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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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Reactive oxygen species are required for spore-wall formation in Physcomitrella patens
A robust spore wall was a key requirement for terrestrialization by early plants. Sporopollenin in spore and pollen grain walls is thought to be polymerized and cross-linked to other macromolecular components, partly through oxidative processes involving H 2 O 2 . Therefore, we investigated effects of scavengers of reactive oxygen species (ROS) on the formation of spore walls in the moss Physcomitrella patens (Hedw.) Bruch, Schimp & W. Gümbel. Exposure of sporophytes, containing spores in the process of forming walls, to ascorbate, dimethylthiourea, or 4-hydroxy-TEMPO prevented normal wall development in a dose, chemical, and stage-dependent manner. Mature spores, exposed while developing to a ROS scavenger, burst when mounted in water on a flat slide under a coverslip (a phenomenon we named “augmented osmolysis” because they did not burst in phosphate-buffered saline or in water on a depression slide). Additionally, the walls of exposed spores were more susceptible to alkaline hydrolysis than those of the control spores, and some were characterized by discontinuities in the exine, anomalies in perine spine structure, abnormal intine and aperture, and occasionally, wall shedding. Our data support the involvement of oxidative cross-linking in spore-wall development, including sporopollenin polymerization or deposition, as well as a role for ROS in intine/aperture development.
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- Award ID(s):
- 1758497
- PAR ID:
- 10201433
- Date Published:
- Journal Name:
- Botany
- Volume:
- 98
- Issue:
- 10
- ISSN:
- 1916-2790
- Page Range / eLocation ID:
- 575 to 587
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1139/cjb-2020-0012
