Molecular Biology of Freezing Tolerance

Abstract

Winter survival for many kinds of animals involves freeze tolerance, the ability to endure the conversion of about 65% of total body water into extracellular ice and the consequences that freezing imposes including interruption of vital processes (e.g., heartbeat and breathing), cell shrinkage, elevated osmolality, anoxia/ischemia, and potential physical damage from ice. Freeze-tolerant animals include various terrestrially hibernating amphibians and reptiles, many species of insects, and numerous other invertebrates inhabiting both terrestrial and intertidal environments. Well-known strategies of freezing survival include accumulation of low molecular mass carbohydrate cryoprotectants (e.g., glycerol), use of ice nucleating agents/proteins for controlled triggering of ice growth and of antifreeze proteins that inhibit ice recrystallization, and good tolerance of anoxia and dehydration. The present article focuses on more recent advances in our knowledge of the genes and proteins that support freeze tolerance and the metabolic regulatory mechanisms involved. Important roles have been identified for aquaporins and transmembrane channels that move cryoprotectants, heat shock proteins and other chaperones, antioxidant defenses, and metabolic rate depression. Genome and proteome screening has revealed many new potential targets that respond to freezing, in particular implicating cytoskeleton remodeling as a necessary facet of low temperature and/or cell volume adaptation. Key regulatory mechanisms include reversible phosphorylation control of metabolic enzymes and microRNA control of gene transcript expression. These help to remodel metabolism to preserve core functions while suppressing energy expensive metabolic activities such as the cell cycle. All of these advances are providing a much more complete picture of life in the frozen state.

Membrane Stress During Thawing Elicits Redistribution of Aquaporin 7 But Not of Aquaporin 9 in Boar Spermatozoa

“…Water will thus change from liquid to solid state and form ice crystals in the extracellular space, increasing even more the osmolarity of the extracellular space 28 . Since glycerol is toxic, a controlled flow of this molecule over the plasma membrane is required in order for the cells to survive, a matter that is controllable at low (5°C) temperature.…”

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

“…Broadly, work on short-term cold shock gene expression changes has shown that the predominant group of genes showing expression changes are those involved in the stress and immune response (e.g. heat shock proteins (Hsps), Turandot genes, etc) (Zhang et al, 2011;Sinclair et al, 2013;Storey and Storey, 2013). In addition, the neuropeptide CAPA has been shown to play an important role in both cold and desiccation resistance in several species of Drosophila, including D. montana, when assessed using cold shock (Terhzaz et al, submitted).…”

Genetic Architecture of Natural Variation in Thermal Responses of Arabidopsis

“…With the predicted increase in global temperatures, and their potential impact on agricultural productivity, there are efforts to understand the genetic basis of temperature responses in plants. Traditionally, temperature effects have been studied in the context of extreme stress responses such as heat shock or cold shock (Kotak et al, 2007;Barrero-Gil and Salinas, 2013;Song et al, 2013;Storey and Storey, 2013). In recent times, there has been an interest in analyzing the response of plants to changes in their growth temperature within the nonstress range of l6°C to 27°C, as even small changes in temperature can have major impacts on plant growth and development (Wigge, 2013;Franklin et al, 2014).…”