The regulatory properties of rubisco activase differ among species and affect photosynthetic induction during light transitions

Authors: Carmo Silva, Ana; Salvucci, Michael

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2013
Publication Date: 2/15/2013
Citation: Carmo Silva, A.E., Salvucci, M.E. 2013. The regulatory properties of rubisco activase differ among species and affect photosynthetic induction during light transitions. Plant Physiology. 161(4):1645-1655.

Interpretive Summary: In the process of photosynthesis, plants convert light into chemical energy. The energy produced by photosynthesis is then used to synthesize the carbon compounds that are harvested for food, fuel, fiber or other natural products. Consequently, photosynthesis determines the overall yield of the plant. Previous research from our group identified an enzyme called Rubisco activase as a regulatory enzyme that controls the activity of Rubisco, the major carbon dioxide-fixing enzyme in plants. In this manuscript, we present important new information about how Rubisco activase itself is regulated in various plant species. We show that species contain different types of Rubisco activase and these different Rubisco activases are regulated in different ways. We also show that a lack of regulation of Rubisco activase in plants affects the rate at which photosynthesis turns on after the light is increased. These findings indicate a possible strategy for enhancing photosynthetic performance in certain variable light environments based on altering the regulatory properties of Rubisco activase.

Technical Abstract: Rubisco’s catalytic chaperone, Rubisco activase (Rca), uses the energy from ATP hydrolysis to restore catalytic competence to Rubisco. In Arabidopsis, inhibition of Rca activity by ADP is fine-tuned by redox regulation of the a-isoform. To elucidate the mechanism for Rca regulation in species containing only the redox-insensitive ß-isoform, the response of activity to ADP was characterized for different Rca forms. When assayed in leaf extracts, Rubisco activation was significantly inhibited by physiological ratios of ADP/ATP in species containing both a- and ß-Rca (Arabidopsis thaliana and Camelina sativa) or just the ß-Rca (Nicotiana tabacum). However, Rca activity was insensitive to ADP inhibition in an Arabidopsis transformant, rwt43, that expresses only Arabidopsis ß-Rca, but not in a transformant of Arabidopsis that expresses a tobacco-like ß-Rca. ATP hydrolysis by recombinant Arabidopsis ß-Rca was much less sensitive to inhibition by ADP than recombinant tobacco ß-Rca. Mutation of 17 amino acids in the tobacco ß-Rca to the corresponding Arabidopsis residues reduced ADP sensitivity. In planta, Rubisco generally deactivated at low irradiance except in the Arabidopsis rwt43 transformant containing an ADP-insensitive Rca. Induction of CO2 assimilation after transition from low to high irradiance was much more rapid in the rwt43 transformant compared with plants containing ADP-sensitive Rca forms. The faster rate of photosynthetic induction by the rwt43 transformant compared with wild-type Arabidopsis suggests that manipulation of Rca regulation might provide a strategy for enhancing photosynthetic performance in certain variable light environments.