Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation

Abstract

A variety of Southern African resurrection plants were surveyed using high-throughput cell wall profiling tools. Species evaluated were the dicotyledons, Myrothamnus flabellifolia and Craterostigma plantagineum; the monocotyledons, Xerophyta viscosa, Xerophyta schlecterii, Xerophyta humilis and the resurrection grass Eragrostis nindensis, as well as a pteridophyte, the resurrection fern, Mohria caffrorum. Comparisons were made between hydrated and desiccated leaf and frond material, with respect to cell wall composition and polymer abundance, using monosaccharide composition analysis, FT-IR spectroscopy and comprehensive microarray polymer profiling in combination with multivariate data analysis. The data obtained suggest that three main functional strategies appear to have evolved to prepare plant cell walls for desiccation. Arabinan-rich pectin and arabinogalactan proteins are found in the resurrection fern M. caffrorum and the basal angiosperm M. flabellifolia where they appear to act as 'pectic plasticizers'. Dicotyledons with pectin-rich walls, such as C. plantagineum, seem to use inducible mechanisms which consist of up-regulating wall proteins and osmoprotectants. The hemicellulose-rich walls of the grass-like Xerophyta spp. and the resurrection grass E. nindensis were found to contain highly arabinosylated xylans and arabinogalactan proteins. These data support a general mechanism of 'plasticising' the cell walls of resurrection plants to desiccation and implicate arabinose-rich polymers (pectin-arabinans, arabinogalactan proteins and arabinoxylans) as the major contributors in ensuring flexibility is maintained and rehydration is facilitated in these plants.

Reversible in vivo cellular changes occur during desiccation and recovery: Desiccation tolerance of the resurrection filmy fern Hymenophyllum dentatum Cav.

“…Cell wall folding upon desiccation has been reported before in mosses and angiosperms (Proctor et al 2007, Vicre et al 2004, Moore et al 2013. The reversible changes in cell wall architecture have been proposed as a mechanism for counteracting mechanical stress (Gechev et al 2012), which is defined as the tension that develops between and within the plasma membrane and the cell wall to a loss of turgor pressure (Walters et al 2002).…”

Orthodox Seeds and Resurrection Plants: Two of a Kind?

“…Water loss leads to cell shrinkage, which induces changes in solute concentration, increases in cytoplasm viscosity, and the plasticizing of cell walls (Moore et al, 2013;Walters, 2015;Leprince et al, 2017). The increase in solute concentration and the consequent increase in cytoplasmic viscosity are due to the accumulation of sugars, proteins, salts, organic acids, and amino acids.…”

“…In addition to the alleviation of mechanical stress via water replacement, as described above, changes in cell wall plasticity and architecture during drying can significantly help minimize the stress associated with the loss of turgor pressure (Moore et al, 2008(Moore et al, , 2013. The use of arabinose-containing polymers and the arabinosylation of existing polymers upon water loss in the cell walls of seeds and resurrection plants plasticize the cell wall and prevent polymer aggregation (for review, see Moore et al, 2013).…”

“…The use of arabinose-containing polymers and the arabinosylation of existing polymers upon water loss in the cell walls of seeds and resurrection plants plasticize the cell wall and prevent polymer aggregation (for review, see Moore et al, 2013). Besides increasing the plasticity and/or fluidity of cell walls, these plasticizers function as mechanosensors in water loss signal perception (Moore et al, 2013).…”

“…Although resurrection plants from different lineages have evolved wall-specific solutions to desiccation, those that have been characterized use (or appear to use) some arabinose-containing polymers (Moore et al, 2013). At the transcriptional level, hydrated C. plantagineum leaves are enriched in the transcripts of genes involved in cell wall remodeling and the maintenance of cell wall plasticity, possibly to ensure timely increases in cell wall flexibility and to prevent mechanical strain upon dehydration (Rodriguez et al, 2010).…”