Occurrence and evolutionary significance of RESISTANT CELL WALLS IN CHAROPHYTES AND BRYOPHYTES

A survey of charophycean green algal and bryophyte taxa revealed the frequent occurrence of vegetative cell walls that were characterized by a specific form of autofluorescence and resistance to high temperature acid treatment (acetolysis). The time of production and the location of resistant, autofluorescent cell walls varied among charophyte and bryophyte taxa in patterns that suggest that bryophytes inherited the capacity to produce such walls from charophyte ancestors. A number of charophytes produced resistant walls in response to desiccation stress, suggesting an evolutionarily early adaptive response. Coleochaete was unique among charophytes, but similar to all bryophytes tested in that sexual reproduction induced autofluorescence in cell walls of well-hydrated tissues at the placental junction. Maternal tissues in apical portions of the pseudoseta bearing Sphagnum sporophytes were characterized by autofluorescent, acetolysis-resistant cell walls similar to those observed in maternal cells adjacent to Coleochaete zygotes. These observations suggest that cell–cell stimulus–response interactions regulate deposition of autofluorescent compounds in placental cell walls, and that this characteristic may have been shared by the earliest embryophytes and their charophyte ancestors. Various bryophytes deposit autofluorescent, acid-resistant compounds at other adaptively significant sites including sporangial epidermis, spiral thickenings of elaters, rhizoids, and leaves in the special case of Sphagnum moss. Sphagnum and liverwort sporangial epidermis, which had been subjected to acetolysis or strong acid procedures commonly used to release microfossils from rock matrices, resembled published photographs of Ordovician–Devonian microfossils consisting of cellular scraps that have been attributed to earliest land plants. Our work suggests that at least some of these fossils, previously thought to represent “dispersed cuticles,” could be reinterpreted as earliest known remains of plant sporophytic tissues, and that they may be homologous with resistant sporangial epidermis of modern bryophytes. In general, the patterns of occurrence of resistant, autofluorescent cell walls in charophytes and bryophytes suggest repeated exaptation. Regulation of deposition appears to have been modified through time, so that resistant wall compounds have had a sequence of functions: desiccation resistance and/or microbial resistance in lower charophytes, a role in embryogenesis in Coleochaete and embryophytes, and finally, decay resistance in innovative structures that characterize bryophytes, such as rhizoids, sporangial epidermis, and elaters.