Submitted to: Journal of Plant Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/1/2000
Publication Date: 11/1/2000
Interpretive Summary: This monograph takes all of the evidence relating to the possible mechanisms by which plants can survive the total loss of water (desiccation) of their vegetative tissues produced to date and formulates a series of testable hypotheses as to how desiccation tolerance evolved in the land plants. The synthesis of the data allows us to propose the following; 1. The initial evolution of vegetative desiccation tolerance wa a crucial step in the colonization of the land by primitive plants. 2. The primitive mechanism of tolerance probably involved constitutive cellular protection coupled with active cellular repair. 3. As plant species evolved, vegetative desiccation tolerance was lost. 4. The mechanism of desiccation tolerance exhibited in seeds, a developmentally induced cellular protection system, evolved from the primitive form of vegetative desiccation tolerance. 5. Modified vegetative desiccation tolerance mechanisms in angiosperms evolved from that programmed into seed development as species spread into arid environments. 6.. Most recently, certain desiccation-tolerant monocots evolved the strategy of losing chlorophyll and chloroplasts during drying to survive and compete in severe habitats with long periods of drought and high light conditions.
Technical Abstract: Vegetative desiccation tolerance is a widespread but uncommon occurrence in the plant kingdom. Most vegetative desiccation-tolerant plants are found in the less complex clades that constitute the algae, lichens and bryophytes. However, within the larger and more complex groups of vascular land plants there are some 60 to 70 species of pteridophytes, and around 60 species of angiosperms that exhibit vegetative desiccation tolerance. In this report we analyze the evidence for the differing mechanisms of desiccation tolerance and couple it with a phylogenetic framework to generate a working hypothesis as to the evolution of desiccation tolerance in land plants. We hypothesize that the initial evolution of vegetative desiccation tolerance was a crucial step in the colonization of the land by primitive plants. The primitive mechanism of tolerance probably involved as constitutive cellular protection coupled with active cellular repair. As plant species evolved, vegetative desiccation tolerance was lost as complexity and higher growth rates were selected for. Genes that had evolved for cellular protection and repair were, in all likelihood, recruited for different but related processes e.g., response to water stress and the desiccation tolerance of reproductive propagules. We thus hypothesize desiccation tolerance exhibited in seeds, a programmed cellular protection system, evolved from the primitive form of vegetative desiccation tolerance. The modified vegetative desiccation tolerance mechanism in angiosperms evolved from that programmed into seed development as species spread into arid environments. Most recently, certain desiccation-tolerant monocots evolved the strategy of poikilochlorophylly to survive and compete in marginal droughting habitats.