Unravelling the responses of metabolism to dehydration points to a role for cytoplasmic viscosity in desiccation tolerance

Tolerance of desiccation in seeds is a multifactorial trait in which the synthesis of protective substances and the repression of degradative processes that are induced during dehydration are equally critical. The most documented degradative reaction linked with desiccation sensitivity in seeds is the accumulation of peroxidative damage following drying. Such oxidative stress is likely to originate from reactive O2 species (ROS) that are generated as a result of uncontrolled respiration and impaired electron flow in mitochondria. Under physiological conditions, the generation of ROS depends on the redox states of the electron-transfer components and the availability of ADP and O2. However, it is not known whether these metabolic conditions prevail in drying seed tissues. Therefore this study focuses on the significance for energy metabolism of the changes in physical properties of water during drying. The effects of the loss of water on the redox states of cytochromes and energy metabolism during drying of imbibed cowpea cotyledons and pollens of Typha latifolia and Impatiens glandulifera were assessed non-invasively. Using electron spin resonance spectroscopy, it was found that viscosity is a valuable parameter to characterize the relation between desiccation and decrease in respiration and energy metabolism. During drying, mitochondrial cytochromes are progressively and synchronously reduced in conjunction with a decline in energy charge. The reduction of mitochondrial cytochromes probably originates from a decreased O2 availability as a result of the increased viscosity and impeded diffusion. The metabolism in desiccation-intolerant tissues shifted partially to ethanolic fermentation during drying, indicating that they experience anoxia during drying. Such metabolic perturbations were absent in desiccation-tolerant tissues. Thus a regulated viscosity increase and controlled O2 diffusion may be regarded as mechanisms of desiccation tolerance.