Genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Abstract

Zygnematophyceae are the algal sisters of land plants. Here we sequenced four genomes of filamentous Zygnematophyceae, including chromosome-scale assemblies for three strains of Zygnema circumcarinatum. We inferred traits in the ancestor of Zygnematophyceae and land plants that might have ushered in the conquest of land by plants: expanded genes for signaling cascades, environmental response, and multicellular growth. Zygnematophyceae and land plants share all the major enzymes for cell wall synthesis and remodifications, and gene gains shaped this toolkit. Co-expression network analyses uncover gene cohorts 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.

Evolutionary assembly of the plant terrestrialization toolkit from protein domains

“…Molecular traits emerging from LGP include the moulding of hallmark signalling, biotic interactions and specialized metabolic processes. This is likely no coincidence, consistent with signalling network remodelling [ 26 , 73 ], biotic stress-driven co-evolution [ 74 ] and the promiscuity of specialized metabolism [ 75 ], and as such a hotbed for biological novelty. Overall, our data suggest that novel combinations of old genomic substrate shaped the plant terrestrialization toolkit.…”

“…Both are prominent across all lineages and showcase an increase in first abundance of proteins followed by orthogroup expansions upon the emergence of Phragmoplastophyta and of land plants ( figure 2 c ). This speaks of a fine-tuning of environmental input and—the likely ancestral—multicellular growth of Phragmoplastophyta [ 26 , 53 ]. Indeed, among the top 100 changes in orthogroup numbers with stress domain-containing proteins, 90.2% of the relevant LCAs show a stronger increase in protein numbers than in orthogroup numbers.…”

“…Extant streptophytes display a mosaic of traits, brought about by processes like parallelism, convergence and rampant gene loss of key traits, concomitant with genomic streamlining in the Zygnematophyceae [ 20 , 26 , 62 , 69 , 70 ]. Yet, it is difficult to infer deep evolutionary processes that underlie genomic novelty by looking only at extant species: properties salient to a terrestrial lifestyle shared by land plants and streptophyte algae can be interpreted as exaptations [ 6 ], or adaptations under the assumption that the LCA of streptophytes was a terrestrial organism [ 71 ]—but there have been multiple habitat transitions [ 72 ].…”

“…Comparative genomic analyses reveal that a substantial fraction of molecular physiological tools that land plants use to cope with terrestrial stressors can also be found in streptophyte algae, their last common ancestors (LCAs), and the LCA of streptophyte algae and land plants; all these ancestors had iterations of the complex genetic networks of land plants [21][22][23][24][25][26][27]. Several aspects have been investigated in the past decade through comparative analyses.…”

“…One of the foremost are the deep evolutionary roots of phytohormone signalling cascades. For example, a complete chassis of homologues for the signalling cascade of the stress hormone abscisic acid (ABA) was found in several Zygnematophyceae [26,28,29] but functional analyses revealed that the protein homologues, albeit inhibiting downstream phosphatases, act ABA-independently [30]. Another interesting evolutionary pattern was recovered for the phytohormone auxin, whose polar distribution determines diverse aspects of growth and development in land plants [31][32][33].…”