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. 2002 Feb;89(2):227-40.
doi: 10.1093/aob/mcf032.

Early development in fern gametophytes: interpreting the transition to prothallial architecture in terms of coordinated photosynthate production and osmotic ion uptake

Richard H Racusen  1
Affiliations

Early development in fern gametophytes: interpreting the transition to prothallial architecture in terms of coordinated photosynthate production and osmotic ion uptake

Richard H Racusen. Ann Bot. 2002 Feb.

Abstract

Gametophytes of Onoclea sensiblis L. were grown under various light and media-ion conditions to gain a better understanding of the source/sink relationships between photosynthetic and ion-absorbing cells. There was a clear interdependency between green cell and rhizoid functions, such that the growth and development of the rhizoids was completely dependent on the internal delivery of photosynthates from green cells, and conversion of the one-dimensional filament into the two-dimensional prothallus required monovalent cations that could only be provided by rhizoid uptake. The need for monovalent cations was related to osmotic demands of dividing and expanding cells; prothallial development was blocked by monovalent cation deficiency, and the system resorted to Na+ uptake to support cell expansion when K+ was absent. Surgical excisions of filament cells further demonstrated the high degree of coordinated growth between the light-absorbing and ion-absorbing regions. It was also learned that excised sub-apical cells of the protonemata, like the intensively studied apical cell, were capable of remodelling remnants of the filament into a normal prothallus.

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Figures

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Fig. 1. A–D, Development of gametophytes grown under different intensities of continuous white light. Two‐day‐old germinated spores were transferred to Petri dishes with four (f × 4), two (f × 2), one (f × 1) or no (full light; FL) neutral density filters covering the plate lid (see Materials and Methods). E–H, Development of gametophytes grown under different photoperiods of white light. Two‐day‐old germinated spores were exposed to photoperiods of continuous darkness (24D), 2 h light (2L22D), 4 h light (4L20D) and continuous light (24L). All photographs were taken 20 d after the start of the experiment. Bar = 100 µm.
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Fig. 2. Changes in aggregate volume of the prothallus (triangles) and rhizoids (circles) during gametophyte development over 10 d. The experiment was started with organisms germinated 2 d earlier in continuous light. Values were calculated by applying simple geometric formulae to measurements of length, width and thickness of representative gametophytes grown in continuous white light. Bars are means ± s.d. for 20 organisms.
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Fig. 3. Position and growth of secondary rhizoids during development of selected gametophytes with 100 µm (A), 200 µm (B) and 250 µm (C) filament lengths. Gametophytes with specific filament lengths were transferred from various‐aged cultures of organisms grown under a 2L22D photoperiod. The x‐axis of each graph represents the length of the filament axes, with the base of the filament at the origin and the apical cell at the highest x‐axis value. For each 25 µm interval along the filament, the lengths of all rhizoids were summed, and this aggregate rhizoid length plotted on the y‐axis. Open bars show rhizoid position and growth after 4 d in full light; hatched bars show rhizoid growth after 20 d in full light. Results are means ± s.d. of eight organisms for each plot.
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Fig. 4. Acropetal migration of secondary rhizoids during development of a filamentous gametophyte with an axial length between the apical cell and the spore of approx. 200 µm. The organism at day 0 (d0) had been grown in the dark for 10 d and then transferred to continuous light. Note progression of secondary rhizoid emergence at locations progressively closer to the expanding prothallus. Bar = 100 µm.
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Fig. 5. A–C, Prothallial development from a very long (>200 µm) filamentous gametophyte. The organism at d0 had been grown in the dark for 40 d and then transferred to continuous light. D–F, Prothallial regeneration from an excised filament containing the apical cell. Explant at d0 was severed from a 30‐d‐old, dark‐grown gametophyte; the apical cell is to the left and the cut end to the right. From d0 onward, the explant was in continuous light. G–I, Prothallial regeneration from an excised segment of subapical cells; both the apical cell and the spore end have been removed. Explant at d0 was excised from a 30‐d‐old dark‐grown gametophyte; from d0 onward, the explant was in continuous light. Rhizoids were present at d5 onward, but protruded below the structure and are not visible in photographs until d19. Bar = 100 µm.
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Fig. 6. Gametophyte development under conditions where specific media ions were removed. Organisms at d0 had been grown in a 2L22D photoperiod for 4 d, then transferred to continuous light. A–D (Z/agar; ‘zero agar’) shows that normal development occurs when organisms were placed on Bacto‐agar with no added salts. E–H (Na/ose; ‘sodium agarose’) shows that development of the prothallus is slower and smaller when organisms were placed on a low‐salt agarose medium containing only 0·1 mm NaCl. I–L (Z/ose; ‘zero agarose’) shows inhibition of prothallus development at about d7 (J) in organisms placed on low‐salt agarose medium with no added salts. Lower‐diagonal portion of L shows the resumption of prothallus development after a further 8 d (d35), when 0·1 mm K+ was added to the d27, Z/ose organism directly above it. Bar = 100 µm.
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Fig. 7. Demonstration that the rhizoid end of the gametophyte, and not the prothallial end, is the primary site of ion uptake. A–L shows development of prothalli on control media (agar with all nutrient ions; A–D), on low‐salt agarose with no added salts (Z/ose, E–L). Organisms were grown in a 2L22D photoperiod for 7 d, and then transferred to continuous light at d0. Ion deficiency symptoms are evident in both the Z/ose treatments by d10 (G and K). M–R shows the response of the same two deficient organisms when K+ is added to the cellophane chip overlying the rhizoid end (Z/ose a, M–O), or to the cellophane chip overlying the prothallus end (Z/ose b, P–R). Bar = 100 µm.
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References

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