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A footprint of desiccation tolerance in the genome of Xerophyta viscosa

Nature Plants volume 3, Article number: 17038 (2017) Cite this article

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Abstract

Desiccation tolerance is common in seeds and various other organisms, but only a few angiosperm species possess vegetative desiccation tolerance. These ‘resurrection species’ may serve as ideal models for the ultimate design of crops with enhanced drought tolerance. To understand the molecular and genetic mechanisms enabling vegetative desiccation tolerance, we produced a high-quality whole-genome sequence for the resurrection plant Xerophyta viscosa and assessed transcriptome changes during its dehydration. Data revealed induction of transcripts typically associated with desiccation tolerance in seeds and involvement of orthologues of ABI3 and ABI5, both key regulators of seed maturation. Dehydration resulted in both increased, but predominantly reduced, transcript abundance of genomic ‘clusters of desiccation-associated genes’ (CoDAGs), reflecting the cessation of growth that allows for the expression of desiccation tolerance. Vegetative desiccation tolerance in X. viscosa was found to be uncoupled from drought-induced senescence. We provide strong support for the hypothesis that vegetative desiccation tolerance arose by redirection of genetic information from desiccation-tolerant seeds.

The grass family (Poaceae) is arguably the most important contributor to global food security. However, poaceous staple crops, such as maize, corn, rice and wheat, do not survive the extreme water loss that is inevitably brought about by extended periods of drought. In contrast, their seeds are desiccation tolerant, and they can be dried to water contents as low as 1–5% on a fresh weight basis without losing viability1. There are some 135 angiosperm species, termed ‘resurrection plants’, which produce desiccation-tolerant seeds and possess desiccation-tolerant vegetative tissues2–4. Vegetative desiccation tolerance (DT) first arose with the transition from aquatic to terrestrial life forms, when both the probability of experiencing adverse conditions and the survival cost of such conditions were high5. As plants expanded into terrestrial habitats and developed tracheids to move water from the substrate to their aerial parts and more complex ecosystems were established, the slow growth characteristic of desiccation-tolerant plants was limiting their competitive ability. This favoured the loss of DT in vegetative tissues, the development of mechanisms to prevent water loss (physiological and morphological) and the confinement of DT to seeds, spores and pollen grains where it was required for dispersal and preservation of genetic resources6,7. It has been proposed that vegetative DT reappeared in the angiosperms, presumably in response to colonization of environmentally demanding habitats, in at least 13 separate lineages to evolve the present day resurrection plants4,7,8.

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Figure 1: X. viscosa phenotypes.
Figure 2: Genomic organization of X. viscosa.
Figure 3: LEAs transcript expression and accumulation patterns during dehydration and rehydration.

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Acknowledgements

We thank E. Parker (owner) and J. Burrows (manager) of Buffelskloof Nature Reserve Mphumulanga for allowing collection of Xerophyta viscosa plants. We thank all members of the Wageningen Seed Lab for discussions. We thank K. Cooper for invaluable assistance in compiling Fig. 1. M.-C.D.C. received financial support from CNPq–National Council for Scientific and Technological Development (201007/2011-8). M.A.S.A. received financial support from CAPES–Brazilian Federal Agency for Support and Evaluation of Graduate Education (BEX0428/09-04, BEX0857/14-9). J.M.F. acknowledges use of funding supplied by the South African Research Chairs Initiative of the DST and NRF of SA (Grant No 98406).

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Author notes

  1. Maria-Cecília D. Costa and Mariana A. S. Artur: These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Plant Physiology, Wageningen University, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands

    Maria-Cecília D. Costa, Mariana A. S. Artur, Julio Maia, Eef Jonkheer, Martijn F. L. Derks, Harm Nijveen, Wilco Ligterink & Henk W. M. Hilhorst

  2. Department of Molecular and Cell Biology, University of Cape Town, Private Bag, 7701 Cape Town, South Africa

    Maria-Cecília D. Costa & Jill M. Farrant

  3. Bioinformatics Group, Wageningen University, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands

    Eef Jonkheer, Martijn F. L. Derks & Harm Nijveen

  4. Centre for Tropical Crops and Biocommodities, Queensland University of Technology, PO Box 2434, Queensland 4001, Brisbane, Australia

    Brett Williams & Sagadevan G. Mundree

  5. Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Cologne, Germany

    José M. Jiménez-Gómez

  6. Bioscience, Wageningen Plant Research International, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands

    Thamara Hesselink & Elio G. W. M. Schijlen

  7. USDA-ARS-MWA-PGRU, 205 Curtis Hall, University of Missouri, Columbia, 65211, Missouri, USA

    Melvin J. Oliver

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  1. Maria-Cecília D. Costa
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Contributions

M.-C.D.C. and M.A.S.A. wrote the article; M.-C.D.C., H.N., E.J. and M.F.L.D. performed the bioinformatics; J.M. and W.L. contributed to the genome and transcriptome analysis; J.M.J.-G. and M.J.O. performed and analysed the transcriptomics; B.W. and S.G.M. provided the autophagy/anti-senescence dataset and performed blasting; T.H. and E.G.W.M.S. prepared the libraries and performed the PacBio sequencing and initial genome analysis; J.M.F. and H.W.M.H. initiated and coordinated the work and directed preparation of the article.

Corresponding author

Correspondence to Henk W. M. Hilhorst.

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Supplementary information

Supplementary Information

Supplementary Figures 1–6, Supplementary Tables 1–6, Supplementary References. (PDF 5201 kb)

Supplementary Data Table

List of 4,914 probe sets used to build the network and network analysis results. Network analysis was done using Cytoscape's built-in tool NetworkAnalyzer. (XLS 1827 kb)

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Costa, MC., Artur, M., Maia, J. et al. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nature Plants 3, 17038 (2017). https://doi.org/10.1038/nplants.2017.38

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