Isolation and manipulation of protoplasts from the unicellular green alga Penium margaritaceum

Raimundo, Sandra Cristina; Sørensen, Iben; Tinaz, Berke; Ritter, Eleanore J.; Rose, Jocelyn K. C.; Domozych, David S.

doi:10.1186/s13007-018-0284-9

Cited by 9 publications

(16 citation statements)

References 101 publications

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“…RNA for ISO-seq was extracted from cells grown for 3 days in mating inducing media (Sørensen et al, 2014) using the RNeasy Mini kit (Qiagen, USA). Nuclei were isolated from the cell pellets (Raimundo et al, 2018) and used as a source of genomic DNA as this yielded far better quality preparations. DNA quality was verified using a Nanodrop™ 2000 Spectrophotometer (Thermo Fisher Scientific, USA) and an Agilent BioAnalyzer (Agilent, Santa Clara, CA, USA).…”

Section: Methodsmentioning

confidence: 99%

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

Jiao

Sørensen

Sun

et al. 2019

Preprint

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30The colonization of land by plants was a pivotal event in the history of the biosphere, and yet the 31 underlying evolutionary features and innovations of the first land plant ancestors are not well 32 understood. Here we present the genome sequence of the unicellular alga Penium margaritaceum, 33 a member of the Zygnematophyceae, the sister lineage to land plants. The P. margaritaceum 34 genome has a high proportion of repeat sequences, which are associated with massive segmental 35 gene duplications, likely facilitating neofunctionalization. Compared with earlier diverging plant 36 lineages, P. margaritaceum has uniquely expanded repertoires of gene families, signaling 37 networks and adaptive responses, supporting its phylogenetic placement and highlighting the 38 evolutionary trajectory towards terrestrialization. These encompass a broad range of physiological 39 processes and cellular structures, such as large families of extracellular polymer biosynthetic and 40 modifying enzymes involved in cell wall assembly and remodeling. Transcriptome profiling of 41 cells exposed to conditions that are common in terrestrial habitats, namely high light and 42 desiccation, further elucidated key adaptations to the semi-aquatic ecosystems that are home to the 43 Zygnematophyceae. Such habitats, in which a simpler body plan would be advantageous, likely 44 provided the evolutionary crucible in which selective pressures shaped the transition to land. 45 Earlier diverging charophyte lineages that are characterized by more complex land plant-like 46 anatomies have either remained exclusively aquatic, or developed alternative life styles that allow 47 109 of 116.1 kb. The nuclear assembly captured most of the k-mers in the Illumina reads and low 110 frequency k-mers representing sequencing errors were absent ( Supplementary Fig. 1B). In addition, 111 the mapping rates of genomic and RNA-Seq reads against the nuclear assembly were 97.5% and 112 5 96.8%, respectively (Supplementary Table 2). The single nucleotide polymorphism (SNP) 113 frequency distribution on the 100 longest scaffolds was consistent with a haploid genome 114 ( Supplementary Fig. 1C). The mitochondrial and chloroplast genomes were also fully assembled, 115 and comprised 95,332 and 145,411 nucleotides, respectively ( Supplementary Fig. 2). 116The assembly contains a large proportion (80.6%) of repeat sequences (Supplementary 117 Table 3), particularly long terminal repeat (LTR) retrotransposons and simple repeats ( Fig. 2A). 118Unlike land plants and C. braunii, in which gypsy is the predominant LTR family, the P. 119 margaritaceum genome has a large proportion of copia retrotransposons, which are rare in other 120 green algae and absent from C. braunii (Nishiyama et al. 2018). An estimation of divergence time 121 indicated that the copia expansion in the P. margaritaceum genome was relatively recent, around 122 2.1 Mya (Fig. 2B). Retrotransposons carrying tyrosine recombinases, such as the DIRS and Ngaro 123 families, which are found in some chlorophyte...

