Abstract
Mounting evidence suggests that terrestrialization of plants started in streptophyte green algae, favoured by their dual existence in freshwater and subaerial/terrestrial environments. Here, we present the genomes of Mesostigma viride and Chlorokybus atmophyticus, two sister taxa in the earliest-diverging clade of streptophyte algae dwelling in freshwater and subaerial/terrestrial environments, respectively. We provide evidence that the common ancestor of M. viride and C. atmophyticus (and thus of streptophytes) had already developed traits associated with a subaerial/terrestrial environment, such as embryophyte-type photorespiration, canonical plant phytochrome, several phytohormones and transcription factors involved in responses to environmental stresses, and evolution of cellulose synthase and cellulose synthase-like genes characteristic of embryophytes. Both genomes differed markedly in genome size and structure, and in gene family composition, revealing their dynamic nature, presumably in response to adaptations to their contrasting environments. The ancestor of M. viride possibly lost several genomic traits associated with a subaerial/terrestrial environment following transition to a freshwater habitat.
Highlights
Transition to a terrestrial environment, termed terrestrialization, is generally regarded as a pivotal event in the evolution and diversification of land plant flora[1]
The draft genomes of M. viride and C. atmophyticus reported here allowed us to address two questions important for plant terrestrialization: (1) did the common ancestor of streptophytes already display embryophyte-like genomic traits that would be indicative for adaptation to a terrestrial environment; and (2) how do the genomes of M. viride and C. atmophyticus differ from each other in light of previous genome studies on two streptophyte algae that occur in contrasting environments but belong to different streptophyte classes (Klebsormidiophyceae and Charophyceae)?
Two major conclusions can be drawn from the comparative analysis of the draft genomes of M. viride and C. atmophyticus: first, the common ancestor of M. viride and C. atmophyticus had already developed traits that reflect adaptations to a subaerial/terrestrial habitat, exemplified by the presence of the canonical embryophyte photoreceptor phytochrome (p-PHY), evolution of transcription factors (TFs) implicated in responses to various abiotic and biotic stresses, near-complete pathways for several phytohormones involved in stress signalling and evolution of orthologues of cellulose synthase and cellulose synthase-like genes characteristic of embryophytes
Summary
Transition to a terrestrial environment, termed terrestrialization, is generally regarded as a pivotal event in the evolution and diversification of land plant flora[1]. Homologues of genes once thought to be restricted to embryophytes are being detected in streptophyte algae Examples include those involved in symbiotic or pathogenic interactions with soil microbes[4], phytohormone signalling[5,6,7,8], desiccation/stress[9], plastid/nucleus retrograde signalling[10,11] and cell wall metabolism[12]. The earliest-diverging streptophyte algae are represented by a clade comprising two monospecific genera, Mesostigma and Chlorokybus[14,15,16,17]. Both are structurally simple but differ in their cellular organization, life history and type of habitat[18]. Photosynthesis:antenna proteins Plant hormone signal transduction Plant–pathogen interaction Starch and sucrose metabolism Carbon fixation in photosynthetic organisms
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