Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Abstract

ABSTRACTThe filamentous and unicellular algae of the class Zygnematophyceae are the closest algal relatives of land plants. Inferring the properties of the last common ancestor shared by these algae and land plants allows us to identify decisive traits that enabled the conquest of land by plants. We sequenced four genomes of filamentous Zygnematophyceae (three strains ofZygnema circumcarinatumand one strain ofZ. cylindricum) and generated chromosome-scale assemblies for all strains of the emerging model systemZ. circumcarinatum. Comparative genomic analyses reveal expanded genes for signaling cascades, environmental response, and intracellular trafficking that we associate with multicellularity. Gene family analyses suggest that Zygnematophyceae share all the major enzymes with land plants for cell wall polysaccharide synthesis, degradation, and modifications; most of the enzymes for cell wall innovations, especially for polysaccharide backbone synthesis, were gained more than 700 million years ago. In Zygnematophyceae, these enzyme families expanded, forming co-expressed modules. Transcriptomic profiling of over 19 growth conditions combined with co-expression network analyses uncover cohorts of genes that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.HIGHLIGHTSGenomes of four filamentous algae (Zygnema) sisters to land plantsZygnemaare rich in genes for multicellular growth and environmental acclimation: signaling, lipid modification, and transportCell wall innovations: diversification of hexameric rosette cellulose synthase in ZygnematophyceaeCo-expression networks reveal conserved modules for balancing growth and acclimation