Orchestration of algal metabolism by protein disorder

Launay, Hélène; Receveur-Brechot, Véronique; Carrière, Frédéric; Gontero, Brigitte

doi:10.1016/j.abb.2019.108070

Cited by 15 publications

(19 citation statements)

References 138 publications

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“…This suggests that the differences in IDR may have been triggered by different evolutionary pressure on the two microalgae in terms of mobility. In other words, Rca may have evolved to optimize photosynthesis under unfavorable conditions (Launay et al ., 2019). Alternative splicing and IDRs in Rca‐α may function in regulating and maintaining a critical ratio of Rca‐α/Rca‐β isoforms in plants.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis plants expressing only the redox‐regulated Rca‐α isoform have constrained photosynthesis and plant growth

et al. 2020

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SUMMARY Rubisco activase (Rca) facilitates the release of sugar‐phosphate inhibitors from the active sites of Rubisco and thereby plays a central role in initiating and sustaining Rubisco activation. In Arabidopsis, alternative splicing of a single Rca gene results in two Rca isoforms, Rca‐α and Rca‐β. Redox modulation of Rca‐α regulates the function of Rca‐α and Rca‐β acting together to control Rubisco activation. Although Arabidopsis Rca‐α alone less effectively activates Rubisco in vitro, it is not known how CO2 assimilation and plant growth are impacted. Here, we show that two independent transgenic Arabidopsis lines expressing Rca‐α in the absence of Rca‐β (‘Rca‐α only’ lines) grew more slowly in various light conditions, especially under low light or fluctuating light intensity, and in a short day photoperiod compared to wildtype. Photosynthetic induction was slower in the Rca‐α only lines, and they maintained a lower rate of CO2 assimilation during both photoperiod types. Our findings suggest Rca oligomers composed of Rca‐α only are less effective in initiating and sustaining the activation of Rubisco than when Rca‐β is also present. Currently there are no examples of any plant species that naturally express Rca‐α only but numerous examples of species expressing Rca‐β only. That Rca‐α exists in most plant species, including many C3 and C4 food and bioenergy crops, implies its presence is adaptive under some circumstances.

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Section: Discussionmentioning

confidence: 99%

Arabidopsis plants expressing only the redox‐regulated Rca‐α isoform have constrained photosynthesis and plant growth

et al. 2020

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“…The CP12 proteins from C. reinhardtii, A. thaliana and S. elongatus have been extensively studied and shown to belong to the IDP family. IDPs, or in other words ductile, dancing, malleable or flexible proteins [54], are common in various proteomes [55][56][57][58][59][60] and occupy a unique structural and functional niche in which function is directly linked to structural disorder [52,[61][62][63]. The absence of structure has been proposed to be a significant advantage for proteins whose functions are related to stress response [64], as e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Since CP12 proteins from other organisms are IDPs [10,12,52], we checked whether CP12 from T. pseudonana was likely to contain disordered regions. The amino acid composition of this CP12 and that from C. reinhardtii, a well-known IDP, were compared to globular proteins.…”

Section: In Silico Characterization Of the Propensity Of Disordermentioning

confidence: 99%

A new type of flexible CP12 protein in the marine diatom Thalassiosira pseudonana

et al. 2021

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Background CP12 is a small chloroplast protein that is widespread in various photosynthetic organisms and is an actor of the redox signaling pathway involved in the regulation of the Calvin Benson Bassham (CBB) cycle. The gene encoding this protein is conserved in many diatoms, but the protein has been overlooked in these organisms, despite their ecological importance and their complex and still enigmatic evolutionary background. Methods A combination of biochemical, bioinformatics and biophysical methods including electrospray ionization-mass spectrometry, circular dichroism, nuclear magnetic resonance spectroscopy and small X ray scattering, was used to characterize a diatom CP12. Results Here, we demonstrate that CP12 is expressed in the marine diatom Thalassiosira pseudonana constitutively in dark-treated and in continuous light-treated cells as well as in all growth phases. This CP12 similarly to its homologues in other species has some features of intrinsically disorder protein family: it behaves abnormally under gel electrophoresis and size exclusion chromatography, has a high net charge and a bias amino acid composition. By contrast, unlike other known CP12 proteins that are monomers, this protein is a dimer as suggested by native electrospray ionization-mass spectrometry and small angle X-ray scattering. In addition, small angle X-ray scattering revealed that this CP12 is an elongated cylinder with kinks. Circular dichroism spectra indicated that CP12 has a high content of α-helices, and nuclear magnetic resonance spectroscopy suggested that these helices are unstable and dynamic within a millisecond timescale. Together with in silico predictions, these results suggest that T. pseudonana CP12 has both coiled coil and disordered regions. Conclusions These findings bring new insights into the large family of dynamic proteins containing disordered regions, thus increasing the diversity of known CP12 proteins. As it is a protein that is more abundant in many stresses, it is not devoted to one metabolism and in particular, it is not specific to carbon metabolism. This raises questions about the role of this protein in addition to the well-established regulation of the CBB cycle. Choregraphy of metabolism by CP12 proteins in Viridiplantae and Heterokonta. While the monomeric CP12 in Viridiplantae is involved in carbon assimilation, regulating phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) through the formation of a ternary complex, in Heterokonta studied so far, the dimeric CP12 is associated with Ferredoxin-NADP reductase (FNR) and GAPDH. The Viridiplantae CP12 can bind metal ions and can be a chaperone, the Heterokonta CP12 is more abundant in all stresses (C, N, Si, P limited conditions) and is not specific to a metabolism.

