The NDH complex reveals a trade-off that constrains maximising photosynthesis in Arabidopsis thaliana

Abstract

The Green Revolution has resulted in major improvements in crop productivity, but left photosynthesis largely unimproved. Despite ample variation of photosynthetic performance in crops and their wild relatives, the photosynthetic capacity of elite breeding lines remains well below its theoretical maximum. As yield is often the primary selective trait, current plant breeding approaches result in photosynthetic trade-offs that prevent positive selection for photosynthetic performance itself. Currently, genetic variation for photosynthetic performance is seldomly validated at the genetic level, and as a result these photosynthetic trade-offs remain poorly understood. Here we reveal the physiological nature of a photosynthetic trade-off caused by the NAD(P)H dehydrogenase (NDH) complex. The use of an Arabidopsis thaliana cybrid panel revealed how a natural allele of the chloroplastic gene NAD(P)H-QUINONE OXIDOREDUCTASE SUBUNIT 6 - a subunit of the NDH complex - results in a faster recovery of photosystem II efficiency after a transition from high to low irradiances. This improvement is due to a reduction in NDH activity. Under low-light conditions this reduction in NDH activity has a neutral effect on biomass, while under highly fluctuating light conditions, including high irradiances, more NDH activity is favoured. This shows that while allelic variation in one gene can have beneficial effects on one aspect of photosynthesis, it can, depending on environmental conditions, have negative effects on other aspects of photosynthesis. As environmental conditions are hardly ever stable in agricultural systems, understanding photosynthetic trade-offs allows us to explore shifting photosynthetic performance closer to the theoretical maximum.