The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum

Abstract

Plant cell walls are essential for proper growth, development, and interaction with the environment. It is generally accepted that land plants arose from aquatic ancestors which are sister groups to the charophycean algae (i.e., Streptophyta), and study of wall evolution during this transition promises insight into structure-function relationships of wall components. In this paper, we explore wall evolutionary history by studying the incorporation of pectin polymers into cell walls of the model organism Penium margaritaceum, a simple single-cell desmid. This organism produces only a primary wall consisting of three fibrillar or fibrous layers, with the outermost stratum terminating in distinct, calcified projections. Extraction of isolated cell walls with trans-1,2-diaminocyclohexane-N,N,N',N'-tetraacetic acid yielded a homogalacturonan (HGA) that was partially methyl esterified and equivalent to that found in land plants. Other pectins common to land plants were not detected, although selected components of some of these polymers were present. Labeling with specific monoclonal antibodies raised against higher-plant HGA epitopes (e.g., JIM5, JIM7, LM7, 2F4, and PAM1) demonstrated that the wall complex and outer layer projections were composed of the HGA which was significantly calcium complexed. JIM5 and JIM7 labeling suggested that highly methyl esterified HGA was secreted into the isthmus zone of dividing cells, the site of active wall secretion. As the HGA was displaced to more polar regions, de-esterification in a non-blockwise fashion occurred. This, in turn, allowed for calcium binding and the formation of the rigid outer wall layer. The patterning of HGA deposition provides interesting insights into the complex process of pectin involvement in the development of the plant cell wall.

Phylogeny and Molecular Evolution of the Green Algae

“…Although some cell wall components do appear to be land plant innovations, cell wall evolution after the colonization of land appears to be characterized mostly by the elaboration of a pre-existing set of cell wall polysaccharides and the enzymes that synthesize them (e.g. cellulose synthase and wall-remodelling enzymes), rather than substantial innovation (Roberts & Roberts, 2004;Domozych et al, 2007;Van Sandt et al, 2007;Eder et al, 2008;Fry et al, 2008;Domozych et al, 2009;Yin et al, 2009;Popper & Tuohy, 2010;Popper et al, 2011).…”

How Have Plant Cell Walls Evolved?

“…A number of studies have provided evidence that in addition to cellulose, many CGA have cell walls that contain components that are common to embryophyte walls (Popper and Fry, 2003;Domozych et al, 2007b;Eder and Lü tz-Meindl, 2009). For example, homogalacturonan (HG) is abundant in the walls of the unicellular desmid Penium margaritaceum and in the charalean species, Chara corallina (Proseus and Boyer, 2006;Domozych et al, 2007b), where in both cases, as is frequently the case in embryophyte walls, it is complexed with calcium.…”

“…For example, homogalacturonan (HG) is abundant in the walls of the unicellular desmid Penium margaritaceum and in the charalean species, Chara corallina (Proseus and Boyer, 2006;Domozych et al, 2007b), where in both cases, as is frequently the case in embryophyte walls, it is complexed with calcium. Moreover, the spatially regulated distribution of HG epitopes with different degrees of methyl esterification (DEs) in P. margaritaceum and Netrium digitus suggest that as in embryophytes, DE is controlled in relation to specific events during cell development (Popper and Fry, 2003;Domozych et al, 2007b;Eder and Lü tz-Meindl, 2009). …”

Evolution of the cell wall components during terrestrialization

“…HG is an important structural component of the primary cell walls, since the pair of HG molecules interconnected by Ca 2+ bridges stiffens the walls [114]. Homogalacturonan seems to be the primary pectin, because it occurs not only in land plants, but also in CGA [11,116,117], where as in embryophytes it may be bridged by calcium. In addition, the distribution of HG epitopes with different degree of esterification with methanol suggests, that in tested algae species, similarly to embryophytes, methyl-esterification is associated with processes of cell growth and differentiation [46,117,118].…”