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“…The CP12 proteins from C. reinhardtii, A. thaliana and S. elongatus have been extensively studied and shown to belong to the IDP family. IDPs, or in other words ductile, dancing, malleable or exible proteins [49], are common in various proteomes [50][51][52][53][54][55] and occupy a unique structural and functional niche in which function is directly linked to structural disorder [47,[56][57][58]. The expression of CP12 from the diatom T. pseudonana is constitutively expressed under dark and light conditions, as well as during the growth, unlike CP12 from A. thaliana that is co-expressed with PRK and GAPDH in the light [59].…”

Section: Discussionmentioning

confidence: 99%

“…Since CP12 proteins from other organisms are IDPs [9,11,47], we checked if this was the case for CP12 from T. pseudonana. The amino acid composition of this CP12 and that from C. reinhardtii, a well-known IDP, were compared to globular proteins.…”

Section: In Silico Characterization Of the Propensity Of Disordermentioning

confidence: 99%

A new type of disordered CP12 protein in the marine diatom Thalassiosira pseudonana

Shao¹,

Huang²,

Avilán³

et al. 2020

Preprint

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Background CP12 is a small chloroplast protein that is widespread in various photosynthetic organisms and is often involved in the redox metabolic on/off switch of the Calvin Benson Bassham (CBB) cycle. The gene encoding this protein is conserved in many diatoms, but the protein has been overlooked in these organisms, despite their ecological predominance and their complex and still enigmatic evolutionary background. Methods A combination of biochemical, bioinformatics and biophysical methods including electrospray ionization-mass spectrometry, circular dichroism, nuclear magnetic resonance and small X ray scattering spectroscopy, was used to characterize a diatom CP12. Results Here, we demonstrate that CP12 is expressed in the marine diatom Thalassiosira pseudonana constitutively in dark-treated and in continuous light-treated cells as well as in all growth phases. This CP12 behaves abnormally under gel electrophoresis, is heat resistant and lacks a structural core, all features of intrinsically disorder family similarly to its homologues in other species. By contrast, unlike other known CP12 proteins that are monomers, this protein is a dimer as shown by native electrospray ionization-mass spectrometry and small angle X-ray scattering. In addition, small angle X-ray scattering showed that this CP12 is an elongated cylinder with kinks. Circular dichroism spectra indicated that CP12, though it has features of disordered proteins, has a high content of α-helices. Nuclear magnetic resonance spectroscopy showed that these helices are unstable and dynamic within a millisecond timescale. Together with in silico predictions, these results suggest that T. pseudonana CP12 has both coiled-coil and disordered regions. Conclusions These findings bring new insights into the large family of intrinsically disordered proteins increasing the diversity of known CP12 proteins. This raises questions about the role of this protein in addition to the well-established regulation of the CBB cycle.

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Orchestration of algal metabolism by protein disorder

Cited by 15 publications

References 138 publications

Arabidopsis plants expressing only the redox‐regulated Rca‐α isoform have constrained photosynthesis and plant growth

Arabidopsis plants expressing only the redox‐regulated Rca‐α isoform have constrained photosynthesis and plant growth

A new type of flexible CP12 protein in the marine diatom Thalassiosira pseudonana

A new type of disordered CP12 protein in the marine diatom Thalassiosira pseudonana

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