Homogalacturonan Accumulation in Cell Walls of the Green Alga Zygnema sp. (Charophyta) Increases Desiccation Resistance

Abstract

Land plants inherited several traits from their green algal ancestors (Zygnematophyceae), including a polysaccharide-rich cell wall, which is a prerequisite for terrestrial survival. A major component of both land plant and Zygnematophyceaen cell walls is the pectin homogalacturonan (HG), and its high water holding capacity may have helped algae to colonize terrestrial habitats, characterized by water scarcity. To test this, HG was removed from the cell walls of Zygnema filaments by pectate lyase (PL), and their effective quantum yield of photosystem II (YII) as a proxy for photosynthetic performance was measured in response to desiccation stress by pulse amplitude modulation (PAM). Old filaments were found to contain more HG and are more resistant against desiccation stress but relatively lose more desiccation resistance after HG removal than young filaments. After rehydration, the photosynthetic performance recovered less efficiently in filaments with a HG content reduced by PL, independently of filament age. Immunolabeling showed that partial or un-methylesterified HG occurs throughout the longitudinal cell walls of both young and old filaments, while no labeling signal occurred when filaments were treated with PL prior labeling. This confirmed that most HG can be removed from the cell walls by PL. The initial labeling pattern was restored after ~3 days. A different form of methylesterified HG was restricted to cell poles and cross cell walls. In conclusion, it was shown that the accumulation of HG in Zygnema filaments increases their resistance against desiccation stress. This trait might have played an important role during the colonization of land by Zygnematophyceae, which founded the evolution of all land plants.

Metatranscriptomic and metabolite profiling reveals vertical heterogeneity within a Zygnema green algal mat from Svalbard (High Arctic)

“…Cell wall modifications of the major pectin compound homogalacturonan have recently described in correlation with an increased desiccation tolerance of older cells of Z . circumcarinatum (Herburger et al ., ). In 12‐month‐old cells, GalA was ~50% higher than in young cells (Herburger et al ., ).…”

“…circumcarinatum (Herburger et al ., ). In 12‐month‐old cells, GalA was ~50% higher than in young cells (Herburger et al ., ). The genome analysis of C .…”

“…Cell wall modifications of the major pectin compound homogalacturonan have recently described in correlation with an increased desiccation tolerance of older cells of Z. circumcarinatum (Herburger et al, 2019). In 12-month-old cells, GalA was~50% higher than in young cells (Herburger et al, 2019). The genome analysis of C. braunii showed land plant like cell wall metabolic pathways (Nishiyama et al, 2018), despite that this organism is strictly aquatic.…”

“…The cell walls of charophyte algae recently received a lot of attention, linking their composition to stress resistance and adhesion ; Holzinger and Pichrtová, 2016, Palacio-López et al, 2019, Herburger et al, 2019. The metatranscriptome of the top layer of the Zygnema mat exhibited an induction of various enzymes involved in cell wall formation and modification.…”

“…Arabinogalactan proteins have been detected in Z. circumcarinatum, possibly participating in adhesion phenomena (Palacio-López et al, 2019). Cell wall modifications of the major pectin compound homogalacturonan have recently described in correlation with an increased desiccation tolerance of older cells of Z. circumcarinatum (Herburger et al, 2019). In 12-month-old cells, GalA was~50% higher than in young cells (Herburger et al, 2019).…”