Cryogenian Glacial Habitats as a Plant Terrestrialisation Cradle - The Origin of the Anydrophytes and Zygnematophyceae Split

Abstract

For tens of millions of years (Ma), the terrestrial habitats of Snowball Earth during the Cryogenian period (between 720 and 635 Ma before present-Neoproterozoic Era) were possibly dominated by global snow and ice cover up to the equatorial sublimative desert. The most recent time-calibrated phylogenies calibrated not only on plants but on a comprehensive set of eukaryotes indicate that within the Streptophyta, multicellular charophytes (Phragmoplastophyta) evolved in the Mesoproterozoic to the early Neoproterozoic. At the same time, Cryogenian is the time of the likely origin of the common ancestor of Zygnematophyceae and Embryophyta and later, also of the Zygnematophyceae-Embryophyta split. This common ancestor is proposed to be called Anydrophyta; here, we use anydrophytes. Based on the combination of published phylogenomic studies and estimated diversification time comparisons, we deem it highly likely that anydrophytes evolved in response to Cryogenian cooling. Also, later in the Cryogenian, secondary simplification of multicellular anydrophytes and loss of flagella resulted in Zygnematophyceae diversification as an adaptation to the extended cold glacial environment. We propose that the Marinoan geochemically documented expansion of first terrestrial flora has been represented not only by Chlorophyta but also by Streptophyta, including the anydrophytes, and later by Zygnematophyceae, thriving on glacial surfaces until today. It is possible that multicellular early Embryophyta survived in less abundant (possibly relatively warmer) refugia, relying more on mineral substrates, allowing the retention of flagella-based sexuality. The loss of flagella and sexual reproduction by conjugation evolved in Zygnematophyceae and zygomycetous fungi during the Cryogenian in a remarkably convergent way. Thus, we support the concept that the important basal cellular adaptations to terrestrial environments were exapted in streptophyte algae for terrestrialization and propose that this was stimulated by the adaptation to glacial habitats dominating the Cryogenian Snowball Earth. Including the glacial lifestyle when considering the rise of land plants increases the parsimony of connecting different ecological, phylogenetic, and physiological puzzles of the journey from aquatic algae to terrestrial floras.

Keywords: Anydrophyta; Charophyta; Cryogenian glaciation; Embryophyta; Snowball Earth; Streptophyta; Zygnematophyceae; plant evolution.

FIGURE 1

(A) The phylogenetic tree with time estimates for the splits of Chlorophyta–Streptophyta and Zygnematophyceae–Embryophyta. Tree adapted from Morris et al. (2018b), projected over timescale based on international geostratigraphic chart (2020). The red lines at the respective node represent 95% highest posterior densities of estimates presented by Hedges et al. (2018), Morris et al. (2018b), Strassert et al. (2021), and Su et al. (2021): a–Streptophyta, Morris et al. (2018b) all calibrations, b–Streptophyta, Hedges et al. (2018) Mesozoic calibrations, c–Streptophyta, Hedges et al. (2018) Spermatophyta calibration, d–Streptophyta, Strassert et al. (2021), e–Embryophyta, Morris et al. (2018b) all calibrations, f–Embryophyta, Hedges et al. (2018) Mesozoic calibrations, g–Embryophyta, Hedges et al. (2018) Spermatophyta calibration, h–Embryophyta, Su et al. (2021), Strassert et al. (2021). j–Influx of terrestrial carbon is apparent in carbonates younger than 850 Ma, according to a study of Knauth and Kennedy (2009), who infer an explosion of photosynthesizing communities on late Precambrian land surfaces. (B) Schematic presentation of the potential freshwater habitats in a low latitude Cryogenian catchment. The picture represents habitats populated by members of streptophyte algae in the current biosphere (A) Lentic habitats (Mesostigma, Chara), (B) fluvial habitats with various Zygnematophyceae in the phytobenthos and e.g., Coleochaete on submerged surfaces, (C) subaeric habitats, moist or periodically submerged surfaces, and biological soil crusts (e.g., Klebsormidium, Chlorokybus, and some Zygnematophyceae).

FIGURE 2

Paleontological and geological evidence for the continental (most probably eukaryotic) organisms and primary production by photosynthetic organisms/plants from the Neoproterozoic through Cryogenian to the early Paleozoic. For our hypothesis, the existence of desmids in the early Ediacaran, as indicated by the Acritarch zygospores ascribed to Desmidiales (Moczydłowska and Liu, 2021), is of central importance.

FIGURE 3

Hypothetical scenario of anydrophyte establishment and Zygnematophyceae split off by the evolutionary reduction under the extended Cryogenian glaciations.