Divergent responses in desiccation experiments in two ecophysiologically different Zygnematophyceae

Abstract

Water scarcity can be considered a major stressor on land, with desiccation being its most extreme form. Land plants have found two different solutions to this challenge: avoidance and tolerance. The closest algal relatives to land plants, the Zygnematophyceae, use the latter, and how this is realized is of great interest for our understanding of the conquest of land. Here, we worked with two representatives of the Zygnematophyceae, Zygnema circumcarinatum SAG 698‐1b and Mesotaenium endlicherianum SAG 12.97, who differ in habitats and drought resilience. We challenged both algal species with severe desiccation in a laboratory setup until photosynthesis ceased, followed by a recovery period. We assessed their morphological, photophysiological, and transcriptomic responses. Our data pinpoint global differential gene expression patterns that speak of conserved responses, from calcium‐mediated signaling to the adjustment of plastid biology, cell envelopes, and amino acid pathways, between Zygnematophyceae and land plants despite their strong ecophysiological divergence. The main difference between the two species appears to rest in a readjustment of the photobiology of Zygnema, while Mesotaenium experiences stress beyond a tipping point.

Time-resolved oxidative signal convergence across the algae–embryophyte divide

“…Mesotaenium endlicherianum SAG 12.97 and Zygnema circumcarinatum SAG 698-1b were obtained from the Culture Collection of Algae at Göttingen University (SAG) and grown on cellophane disks (folia®, Max Bringmann KG) as described 86 prior to stress treatment with the exception that in both cases agarized (1%) Woods Hole Medium (WHM) 87 was used. In short, fully-grown plates of stock cultures were suspended and inoculated on fresh WHM plates.…”

A multidisciplinary view on plant terrestrialization and the evolution of land plants

“…Streptophyte algae diversified over several hundred million years and, like land plants, it can be expected that not all algae are able to tolerate abiotic challenges to the same extent. Here, Rieseberg et al (2023) investigated two Zygnematophyceae that differ in their tolerance to drought. Yet, despite their million years divergence, their response to stress appears to employ a similar molecular network, which mirrors that of embryophyte responses, including calcium‐integrated signaling, amino acid metabolism and molding of plastid biology.…”

“…These studies clearly showed the general ability of streptophyte algae to adapt to different abiotic conditions. Yet, it also appears that this adaptability is broadly diversified even within the same streptophyte algal class (Rieseberg et al, 2023). Another perspective on abiotic stress responses in the Zygnematophyceae was presented by Permann et al (2024), who investigated freezing tolerance in two Mougeotia strains.…”

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

“…Multiple detailed reviews on the abiotic stress tolerance of streptophyte green algae have been conducted over the past decade (Holzinger & Karsten, 2013 ; Holzinger & Pichrtová, 2016 ; Becker et al, 2020 ; Permann et al, 2022a ). Just recently, a comprehensive study on the morphological, photophysiological, and transcriptomic response of two Zygnematophyceae to desiccation stress was also performed (Rieseberg et al, 2023 ). Briefly, vegetative filaments have been shown to accumulate cellular storage/ protective compounds and to increase their cell wall thickness for protection (Herburger & Holzinger, 2015 ; Pichrtová et al, 2016 ; Holzinger et al, 2018 ; Herburger et al, 2019 ).…”