Aquaphotomics and resurrection plant Haberlea rhodopensis uncover the secrets of the unique desiccation tolerance

Тwo laboratories, leaders in different scientific fields – Prof. Dr Roumiana Tsenkova (Kobe University, Japan) performing in-vivo non-destructive near infrared (NIR) spectral monitoring of living systems and Prof. Dr Dimitar Djilianov (Agrobioinsitute, Sofia, Bulgaria) working on resurrection plants, especially H. rhodopensis joined their efforts to uncover the mechanisms of extreme desiccation tolerance in some plants.

Haberlea rhodopensis; Credit: D. Djilianov

Water is of crucial importance for the life on our planet – both as part of the environment and/or component of the living systems. During their evolution, the organisms have developed various mechanisms to cope with stress, resulting from water deficiency. This is particularly true for plant kingdom, since plants have to survive water stress “on the spot” being unable to leave the unfavorable conditions.

There is a small group of plants, known as “resurrection plants” that can survive long periods (months, years) with almost completely desiccated vegetative tissues and recover fast and fully when water is available again. Obviously, such plant species are very useful model systems. This is particularly true for the Balkan endemite Haberlea rhodopensis which, despite the favorable conditions in most of its habitats in Bulgaria and Greece, keeps in its ‘genome, resurrection behavior coming back from more than 40 million years ago!

Enormous progress has been done recently at various levels to elucidate the mechanisms of desiccation tolerance of resurrection plants. As a rule, however they are focused on the biological components of these bio-aqueous systems. Little or no attention was paid so far to the role of water, as a partner during desiccation and recovery after severe stress!

And here came AQUAPHOTOMICS!!!

Researchers developed an experimental design to compare the reaction of H. rhodopensis and a non-resurrection plant species, belonging to the same botanical family during desiccation and recovery and to apply NIR spectroscopy studies to study the water structures in leaves of both species. In a paper, published recently in Scientific Report, the scientists showed that:

  • Water in the living organism is an aggregate (sum) of a defined number of different molecular structures (water species);
  • All other components and perturbations of the bio-aqueous system are “shaping up” the water matrix which, as a collective mirror, reflects molecular and environmental changes;
  • Fine restructuring and changes of the ratios of water molecular species allow the resurrection plant to adapt to the changes imposed by desiccation;
  • All water molecular structures (with different weight, hence different influence and role) are directly related to the respective functionality of the whole biological system;
  • Water spectral pattern is an integrative marker of the biological system functionality;
  • At desiccation, the resurrection plant water matrix is finely tuned by the biological components of the system. This provides constant ration of the water species regardless of the fast water content decrease. At full desiccation a sharp decrease of free water molecules and increase of water dimers and water molecules with 4 hydrogen bonds occurs.
  • During the rehydration of the resurrection plant, orderly incremental changes of mostly all water species take place;
  • The non-resurrection plant species, subjected to desiccation showed no changes in its water structures during desiccation while still alive.
Dynamics of different water species during dehydration and rehydration of Haberlea rhodopensis (A) and non ressurection plant (B). Sr – protonated water clusters, S0 – free water molecules, S1 – water dimers, S2, S3 and S4 – water molecules with 2, 3 and 4 hydrogen bonds, respectively. Credit: Kuroki, S. et al. Sci. Rep. (2019)

This research can be regarded as a pioneering effort with a valuable addition to our growing understanding of the mechanisms by which some organisms achieve their remarkable tolerance to extreme dehydration.

Shinichiro Kuroki et al. Water molecular structure underpins extreme desiccation tolerance of the resurrection plant Haberlea rhodopensis, Scientific Reports (2019). DOI: 10.1038/s41598-019-39443-4