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Sexual reproduction in Charophyceae abounds in complex traits. Their gametangia develop as intricate structures, with oogonia spirally surrounded by envelope cells and richly pigmented antheridia. The red—probably protectant—pigmentation of antheridia is conserved across Charophyceae. Chara tomentosa is, however, unique in exhibiting this pigmentation and also in vegetative tissue. Here, we investigated the two sympatric species, C. tomentosa and Chara baltica, and compared their molecular chassis for pigmentation. Using reversed phase C30 high performance liquid chromatography (RP-C30-HPLC), we uncover that the major pigments are β-carotene, δ-carotene and γ-carotene; using headspace solid-phase microextraction coupled to gas chromatography equipped with a mass spectrometer (HS-SPME-GC-MS), we pinpoint that the unusually large carotenoid pool in C. tomentosa gives rise to diverse volatile apocarotenoids, including abundant 6-methyl-5-hepten-2-one. Based on transcriptome analyses, we uncover signatures of the unique biology of Charophycaee and genes for pigment production, including monocyclized carotenoids. The rich carotenoid pool probably serves as a substrate for diverse carotenoid-derived metabolites, signified not only by (i) the volatile apocarotenoids we detected but (ii) the high expression of a gene coding for a cytochrome P450 enzyme related to land plant proteins involved in the biosynthesis of carotenoid-derived hormones. Overall, our data shed light on a key protection strategy of sexual reproduction in the widespread group of macroalgae. The genetic underpinnings of this are shared across hundreds of millions of years of plant and algal evolution. This article is part of the theme issue 'The evolution of plant metabolism'. [ABSTRACT FROM AUTHOR]

Water scarcity can be considered a major stressor on land, with desiccation being its most extreme form. Land plants have found two different solutions to this challenge: avoidance and tolerance. The closest algal relatives to land plants, the Zygnematophyceae, use the latter, and how this is realized is of great interest for our understanding of the conquest of land. Here, we worked with two representatives of the Zygnematophyceae, Zygnema circumcarinatum SAG 698‐1b and Mesotaenium endlicherianum SAG 12.97, who differ in habitats and drought resilience. We challenged both algal species with severe desiccation in a laboratory setup until photosynthesis ceased, followed by a recovery period. We assessed their morphological, photophysiological, and transcriptomic responses. Our data pinpoint global differential gene expression patterns that speak of conserved responses, from calcium‐mediated signaling to the adjustment of plastid biology, cell envelopes, and amino acid pathways, between Zygnematophyceae and land plants despite their strong ecophysiological divergence. The main difference between the two species appears to rest in a readjustment of the photobiology of Zygnema, while Mesotaenium experiences stress beyond a tipping point. [ABSTRACT FROM AUTHOR]

The 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 of Zygnema circumcarinatum and one strain of Z. cylindricum ) and generated chromosome-scale assemblies for all strains of the emerging model system Z. 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., Competing Interests: Declaration of Interests The authors declare no competing interests.