3D‐reconstructions of zygospores in Zygnema vaginatum (Charophyta) reveal details of cell wall formation, suggesting adaptations to extreme habitats

Abstract

The streptophyte green algal class Zygnematophyceae is the immediate sister lineage to land plants. Their special form of sexual reproduction via conjugation might have played a key role during terrestrialization. Thus, studying Zygnematophyceae and conjugation is crucial for understanding the conquest of land. Moreover, sexual reproduction features are important for species determination. We present a phylogenetic analysis of a field‐sampled Zygnema strain and analyze its conjugation process and zygospore morphology, both at the micro‐ and nanoscale, including 3D‐reconstructions of the zygospore architecture. Vegetative filament size (26.18 ± 1.07 μm) and reproductive features allowed morphological determination of Zygnema vaginatum, which was combined with molecular analyses based on rbcL sequencing. Transmission electron microscopy (TEM) depicted a thin cell wall in young zygospores, while mature cells exhibited a tripartite wall, including a massive and sculptured mesospore. During development, cytological reorganizations were visualized by focused ion beam scanning electron microscopy (FIB‐SEM). Pyrenoids were reorganized, and the gyroid cubic central thylakoid membranes, as well as the surrounding starch granules, degraded (starch granule volume: 3.58 ± 2.35 μm3 in young cells; 0.68 ± 0.74 μm3 at an intermediate stage of zygospore maturation). Additionally, lipid droplets (LDs) changed drastically in shape and abundance during zygospore maturation (LD/cell volume: 11.77% in young cells; 8.79% in intermediate cells, 19.45% in old cells). In summary, we provide the first TEM images and 3D‐reconstructions of Zygnema zygospores, giving insights into the physiological processes involved in their maturation. These observations help to understand mechanisms that facilitated the transition from water to land in Zygnematophyceae.

Striking differences in frost hardiness and inability to cold acclimate in two Mougeotia species (Zygnematophyceae) from alpine and lowland habitats

“…While the thylakoid membranes of M. scalaris were more loosely arranged, gyroid cubic membranes (CM) with a moniliform appearance were observed. A complex thylakoid morphology has also been reported at the late log phase and stationary phase of cell growth in Zygnema filaments (Zhan et al, 2017 ) and in the intra‐pyrenoidal membranes of Zygnema zygospores (Permann et al, 2023 ). While in vegetative Zygnema , the transition from lamellar‐like thylakoid membrane morphology to gyroid CM affected the entire chloroplasts (Zhan et al, 2017 ), Mougeotia scalaris , investigated in the present study only showed an occasional formation of the moniliform superstructures.…”

Divergent responses in desiccation experiments in two ecophysiologically different Zygnematophyceae

“…In addition, Zygnema is a special case. In Zygnematophyceae, the most resilient cell types that endure adverse conditions are the zygospores (see, e.g., the detailed investigation by Permann et al [2023] in this special issue). However , Zygnema spp.…”

In the Spotlight: Walk on the Wild Side

“…In the article by Permann et al, (2023), the authors aim to shine a light on the zygospore of Zygnema vaginatum , and its structural adaptations that allow it to survive harsh conditions (Figure 1). The cell wall and the internal cell architecture might provide information on zygospore maturation and their resistance to stress.…”

“…Plants have had a tremendous influence on Earth, and shaped our planet as we know it today. Permann et al, (2023) have added a small part to the story, a story that tells us how it all began.…”