The Dynamic Plant: Capture, Transformation, and Management of Energy

Abstract

1 Plants are exquisite in their capacity to convert photons of light through photosynthetic carbon diox-ide (CO 2) fixation into carbohydrate resources that are assimilated and partitioned from photosynthetic source to sink tissues. The chemical energy gained from photosynthesis includes ATP and NADPH that along with sugars are vital to biosynthetic processes, cell proliferation, biomass production, and reproductive fitness. As in all eukaryotes, plants are dependent upon dioxygen (O 2) for efficient production of ATP through aerobic respiration by mitochondria. Therefore, O 2 is crucial for the efficient catabolism of carbohydrates, lipids, and protein into chemical energy in leaves in the light and darkness, as well as in sink tissues. In this Focus Issue, numerous reviews and research articles explore the integration of light, O 2 , and energy meta-bolism from the cellular to the whole-plant level. The articles analyze molecular, biochemical, physiological, and developmental mechanisms that contribute to the plant's energy balance. A recurrent theme is the in-tegration of light, O 2 , and sugar sensing with signal transduction and gene regulation, resulting in metabolic and developmental plasticity that maximizes available energy for growth. This knowledge expands opportu-nities to enhance photosynthetic efficiency and fine-tune energy allocation to maximize yields of crops. LET THERE BE LIGHT: DYNAMICS OF CHLOROPLAST BIOGENESIS AND DIFFERENTIATION The biogenesis of photosynthetically active chloro-plasts involves the coordinated regulation of the nuclear and proplastid genomes. This synchronization involves both anterograde (nucleus to plastid) and retrograde (plastid to nucleus or another compartment) signaling (de Souza et al., 2017; Hernández-Verdeja and Strand, 2018). Using a single-cell system of Arabidopsis (Arabidopsis thaliana), Dubreuil et al. (2018) tracked dynamics in tran-scripts and metabolites to refine the definition of the early light-induced anterograde phase that includes chlorophyll synthesis and rudimentary thylakoid membrane for-mation. Their analysis resolved a second phase that is characterized by retrograde signaling from the plastid to the nucleus that dramatically bolsters the expression of nucleus-encoded photosynthetic genes and the transi-tion to photosynthetic competence. Modeling confirmed that this second phase involves positive feedback from the plastid itself. The two-phase biogenesis is demarked by distinct morphological changes, including movement of chloroplasts to the cell periphery. Intriguingly, the retrograde phase is inhibited by high levels of Suc, indicating that a surplus of carbon restricts the maturation of chloroplasts. Chloroplasts coordinate a range of cellular and devel-opmental processes, as covered in two reviews (de Souza et al., 2017; Hernández-Verdeja and Strand, 2018). These processes include signaling through the produc-tion of photosynthesis-derived reactive oxygen species (ROS) that cause inhibition of PSII (photoinhibition). The ephemeral superoxide and more enduring hydro-gen peroxide generated by photooxidative stress have well-studied impacts on signaling and physiology in leaves. These active oxygens also act as signaling molecules during development of flowers and fruits that may augment photoprotection, stimulate pigment production, and trigger chloroplast differentiation to chromoplasts and other forms with specific biochemical activities and structural features (Muñ oz and Munné-Bosch, 2018).