Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae

Mikkelsen, Maria Dalgaard; Harholt, Jesper; Ulvskov, Peter; Johansen, Ida Elisabeth; Fangel, Jonatan U.; Doblin, Monika S.; Bacic, Antony; Willats, William G. T.

doi:10.1093/aob/mcu171

Cited by 72 publications

(92 citation statements)

References 169 publications

(230 reference statements)

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“…If living in an aquatic environment, positioning yourself optimally for photosynthesis or your position in the water column is crucial; by contrast, if living terrestrially, different systems are required. Finally, analysis of common streptophyte genes in the K. flaccidum genome identified key physiological adaptations to terrestrial habitats, including oxidative stress, high light, and desiccation [11]. These traits provide the [ 2 1 _ T D $ D I F F ] algae with a competitive advantage in the terrestrial environment, as does the cell wall features identified by our genomic analysis.…”

Section: Does Previously Published Data Now Make More Evolutionary Sementioning

confidence: 73%

“…Comparative genomics of 'primitive' and higher plants established genetic orthology between all the major polysaccharides in embryophytes [10]. Using transcriptomes instead of genomes, orthology was also established between land plants and charophytes [11]. Evidence for rosette-forming cellulose synthases was found as far back as in Chlorokybus, a very early divergent charophyte.…”

Section: The Cell Wall Provides Cluesmentioning

confidence: 99%

“…Our finding of rosette-forming CESA[ 1 _ T D $ D I F F ] in [ 7 _ T D $ D I F F ] Chlorokybus indicates a later location for [ 8 _ T D $ D I F F ] it, rather than clustering in a clade with Mesostigmatophyceae[11].…”

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confidence: 92%

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Why Plants Were Terrestrial from the Beginning

Harholt

Moestrup

Ulvskov

2016

Trends in Plant Science

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131

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Section: Does Previously Published Data Now Make More Evolutionary Sementioning

confidence: 73%

Section: The Cell Wall Provides Cluesmentioning

confidence: 99%

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Why Plants Were Terrestrial from the Beginning

Harholt

Moestrup

Ulvskov

2016

Trends in Plant Science

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131

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“…The link between cell elongation and ethylene in algae has been largely unexplored, despite extensive research on cell wall composition and evolution in algae (Sørensen et al, 2010;Mikkelsen et al, 2014). Cellular elongation requires relaxation of the cell wall in order to facilitate turgor-driven longitudinal expansion (Cosgrove, 2000).…”

Section: Ethylene Regulates Spirogyra Cell Wall Modificationmentioning

confidence: 99%

Transcriptome Profiling of the Green Alga Spirogyra pratensis (Charophyta) Suggests an Ancestral Role for Ethylene in Cell Wall Metabolism, Photosynthesis, and Abiotic Stress Responses

et al. 2016

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It is well known that ethylene regulates a diverse set of developmental and stress-related processes in angiosperms, yet its roles in early-diverging embryophytes and algae are poorly understood. Recently, it was shown that ethylene functions as a hormone in the charophyte green alga Spirogyra pratensis. Since land plants evolved from charophytes, this implies conservation of ethylene as a hormone in green plants for at least 450 million years. However, the physiological role of ethylene in charophyte algae has remained unknown. To gain insight into ethylene responses in Spirogyra, we used mRNA sequencing to measure changes in gene expression over time in Spirogyra filaments in response to an ethylene treatment. Our analyses show that at the transcriptional level, ethylene predominantly regulates three processes in Spirogyra: (1) modification of the cell wall matrix by expansins and xyloglucan endotransglucosylases/hydrolases, (2) down-regulation of chlorophyll biosynthesis and photosynthesis, and (3) activation of abiotic stress responses. We confirmed that the photosynthetic capacity and chlorophyll content were reduced by an ethylene treatment and that several abiotic stress conditions could stimulate cell elongation in an ethylene-dependent manner. We also found that the Spirogyra transcriptome harbors only 10 ethylene-responsive transcription factor (ERF) homologs, several of which are regulated by ethylene. These results provide an initial understanding of the hormonal responses induced by ethylene in Spirogyra and help to reconstruct the role of ethylene in ancestral charophytes prior to the origin of land plants.

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“…Phylogenetic analyses have suggested to some investigators that streptophyte CSC‐encoding genes might have had a common origin before divergence into separate clades (Mikkelsen et al. ). Chlorophytes and streptophytes also differ in other cell‐wall carbohydrate polymers, such as hemicelluloses and matrix carboxylic polysaccharides.…”

mentioning

confidence: 99%

Genome‐wide analysis of carbohydrate‐active enzymes in Pyramimonas parkeae (Prasinophyceae)

Satjarak

Graham

2017

Journal of Phycology

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The wall-less green flagellate Pyramimonas parkeae is classified in clade I of the prasinophytes, a paraphyletic assemblage representing the last common ancestor of Viridiplantae, a monophyletic group composed of the green algae and land plants. Consequently, P. parkeae and other prasinophytes illuminate early-evolved Viridiplantae traits likely fundamental in the systems biology of green algae and land plants. Cellular structure and organellar genomes of P. parkeae are now well understood, and transcriptomic sequence data are also publically available for one strain of this species, but corresponding nuclear genomic sequence data are lacking. For this reason, we obtained shotgun genomic sequence and assembled a draft nuclear genome for P. parkeaeNIES254 to use along with existing transcriptomic sequence to focus on carbohydrate-active enzymes. We found that the P. parkeae nuclear genome encodes carbohydrate-active protein families similar to those previously observed for other prasinophytes, green algae, and early-diverging embryophytes for which full nuclear genomic sequence is publically available. Sequences homologous to genes related to biosynthesis of starch and cell wall carbohydrates were identified in the P. parkeae genome, indicating molecular traits common to Viridiplantae. For example, the P. parkeae genome includes sequences clustering with bacterial genes that encode cellulose synthases (Bcs), including regions coding for domains common to bacterial and plant cellulose synthases; these new sequences were incorporated into phylogenies aimed at illuminating the evolutionary history of cellulose production by Viridiplantae. Genomic sequences related to biosynthesis of xyloglucans, pectin, and starch likewise shed light on the origin of key Viridiplantae traits.

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Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae

Cited by 72 publications

References 169 publications

Why Plants Were Terrestrial from the Beginning

Why Plants Were Terrestrial from the Beginning

Transcriptome Profiling of the Green Alga Spirogyra pratensis (Charophyta) Suggests an Ancestral Role for Ethylene in Cell Wall Metabolism, Photosynthesis, and Abiotic Stress Responses

Genome‐wide analysis of carbohydrate‐active enzymes in Pyramimonas parkeae (Prasinophyceae)

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