Marius Arend

University of Potsdam

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Zoran Nikoloski

Max Planck Institute of Molecular Plant Physiology

Yizhong Yuan

Carnegie Institution for Science

MÁ

M. Águila Ruiz‐Sola

ETH Zurich

Dimitris Petroutsos

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

Georgios Kepesidis

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

Angeliki Tsichla

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

Philipp Wendering

Max Planck Institute of Molecular Plant Physiology

Jun Minagawa

The Graduate University for Advanced Studies, SOKENDAI

Guillaume Allorent

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

Petra Redekop

Carnegie Institution for Science

Cooperative Institutions

Centre National de la Recherche Scientifique

Commissariat à l'Énergie Atomique et aux Énergies Alternatives

Université Grenoble Alpes

CEA Grenoble

Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement

Max Planck Institute of Molecular Plant Physiology

Chinese Academy of Sciences

Guangzhou Institutes of Biomedicine and Health

Guangzhou Medical University

Laboratoire de Physiologie Cellulaire

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Widening the landscape of transcriptional regulation of green algal photoprotection

Nature Communications (2023)

Marius Arend Yizhong Yuan M. Águila Ruiz‐Sola Nooshin Omranian Zoran Nikoloski

Abstract Availability of light and CO 2 , substrates of microalgae photosynthesis, is frequently far from optimal. Microalgae activate photoprotection under strong light, to prevent oxidative damage, and the CO 2 Concentrating Mechanism (CCM) under low CO 2 , to raise intracellular CO 2 levels. The two processes are interconnected; yet, the underlying transcriptional regulators remain largely unknown. Employing a large transcriptomic data compendium of Chlamydomonas reinhardtii’s responses to different light and carbon supply, we reconstruct a consensus genome-scale gene regulatory network from complementary inference approaches and use it to elucidate transcriptional regulators of photoprotection. We show that the CCM regulator LCR1 also controls photoprotection, and that QER7, a Squamosa Binding Protein, suppresses photoprotection- and CCM-gene expression under the control of the blue light photoreceptor Phototropin. By demonstrating the existence of regulatory hubs that channel light- and CO 2 -mediated signals into a common response, our study provides an accessible resource to dissect gene expression regulation in this microalga.

Photoprotection

Endomembrane system

Chlamydomonas reinhardtii

Regulon

Gene regulatory network

10.1038/s41467-023-38183-4

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Citations (15)

Light-independent regulation of algal photoprotection by CO2 availability

Nature Communications (2023)

M. Águila Ruiz‐Sola Serena Flori Yizhong Yuan Gaëlle Villain Emanuel Sanz‐Luque

Abstract Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO 2 conditions. When light energy exceeds CO 2 fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO 2 Concentrating Mechanism (CCM). How light and CO 2 signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO 2 concentrations and that depletion of CO 2 drives these responses, even in total darkness. High CO 2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3 /CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO 2 and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO 2 levels.

Photoprotection

Chlamydomonas reinhardtii

Carbon fixation

Photobiology

10.1038/s41467-023-37800-6

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Citations (36)

Pluripotency reprogramming by competent and incompetent POU factors uncovers temporal dependency for Oct4 and Sox2

Nature Communications (2019)

Vikas Malik Laura V. Glaser Dennis Zimmer Sergiy Velychko Mingxi Weng

Abstract Oct4, along with Sox2 and Klf4 (SK), can induce pluripotency but structurally similar factors like Oct6 cannot. To decode why Oct4 has this unique ability, we compare Oct4-binding, accessibility patterns and transcriptional waves with Oct6 and an Oct4 mutant defective in the dimerization with Sox2 (Oct4 defSox2 ). We find that initial silencing of the somatic program proceeds indistinguishably with or without Oct4. Oct6 mitigates the mesenchymal-to-epithelial transition and derails reprogramming. These effects are a consequence of differences in genome-wide binding, as the early binding profile of Oct4 defSox2 resembles Oct4, whilst Oct6 does not bind pluripotency enhancers. Nevertheless, in the Oct6-SK condition many otherwise Oct4-bound locations become accessible but chromatin opening is compromised when Oct4 defSox2 occupies these sites. We find that Sox2 predominantly facilitates chromatin opening, whilst Oct4 serves an accessory role. Formation of Oct4/Sox2 heterodimers is essential for pluripotency establishment; however, reliance on Oct4/Sox2 heterodimers declines during pluripotency maintenance.

