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Darienko, T.

Publications and source records attributed to Darienko, T..

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Signatures for conserved phenolic-based acclimation responses to UV in a unicellular algal sister of land plants

Ultraviolet (UV) light is a major stressor that particularly comes to bear in the terrestrial habitat. As such it is among the major challenges that the earliest land plants had to overcome. The closest algal relatives of land plants, the zygnematophytes, are single celled and filamentous algae that - in the context of their terrestrial and freshwater habitats - have diverse adaptations to UV irradiance. As such, contextualized with data on land plants, zygnematophyte algae harbor important information for inferring how the earliest land plants have acclimated to UV. Here we exposed the unicellular zygnematophyte model Mesotaenium to daily UV irradiance and assessed its response through microscopy, untargeted metabolomics, and global gene expression profiling using transcriptomics. Our data reveal cell biological acclimation by formation of lipid droplets. Further, we find that the cells accumulated chemodiverse coumarin-like derivatives. Altogether, our data suggest that acclimation to long-term UV exposure is composed of building blocks of a molecular chassis conserved with that of land plants, underpinned by phenolics and genes that are tied to their biosynthesis. From this chassis, divergent evolutionary trajectories have assembled them into a divergent conformation - one of which ushering in the emergence of the phenylpropanoid pathway.

evolutionary biology↗

A deep genetic structure phylogenomically frames the closest algal relatives of land plants

To discern the nature of the closest streptophyte algal relatives of land plants (embryophytes) is a major question in the field of plant evolutionary biology; discerning that nature is essential for our ability to infer the last common ancestor of embryophytes and algae, allowing to retrace the adaptations that ushered in the conquest of land by plants. Albeit initially coming as a surprise, all major phylogenomic efforts have concluded that the Zygnematophyceae are the algal sisters to land plants1-6. The Zygnematophyceae are the streptophyte algal class with the greatest species richness7 and while we now have ample genome information on a few select members of zygnematophytes8-13, our understanding of the genetic and genomic divergence as well as potential is limited by a lack of phylodiverse data that accounts for this diversity and integrates it into a phylogenomic framework. We here sequenced 43 new transcriptome datasets for the Zygnematophyceae and built a phylogenomic tree based on a total of 104 zygnematophyceaen transcriptomes and 2243 loci. We recover a deep genetic structure for the Zygnematophyceae, revealing that this algal class is ancient. Despite the deep split between Spirogyrales and their unicellular sister group Desmidiales, most Spirogyrales emerged after pronounced genetic divergence, accommodating the attainment of multicellularity and divergent traits such as unique cell and plastid division13. Overall, our data capture signatures of massive ancient radiations. Zygnematophyceae are characterized by deep genetic divergences that necessitated a phylodiverse sampling to be revealed, together with their vast evolutionary history, and to illuminate the nature of the algal progenitors of land plants.

evolutionary biology↗

Chemodiverse cell systems responses to UV in an algal sister of land plants

Plant terrestrialization necessitated that a barrage of stressors had to be overcome1. Land plants use an integrated response network in adjusting their molecular physiology to terrestrial stressors2--one of the foremost being UV irradiance. The zygnematophytes are the closest streptophyte algal relatives of land plants3-5, are renowned for their resilience to UV stress6-8, and thus allow to glean key information for inferring the UV response toolkit of the earliest land plants9,10. Throughout streptophyte evolution, specialised metabolism radiated into creating diverse compounds used for responses to environmental challenges, such as sun-shielding compounds and antioxidants11-14. This includes UV-shielding compounds like flavonoids and coumarins but also the land plant specific polymer lignin, giving structural support in vascular plants15; homologs of the underpinning core pathway occur in streptophyte algae16. Here, we exposed the zygnematophyte Mesotaenium to UV-B irradiation and profiled its physiology, morphology, transcriptomics as well as metabolomic features. After UV-B exposure, cells showed rapid photophysiological responses and progressively growing terminal vacuoles. Our transcriptome data capture dynamic changes in gene expression of (i) core downstream responses such as genes homologous to phenol metabolic enzymes, photophysiological homeostats, and DNA repair factors; but also (ii) upstream components featuring key homologs of kinase-mediated signalling cascades, as well as light quality and abscisic acid-mediated signalling components. To scrutinize the acclimatory chassis, we created a metabolite feature database specifically for the Mesotaenium metabolome. Upon UV-B exposure, the metabolome displayed pronounced temporal shifts, with several phenolic features that accumulate along the stress-acclimation kinetics. Overall, we capture a chemodiverse response including various phenolics such as purpurogallin-like, methoxypsoralen-like derivatives and coumarins. Our data establish an integrated model for UV responses in the closest algal relatives of land plants, shedding light on the toolkit that allowed the progenitors of land plants to move out of a protective water column.

