Chloroplast breakdown during dehydration of a homoiochlorophyllous resurrection plant proceeds via senescence-like processes

The vegetative tissues of resurrection plants are able to withstand severe protoplasmic dehydration and revive quickly upon rehydration. Resurrection species defined as 'homoiochlorophyllous' retain most or part of their chlorophyll and photosynthetic complement in the dry state, and rely on various mechanisms to protect themselves against photo-damage. In this study, we investigated the changes in chlorophyll distribution, light absorption gradients as well as the alterations in ultrastructure that take place during dehydration of the homoiochlorophyllous species Craterostigma pumilum. Chlorophyll fluorescence profiles show that light absorption is attenuated in dry leaves, likely minimizing generation of reactive oxygen species. These are accompanied by changes that take place in the supramolecular organization of the photosynthetic protein complexes, and ordered functional adjustments of the photosynthetic apparatus, further lessening the excitation and electron pressures. Albeit these, the ultrastructural studies reveal that chloroplasts in dehydrated leaf tissues exhibit features indicative of oxidative stress, which are also reminiscent of senescing chloroplasts. These include mass proliferation of plastoglobules, variable degrees of thylakoid dismantling, as well as chloroplast fragmentation and seemingly vacuolar degradation of such fragments. In addition, unique vesicular structures between the two chloroplast envelope membranes were visualized, some of which appeared to detach from chloroplasts, likely en route to degradation. Together, the data indicate that homoiochlorophyllous resurrection species handle photo-induced damage during dehydration on two levels. Minimization of photo-damage is achieved by attenuation of light absorption and other photo-protective mechanisms. When this is insufficient and significant damage does occur, elimination of damaged components takes place via processes resembling senescence. Nevertheless, these processes are reversible, enabling the plants to avoid the terminal steps of senescence and, hence, to recover.