants such as Physcomitrium patens. In this study, the complete process of P. patens sporogenesis is detailed from capsule expansion to mature spore formation, with emphasis on the construction of the complex spore wall and proximal aperture. Both diploid (sporophytic) and haploid (spores) cells contribute to the development and maturation of spores. During capsule expansion, the diploid cells of the capsule, including spore mother cells (SMCs), inner capsule wall layer (spore sac), and columella, contribute a locular fibrillar matrix that contains the machinery and nutrients for spore ontogeny. Nascent spores are enclosed in a second matrix that is surrounded by a thin SMC wall and suspended in the locular material. As they expand and separate, a band of exine is produced external to a thin foundation layer of tripartite lamellae. Dense globules assemble evenly throughout the locule, and these are incorporated progressively onto the spore surface to form the perine external to the exine. On the distal spore surface, the intine forms internally, while the spiny perine ornamentation is assembled. The exine is at least partially extrasporal in origin, while the perine is derived exclusively from outside the spore. Across the proximal surface of the polar spores, an aperture begins formation at the onset of spore development and consists of an expanded intine, an annulus, and a central pad with radiating fibers. This complex aperture is elastic and enables the proximal spore surface to cycle between being compressed (concave) and expanded (rounded). In addition to providing a site for water intake and germination, the elastic aperture is likely involved in desiccation tolerance. Based on the current phylogenies, the ancestral plant spore contained an aperture, exine, intine, and perine. The reductive evolution of liverwort and hornwort spores entailed the loss of perine in both groups and the aperture in liverworts. This research serves as the foundation for comparisons with other plant groups and for future studies of the developmental genetics and evolution of spores across plants. Frontiers Media S.A. 2023-04-13 /pmc/articles/PMC10133578/ /pubmed/37123413 http://dx.doi.org/10.3389/fcell.2023.1165293 Text en Copyright © 2023 Renzaglia, Ashton and Suh. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Renzaglia, Karen S.
Ashton, Neil W.
Suh, Dae-Yeon
Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture
title Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture
title_full Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture
title_fullStr Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture
title_full_unstemmed Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture
title_short Sporogenesis in Physcomitrium patens: Intergenerational collaboration and the development of the spore wall and aperture
title_sort sporogenesis in physcomitrium patens: intergenerational collaboration and the development of the spore wall and aperture
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10133578/
https://www.ncbi.nlm.nih.gov/pubmed/37123413
http://dx.doi.org/10.3389/fcell.2023.1165293
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