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 modelling 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.

The phase separated CO2-fixing pyrenoid proteome determined by TurboID

“…Investigating the role of these proteins in pyrenoid structural organization and function could provide novel insights into pyrenoid assembly needed for future engineering of a functional pyrenoid into higher plants (Adler et al, 2022).…”

“…Both proteins possess a second functional domain, with this domain arrangement also seen in SAGA1 and LCI9 which incidentally share a similar localization pattern (Mackinder et al, 2017). Investigating the role of these proteins in pyrenoid structural organization and function could provide novel insights into pyrenoid assembly needed for future engineering of a functional pyrenoid into higher plants (Adler et al, 2022).…”

What can hornworts teach us?

“…Currently, there are attempts towards engineering algal pyrenoids into crops. This mainly includes proof of concept application in A. thaliana and tobacco ( Adler et al., 2022 ). For example, engineering a chimeric A. thaliana RuBisCO by replacement of the two surface α-helices of its small subunit (S-subunit) with those of C. reinhardtii , results in a functional RuBisCO ( Atkinson et al., 2017 ).…”

Epigenetic reprogramming of Nannochloropsis oceanica in response to CO 2 fluctuated environment

“…At the same time, oxygenic photosynthesis caused O 2 to increase in abundance, but with the latter's competition with CO 2 for Rubisco's active site, there is a loss of xed CO 2 due to photorespiration (Bauwe et al, 2010). Therefore, in order to improve CO 2 xation and overcome the challenges posed by the current atmospheric composition, a number of photosynthetic organisms use CO 2 -concentrating mechanisms (CCMs) to increase the ratio of CO 2 :O 2 near Rubisco's active site, thereby decreasing photorespiration while enhancing the assimilation of CO 2 (Adler et al, 2022). Most marine photoautotrophs, including eukaryotic algae and cyanobacteria (Reinfelder, 2011) possess CCMs, and altogether, they are responsible for 50% of the global carbon xation (Santhanagopalan et al, 2021;Wu et al, 2021).…”