Arabidopsis stromal carbonic anhydrases exhibit non‐overlapping roles in photosynthetic efficiency and development

Abstract

Carbonic anhydrases (CAs) are ubiquitous enzymes that accelerate the reversible conversion of CO 2 to HCO 3 À . The Arabidopsis genome encodes members of the a-, band c-CA families, and it has been hypothesized that bCA activity has a role in photosynthesis. In this work, we tested this hypothesis by characterizing the two plastidial bCAs, bCA1 and bCA5, in physiological conditions of growth. We conclusively established that both proteins are localized in the chloroplast stroma and that the loss of bCA5 induced the expression of bCA1, supporting the existence of regulatory mechanisms to control the expression of stromal bCAs. We also established that bCA1 and bCA5 have markedly different enzymatic kinetics and physiological relevance. Specifically, we found that bCA5 had a first-order rate constant ~10-fold lower than bCA1, and that the loss of bCA5 is detrimental to growth and could be rescued by high CO 2 . Furthermore, we established that, while a bCA1 mutation showed near wild-type growth and no significant impact on photosynthetic efficiency, the loss of bCA5 markedly disrupted photosynthetic efficiency and light-harvesting capacity at ambient CO 2 . Therefore, we conclude that in physiological autotrophic growth, the loss of the more highly expressed bCA1 does not compensate for the loss of a less active bCA5, which in turn is involved in growth and photosynthesis at ambient CO 2 levels. These results lend support to the hypothesis that, in Arabidopsis,bCAs have non-overlapping roles in photosynthesis and identify a critical activity of stromal bCA5 and a dispensable role for bCA1.

Natural genetic variation underlying the negative effect of elevated CO2 on ionome composition in Arabidopsis thaliana

“…We also identified the CA1 gene, coding for a carbonic anhydrase, in the vicinity of a QTL associated with C variation under high CO 2 . CA1 is involved in the regulation of stomatal opening by elevated CO 2 ( Hu et al, 2015 ), and the β carbonic anhydrase family of which CA1 belongs is involved in the regulation of photosynthetic efficiency, although CA1 shows no significant effect under standard conditions ( Sharma et al, 2023 ). It would be therefore interesting to assess the role of CA1 natural genetic variation under elevated CO 2 .…”

Genome-wide mapping, allelic fingerprinting, and haplotypes validation provide insights into the genetic control of carbon dioxide responsiveness in rice

“…For instance, among the 4 candidate genes identified in the CRI QTN, 3 of them encode for carbonic anhydrases. Carbonic anhydrases are known to play a vital role in facilitating the transfer of [CO 2 ] from the atmosphere to the systems involved in photosynthesis (Sharma et al, 2023). This process is regarded as a potential limiting factor when there is a low availability of [CO 2 ] within a leaf (Sharma et al, 2023).…”

“…Carbonic anhydrases are known to play a vital role in facilitating the transfer of [CO 2 ] from the atmosphere to the systems involved in photosynthesis (Sharma et al, 2023). This process is regarded as a potential limiting factor when there is a low availability of [CO 2 ] within a leaf (Sharma et al, 2023). Further, genes associated with different grain yield QTNs under LPD, encoding proteins/products such as serine/threonine protein kinase (Jia et al, 2020), MADS box TF (Liu et al, 2018), PIN protein (Borrell et al, 2022), Crinkly4 receptor-like kinase (Chun et al, 2020), among others have been reported to regulate grain yield and related traits in rice and other cereals.…”