evolutionary biology↗

The Spirogyra genome: signatures of shared and divergent division and differentiation

Zygnematophytes emerged as the unexpected closest algal relatives of land plants despite their simple body plans, raising questions about the morphogenetic toolkit present in the last common ancestor of land plants and algae. Genomic analyses have revealed that zygnematophytes are cellular giants, sharing homologous frameworks for several phytohormones, secondary metabolites, and key morphogenetic and transcriptional regulatory processes. Zygnematophytes fall into five orders, each of which has charted its own evolutionary path. Here, we have sequenced a contiguous genome of Spirogyra pratensis, the eponymous representative of Spirogyrales and a classical model system for evolutionary cell biology in the green lineage. Building on this genome, we transcriptionally profiled the tractable life cycle of Spirogyra and its responses to a bifactorial gradient of light and temperature. Our data highlight the activation of quiescence and homeostatic programs. Yet what stands out most in Spirogyra is its spiral chloroplast--undulating intracellularly and abscising during mixed phragmoplast formation and furrowing. Leveraging the genome in tandem with co-expression network analyses, we describe the molecular underpinnings of the unique cytokinetic processes that govern both cell and plastid division. We find that Spirogyra deploys a molecular program characteristic of Phragmoplastophyta, yet lacks the deeply conserved plastid division machinery found in other archaeplastid plastids.

plant biology↗

Systems acclimation to osmotic stress in zygnematophyte cells

Zygnematophytes are the closest algal relatives of land plants. They hold key information to infer how the earliest land plants overcame the barrage of terrestrial stressors, prime of which is osmotic stress. Here, we applied two osmotic stressors on a unicellular and a multicellular representative of zygnematophytes and studied their response over a 25-hour time course generating 130, 60, and 30 of transcriptomic, proteomic, and metabolomic samples combined with photophysiology, sugar analysis, immunocytochemical glycoprotein analysis, and microscopy. Our data highlight a shared protein chassis that shows divergent responses with the same outcome: successful acclimation to osmotic challenges. We establish a model of how the algal sisters of land plants can overcome a prime stressor in the terrestrial habitat and highlight components of the plant terrestrialization toolkit.

evolutionary biology↗

Time-resolved oxidative signal convergence across the algae-embryophyte divide

The earliest land plants faced a significant challenge in adapting to environmental stressors. Stress on land is unique in its dynamics, entailing swift and drastic changes in light and temperature. While we know that land plants share with their closest streptophyte algal relatives key components of the genetic makeup for dynamic stress responses, their concerted action is little understood. Here, we combined time-course stress profiling using photophysiology, transcriptomics on 2.7 Tbp of data, and metabolite profiling analyses on more than 270 distinct samples, to study stress kinetics across three 600-million-year-divergent streptophytes. Through co-expression analysis and Granger causal inference we predict a gene regulatory network that retraces a web of ancient signal convergence at ethylene signaling components, osmosensors, and chains of major kinases. These kinase hubs already integrated diverse environmental inputs since before the dawn of plants on land.

