Callose deposition is essential for the completion of cytokinesis in the unicellular alga, Penium margaritaceum

Abstract

Cytokinesis in land plants involves the formation of a cell plate that develops into the new cell wall. Callose, a β-1,3 glucan accumulates at later stages of cell plate development presumably to stabilize this delicate membrane network during expansion. Cytokinetic callose is considered specific to multicellular plant species, as it has not been detected in unicellular algae. Here we present callose at the cytokinesis junction of the unicellular charophyte, P. margaritaceum. Callose deposition at the division plane of P. margaritaceum showed distinct, spatiotemporal patterns likely representing distinct roles of this polymer in cytokinesis. Pharmacological inhibition by Endosidin 7 resulted in cytokinesis defects, consistent with the essential role for this polymer in P. margaritaceum cell division. Cell wall deposition at the isthmus zone was also affected by the absence of callose, demonstrating the dynamic nature of new wall assembly in P. margaritaceum. The identification of candidate callose synthase genes provides molecular evidence for callose biosynthesis in P. margaritaceum. The evolutionary implications of cytokinetic callose in this unicellular Zygnematopycean alga is discussed in the context of the conquest of land by plants.

Search for evolutionary roots of land plant arabinogalactan‐proteins in charophytes: presence of a rhamnogalactan‐protein in Spirogyra pratensis (Zygnematophyceae)

“…Mixed-linked glucans known from grasses ( Gibeaut and Carpita, 1993 ) and also from Equisetum ( Fry et al, 2008 ) have also been detected in different CGA, although they were mainly present in the alkalisoluble fractions ( Eder et al, 2008 ; Sørensen et al, 2011 ). Callose was not found in cell walls of Micrasterias but was present in Zygnema ( Herburger and Holzinger, 2015 ) and it is essential for the completion of cytokinesis in Penium ( Davis et al, 2020 ).…”

Kinetin induces microtubular breakdown, cell cycle arrest and programmed cell death in tobacco BY-2 cells

“…Analysis of the massue mutant in A. thaliana indicate that callose is required for cytokinesis, although it is replaced by cellulose, xyloglucans and pectins in the maturating cell wall (Thiele et al 2009), whilst persisting around the plasmodesmata (Wu et al 2018). The synthesis of callose to delineate borders might have been an acquisition of the ancestral line within the pteridophytes that gave rise to the seed plants (Drábková and Honys 2017), but precursors might be even older, because the functional link between callose and cytokinesis is also present in the Zygnematophyceae, a sister clade of the terrestrial plant lineage (Davis et al 2020). Our finding that callose intensity increases more than twofold in response to kinetin is congruent with a role of callose as a barrier between living and dying cells, a phenomenon that had already been reported for male sex differentiation in gametophytes of Anemia phyllitidis (Kaźmierczak 2008).…”

NMR spectroscopy analysis reveals differential metabolic responses in arabidopsis roots and leaves treated with a cytokinesis inhibitor

“…In addition, it does not affect wound-induced callose deposition or plug formation in sieve elements [2]. Consistent effects of endosidin-7 across the plant kingdom, from early diverging algae, e.g., Charophyte Penium margaritaceum, to higher plants, demonstrate that the pathways affected by endosidin-7 are evolutionarily conserved [9].…”