One of the most important questions in all multicellular organisms is how to define and maintain different cell fates during continuous cell division and proliferation. Plant meristems provide a unique research system to address this fundamental question because meristems dynamically maintain themselves and sustain organogenesis through balancing cell division and cell differentiation. Different from the gametophytes of seed plants that depend on their sporophytes and lack meristems, the gametophytes of seed-free ferns develop different types of meristems (including apical cell-based meristems and multicellular apical and marginal meristems) to promote independent growth and proliferation during the sexual gametophyte phase. Recent studies combining confocal time-lapse imaging and computational image analysis reveal the cellular basis of the initiation and proliferation of different types of meristems in fern gametophytes, providing new insights into the evolution of meristems in land plants. In this review, we summarize the recent progress in understanding the cell growth dynamics in fern gametophytes and discuss both conserved and diversified mechanisms underlying meristem cell proliferation in seed-free vascular plants.
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Hymenasplenium volubile: documentation of its gametophytes and the first record of a hemiepiphyte in the Aspleniaceae
Abstract Background and Aims Through careful field examination of the growth habit of the gametophytes and sporophytes of Hymenasplenium volubile across an ontogenetic series, we aim to understand better the evolution of epiphytism in this poorly understood group of ferns Methods We made field observations of H. volubile sporophytes and gametophytes, and brought specimens back to the lab for microscopic analysis. In the field, sporophytes at each ontogenetic stage were photographed to document the species’ growth habit. We used an existing phylogeny to optimize growth form of New World Hymenasplenium. Key Results Young sporophytes were at first fully epiphytic and produced one or two long feeding roots that extend to the soil where they branch profusely. The feeding roots remain in contact with the soil throughout the life of the plant. Thus, H. volubile is a hemiepiphyte. While immature, gametophytes are appressed to the tree trunk, but, as their gametangia mature, their lower margin lifts upward, imparting a shelf-like appearance to the thallus. The thallus attaches to the substrate by branched rhizoids produced along the margin of the thallus in contact with the substrate. Conclusions Hemiepiphytes are a key link in the evolution of epiphytic ferns and may act as a bridge between the forest floor and the canopy. Our finding is the first report of hemiepiphytism in Aspleniaceae, a large lineage with many epiphytic and terrestrial taxa. This work serves as an important model to understand the evolution of epiphytism in this group specifically and in ferns in general. The majority of our understanding of fern gametophyte biology is derived from laboratory studies. Our efforts represent a fundamental contribution to understanding fern gametophyte ecology in a field setting.
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- Award ID(s):
- 1656801
- NSF-PAR ID:
- 10351845
- Date Published:
- Journal Name:
- Annals of Botany
- Volume:
- 124
- Issue:
- 5
- ISSN:
- 0305-7364
- Page Range / eLocation ID:
- 829 to 835
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary The expansion of angiosperm‐dominated forests in the Cretaceous and early Cenozoic had a profound effect on terrestrial biota by creating novel ecological niches. The majority of modern fern lineages are hypothesized to have arisen in response to this expansion, particularly fern epiphytes that radiated into the canopy. Recent evidence, however, suggests that epiphytism does not correlate with increased diversification rates in ferns, calling into question the role of the canopy habitat in fern evolution.
To understand the role of the canopy in structuring fern community diversity, we investigated functional traits of fern sporophytes and gametophytes across a broad phylogenetic sampling on the island of Moorea, French Polynesia, including > 120 species and representatives of multiple epiphytic radiations.
While epiphytes showed convergence in small size and a higher frequency of noncordate gametophytes, they showed greater functional diversity at the community level relative to terrestrial ferns.
These results suggest previously overlooked functional diversity among fern epiphytes, and raise the hypothesis that while the angiosperm canopy acted as a complex filter that restricted plant size, it also facilitated diversification into finely partitioned niches. Characterizing these niche axes and adaptations of epiphytic ferns occupying them should be a priority for future pteridological research.
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Melzer, Rainer (Ed.)Abstract The alternation of generations in land plants occurs between the sporophyte phase and the gametophyte phase. The sporophytes of seed plants develop self-maintained, multicellular meristems, and these meristems determine plant architecture. The gametophytes of seed plants lack meristems and are heterotrophic. In contrast, the gametophytes of seed-free vascular plants, including ferns, are autotrophic and free-living, developing meristems to sustain their independent growth and proliferation. Compared with meristems in the sporophytes of seed plants, the cellular mechanisms underlying meristem development in fern gametophytes remain largely unknown. Here, using confocal time-lapse live imaging and computational segmentation and quantification, we determined different patterns of cell divisions associated with the initiation and proliferation of two distinct types of meristems in gametophytes of two closely related Pteridaceae ferns, Pteris vittata and Ceratopteris richardii. Our results reveal how the simple timing of a switch between two meristems has considerable consequences for the divergent gametophyte morphologies of the two ferns. They further provide evolutionary insight into the function and regulation of gametophyte meristems in seed-free vascular plants.more » « less
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Abstract Fern gametophytes are autotrophic and independent of sporophytes, and they develop pluripotent meristems that drive prothallus development and sexual reproduction. To reveal cellular dynamics during meristem development in fern gametophytes, we performed long-term time-lapse imaging and determined the real-time lineage, identity and division activity of each single cell from meristem initiation to establishment in gametophytes of the fern
Ceratopteris richardii . Our results demonstrate that in Ceratopteris gametophytes, only a few cell lineages originated from the marginal layer contribute to meristem initiation and proliferation, and the meristem lacks a distinguishable central zone or apical cell with low division activity. Within the meristem, cell division is independent of cell lineages and cells at the marginal layer are more actively dividing than inner cells. Furthermore, the meristem triggers differentiation of adjacent cells into egg-producing archegonia in a position-dependent manner. These findings advance the understanding of diversified meristem and gametophyte development in land plants. -
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SUMMARY In contrast to seed plants, the gametophytes of seed‐free plants develop pluripotent meristems, which promote and sustain their independent growth and development. To date, the cellular basis of meristem development in gametophytes of seed‐free ferns remains largely unknown. In this study, we used
Woodsia obtusa , the blunt‐lobe cliff fern, to quantitatively determine cell growth dynamics in two different types of apical meristems – the apical initial centered meristem and the multicellular apical meristem in gametophytes. Through confocal time‐lapse live imaging and computational image analysis and quantification, we determined unique patterns of cell division and growth that sustain or terminate apical initials, dictate the transition from apical initials to multicellular apical meristems, and drive proliferation of apical meristems in ferns. Quantitative results showed that small cells correlated to active cell division in fern gametophytes. The marginal cells of multicellular apical meristems in fern gametophytes undergo division in both anticlinal and periclinal orientations, not only increasing cell numbers but also playing a dominant role in increasing cell layers during gametophyte development. All these findings provide insights into the function and regulation of meristems in gametophytes of seed‐free vascular plants, suggesting both conserved and diversified mechanisms underlying meristem cell proliferation across land plants.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/aob/mcz124
