Cellular and Genetic Responses of Plants to Sugar Starvation

Abstract

Photosynthesis converts solar energy to chemical energy, which then drives the synthesis of sugars from carbon dioxide and water. Sugars play multiple roles in all aspects of plant life. First, they provide the main respiratory substrates for the generation of energy and metabolic intermediates that are then used for the synthesis of macromolecules and other cell constituents. Second, Rib and deoxy-Rib sugars form part of the structure of DNA and RNA. Third, polysaccharides are the major structural elements of plant cell walls. Fourth, linkage to sugar is required for proper functioning of many proteins and lipids. As a consequence, the abundance and depletion of sugars or their derivatives initiate various responses in plants and have profound effects on plant metabolism, growth, and development. Plants are considered to be carbon autotrophs, but they can be considered as carbon heterotrophs during some part of their life cycle and in some of their non-green organs such roots, stems, and flowers, which are not involved in photosynthesis. Furthermore, carbohydrate depletion can occur and is a fact of life in most plants. For instance, variations in environmental factors such as light, water, or temperature and attacks by pathogens or herbivores may lead to a significant decrease in the efficiency of photosynthesis in source tissues (such as leaves that synthesize and export carbohydrates) and thus reduce the supply of carbohydrates to sink tissues (such as the non-green tissues that import carbohydrates for respiration, growth, and development). Under certain growth conditions, such as during an annual resting season or after leaf shedding, photosynthesis is turned off or operates to a lower degree, and carbohydrate reserves must be utilized and may become limited in nonphotosynthetic tissues. In germinating seeds under unfavorable environmental conditions the mobilization of stores in the cotyledons is delayed, which may result in the depletion of available carbohydrates and a decrease in seedling vigor. Knowledge about the response to sugar starvation and adaptation mechanisms in plants is of both fundamental and agronomic importance. In nature, the cessation of growth of a heterotrophic living organism is often brought about by a poor nutrient environment, a commonly encountered stress. Environmental changes affect various biochemical reactions, often disturbing the balanced distribution of metabolites within cells. In most instances, living cells show a rapid molecular response to overcome adverse environmental conditions. How a living organism survives during periods of environmental stress is an exciting area of research. The most extensive studies have been done with microorganisms. The ability of microorganisms to sense and respond to unscheduled changes in their environment is crucial to their survival. When cells of microorganisms encounter unfavorable nutrient conditions, they ultimately enter a stationary phase. Cells in the stationary phase are physiologically, biochemically, and morphologically different from cells growing exponentially. Studies using Escherichia coliand yeast (Saccharomyces cerevisiae) have indicated that entry into the stationary phase is a complex, highly regulated process that activates a program for long-term survival. The program includes the lack of a requirement for added nutrients and an absence of cell division. The similarities of eukaryotic and prokaryotic microorganisms in their responses to nutrient limitations suggest that such responses are based on evolutionarily conserved genetic mechanisms. Similarly, sugar starvation initiates changes in substantial physiological and biochemical processes with the goal of sustaining respiration and other essential metabolic processes in plants. Sugar starvation also initiates changes in cellular processes to recycle cellular constituents and dramatically changes the pattern of gene expression. However, the underlying mechanisms used by plant cells to cope with sugar starvation are largely unknown, and only recently have these questions been addressed experimentally. This lack of knowledge contrasts with the situation in bacteria and yeast, where the molecular biology and physiology of mutants have yielded extensive information about responses to sugar starvation. This review discusses the recent advances made in our understanding of the molecular events that operate in microorganisms upon sugar starvation, as well as the cellular and genetic responses of plants to sugar starvation. The majority of bacteria spend most of their time in a nutrient-limited starvation phase and as a result have evolved mechanisms that allow them to survive under these conditions and to resume growth once nutrients become available. Some bacteria, e.g.Bacillus spp., undergo major differentiation programs that lead to the formation of highly stress-resistant endospores or cysts. Other bacteria, e.g. E. coli, even without the formation of different