Photosynthetic acclimation, vernalization, crop productivity and 'the grand design of photosynthesis'

Daniel Arnon first proposed the notion of a 'grand design of photosynthesis' in 1982 to illustrate the central role of photosynthesis as the primary energy transformer for all life on Earth. However, we suggest that this concept can be extended to the broad impact of photosynthesis not only in global energy transformation but also in the regulation of plant growth, development, survival and crop productivity through chloroplast redox signalling. We compare and contrast the role of chloroplast redox imbalance, measured as excitation pressure, in governing acclimation to abiotic stress and phenotypic plasticity. Although all photoautrophs sense excessive excitation energy through changes in excitation pressure, the response to this chloroplast redox signal is species dependent. Due to a limited capacity to adjust metabolic sinks, cyanobacteria and green algae induce photoprotective mechanisms which dissipate excess excitation energy at a cost of decreased photosynthetic performance. In contrast, terrestrial, cold tolerant plants such as wheat enhance metabolic sink capacity which leads to enhanced photosynthetic performance and biomass accumulation with minimal dependence on photoprotection. We suggest that the family of nuclear C-repeat binding transcription factors (CBFs) associated with the frost resistance locus, FR2, contiguous with the vernalization locus, VRN1, and mapped to chromosome 5A of wheat, may be critical components that link leaf chloroplast redox regulation to enhanced photosynthetic performance, the accumulation of growth-active gibberellins and the dwarf phenotype during cold acclimation prior to the vegetative to reproductive transition controlled by vernalization in winter cereals. Further genetic, molecular and biochemical research to confirm these links and to elucidate the molecular mechanism by which chloroplast redox modulation of CBF expression leads to enhanced photosynthetic performance is required. Because of the superior abiotic stress tolerance of cold tolerant winter wheat and seed yields that historically exceed those of spring wheat by 30-40%, we discuss the potential to exploit winter cereals for the maintenance or perhaps even the enhancement of cereal productivity under future climate change scenarios that will be required to feed a growing human population. (C) 2016 Elsevier GmbH. All rights reserved.