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

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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.

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Abbreviations

AIR:

Alcohol insoluble residue

CoMPP:

Comprehensive microarray polymer profiling

CBM:

Carbohydrate binding module

mAb:

Monoclonal antibody

FT-IR:

Fourier transform-infrared spectroscopy

RG:

Rhamnogalacturonan

HG:

Homogalacturonan

XyG:

Xyloglucan

AXyG:

Arabinoxyloglucan

AX:

Arabinoxylan

AGP:

Arabinogalactan protein

XTH:

Xyloglucan transhydrolase

XET:

Xyloglucan endotransglycosylase

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Acknowledgments

Our thanks go to Borakalalo National Park for donation of X. humilis, John and Sandy Burrows and Elizabeth Parker (Lydenberg district) for donation of C. wilmsii and X. viscosa, and Rupert and Tanya Baber (Waterberg district) for donation of M. flabellifolia, Professor Martin Kidd (Centre for Statistical Consultation, Stellenbosch University) is thanked for help and discussions on statistical data analysis. We would like to thank Jonatan Fangel (University of Copenhagen, Denmark) for help with the CoMPP figure artwork. The work was supported by grants to Jill Farrant from the Harry Oppenheimer Trust Foundation and University of Cape Town.

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Author notes

  1. Iben Sørensen

    Present address: Department of Plant Biology, Cornell University, Ithaca, NY, 14853, USA

Authors and Affiliations

  1. Institute for Wine Biotechnology, Department of Viticulture and Oenology, Faculty of AgriSciences, Stellenbosch University, Matieland, 7602, South Africa

    John P. Moore & Eric E. Nguema-Ona

  2. Laboratoire ‘Glycobiologie et Matrice Extracellulaire Végétale’, Glyco-MEV, IFRMP23-PRIMACEN IBiSA, Université de Rouen, 76821, Mont-Saint-Aignan, France

    Eric E. Nguema-Ona, Mäite Vicré-Gibouin & Azeddine Driouich

  3. Department of Plant Biology and Biotechnology, Faculty of Life Sciences, University of Copenhagen, 1001, Copenhagen, Denmark

    Iben Sørensen & William G.T. Willats

  4. Department of Molecular and Cell Biology, University of Cape Town, Rondebosch, 7701, South Africa

    Jill M. Farrant

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Correspondence to John P. Moore.

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Moore, J.P., Nguema-Ona, E.E., Vicré-Gibouin, M. et al. Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237, 739–754 (2013). https://doi.org/10.1007/s00425-012-1785-9

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