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Section: Methodsmentioning

confidence: 99%

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

Jiao

Sørensen

Sun

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…RNA for ISO-seq was extracted from cells grown for 3 days in mating inducing media (Sørensen et al, 2014) using the RNeasy Mini kit (Qiagen, USA). Nuclei were isolated from the cell pellets (Raimundo et al, 2018) and used as a source of genomic DNA as this yielded far better quality preparations. DNA quality was verified using a Nanodrop™ 2000 not certified by peer review) is the author/funder.…”

Section: Dna and Rna Extractionmentioning

confidence: 99%

The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants

Jiao

Sørensen

Sun

et al. 2020

Cell

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201

192

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The colonization of land by plants was a pivotal event in the history of the biosphere, and yet the underlying evolutionary features and innovations of the first land plant ancestors are not well understood. Here we present the genome sequence of the unicellular alga Penium margaritaceum, a member of the Zygnematophyceae, the sister lineage to land plants. The P. margaritaceum genome has a high proportion of repeat sequences, which are associated with massive segmental gene duplications, likely facilitating neofunctionalization. Compared with earlier diverging plant lineages, P. margaritaceum has uniquely expanded repertoires of gene families, signaling networks and adaptive responses, supporting its phylogenetic placement and highlighting the evolutionary trajectory towards terrestrialization. These encompass a broad range of physiological processes and cellular structures, such as large families of extracellular polymer biosynthetic and modifying enzymes involved in cell wall assembly and remodeling. Transcriptome profiling of cells exposed to conditions that are common in terrestrial habitats, namely high light and desiccation, further elucidated key adaptations to the semi-aquatic ecosystems that are home to the Zygnematophyceae. Such habitats, in which a simpler body plan would be advantageous, likely provided the evolutionary crucible in which selective pressures shaped the transition to land.Earlier diverging charophyte lineages that are characterized by more complex land plant-like anatomies have either remained exclusively aquatic, or developed alternative life styles that allow periods of desiccation.

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“…Based on the presence of Hechtian strands associated with rapid tip growth [ 6 ], we extrapolated Mitchell’s original chemiosmotic hypothesis to include Ca 2+ signalling. This implies incredible evolutionary conservation and an early origin of the Hechtian pscillator in unicellular Chlorophycean algae such as Closterium [ 22 ] and Penium [ 23 ], as both exhibit tip growth with prominent Hechtian strands ( Figure 1 ).…”

Section: The Evolution Of Morphogenesismentioning

confidence: 99%

“… Hechtian strand occurrence: from algae to chloroplast guard cells. ( A ) Closterium desmid in 12% sucrose: reprinted from [ 22 ], Scale bar = 2.1 µm; ( B ) Penium margaritaceum : reprinted from [ 23 ], Scale bar = 2 µm; ( C ). Ginkgo cells plasmolysed in 0.3 M NaCl reprinted from [ 24 ], Scale bar is 10 µm; Arrows in ( A – C ) show location of Hechtian strands.…”

Section: Figurementioning

confidence: 99%

The Role of the Primary Cell Wall in Plant Morphogenesis

Lamport

Held

et al. 2018

IJMS

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Morphogenesis remains a riddle, wrapped in a mystery, inside an enigma. It remains a formidable problem viewed from many different perspectives of morphology, genetics, and computational modelling. We propose a biochemical reductionist approach that shows how both internal and external physical forces contribute to plant morphogenesis via mechanical stress–strain transduction from the primary cell wall tethered to the plasma membrane by a specific arabinogalactan protein (AGP). The resulting stress vector, with direction defined by Hechtian adhesion sites, has a magnitude of a few piconewtons amplified by a hypothetical Hechtian growth oscillator. This paradigm shift involves stress-activated plasma membrane Ca2+ channels and auxin-activated H+-ATPase. The proton pump dissociates periplasmic AGP-glycomodules that bind Ca2+. Thus, as the immediate source of cytosolic Ca2+, an AGP-Ca2+ capacitor directs the vectorial exocytosis of cell wall precursors and auxin efflux (PIN) proteins. In toto, these components comprise the Hechtian oscillator and also the gravisensor. Thus, interdependent auxin and Ca2+ morphogen gradients account for the predominance of AGPs. The size and location of a cell surface AGP-Ca2+ capacitor is essential to differentiation and explains AGP correlation with all stages of morphogenetic patterning from embryogenesis to root and shoot. Finally, the evolutionary origins of the Hechtian oscillator in the unicellular Chlorophycean algae reflect the ubiquitous role of chemiosmotic proton pumps that preceded DNA at the dawn of life.

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Isolation and manipulation of protoplasts from the unicellular green alga Penium margaritaceum

Cited by 9 publications

References 101 publications

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants

The Role of the Primary Cell Wall in Plant Morphogenesis

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