Hornworts reveal a spatial model for pyrenoid-based CO₂-concentrating mechanisms in land plants

Abstract

Pyrenoid-based CO2-concentrating mechanisms (pCCMs) turbocharge photosynthesis by saturating CO2around Rubisco. Hornworts are the only land plants with a pCCM. Owing to their closer relationship to crops, hornworts could offer greater translational potential compared to the green alga Chlamydomonas, the traditional model for studying pCCM. Here we report the first thorough investigation of a hornwort pCCM using the emerging modelAnthoceros agrestis. The pyrenoids inA. agrestisexhibit liquid-like properties similar to Chlamydomonas, but differ by lacking starch sheaths and being enclosed by multiple thylakoids. We found that the core pCCM components in Chlamydomonas, including BST, LCIB, and CAH3, are conserved inA. agrestisand likely have similar functions based on their subcellular localizations. Therefore, the underlying chassis for concentrating CO2might be shared between hornworts and Chlamydomonas, and ancestral to land plants. Our study presents the first spatial model for pCCM in a land plant, paving the way for future biochemical and genetic investigations.