Abstract
Penium margaritaceum is a unicellular zygnematophyte (basal Streptophyteor Charophyte) that has been used as a model organism for the study of cell walls of Streptophytes and for elucidating organismal adaptations that were key in the evolution of land plants.. When Penium is incubated in sorbitol-enhance medium, i.e., hyperosmotic medium, 1000–1500 Hechtian strands form within minutes and connect the plasma membrane to the cell wall. As cells acclimate to this osmotic stress over time, further significant changes occur at the cell wall and plasma membrane domains. The homogalacturonan lattice of the outer cell wall layer is significantly reduced and is accompanied by the formation of a highly elongate, “filamentous” phenotype. Distinct peripheral thickenings appear between the CW and plasma membrane and contain membranous components and a branched granular matrix. Monoclonal antibody labeling of these thickenings indicates the presence of rhamnogalacturonan-I epitopes. Acclimatization also results in the proliferation of the cell’s vacuolar networks and macroautophagy. Penium’s ability to acclimatize to osmotic stress offers insight into the transition of ancient zygnematophytes from an aquatic to terrestrial existence.
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Acknowledgements
The authors dedicate this paper to Professor Ursula Lütz-Meindl whose outstanding research career provided keen insight into zygnematophyte biology and who was a true inspiration to colleagues and students. The authors also thank the US-National Science Foundation (NSF; NSF-MCB 1517345) for support of this project.
Funding
This work was funded by the National Science Foundation (USA) grant: MCB-1517546.
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Supplementary Fig 1
a Neutral red labeling (arrows) of vacuoles in control cell. b After 48 h of incubation in 200 mM sorbitol, the number and size (arrows) of vacuoles increase. c, d After 96 h of acclimatization in sorbitol the number of vacuolesincrease and ollect in the cell center (c) and polar zones (d). All images- DIC, a 17 μm. b 9 μm, c 12 μm, d 10 μm. Supplementray Fig 2 TEM imaging highlights of Hechtian strands. a After 5 min of incubation in 300 mM sorbitol, a strand emerges evey approximately 300 nm. b and c The strand measures 47 +/- 5 nm in diameter and often has a distinct coating (arrows). This coating could be material found between the PM and CW or an artifact of fixation. d In the early formation of the peripheral thickenings, Hechtian strands fill an invaginating pocket (arrow). a 215 nm, b 50 nm, c 120 nm, d 320 nm. Supplementary Fig 3 TEM imaging of the peripheral thickenings and vacuoles. a After 72 h of acclimatization in sorbitol the thickenings include both membranous components (white arrows) and the homogenous inclusions (dark arrows). b Glancing section through the thickening reveals the large amount of the homogenous inclusion (black arrows) interspersed with membranous components (white arrows). c Magnified view of the membranous components (white arrow) of the thickening. Note the different sized components. The homogenous inclusion (black arrow) has a granular appearance. d Part of the large peripheral vacuole containing membranous components (arrow) after 96 h acclimatization. e Phagophore-like membranes (arrow) in early stage of autophagosome production after 96 h of acclimatization. F Phagophore (arrows) surrounding membranes in cell acclimatized for 96 h. a 800 nm, b 800 nm, c 420 nm, d 1 μm, e 750 nm, f 400 nm (PPTX 12924 kb)
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Domozych, D.S., Kozel, L. & Palacio-Lopez, K. The effects of osmotic stress on the cell wall-plasma membrane domains of the unicellular streptophyte, Penium margaritaceum. Protoplasma 258, 1231–1249 (2021). https://doi.org/10.1007/s00709-021-01644-y
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DOI: https://doi.org/10.1007/s00709-021-01644-y