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 CO2 around Rubisco. Hornworts are the only land plants with a pCCM. Owing to their closer relationship to crops, hornworts could offer greater translational potential than the green alga Chlamydomonas, the traditional model for studying pCCMs. Here we report a thorough investigation of a hornwort pCCM using the emerging model Anthoceros agrestis. The pyrenoids in A. agrestis exhibit liquid-like properties similar to those in Chlamydomonas, but they 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 in A. agrestis and probably have similar functions on the basis of their subcellular localizations. The underlying chassis for concentrating CO2 might therefore be shared between hornworts and Chlamydomonas, and ancestral to land plants. Our study presents a spatial model for a pCCM in a land plant, paving the way for future biochemical and genetic investigations. Hornworts are the only land plants with a pyrenoid-based CO2-concentrating mechanism. This study presents evidence that some of the key components in algal pyrenoid-based CO2-concentrating mechanisms are conserved in hornworts and probably serve similar functions.