Experimental and computational analyses of KEA3-dependent photosynthetic responses uncover species-specific molecular variation

Abstract

- NPQ relaxation is thought to limit crop biomass and yield under natural, fluctuating light. The thylakoid K/H exchanger KEA3 accelerates NPQ relaxation by lowering the lumen proton concentration and thus should affect biomass and yield under frequent light fluctuations. - To investigate the impact of KEA3-dependent NPQ relaxation on Solanum lycopersicum (tomato), we generated knock-out and over-expression lines and measured NPQ, gas exchange, biomass and yield. We constructed a mathematical model to compare species-specific NPQ relaxation dynamics in tomato and the model plant Arabidopsis thaliana. - In polytunnel and controlled fluctuating-light conditions, KEA3-mediated NPQ relaxation did not translate into consistent differences in tomato biomass or yield. Although KEA3 levels strongly affected NPQ relaxation, more so than in A.thaliana, the resulting effects on CO2 assimilation were minor. Modeling results indicated that, besides minor changes in KEA3 regulation, the activity of PsbS, the primary NPQ trigger, largely determines the species-specific differences in NPQ relaxation. Structural models from both species predict sequence variation with impact on PsbS activation. - Manipulating KEA3 levels in tomato did not link NPQ relaxation with productivity. However, the results support robust cross-species mathematical model that accurately predicts the molecular interactions governing NPQ dynamics.