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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 algaChlamydomonas reinhardtii. Our model recapitulates allChlamydomonasPCCM-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.
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New horizons for building pyrenoid-based CO2-concentrating mechanisms in plants to improve yields
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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- Award ID(s):
- 1734030
- PAR ID:
- 10382456
- Date Published:
- Journal Name:
- Plant Physiology
- Volume:
- 190
- Issue:
- 3
- ISSN:
- 0032-0889
- Page Range / eLocation ID:
- 1609 to 1627
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/plphys/kiac373
