Phylogenomic insights into the first multicellular streptophyte

Bierenbroodspot, Maaike J.; Darienko, Tatyana; de Vries, Sophie; Fürst-Jansen, Janine M.R.; Buschmann, Henrik; Pröschold, Thomas; Irisarri, Iker; de Vries, Jan

doi:10.1016/j.cub.2023.12.070

Cited by 25 publications

(6 citation statements)

References 123 publications

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“…Owing to the intensified efforts to understand the origin of land plants, it becomes apparent that many of the key traits of land plants have deep evolutionary roots (Hori et al, 2014;Delaux et al, 2015;Feng et al, 2023;Dadras et al, 2023b;Bierenbroodspot et al, 2024;Kuhn et al, 2024)-and chemodiversity is a point in case. One major contributor to the specialized metabolism that makes up embryophytic chemodiversity is the CYPs.…”

Section: Discussionmentioning

confidence: 99%

Sequence similarity networks bear out hierarchical relationships of green cytochrome P450

Dhabalia Ashok,

Freitag,

Irisarri

et al. 2024

Physiologia Plantarum

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Land plants have diversified enzyme families. One of the most prominent is the cytochrome P450 (CYP or CYP450) family. With over 443,000 CYP proteins sequenced across the tree of life, CYPs are ubiquitous in archaea, bacteria, and eukaryotes. Here, we focused on land plants and algae to study the role of CYP diversification. CYPs, acting as monooxygenases, catalyze hydroxylation reactions crucial for specialized plant metabolic pathways, including detoxification and phytohormone production; the CYPome consists of one enormous superfamily that is divided into clans and families. Their evolutionary history speaks of high substrate promiscuity; radiation and functional diversification have yielded numerous CYP families. To understand the evolutionary relationships within the CYPs, we employed sequence similarity network analyses. We recovered distinct clusters representing different CYP families, reflecting their diversified sequences that we link to the prediction of functionalities. Hierarchical clustering and phylogenetic analysis further elucidated relationships between CYP clans, uncovering their shared deep evolutionary history. We explored the distribution and diversification of CYP subfamilies across plant and algal lineages, uncovering novel candidates and providing insights into the evolution of these enzyme families. This identified unexpected relationships between CYP families, such as the link between CYP82 and CYP74, shedding light on their roles in plant defense signaling pathways. Our approach provides a methodology that brings insights into the emergence of new functions within the CYP450 family, contributing to the evolutionary history of plants and algae. These insights can be further validated and implemented via experimental setups under various external conditions.

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Section: Discussionmentioning

confidence: 99%

Sequence similarity networks bear out hierarchical relationships of green cytochrome P450

Dhabalia Ashok,

Freitag,

Irisarri

et al. 2024

Physiologia Plantarum

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“…Throughout their evolutionary history, Zygnematophyceae have transitioned several times between multicellular and unicellular body plans 6 . A parsimonious explanation is that streptophytes share an ancient toolkit for multicellularity 82 , 83 , which comes to bear in filamentous genera but is still lingering as genetic potential in zygnematophyte unicells. And indeed, our data on shared OG expansions recover several important regulatory genes for increasing cellular complexity in the LCAs both of Z + E and of Zygnematophyceae.…”

Section: Discussionmentioning

confidence: 99%

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

Feng,

Zheng,

Irisarri

et al. 2024

Nat Genet

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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.

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“…More recently, Glass et al 2 sequenced the plastid genome of S. capillatum and corroborated its separate phylogenetic status by analyzing a set of 44 plastid-encoded proteins, placing the alga with full support sister to nearly all other streptophytes combined except for the more basally positioned genera Mesostigma and Chlorokybus . From this perspective, the results of the phylotranscriptomic analysis reported by Bierenbroodspot et al 3 are highly surprising: having S. capillatum positioned within Klebsormidiophyceae in a tight clade together with representatives of the genus Interfilum (even making the genus paraphyletic), their tree separates the alga from the position implied by the plastid genes-based phylogeny by five fully supported nodes.…”

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confidence: 94%

“…A subsequent phylogenetic analysis of plastid genome-encoded proteins resolved Streptofilum as a sister group of nearly all known streptophytes, including Klebsormidiophyceae and Phragmoplastophyta (Charophyceae, Coleochaetophyceae, Zygnematophyceae, and embryophytes) 2 . In a stark contrast, another recent report, published in Current Biology by Bierenbroodspot et al 3 , presented a phylogenetic analysis of 845 nuclear loci resolving S. capillatum as a member of Klebsormidiophyceae, nested among species of the genus Interfilum . Here we demonstrate that the latter result is an artefact stemming from an unrecognized contamination of the transcriptome assembly from S. capillatum by sequences from Interfilum paradoxum .…”

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Phylogenomics definesStreptofilumas a novel deep branch of streptophyte algae

Žárský,

Eliáš

2024

Preprint

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Streptophytes constitute a major organismal clade comprised of land plants (embryophytes) and several related green algal lineages. Their seemingly well-studied phylogenetic diversity was recently enriched by the discovery ofStreptofilum capillaum, a simple filamentous alga forming a novel deep streptophyte lineage in a two-gene phylogeny. A subsequent phylogenetic analysis of plastid genome-encoded proteins resolvedStreptofilumas a sister group of nearly all known streptophytes, including Klebsormidiophyceae and Phragmoplastophyta (Charophyceae, Coleochaetophyceae, Zygnematophyceae, and embryophytes). In a stark contrast, another recent report (Bierenbroodspot et al. "Phylogenomic insights into the first multicellular streptophyte."Current Biology34.3 (2024): 670-681.), presented a phylogenetic analysis of 845 nuclear loci resolvingS. capillatumas a member of Klebsormidiophyceae, nested among species of the genusInterfilum. Here we demonstrate that the latter result is an artefact stemming from an unrecognized contamination of the transcriptome assembly fromS. capillatumby sequences fromInterfilum paradoxum. When genuineS. capillatumsequences are employed in the analysis, the position of the alga in the nuclear genes-based tree fully agrees with the plastid genes-based phylogeny. The "intermediate" phylogenetic position ofS. capillatumpredicts it to possess a unique combination of derived and plesiomorphic traits, here exemplified, respectively, by the "Rho of plants" (ROP) signaling system and the cyanobacteria-derived plastidial transfer-messenger ribonucleoprotein complex (tmRNP). Our results underscoreS. capillatumas a lineage pivotal for the understanding of the evolutionary genesis of streptophyte, and ultimately embryophyte, traits.

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Phylogenomic insights into the first multicellular streptophyte

Cited by 25 publications

References 123 publications

Sequence similarity networks bear out hierarchical relationships of green cytochrome P450

Sequence similarity networks bear out hierarchical relationships of green cytochrome P450

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

Phylogenomics definesStreptofilumas a novel deep branch of streptophyte algae

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