Abstract Many photosynthetic species have evolved CO2-concentrating mechanisms (CCMs) to improve the efficiency of CO2 assimilation by Rubisco and reduce the negative impacts of photorespiration. However, the majority of plants (i.e. C3 plants) lack an active CCM. Thus, engineering a functional heterologous CCM into important C3 crops, such as rice (Oryza sativa) and wheat (Triticum aestivum), has become a key strategic ambition to enhance yield potential. Here, we review recent advances in our understanding of the pyrenoid-based CCM in the model green alga Chlamydomonas reinhardtii and engineering progress in C3 plants. We also discuss recent modeling work that has provided insights into the potential advantages of Rubisco condensation within the pyrenoid and the energetic costs of the Chlamydomonas CCM, which, together, will help to better guide future engineering approaches. Key findings include the potential benefits of Rubisco condensation for carboxylation efficiency and the need for a diffusional barrier around the pyrenoid matrix. We discuss a minimal set of components for the CCM to function and that active bicarbonate import into the chloroplast stroma may not be necessary for a functional pyrenoid-based CCM in planta. Thus, the roadmap for building a pyrenoid-based CCM into plant chloroplasts to enhance the efficiency of photosynthesis now appears clearer with new challenges and opportunities.
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Prospects for Engineering Biophysical CO2 Concentrating Mechanisms into Land Plants to Enhance Yields
Although cyanobacteria and algae represent a small fraction of the biomass of all primary producers, their photosynthetic activity accounts for roughly half of the daily CO2 fixation that occurs on Earth. These microorganisms are able to accomplish this feat by enhancing the activity of the CO2-fixing enzyme Rubisco using biophysical CO2 concentrating mechanisms (CCMs). Biophysical CCMs operate by concentrating bicarbonate and converting it into CO2 in a compartment that houses Rubisco (in contrast with other CCMs that concentrate CO2 via an organic intermediate, such as malate in the case of C4 CCMs). This activity provides Rubisco with a high concentration of its substrate, thereby increasing its reaction rate. The genetic engineering of a biophysical CCM into land plants is being pursued as a strategy to increase crop yields. This review focuses on the progress toward understanding the molecular components of cyanobacterial and algal CCMs, as well as recent advances toward engineering these components into land plants.
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- Award ID(s):
- 1935444
- NSF-PAR ID:
- 10175258
- Date Published:
- Journal Name:
- Annual review of plant biology
- Volume:
- 71
- ISSN:
- 1543-5008
- Page Range / eLocation ID:
- 461-485
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Many eukaryotic photosynthetic organisms enhance their carbon uptake by supplying concentrated CO2to the CO2-fixing enzyme Rubisco in an organelle called the pyrenoid. Ongoing efforts seek to engineer this pyrenoid-based CO2-concentrating mechanism (PCCM) into crops to increase yields. Here we develop a computational model for a PCCM on the basis of the postulated mechanism in the green alga
Chlamydomonas reinhardtii . Our model recapitulates allChlamydomonas PCCM-deficient mutant phenotypes and yields general biophysical principles underlying the PCCM. We show that an effective and energetically efficient PCCM requires a physical barrier to reduce pyrenoid CO2leakage, as well as proper enzyme localization to reduce futile cycling between CO2and HCO3−. Importantly, our model demonstrates the feasibility of a purely passive CO2uptake strategy at air-level CO2, while active HCO3−uptake proves advantageous at lower CO2levels. We propose a four-step engineering path to increase the rate of CO2fixation in the plant chloroplast up to threefold at a theoretical cost of only 1.3 ATP per CO2fixed, thereby offering a framework to guide the engineering of a PCCM into land plants. -
null (Ed.)Many photosynthetic organisms employ a CO 2 concentrating mechanism (CCM) to increase the rate of CO 2 fixation via the Calvin cycle. CCMs catalyze ≈50% of global photosynthesis, yet it remains unclear which genes and proteins are required to produce this complex adaptation. We describe the construction of a functional CCM in a non-native host, achieved by expressing genes from an autotrophic bacterium in an Escherichia coli strain engineered to depend on rubisco carboxylation for growth. Expression of 20 CCM genes enabled E. coli to grow by fixing CO 2 from ambient air into biomass, with growth in ambient air depending on the components of the CCM. Bacterial CCMs are therefore genetically compact and readily transplanted, rationalizing their presence in diverse bacteria. Reconstitution enabled genetic experiments refining our understanding of the CCM, thereby laying the groundwork for deeper study and engineering of the cell biology supporting CO 2 assimilation in diverse organisms.more » « less
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Summary Photosynthesis in C3 plants is limited by features of the carbon‐fixing enzyme Rubisco, which exhibits a low turnover rate and can react with O2instead of
CO 2, leading to photorespiration. In cyanobacteria, bacterial microcompartments, known as carboxysomes, improve the efficiency of photosynthesis by concentratingCO 2near the enzyme Rubisco. Cyanobacterial Rubisco enzymes are faster than those of C3 plants, though they have lower specificity towardCO 2than the land plant enzyme. Replacement of land plant Rubisco by faster bacterial variants with lowerCO 2specificity will improve photosynthesis only if a microcompartment capable of concentratingCO 2can also be installed into the chloroplast. We review current information about cyanobacterial microcompartments and carbon‐concentrating mechanisms, plant transformation strategies, replacement of Rubisco in a model C3 plant with cyanobacterial Rubisco and progress toward synthesizing a carboxysome in chloroplasts. -
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Abstract Many carbon‐fixing organisms have evolved CO2concentrating mechanisms (CCMs) to enhance the delivery of CO2to RuBisCO, while minimizing reactions with the competitive inhibitor, molecular O2. These distinct types of CCMs have been extensively studied using genetics, biochemistry, cell imaging, mass spectrometry, and metabolic flux analysis. Highlighted in this paper, the cyanobacterial CCM features a bacterial microcompartment (BMC) called ‘carboxysome’ in which RuBisCO is co‐encapsulated with the enzyme carbonic anhydrase (CA) within a semi‐permeable protein shell. The cyanobacterial CCM is capable of increasing CO2around RuBisCO, leading to one of the most efficient processes known for fixing ambient CO2. The carboxysome life cycle is dynamic and creates a unique subcellular environment that promotes activity of the Calvin–Benson (CB) cycle. The carboxysome may function within a larger cellular metabolon, physical association of functionally coupled proteins, to enhance metabolite channelling and carbon flux. In light of CCMs, synthetic biology approaches have been used to improve enzyme complex for CO2fixations. Research on CCM‐associated metabolons has also inspired biologists to engineer multi‐step pathways by providing anchoring points for enzyme cascades to channel intermediate metabolites towards valuable products.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1146/annurev-arplant-081519-040100
