Mechanisms of Desiccation Tolerance in Angiosperm Resurrection Plants

Abstract

The mechanisms of protection against mechanical and oxidative stress were identified and compared in the angiosperm resurrection plants Craterostigma wilmsii, Myrothamnus flabellifolius and Xerophyta humilis. Dryinginduced ultrastructural changes within mesophyll cells were followed to gain an understanding of the mechanisms of mechanical stabilisation. In all three species, water filled vacuoles present in hydrated cells were replaced by several smaller vacuoles filled with non-aqueous substances. In X. humilis, these occupied a large proportion of the cytoplasm, preventing plasmalemma withdrawal and cell wall collapse. In C. wilmsii, vacuoles were small but extensive cell wall folding occurred to prevent plasmalemma withdrawal. In M. flabellifolius, some degree of vacuolation and wall folding occurred, but neither were sufficient to prevent plasmalemma withdrawal. This membrane was not ruptured, possibly due to membrane repair at plasmodesmata junctions where tearing might have occurred. In addition, the extra-cytoplasmic compartment appeared to contain material (possibly similar to that in vacuoles) which could facilitate stabilisation of dry cells.Photosynthesis and respiration are particularly susceptible to oxidative stress during drying. Photosynthesis ceased at high water contents and it is proposed that a controlled shut down of this metabolism occurred in order to minimise the potential for photo-oxidation. The mechanisms whereby this was achieved varied among the species. In X. humilis, chlorophyll was degraded and thylakoid membranes dismantled during drying. In both C. wilmsii and M. flabellifolius, chlorophyll was retained, but photosynthesis was stopped due to chlorophyll shading from leaf folding and anthocyanin accumulation. Furthermore, in M. flabellifolius thylakoid membranes became unstacked during drying. All species continued respiration during drying to 10% relative water content, which is proposed to be necessary for energy to establish protection mechanisms. Activity of antioxidant enzymes increased during drying and remained high at low water contents in all species, ameliorating free radical damage from both photosynthesis and respiration. The nature and extent of antioxidant upregulation varied among the species. In C. wilmsii, only ascorbate peroxidise activity increased, but in M. flabellifolius and X. humilis ascorbate peroxidise, glutathione reductase and superoxide dismutase activity increased, to various extents, during drying. Anthocyanins accumulated in all species but this was more extensive in the homoiochlorophyllous types, possibly for protection against photo-oxidation.

Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis

“…The role of sugar metabolism for the adaptation of H. rhodopensis to drought and desiccation was further substantiated by the presence of two transketolases in the list of the most abundant transcripts (Supplemental Table 3). Conversion of sugars and sugar derivatives is very important not only for the synthesis of osmoprotectants but also for cell-wall remodeling, which is essential for making the wall more flexible and countering the mechanical stress plant cells experience during desiccation [6]. A more flexible cell wall not only prevents breaking of plasmodesmata bridges during plasmolysis but also allows leaves to fold or roll, thereby reducing the surface exposed to solar radiation.…”

“…1). Such leaf rolling and folding is observed in other resurrection species such as Craterostigma wilmsii, C. plantagineum, and the woody shrub Myrothamnus flabellifolia [6,19]. This acts in concert with biochemical and molecular mechanisms such as the accumulation of anthocyanins and other polyphenols to protect against UV light and other radiation [57].…”

“…While the exact alterations in the cell wall remain undefined, the importance of cell wall remodeling and reversible changes in cell wall architecture in counteracting the mechanical stress that follows from dehydration has been shown for a number of species [6]. Biochemical changes in the plant cell wall polysaccharides and proteins take place, making the cell wall more flexible [71], thus enabling the morphological rolling and reversible folding of the leaves (Fig.…”

“…In addition, novel types of hydrophilic proteins are expressed during desiccation in resurrection plants, such as CpEdi-9 in C. plantagineum [83]. The small heat shock proteins (HSPs) have similar properties but some of them also act as molecular chaperones for other proteins, thus preventing proteins from aggregating and denaturing [6]. Both LEAs and HSPs are not normally expressed at high levels in hydrated vegetative tissues; however, they are found in seeds and in tissues experiencing water deficiency.…”

“…The mechanism of desiccation tolerance is common in bryophytes and lichens, less common in pteridophytes, rare in angiosperms, and absent from gymnosperms [5,6]. The complex plant tissues require mechanisms that prevent desiccation-induced cell and tissue damage in the first place; notably, the recovery from desiccation can be fast [7,8].…”