The discovery, scope, and puzzle of desiccation tolerance in plants

Abstract

The modern scientific study of desiccation tolerance began in 1702 when Anthony von Leeuwenhoek discovered that rotifers could survive without water for months. By 1860, the controversy over whether organisms could dry up without dying had reached such a pitch that a special French commission was convened to adjudicate the dispute. In 2000, we know that a few groups of animals and a wide variety of plants can tolerate desiccation in the active, adult stages of their life cycles. Among plants, this includes many lichens and bryophytes, a few ferns, and a very few flowering plants, but no gymnosperms nor trees. Some desiccation-tolerant species can survive without water for over ten years, recover from desiccation to unmeasurably low water potentials, and, when plants are desiccated, endure temperature extremes from −272 to 100 °C. Desiccation-tolerant plants occur on all continents but mainly in xeric habitats or microhabitats where the cover of desiccation-sensitive species is low. Two main puzzles arise from these patterns: What are the mechanisms by which plants tolerate desiccation? and Why are desiccation-tolerant plants not more ecologically widespread? Recent molecular and biochemical studies suggest that there are multiple mechanisms of tolerance, many of which involve protection from oxidants and from the loss of configuration of macromolecules during dehydration. Hypotheses to explain the restricted ecological range of desiccation-tolerance plants include inability to maintain a cumulative positive carbon balance during repeated cycles of wetting and drying and inherent trade offs between desiccation tolerance and growth rate.