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

Abstract

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.

Cracking the floral quartet code: How do multimers of MIKCC-type MADS-domain transcription factors recognize their target genes?

“…MIKC-type genes have so far been found in all the five major clades of charophytes, but not in chlorophytes yet, corroborating the view that they are a genuine ‘synapomorphy’ (shared derived trait) of streptophytes (that is charophytes + embryophytes) [21-23, 27]. This finding strongly suggests that MIKC-type genes originated in the stem group of extant streptophytes when a Type II MADS-box gene acquired a K box by unresolved mutation or recombination events.…”

“…These MTFs were hence termed MIKC-type proteins, the corresponding genes MIKC-type genes. However, the analysis of the genomes of diverse charophytes -a grade of green algae that represents the closest relatives of land plants (embryophytes) -revealed that they contain Type II gene lineages that have K boxes and others that do not [21][22][23], implying that the terms 'Type II genes of plants' and 'MIKC-type genes' should not be used synonymously anymore. This finding also corroborates the view that the absence of a K-box is not a sufficient criterion for classifying a plant MADS-box gene as Type I (as, unfortunately, can sometimes be seen in the literature).…”

“…This finding strongly suggests that MIKC-type genes originated in the stem group of extant streptophytes when a Type II MADS-box gene acquired a K box by unresolved mutation or recombination events. Whole genome analyses revealed that there are very few MIKC-type genes in extant charophyte species [22, 23, 27], suggesting that there possibly might have been just one MIKC-type gene in the most recent common ancestor (MRCA) of extant land plants.…”

Green land: Multiple perspectives on green algal evolution and the earliest land plants

“…The last common ancestor of all embryophytes likely possessed many adaptations to living on land; further, being the last common ancestor, it had the genetic chassis that underpins traits that count among the synapomorphies of the land plant clade. Recent comparative (functional) genomic studies have revealed that various traits—or at least the genes that underpin these traits in land plants—that were considered embryophyte‐specific are also found in streptophyte algae (Hori et al, 2014; de Vries et al, 2017, 2018; Nishiyama et al, 2018; Feng et al, 2023). These include genes for phytohormone signaling cascades (Hori et al, 2014; de Vries et al, 2018; Nishiyama et al, 2018; Cheng et al, 2019; Jiao et al, 2020), transcription factors (Wilhelmsson et al, 2017), specialized metabolism (Rieseberg et al, 2023), and biotic interactions (Delaux et al, 2015; Delaux and Schornack, 2021).…”

“…Functional work on the PYL homolog of Zygnema revealed a partial mechanistic conservation: while PYL does interact with its downstream target, PP2C, this interaction is not modulated by ABA (Sun et al, 2019). Genomic data have confirmed the presence of PYL homologs in several zygnematophytes (Cheng et al, 2019;Feng et al, 2023). Hence, the question of how the PYL-PP2C signaling cascade contributes to the molecular physiology of zygnematophytes remains wide open.…”