The charophycean green algae provide insights into the early origins of plant cell walls

Abstract

SUMMARYNumerous evolutionary innovations were required to enable freshwater green algae to colonize terrestrial habitats and thereby initiate the evolution of land plants (embryophytes). These adaptations probably included changes in cell-wall composition and architecture that were to become essential for embryophyte development and radiation. However, it is not known to what extent the polymers that are characteristic of embryophyte cell walls, including pectins, hemicelluloses, glycoproteins and lignin, evolved in response to the demands of the terrestrial environment or whether they pre-existed in their algal ancestors. Here we show that members of the advanced charophycean green algae (CGA), including the Charales, Coleochaetales and Zygnematales, but not basal CGA (Klebsormidiales and Chlorokybales), have cell walls that are comparable in several respects to the primary walls of embryophytes. Moreover, we provide both chemical and immunocytochemical evidence that selected Coleochaete species have cell walls that contain small amounts of lignin or lignin-like polymers derived from radical coupling of hydroxycinnamyl alcohols. Thus, the ability to synthesize many of the components that characterize extant embryophyte walls evolved during divergence within CGA. Our study provides new insight into the evolutionary window during which the structurally complex walls of embryophytes originated, and the significance of the advanced CGA during these events.

On plant defense signaling networks and early land plant evolution

“…As discussed above, a PAL-encoding orthologous gene was detected in the genome of K. nitens [121], suggesting that this early-branching streptophyte alga is capable of producing PPs. This is in agreement with the aforementioned detection of lignin-like compounds in streptophyte algae [see 49, 57, 58, 59], which are also derived from the PP pathway. While this suggests that both mechanisms are ancient, we do not know whether PPs and their derivatives are used by streptophyte algae for pathogen and parasite defense.…”

“…How so? Pectin is a cell wall component characteristic of land plants and streptophyte algae (reviewed in [49]). Berbee et al [47] argue that since pectinase-harboring fungal lineages are older than the land plant clade, these fungi used their pectinases for the degradation of streptophyte algal cell walls.…”

“…Streptophyte algae such as Coleochaete and Nitella have been found to contain lignin-like components [49,57-59], potentially used for cell wall reinforcement during pathogen attack. Moreover, the basal-branching streptophyte algae Klebsormidium spp.…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…Some groups in this order divide centripetally (e.g., filamentous desmids) (Hall et al 2008) whereas others, such as the genus Spirogyra, appear to use a reduced but recognizable phragmoplast (Fowke and Pickett-Heaps 1969;Galway and Hardham 1991), although with some functional distinction from embryophyte phragmoplasts (Sawitzky and Grolig 1995). It is not known whether the shared wall between primitive filamentous charophyte algal cells are specialized in any way, but it is known that their walls lack many of the complex carbohydrate polymers present in advanced charophytes and embryophytes (Sørensen et al 2010(Sørensen et al , 2011Domozych et al 2012). The more advanced charophyte algae (Charophyceae, Coleochaetophyceae) do have a recognizable phragmoplast that resembles those of embryophytes (PickettHeaps 1967;Marchant and Pickett Heaps 1973).…”

“…Cellulosic walls are found throughout the green algal lineage and in other taxa, but a hexameric cellulose synthase complex evolved uniquely in streptophytes (Tsekos 1999). Other distinctive characteristics of embryophyte cell walls, including complex carbohydrate polymer linkages, first appeared in advanced charophyte green algae (Van Sandt et al 2007;Popper et al 2011;Sørensen et al 2011;Domozych et al 2012;Proseus and Boyer 2012). The recent discovery of expansin genes in the Zygnematophycean alga Micrasterias suggests that these critical cell wall remodeling proteins from embryophytes originated in charophyte algae (Cosgrove 2000;Vannerum et al 2011).…”