Dynamics of intracellular mannan and cell wall folding in the drought responses of succulent Aloe species

• Published in: Plant, cell and environment cell and environment, 2019-08, Vol.42 (8), p.2458-2471
• Main Authors: Ahl, Louise Isager, Mravec, Jozef, Jørgensen, Bodil, Rudall, Paula J., Rønsted, Nina, Grace, Olwen M.
• Format: Article
• Language: English
• Subjects: Adaptation; Aloe; Aloe - cytology; Aloe - metabolism; Aloe - physiology; Biological evolution; Cell Wall - metabolism; Cell walls; Composition; CoMPP; Drought; Drought resistance; Dynamic structural analysis; Folding; hydrenchyma; Intracellular; leaf anatomy; Mannan; Mannans - analysis; Mannans - metabolism; Moisture content; morphology; Original; Pectin; plant cell walls; Polymers; Polysaccharides; Polysaccharides - metabolism; Polysaccharides - physiology; Saccharides; Stress, Physiological; succulence; Water - metabolism; Water content; Water shortages; Water storage
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13560

Plants have evolved a multitude of adaptations to survive extreme conditions. Succulent plants have the capacity to tolerate periodically dry environments, due to their ability to retain water in a specialized tissue, termed hydrenchyma. Cell wall polysaccharides are important components of water storage in hydrenchyma cells. However, the role of the cell wall and its polysaccharide composition in relation to drought resistance of succulent plants are unknown. We investigate the drought response of leaf‐succulent Aloe (Asphodelaceae) species using a combination of histological microscopy, quantification of water content, and comprehensive microarray polymer profiling. We observed a previously unreported mode of polysaccharide and cell wall structural dynamics triggered by water shortage. Microscopical analysis of the hydrenchyma cell walls revealed highly regular folding patterns indicative of predetermined cell wall mechanics in the remobilization of stored water and the possible role of homogalacturonan in this process. The in situ distribution of mannans in distinct intracellular compartments during drought, for storage, and apparent upregulation of pectins, imparting flexibility to the cell wall, facilitate elaborate cell wall folding during drought stress. We conclude that cell wall polysaccharide composition plays an important role in water storage and drought response in Aloe. This paper highlights the significance of structured cell wall folding in the drought‐stressed hydrenchyma tissue of Aloe helenae and Aloe vera. Dynamic changes in cell wall polysaccharide composition, especially mannan polymers, reveal a potential mechanism for plant leaf succulence.