Maintaining homeostasis by controlled alternatives for energy distribution in plant cells under changing conditions of supply and demand

Abstract

Plants depend on light energy for the generation of ATP and reductant as well as on supply of nutrients (inorganic C, N, and S compounds) to successfully produce biomass. Any excess of reducing power or lack of electron acceptors can lead to the formation of reactive oxygen species (ROS). Multiple systems are operating to avoid imbalances and subsequent oxidative stress by efficiently scavenging any formed ROS. Plants can sense an upcoming imbalance and correspondingly adapt to changed conditions not only by an increase of ROS scavengers, but also by using excess incoming light energy productively for assimilatory processes in actively metabolizing cells of growing leaves. CO2 assimilation in chloroplasts is controlled by various redox-regulated enzymes; their activation state is strictly linked to metabolism due to the effects of small molecules on their actual activation state. Shuttle systems for indirect transfer of reducing equivalents and ATP specifically distribute the energy fluxes between compartments for optimal biomass production. Integration of metabolic and redox signals involves the cytosolic enzyme glyceraldehyde-3-P dehydrogenase (GapC) and some of its many moonlighting functions. Its redox- and metabolite-dependent interactions with the mitochondrial outer membrane, the cytoskeleton, and its occurrence in the nucleus are examples of these additional functions. Induction of the genes required to achieve an optimal response suitable for the respective conditions allows for growth when plants are exposed to different light intensities and nutrient conditions with varying rates of energy input and different assimilatory pathways for its consumption are the required in the long term. A plant-specific respiratory pathway, the alternative oxidase (AOX), functions as a site to convert excess electrons into heat. For acclimation, any imbalance is sensed and elicits signal transduction to induce the required genes. Examples for regulated steps in this sequence of events are given in this review. Continuous adjustment under natural conditions allows for adaptive responses. In contrast, sudden light stress, as employed when analyzing stress responses in lab experiments, frequently results in cell destruction. Knowledge of all the flexible regulatory mechanisms, their responsiveness, and their interdependencies is needed when plant growth is to be engineered to optimize biomass and production of any desired molecules.