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.

The origin and early evolution of plants

“…Viridiplantae were well adapted to the cryoconite meltwater ponds that would have formed on snowball Earth [142]. In addition, based on divergence time estimates and adaptations of extant glacier algae (i.e., to desiccation, high irradiance, and extreme temperatures), it has been proposed that streptophyte algae dominated surface ice environments of Cryogenian Snowball Earth [143]. Extant glacier algae produce dark pigmentation, which protects them from exposure to high irradiance [123].…”

Zygospores of the green alga Spirogyra: new insights from structural and chemical imaging

“…The majority of research conducted on the stress tolerance of Zygnematophyceae focuses on the physiology and cell biology of their vegetative state. While vegetative adaptation strategies are necessary for the persistence of streptophyte green algae in semi-terrestrial habitats, another strategy might have been crucial for the process of terrestrialization, and as shown recently the evolution of sexual reproduction in the Cryogenian had remarkable similarities in Zygnematophyceae and zygomycetous fungi ( Žárský et al., 2022 ). Sexual reproduction in Zygnematophyceae strictly occurs by conjugation and does not involve the presence of flagellated male gametes, decoupling this process from the availability of water.…”

A nuclear Pandora’s box: functions of nuclear envelope proteins in cell division

“…Evolution of land plants not only provides distinct gene copy numbers, but also divergence of mitotic apparatus. For instance, P. patens do not form characteristic microtubular PPB ( Buschmann and Zachgo 2016 ), Zygnematophyceae lacks phragmoplast ( Žárský et al 2022 ), basal streptophyte algae use microtubules asters and cleavage furrow instead of PPB and phragmoplast, respectively ( Buschmann and Zachgo 2016 ). At the same time, genetic materials are available with double PPB in cycb1;1 cycb1;2 ( Romeiro Motta et al 2022 ) or PPB-depleted cells in trm678 mutant ( Schaefer et al 2017 ).…”