Cell growth dynamics in two types of apical meristems in fern gametophytes

Abstract

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.

Cell Division and Meristem Dynamics in Fern Gametophytes

“…Computational segmentation and quantification results further demonstrated that active division and expansion of the AC and its immediate progenies contributed to notch formation and prothallus expansion in S. chinensis gametophytes [ 24 ]. The characterizations of ACs in different fern gametophytes altogether [ 14 , 21 , 22 , 23 , 24 , 52 , 54 , 55 ] suggest that the activity of wedge-shaped ACs in gametophytes likely independently evolved in fern taxa [ 24 ].…”

“…Independent studies all demonstrated that the conserved oblique division in the AC resulted in one new wedge-shaped apical cell and one adjacent trapezoid-shaped cell, leading to the renewal of the ACs in fern gametophytes ( Figure 2 B) [ 21 , 22 , 24 ]. By contrast, in the gametophytes of many fern species, including Woodsia obtusa and Lygodium japonicum , the oblique division is only maintained for a limited time [ 21 , 23 ]. After only a few rounds of oblique division, the AC undergoes the division in a periclinal orientation, resulting in one trapezoid-shaped daughter cell outside and one triangular daughter cell inside ( Figure 2 C) [ 23 ].…”

“…Previous characterizations have shown that fern gametophytes develop different types of meristems, including the apical cell (AC)-based meristems and the AC-independent multicellular meristems, to sustain prothallus development and sexual organ formation [ 12 , 13 , 14 , 20 , 21 ]. Recent studies established a quantitative research platform, combining noninvasive confocal time-lapse imaging, image segmentation, and computational quantification to examine meristem development in fern gametophytes [ 22 , 23 , 24 , 25 ]. Using this platform, the variations in meristem development and activity were determined at single-cell resolution among different fern species, including Ceratopteris richardii (a model fern), Pteris vittata (the ladder brake), Woodsia obtusa (the blunt-lobe cliff fern), and Sphenomeris chinensis (the lace fern) [ 22 , 23 , 24 , 25 ].…”

“…Recent studies established a quantitative research platform, combining noninvasive confocal time-lapse imaging, image segmentation, and computational quantification to examine meristem development in fern gametophytes [ 22 , 23 , 24 , 25 ]. Using this platform, the variations in meristem development and activity were determined at single-cell resolution among different fern species, including Ceratopteris richardii (a model fern), Pteris vittata (the ladder brake), Woodsia obtusa (the blunt-lobe cliff fern), and Sphenomeris chinensis (the lace fern) [ 22 , 23 , 24 , 25 ]. The dynamics of different meristems (apical cell-based meristems and multicellular meristems), including their initiation, maintenance, transition between different identities, and termination during fern gametophyte development, were also quantitively examined [ 22 , 23 , 24 , 25 ].…”

“…Using this platform, the variations in meristem development and activity were determined at single-cell resolution among different fern species, including Ceratopteris richardii (a model fern), Pteris vittata (the ladder brake), Woodsia obtusa (the blunt-lobe cliff fern), and Sphenomeris chinensis (the lace fern) [ 22 , 23 , 24 , 25 ]. The dynamics of different meristems (apical cell-based meristems and multicellular meristems), including their initiation, maintenance, transition between different identities, and termination during fern gametophyte development, were also quantitively examined [ 22 , 23 , 24 , 25 ]. In this review, we summarize the current progress in understanding the diversified meristem activities and discuss the conserved and unique division patterns that dictate meristem dynamics in fern gametophytes ( Figure 1 A–F and Figure 2 A–H).…”