A footprint of desiccation tolerance in the genome of Xerophyta viscosa

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.

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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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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.

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Correspondence to Henk W. M. Hilhorst.

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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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