Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts

Atkinson, Nicky; Mao, Yuwei; Chan, Kher Xing; McCormick, Alistair J.

doi:10.1038/s41467-020-20132-0

Cited by 80 publications

(62 citation statements)

References 52 publications

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“…By increasing CO 2 supplies and thereby suppressing photorespiration, plant CCMs began evolving from C 3 species, probably in the early Oligocene (circa 30 ma) in response to decreasing CO 2 levels, as an efficient way of increasing photosynthesis in the more challenging environmental conditions (Sage, 2004). The evolutionary success of C 4 photosynthesis and the observation of increased carbon assimilation in some C 3 crops under elevated CO 2 (Xu et al, 2016;Thompson et al, 2017) have stimulated research into the possibility of incorporating CCMs into C 3 plant species via genetic modification (McGrath and Long, 2014;Jurić et al, 2019;Kubis and Bar-Even, 2019;Atkinson et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants

Cummins

2021

Front. Plant Sci.

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Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO) is the carbon-fixing enzyme present in most photosynthetic organisms, converting CO2 into organic matter. Globally, photosynthetic efficiency in terrestrial plants has become increasingly challenged in recent decades due to a rapid increase in atmospheric CO2 and associated changes toward warmer and dryer environments. Well adapted for these new climatic conditions, the C4 photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO2 concentrations surrounding RuBisCO, suppressing photorespiration from the oxygenase catalyzed reaction with O2. The energy efficiency of C3 photosynthesis, from which the C4 pathway evolved, is thought to rely critically on an uninterrupted supply of chloroplast CO2. Part of the homeostatic mechanism that maintains this constancy of supply involves the CO2 produced as a byproduct of photorespiration in a negative feedback loop. Analyzing the database of RuBisCO kinetic parameters, we suggest that in genera (Flaveria and Panicum) for which both C3 and C4 examples are available, the C4 pathway evolved only from C3 ancestors possessing much lower than the average carboxylase specificity relative to that of the oxygenase reaction (SC/O=SC/SO), and hence, the higher CO2 levels required for development of the photorespiratory CO2 pump (C2 photosynthesis) essential in the initial stages of C4 evolution, while in the later stage (final optimization phase in the Flaveria model) increased CO2 turnover may have occurred, which would have been supported by the higher CO2 levels. Otherwise, C4 RuBisCO kinetic traits remain little changed from the ancestral C3 species. At the opposite end of the spectrum, C3 plants (from Limonium) with higher than average SC/O, which may be associated with the ability of increased CO2, relative to O2, affinity to offset reduced photorespiration and chloroplast CO2 levels, can tolerate high stress environments. It is suggested that, instead of inherently constrained by its kinetic mechanism, RuBisCO possesses the extensive kinetic plasticity necessary for adaptation to changes in photorespiration that occur in the homeostatic regulation of CO2 supply under a broad range of abiotic environmental conditions.

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Section: Introductionmentioning

confidence: 99%

The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants

Cummins

2021

Front. Plant Sci.

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“…There has been research aimed at enhancing the CO 2 -fixing capacity of Rubisco by introducing algal CCMs into the chloroplasts of terrestrial plants. Because the interaction between Rubisco and the Rubisco linker EPYC1 is sufficient to form phase-separated structures and the motif sequences of proteins that bind to Rubisco have been identified ( He et al, 2020 ; Meyer et al, 2020 ), it should be possible to reconstitute functional pyrenoids by heterologous expression of algal proteins ( Atkinson et al, 2020 ). Furthermore,

and CO 2 transporters/channels associated with Ci-uptake have also been identified, and it would also be possible to express and localize them to the correct positions in land plant cells.…”

Section: Discussionmentioning

confidence: 99%

CO2-dependent migration and relocation of LCIB, a pyrenoid-peripheral protein in Chlamydomonas reinhardtii

et al. 2021

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Most microalgae overcome the difficulty of acquiring inorganic carbon (Ci) in aquatic environments by inducing a CO2-concentrating mechanism (CCM). In the green alga Chlamydomonas reinhardtii, two distinct photosynthetic acclimation states have been described under CO2-limiting conditions (low-CO2 [LC] and very low-CO2 [VLC]). LC-inducible protein B (LCIB), structurally characterized as carbonic anhydrase, localizes in the chloroplast stroma under CO2-supplied and LC conditions. In VLC conditions, it migrates to aggregate around the pyrenoid, where the CO2-fixing enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase is enriched. Although the physiological importance of LCIB localization changes in the chloroplast has been shown, factors necessary for the localization changes remain uncertain. Here, we examined the effect of pH, light availability, photosynthetic electron flow, and protein synthesis on the localization changes, along with measuring Ci concentrations. LCIB dispersed or localized in the basal region of the chloroplast stroma at 8.3–15 µM CO2, whereas LCIB migrated toward the pyrenoid at 6.5 µM CO2. Furthermore, LCIB relocated toward the pyrenoid at 2.6–3.4 µM CO2, even in cells in the dark or treated with 3-(3,4-dichlorophenyl)-1,1-dimethylurea and cycloheximide in light. In contrast, in the mutant lacking CCM1, a master regulator of CCM, LCIB remained dispersed even at 4.3 µM CO2. Meanwhile, a simultaneous expression of LCIC, an interacting protein of LCIB, induced the localization of several speckled structures at the pyrenoid periphery. These results suggest that the localization changes of LCIB require LCIC and are controlled by CO2 concentration with ∼7 µM as the boundary.

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“…Five repeat regions of EPYC1 associate with the surface-exposed a-helices of the Rubisco small subunit to determine regular spacing and arrangement of Rubisco in the pyrenoid (Meyer et al, 2012;Mackinder et al, 2016;He et al, 2020). Consistently, EPYC1 colocalizes with Rubisco throughout the pyrenoid and is essential for normal pyrenoid size, number, and morphology, Rubisco content, and efficient carbon fixation at low CO 2 (Mackinder et al, 2016;Atkinson et al, 2020).…”

Section: Phase Separation In Chloroplastsmentioning

confidence: 99%

Get closer and make hotspots: liquid–liquid phase separation in plants

Kim

Lee

et al. 2021

EMBO Reports

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Liquid-liquid phase separation (LLPS) facilitates the formation of membraneless compartments in a cell and allows the spatiotemporal organization of biochemical reactions by concentrating macromolecules locally. In plants, LLPS defines cellular reaction hotspots, and stimulus-responsive LLPS is tightly linked to a variety of cellular and biological functions triggered by exposure to various internal and external stimuli, such as stress responses, hormone signaling, and temperature sensing. Here, we provide an overview of the current understanding of physicochemical forces and molecular factors that drive LLPS in plant cells. We illustrate how the biochemical features of cellular condensates contribute to their biological functions. Additionally, we highlight major challenges for the comprehensive understanding of biological LLPS, especially in view of the dynamic and robust organization of biochemical reactions underlying plastic responses to environmental fluctuations in plants.

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Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts

Cited by 80 publications

References 52 publications

The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants

The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants

CO2-dependent migration and relocation of LCIB, a pyrenoid-peripheral protein in Chlamydomonas reinhardtii

Get closer and make hotspots: liquid–liquid phase separation in plants

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