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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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Timing of meristem initiation and maintenance determines the morphology of fern gametophytes
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.
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- Award ID(s):
- 1931114
- PAR ID:
- 10332635
- Editor(s):
- Melzer, Rainer
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- Volume:
- 72
- Issue:
- 20
- ISSN:
- 0022-0957
- Page Range / eLocation ID:
- 6990 to 7001
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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The life cycle of land plants is characterized by alternating generations of sexual gametophytes and asexual sporophytes. Unlike seed plants, seed-free vascular plants, including ferns, initiate and maintain pluripotent meristems during their gametophyte phase to sustain body expansion and drive the formation of sexual organs for reproduction. This review summarizes meristem development among various fern species during the gametophyte phase, focusing on the cellular basis of meristem initiation, proliferation, and termination. We review the different types of gametophytic meristems in ferns, including apical cell (AC)-based meristems, multicellular apical meristems, and multicellular marginal meristems. We highlight both conserved and lineage-specific patterns of cell division, which are closely associated with these meristem identities and play crucial roles in shaping gametophytic morphology. Additionally, we highlight recent progress in understanding the dynamics of cell division and growth that drive meristem development, through studies that integrate confocal live imaging and computational quantitative analysis. Furthermore, we discuss the influence of environmental and genetic factors on cell division activity in fern gametophytes, including conserved transcriptional regulators that sustain meristem indeterminacy and proliferation in the model fern Ceratopteris richardii.more » « less
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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 usedWoodsia 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.more » « less
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ABSTRACT A fascinating feature of land plants is their ability to continually initiate new tissues and organs throughout their lifespan, driven by a pool of pluripotent stem cells located in meristems. In seed plants, various types of meristems are initiated and maintained during the sporophyte generation, while their gametophytes lack meristems and rely on sporophyte tissues for growth. In contrast, seed‐free vascular plants, such as ferns, develop meristems during both the sporophyte and gametophyte generations, allowing for the independent growth of both generations. Recent findings have highlighted both conserved and lineage‐specific roles of the HAIRY MERISTEM (HAM) family of GRAS‐domain transcriptional regulators in various meristems throughout the land plant lifecycle. Here, we review and discuss howHAMgenes maintain meristem indeterminacy in both sporophytes and gametophytes, with a focus on studies performed in two model species: the flowering plantArabidopsis thalianaand the fernCeratopteris richardii. Additionally, we summarize the crucial and tightly regulated functions of the microRNA171 (miR171)‐HAM regulatory modules, which define HAM spatial patterns and activities during meristem development across various meristem identities in land plants.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/jxb/erab307
