Effects of De‐ and Rehydration in Desiccation‐Tolerant Liverworts: A Cytological and Physiological Study

Abstract

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. The University of Chicago Press is collaborating with JSTOR to digitize, preserve and extend access to International Journal of Plant Sciences.Liverworts are probably the earliest-diverging group of green land plants, but in contrast to mosses and vascular plants, there has been only limited information on the physiology of desiccation tolerance and none on the cytological consequences of de-and rehydration in this group. We explore the physiological and cytological effects of drying and rewetting in several desiccation-tolerant liverworts and examine parallels with and differences from vascular plants and mosses. Observations were made of water-stress responses and recovery using infrared gas analysis and modulated chlorophyll fluorescence, and structural and ultrastructural changes were observed with light and electron microscopy. Dehydration elicits profound cytological changes: fragmentation of the vacuole, rounding of the chloroplasts and mitochondria with thylakoids, and cristae becoming rearranged but remaining undamaged. These changes closely parallel those seen in mosses and desiccationtolerant vascular plants, as does recovery of the chlorophyll-fluorescence parameter F v =F m , which shows halfrecovery within minutes or an hour or two but returns to normal, unstressed values only after 24-48 h. As in mosses, de-and rehydration are associated with the de-and repolymerization of the cortical microtubule cytoskeleton. Particularly interesting and described here for the first time is the behavior of the oil bodies, membrane-bound organelles unique to liverworts. In the dry state, these remain substantially unchanged, but after rewetting, they become flattened and regain their normal morphology only after 48 h. When subjected to unnaturally fast rate of drying, the oil bodies, together with other organelles, disintegrate on rewetting. Our findings-that the major changes associated with de-and rehydration in liverworts closely parallel those in mosses and, indeed, vascular plants-imply that the basic physiology and cytology of desiccation tolerance is ancestral in land plants. The unexpected discovery that the oil bodies, while retaining their original volume during drying, collapse during rehydration suggests a shifting of soluble carbohydrates or other moieties into the cytosol and provides the first experimental evidence that the oil bodies may have a crucial role in desiccation tolerance.

Cytological insights into the desiccation biology of a model system: moss protonemata

“…In chloronemata, these changes and subsequent recovery closely resemble those in leaf cells of mosses (Tucker et al, 1975;Proctor et al, 2007b), liverworts (Pressel et al, 2009), pteridophytes (Platt et al, 1997) and angiosperms (Gaff et al, 1976;Gaff, 1997;Dalla Vecchia et al, 1998); In caulonemata, instead, there are remarkable similarities to FCCs (Pressel et al, 2006). Although some of the ultrastructural changes elicited by dehydration can simply be ascribed to the general withdrawal of water from the cells and are, indeed, also observed in fast-desiccated cells that do not recover following rehydration, for example close packing of free ribosomes, reduction in the volume of plastids and mitochondria, and chromatin condensation in the nuclei, others are clearly indicative of more active processes.…”

“…The same is also true for the meristematic cells of Po. formosum (Pressel et al, 2006) and those of the liverwort Southbya nigrella (Pressel et al, 2009). Changes in MT dynamics have also been described in higher plants in response to cold and freezing stress (Pressel et al, 2006 and references therein), and Wang et al (2007) have shown recently that salt tolerance in Arabidopsis requires the reorganization of the cortical MTs.…”

Physiology of Photosynthetic Organisms Within Biological Soil Crusts: Their Adaptation, Flexibility, and Plasticity

“…This "resaturation respiration" is different from basal respiration; it is cyanide sensitive in the lichen Hypogymnia physodes (and perhaps generally), which basal (dark) respiration is not, and decays in a comparable time that it takes for the fine structural changes to be completed (Farrar and Smith 1976;Proctor et al 2007a). Recovery from desiccation takes place regardless of the presence of protein synthesis inhibitors (Proctor and Smirnoff 2000;Proctor et al 2007a, b;Pressel et al 2009). The pattern of protein synthesis alters dramatically in the first hours following rewetting, and the sequence of events during recovery is complex (Oliver 2009).…”

“…The pattern of protein synthesis alters dramatically in the first hours following rewetting, and the sequence of events during recovery is complex (Oliver 2009). Morphological change at the subcellular level is most active in the first few hours of rehydration, but full return of organelles to their pre-desiccation form and disposition, and reassembly of the cytoskeleton may take 24-48 h (Pressel et al 2006(Pressel et al , 2009. This is essential for active translocation (Ligrone and Duckett 1994;Pressel et al 2006) and for the cell cycle, cell division, and cell growth (Mansour and Hallet 1981), but apparently not for photosynthesis or carbon fixation (Pressel et al 2009).…”

“…The "oil bodies" of liverworts appear to play a crucial role in recovery of Southbya nigrella and probably other species (Pressel et al 2009;Proctor 2010). Some species of liverworts, particularly small Marchantiales (Corsinia, Exormotheca, Mannia, Oxymitra, Plagiochasma, and Riccia spp.…”