The evolution of vegetative desiccation tolerance in land plants

Vegetative desiccation tolerance is a widespread but uncommon occurrence in the plant kingdom generally. The majority of vegetative desiccation-tolera nt plants are found in the less complex clades that constitute the algae, l ichens and bryophytes. However, within the larger and more complex groups o f vascular land plants there are some 60 to 70 species of ferns and fern al lies, and approximately 60 species of angiosperms that exhibit some degree of vegetative desiccation tolerance. In this report we analyze the evidence for the differing mechanisms of desiccation tolerance in different plants, including differences in cellular protection and cellular repair, and coup le this evidence with a phylogenetic framework to generate a working hypoth esis as to the evolution of desiccation tolerance in land plants. We hypoth esize that the initial evolution of vegetative desiccation tolerance was a crucial step in the colonization of the land by primitive plants from an or igin in fresh water. The primitive mechanism of tolerance probably involved constitutive cellular protection coupled with active cellular repair, simi lar to that described for modern-day desiccation-tolerant bryophytes. As pl ant species evolved, vegetative desiccation tolerance was lost as increased growth rates, structural and morphological complexity, and mechanisms that conserve water within the plant and maintain efficient carbon fixation wer e selected for. Genes that had evolved for cellular protection and repair w ere, in all likelihood, recruited for different but related processes such as response to water stress and the desiccation tolerance of reproductive p ropagules. We thus hypothesize that the mechanism of desiccation tolerance exhibited in seeds, a developmentally induced cellular protection system, e volved from the primitive form of vegetative desiccation tolerance. Once es tablished in seeds, this system became available for induction in vegetativ e tissues by environmental cues related to drying. The more recent, modifie d vegetative desiccation tolerance mechanism in angiosperms evolved from th at programmed into seed development as species spread into very arid enviro nments. Most recently, certain desiccation-tolerant monocots evolved the st rategy of poikilochlorophylly to survive and compete in marginal habitats w ith variability in watts availability.