The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants.

The evolutionary features and molecular innovations that enabled plants to first colonize land are not well understood. Here, insights are provided through our report of the genome sequence of the unicellular alga Penium margaritaceum, a member of the Zygnematophyceae, the sister lineage to land plants. The genome has a high proportion of repeat sequences that are associated with massive segmental gene duplications, likely facilitating neofunctionalization. Compared with representatives of earlier diverging algal lineages, P. margaritaceum has expanded repertoires of gene families, signaling networks, and adaptive responses that highlight the evolutionary trajectory toward terrestrialization. These encompass a broad range of physiological processes and protective cellular features, such as flavonoid compounds and large families of modifying enzymes involved in cell wall biosynthesis, assembly, and remodeling. Transcriptome profiling further elucidated adaptations, responses, and selective pressures associated with the semi-terrestrial ecosystems of P. margaritaceum, where a simple body plan would be an advantage.

Endomembrane architecture and dynamics during secretion of the extracellular matrix of the unicellular charophyte, Penium margaritaceum.

The extracellular matrix (ECM) of many charophytes, the assemblage of green algae that are the sister group to land plants, is complex, produced in large amounts, and has multiple essential functions. An extensive secretory apparatus and endomembrane system are presumably needed to synthesize and secrete the ECM, but structural details of such a system have not been fully characterized. Penium margaritaceum is a valuable unicellular model charophyte for studying secretion dynamics. We report that Penium has a highly organized endomembrane system, consisting of 150-200 non-mobile Golgi bodies that process and package ECM components into different sets of vesicles that traffic to the cortical cytoplasm, where they are transported around the cell by cytoplasmic streaming. At either fixed or transient areas, specific cytoplasmic vesicles fuse with the plasma membrane and secrete their constituents. Extracellular polysaccharide (EPS) production was observed to occur in one location of the Golgi body and sometimes in unique Golgi hybrids. Treatment of cells with brefeldin A caused disruption of the Golgi body, and inhibition of EPS secretion and cell wall expansion. The structure of the endomembrane system in Penium provides mechanistic insights into how extant charophytes generate large quantities of ECM, which in their ancestors facilitated the colonization of land.