Reprogramming

POU domain

10.1038/s41467-019-11054-7

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Citations (68)

Widening the landscape of transcriptional regulation of green algal photoprotection

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Marius Arend Yizhong Yuan M. Águila Ruiz‐Sola Nooshin Omranian Zoran Nikoloski

Abstract Availability of light and CO2, substrates of microalgae photosynthesis, is frequently far from optimal. Microalgae activate photoprotection under strong light, to prevent oxidative damage, and the CO2 Concentrating Mechanism (CCM) under low CO2, to raise intracellular CO2 levels. The two processes are interconnected; yet, the underlying transcriptional regulators remain largely unknown. Employing a large transcriptomics data compendium of Chlamydomonas reinhardtii’s responses to different light and carbon supply, we reconstructed a consensus genome-scale gene regulatory network from complementary inference approaches and used it to elucidate transcriptional regulators of photoprotection. We showed that the CCM regulator LCR1 also controls photoprotection, and that QER7, a Squamosa Binding Protein, suppresses photoprotection- and CCM-gene expression under the control of the blue light photoreceptor Phototropin. By demonstrating the existence of regulatory hubs that channel light- and CO2-mediated signals into a common response, our study provides an accessible resource to dissect gene expression regulation in this microalga.

Photoprotection

Endomembrane system

Gene regulatory network

Chlamydomonas reinhardtii

Regulon

10.1101/2022.02.25.482034

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Citations (0)

Widening the landscape of transcriptional regulation of algal photoprotection

Research Square (Research Square) (2022)

Marius Arend Yizhong Yuan M. Águila Ruiz‐Sola Nooshin Omranian Zoran Nikoloski

Abstract Availability of light and CO2, substrates of microalgae photosynthesis, is frequently far from optimal. Microalgae activate photoprotection under strong light, to prevent oxidative damage, and the CO2 Concentrating Mechanism (CCM) under low CO2, to raise intracellular CO2 levels. The two processes are interconnected; yet, the underlying transcriptional regulators remain largely unknown. By employing a large transcriptomics data compendium of Chlamydomonas reinhardtii responses to different light and carbon supply we reconstructed a consensus genome-scale gene regulatory network from complementary inference approaches and used it to elucidate the transcriptional regulation of photoprotection. We showed that the CCM regulator LCR1 also controls photoprotection, and that QER7, a Squamosa Binding Protein, suppresses photoprotection- and CCM-gene expression under the control of the blue light photoreceptor Phototropin. Along with demonstrating the existence of regulatory hubs that channel light- and CO2-mediated signals into a common response, our study provides a unique resource to dissect gene expression regulation in this microalga.

Photoprotection

Endomembrane system

Chlamydomonas reinhardtii

Regulon

Gene regulatory network

10.21203/rs.3.rs-1527293/v1

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Citations (3)

Light-independent regulation of algal photoprotection by CO2 availability

Research Square (Research Square) (2022)

M. Águila Ruiz‐Sola Serena Flori Yizhong Yuan Gaëlle Villain Emanuel Sanz‐Luque

Abstract Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO2 conditions. When light energy exceeds CO2 fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO2 Concentrating Mechanism (CCM). How light and CO2 signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO2 concentrations and that depletion of CO2 drives these responses, even in total darkness. High CO2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3/CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO2 and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO2 levels.

Photoprotection

Chlamydomonas reinhardtii

Carbon fixation

Photobiology

10.21203/rs.3.rs-1886294/v1

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Citations (0)

Cross-stress gene expression atlas of Marchantia polymorpha reveals the hierarchy and regulatory principles of abiotic stress responses

Nature Communications (2023)

Qiao Wen Tan Peng Ken Lim Zhong Chen Asher Pasha Nicholas J. Provart

Abstract Abiotic stresses negatively impact ecosystems and the yield of crops, and climate change will increase their frequency and intensity. Despite progress in understanding how plants respond to individual stresses, our knowledge of plant acclimatization to combined stresses typically occurring in nature is still lacking. Here, we used a plant with minimal regulatory network redundancy, Marchantia polymorpha , to study how seven abiotic stresses, alone and in 19 pairwise combinations, affect the phenotype, gene expression, and activity of cellular pathways. While the transcriptomic responses show a conserved differential gene expression between Arabidopsis and Marchantia , we also observe a strong functional and transcriptional divergence between the two species. The reconstructed high-confidence gene regulatory network demonstrates that the response to specific stresses dominates those of others by relying on a large ensemble of transcription factors. We also show that a regression model could accurately predict the gene expression under combined stresses, indicating that Marchantia performs arithmetic multiplication to respond to multiple stresses. Lastly, two online resources ( https://conekt.plant.tools and http://bar.utoronto.ca/efp_marchantia/cgi-bin/efpWeb.cgi ) are provided to facilitate the study of gene expression in Marchantia exposed to abiotic stresses.