evolutionary biology↗

Phylogenomic insights into the first multicellular streptophyte

Streptophytes are best known as the clade containing the teeming diversity of embryophytes (land plants)1-4. Next to embryophytes are however a range of freshwater and terrestrial algae that bear important information on the emergence of key traits of land plants. Among these, the Klebsormidiophyceae stand out. Thriving in diverse environments--from mundane (ubiquitous occurrence on tree barks and rocks) to extreme (from the Atacama Desert to the Antarctic); Klebsormidiophyceae can exhibit filamentous body plans and display remarkable resilience as colonizers of terrestrial habitats5,6. Currently, the lack of a robust phylogenetic framework for the Klebsormidiophyceae hampers our understanding of the evolutionary history of these key traits. Here, we conducted a phylogenomic analysis utilizing advanced models that can counteract systematic biases. We sequenced 24 new transcriptomes of Klebsormidiophyceae and combined them with 14 previously published genomic and transcriptomic datasets. Using phylogenomic analysis built on 420 loci and sophisticated models, we establish a novel phylogenetic structure, dividing the six distinct genera of Klebsormidiophyceae in a novel four-order-system, with deep divergences more than 898, 765, and 734 million years ago. The reconstruction of ancestral states for habitat suggests an evolutionary history of multiple transitions between terrestrial-aquatic habitats, with Klebsormidiales having conquered land earlier than embryophytes. Focusing on the body plan of the last common ancestor of Klebsormidiophyceae, we postulate it was likely filamentous whereas the sarcinoids and unicells in Klebsormidiophyceae are likely derived states. Our data reveal that the first multicellular streptophytes likely lived more than 900 million years ago.

evolutionary biology↗

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

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. HIGHLIGHTSO_LIGenomes of four filamentous algae (Zygnema) sisters to land plants C_LIO_LIZygnema are rich in genes for multicellular growth and environmental acclimation: signaling, lipid modification, and transport C_LIO_LICell wall innovations: diversification of hexameric rosette cellulose synthase in Zygnematophyceae C_LIO_LICo-expression networks reveal conserved modules for balancing growth and acclimation C_LI

evolutionary biology↗

Environmental gradients reveal stress hubs predating plant terrestrialization

Plant terrestrialization brought forth the land plants (embryophytes). Embryophytes account for most of the biomass on land and evolved from streptophyte algae in a singular event. Recent advances have unraveled the first full genomes of the closest algal relatives of land plants; among the first such species was Mesotaenium endlicherianum. Here, we used fine-combed RNAseq in tandem with photophysiological assessment on Mesotaenium exposed to a continuous range of temperature and light cues. Our data establish a grid of 42 different conditions, resulting in 128 transcriptomes and ~1.5 Tbp (~9.9 billion reads) of data to study combinatory effects of stress response using clustering along gradients. We describe major hubs in genetic networks underpinning stress response and acclimation in the molecular physiology of Mesotaenium. Our data suggest that lipid droplet formation, plastid and cell wall-derived signals denominate molecular programs since more than 600 million years of streptophyte evolution--before plants made their first steps on land.

evolutionary biology↗

A phylogenomically informed five-order system for the closest relatives of land plants

The evolution of streptophytes had a profound impact on life on Earth. They brought forth those photosynthetic eukaryotes that today dominate the macroscopic flora: the land plants (Embryophyta) [1]. There is convincing evidence that the unicellular/filamentous Zygnematophyceae--and not the morphologically more elaborate Coleochaetophyceae or Charophyceae--are the closest algal relatives of land plants [2, 3, 4, 5, 6]. Despite the species richness (>4,000), wide distribution, and key evolutionary position of the zygnematophytes, their internal phylogeny remains largely unresolved [7, 8]. There are also putative zygnematophytes with interesting body plan modifications (e.g., filamentous growth) whose phylogenetic affiliations remain unknown. Here, we studied a filamentous green alga (strain MZCH580) from an Austrian peat bog with central or parietal chloroplasts that lack discernible pyrenoids. It represents Mougeotiopsis calospora PALLA, an enigmatic alga that was described more than 120 years ago [9], but never subjected to molecular analyses. We generated transcriptomic data of M. calospora strain MZCH580, and conducted comprehensive phylogenomic analyses (326 nuclear loci) for 46 taxonomically diverse zygnematophytes. Strain MZCH580 falls in a deep-branching zygnematophycean clade together with some unicellular species, and thus represents a formerly unknown zygnematophycean lineage with filamentous growth. Our well-supported phylogenomic tree lets us propose a new five-order system for the Zygnematophyceae, and provides evidence for at least five independent origins of true filamentous growth in the closest algal relatives of land plants. This phylogeny provides a robust and comprehensive framework for performing comparative analyses and inferring the evolution of cellular traits and body plans in the closest relatives of land plants.

evolutionary biology↗