Submitted to: Trade Journal Publication
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: September 10, 2005
Publication Date: December 1, 2005
Citation: Oliver, M.J., Velten, J.P., Mishler, B. 2005. Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats?. Integrated Comparative Biology. 45: 788-799. Interpretive Summary: This manuscript is part of our ongoing studies into natural stress tolerance mechanisms exhibited in plants whose natural habitats experience extreme environments, in this case severe water deficits leading to desiccation. In this manuscript we describe a functional genomics approach to gain insight not only into the mechanism of desiccation tolerance in plants but also its evolution. We present new data to suggest that early in the evolution of desiccation tolerance, LEA proteins (first described in seeds) are predominantly expressed during the rehydration phase following desiccation. Biochemical evidence suggests that these early LEAs are involved in the sequestration of membranes enabling a rapid recovery of the cell from damage incurred during desiccation and rehydration. Phylogenetic analysis using one of these primitive LEA protein genes has enabled us to revisit our present working hypothesis on the evolution of desiccation tolerance in plants and to suggest a new origin. Such studies lead to discoveries that will impact our ability to modify crop germplasm for tolerance to dehydration and drought.
Technical Abstract: Bryophytes are a non-monophyletic group of three major lineages (liverworts, hornworts, and mosses) that descend from the earliest branching events in the phylogeny of land plants. We postulate that desiccation tolerance is a primitive trait, thus mechanisms by which the first land plants achieved tolerance may be reflected in how extant desiccation-tolerant bryophytes survive drying. Evidence is consistent with extant bryophytes employing a tolerance strategy of constitutive cellular protection coupled with induction of a recovery/repair mechanism upon rehydration. Cellular structures appear intact in the desiccated state but are disrupted by rapid uptake of water upon rehydration, but cellular integrity is rapidly regained. The photosynthetic machinery appears to be protected such that photosynthetic activity recovers quickly. Gene expression responds following rehydration and not during drying. Gene expression is translationally controlled and results in the synthesis of a number of proteins, collectively called rehydrins. Some prominent rehydrins are similar to Late Embryogenesis Abundant (LEA) proteins, classically ascribed a protection function during desiccation. The role of LEA proteins in a rehydrating system is unknown but data indicates a function in stabilization and reconstitution of membranes. Phylogenetic studies using a Tortula ruralis LEA-like rehydrin led to a re-examination of the evolution of desiccation tolerance. A new phylogenenetic analysis suggests that: (i) the basic mechanisms of tolerance seen in modern day bryophytes have changed little from the earliest manifestations of desiccation tolerance in land plants, and (ii) vegetative desiccation tolerance in the early land plants may have evolved from a mechanism present first in spores.