Marchantia polymorpha

10.1038/s41467-023-36517-w

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Citations (32)

Proteomics and constraint-based modelling reveal enzyme kinetic properties ofChlamydomonas reinhardtiion a genome scale

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Marius Arend David Zimmer Rudan Xu Frederick Sommer Timo Mühlhaus

Abstract Biofuels produced from microalgae offer a promising solution for carbon neutral economy, and integration of turnover numbers into metabolic models can improve the design of metabolic engineering strategies towards achieving this aim. However, the coverage of enzyme turnover numbers for Chlamydomonas reinhardtii , a model eukaryotic microalga accessible to metabolic engineering, is 17-fold smaller compared to the heterotrophic model Saccharomyces cerevisiae often used as a cell factory. Here we generated protein abundance data from Chlamydomonas reinhardtii cells grown in various experiments, covering between 2337 and 3708 proteins, and employed these data with constraint-based metabolic modeling approaches to estimate in vivo maximum apparent turnover numbers for this model organism. The gathered data allowed us to estimate maximum apparent turnover numbers for 568 reactions, of which 46 correspond to transporters that are otherwise difficult to characterize. The resulting, largest-to-date catalogue of proxies for in vivo turnover numbers increased the coverage for C. reinhardtii by more than 10-fold. We showed that incorporation of these in vivo turnover numbers into a protein-constrained metabolic model of C. reinhardtii improves the accuracy of predicted enzyme usage in comparison to predictions resulting from the integration on in vitro turnover numbers. Together, the integration of proteomics and physiological data allowed us to extend our knowledge of previously uncharacterized enzymes in the C. reinhardtii genome and subsequently increase predictive performance for biotechnological applications. Significance statement Current metabolic modelling approaches rely on the usage of in vitro turnover numbers ( k cat ) that provide limited information on enzymes operating in their native environment. This knowledge gap can be closed by data-integrative approaches to estimate in vivo k cat values that can improve metabolic modelling and design of metabolic engineering strategies. In this work, we assembled a high-quality proteomics data set containing 27 samples of various culture conditions and strains of Chlamydomonas reinhardtii . We used this resource to create the largest data set of estimates for in vivo turnover numbers to date. Subsequently, we showed that metabolic models parameterized with these estimates provide better predictions of enzyme abundance than those obtained by using in vitro turnover numbers.

Chlamydomonas reinhardtii

Metabolic Engineering

Protein turnover

Chlamydomonas

Turnover number

10.1101/2022.11.06.515318

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Citations (1)

Proteomics and constraint-based modelling reveal enzyme kinetic properties of Chlamydomonas reinhardtii on a genome scale

Nature Communications (2023)

Marius Arend David Zimmer Rudan Xu Frederik Sommer Timo Mühlhaus

Metabolic engineering of microalgae offers a promising solution for sustainable biofuel production, and rational design of engineering strategies can be improved by employing metabolic models that integrate enzyme turnover numbers. However, the coverage of turnover numbers for Chlamydomonas reinhardtii, a model eukaryotic microalga accessible to metabolic engineering, is 17-fold smaller compared to the heterotrophic cell factory Saccharomyces cerevisiae. Here we generate quantitative protein abundance data of Chlamydomonas covering 2337 to 3708 proteins in various growth conditions to estimate in vivo maximum apparent turnover numbers. Using constrained-based modeling we provide proxies for in vivo turnover numbers of 568 reactions, representing a 10-fold increase over the in vitro data for Chlamydomonas. Integration of the in vivo estimates instead of in vitro values in a metabolic model of Chlamydomonas improved the accuracy of enzyme usage predictions. Our results help in extending the knowledge on uncharacterized enzymes and improve biotechnological applications of Chlamydomonas.

Chlamydomonas reinhardtii

Chlamydomonas

10.1038/s41467-023-40498-1

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Citations (13)

Phototropin connects blue light perception to starch metabolism in green algae

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Yizhong Yuan Anthony A. Iannetta Minjae Kim Patric W. Sadecki Marius Arend

Abstract In photosynthetic organisms light acts as an environmental signal to control their development and physiology, and as energy source to drive the conversion of CO 2 into carbohydrates used for growth or storage. The main storage carbohydrate in green algae is starch, which accumulates during the day and is broken down at night to meet cellular energy demands. The signalling role of light quality in the regulation of starch accumulation remains unexplored. Here, we identify PHOTOTROPIN-MEDIATED SIGNALLING KINASE 1 (PMSK1) as a key regulator of starch metabolism in Chlamydomonas reinhardtii . In its phosphorylated form (PMSK1-P), it activates GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (GAP1), promoting starch biosynthesis. We show that blue light, perceived by PHOTOTROPIN, induces PMSK1 dephosphorylation that in turn represses GAP1 mRNA levels and reduces starch accumulation. These findings reveal a novel blue light-mediated signaling pathway that advances our understanding of photoreceptor-controlled carbon metabolism in microalgae. One-Sentence Summary Blue light perception by PHOTOTROPIN triggers kinase-mediated signaling to inhibit starch accumulation in the green alga Chlamydomonas .

Phototropin

Blue green algae

Green algae

10.1101/2024.02.12.579879

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Citations (3)