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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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References

  1. Kermode, A. R. Approaches to elucidate the basis of desiccation-tolerance in seeds. Seed Sci. Res. 7, 75–95 (1997).

    Google Scholar 

  2. Black, M. & Pritchard, H. W. (eds) in Desiccation and Survival in Plants 207–237 (CABI, 2002); http://www.cabi.org/cabebooks/ebook/20023069464

    Google Scholar 

  3. Gaff, D. F. Desiccation-tolerant flowering plants in Southern Africa. Science 174, 1033–1034 (1971).

    Google Scholar 

  4. Porembski, S. in Plant Desiccation Tolerance Vol. 215 (eds Lüttge, U., Beck, E. & Bartels, D. ) 139–156 (Springer, 2011).

    Google Scholar 

  5. Jönsson, K. I. & Järemo, J. A model on the evolution of cryptobiosis. Ann. Zool. Fennici. 40, 331–34040 (2003).

    Google Scholar 

  6. Alpert, P. Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J. Exp. Biol. 209, 1575–1584 (2006).

    Google Scholar 

  7. Oliver, M. J., Tuba, Z. & Mishler, B. D. The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 151, 85–100 (2000).

    Google Scholar 

  8. Oliver, M. J., Velten, J. & Mishler, B. D. Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr. Comp. Biol. 45, 788–799 (2005).

    Google Scholar 

  9. Farrant, J. M. et al. A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker). Planta 242, 407–426 (2015).

    Google Scholar 

  10. Dai, A. Increasing drought under global warming in observations and models. Nat. Clim. Change 3, 52–58 (2013).

    Google Scholar 

  11. Chin, C.-S. et al. Phased diploid genome assembly with single molecule real-time sequencing. Nat. Methods 13, 1050–1054 (2016).

    Google Scholar 

  12. Song, L., Florea, L. & Langmead, B. Lighter: fast and memory-efficient sequencing error correction without counting. Genome Biol. 15, 509 (2014).

    Google Scholar 

  13. Ye, C. et al. Exploiting sparseness in de novo genome assembly. BMC Bioinformatics 13, S1 (2012).

    Google Scholar 

  14. Ye, C., Hill, C., Wu, S., Ruan, J. & Ma, Z. DBG2OLC: efficient assembly of large genomes using long erroneous reads of the third generation sequencing technologies. Sci. Rep. 6, 31900 (2016).

    Google Scholar 

  15. Boetzer, M. et al. SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information. BMC Bioinformatics 15, 211 (2014).

    Google Scholar 

  16. Yoshida, K. et al. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife 2, e00731 (2013).

    Google Scholar 

  17. de Melo, N. F. et al. Cytogenetics and cytotaxonomy of velloziaceae. Plant Syst. Evol. 204, 257–273 (1997).

    Google Scholar 

  18. VanBuren, R. et al. Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum. Nature 527, 508–511 (2015).

    Google Scholar 

  19. Xiao, L. et al. The resurrection genome of Boea hygrometrica: a blueprint for survival of dehydration. Proc. Natl Acad. Sci. USA 112, 5833–5837 (2015).

    Google Scholar 

  20. Yasui, Y. et al. Draft genome sequence of an inbred line of Chenopodium quinoa, an allotetraploid crop with great environmental adaptability and outstanding nutritional properties. DNA Res. 23, 535–546 (2016).

    Google Scholar 

  21. Šmarda, P. et al. Ecological and evolutionary significance of genomic GC content diversity in monocots. Proc. Natl Acad. Sci. USA 111, E4096–E4102 (2014).

    Google Scholar 

  22. Boeckmann, B. et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 31, 365–370 (2003).

    Google Scholar 

  23. Mitchell, A. et al. The InterPro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213–D221 (2015).

    Google Scholar 

  24. Wilson, G. A. et al. Orphans as taxonomically restricted and ecologically important genes. Microbiology 151, 2499–2501 (2005).

    Google Scholar 

  25. Hilbricht, T. et al. Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol. 179, 877–887 (2008).

    Google Scholar 

  26. Cannarozzi, G. et al. Genome and transcriptome sequencing identifies breeding targets in the orphan crop tef (Eragrostis tef). BMC Genomics 15, 581 (2014).

    Google Scholar 

  27. Gaff, D. F. & Oliver, M. J. The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct. Plant Biol. 40, 315–328 (2013).

    Google Scholar 

  28. Mundree, S. G. & Farrant, J. M. in Plant Tolerance to Abiotic Stress in Agriculture: Role of Genetic Engineering (eds Cherry, J. H., Locy, R. D. & Rychter, A. ) 201–222 (Springer, 2000).

    Google Scholar 

  29. Gaff, D. F. & Loveys, B. Abscisic acid levels in drying plants of a resurrection grass. Trans. Malaysian Soc. Plant Physiol. 3, 286–287 (1993).

    Google Scholar 

  30. Farrant, J. M., Cooper, K., Dace, H. J. W., Bentely, J. & Hilgart, A. in Plant Stress Physiology (ed Shabala, S. ) 217–252 (CAB International, 2016).

    Google Scholar 

  31. Bewley, J. D. Physiological aspects of desiccation tolerance. Annu. Rev. Plant Physiol. 30, 195–238 (1979).

    Google Scholar 

  32. Csintalan, Z., Tuba, Z., Lichtenthaler, H. K. & Grace, J. Reconstitution of photosynthesis upon rehydration in the desiccated leaves of the poikilochlorophyllous shrub Xerophyta scabrida at elevated CO2 . J. Plant Physiol. 148, 345–350 (1996).

    Google Scholar 

  33. Tuba, Z., Protor, M. C. F. & Csintalan, Z. Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective. Plant Growth Regul. 24, 211–217 (1998).

    Google Scholar 

  34. Gechev, T. S. et al. Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cell. Mol. Life Sci. 70, 689–709 (2013).

    Google Scholar 

  35. Dinakar, C. & Bartels, D. Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. Front. Plant Sci. 4, 482 (2013).

    Google Scholar 

  36. Rodriguez, M. C. S. et al. Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J. 63, 212–228 (2010).

    Google Scholar 

  37. Costa, M.-C. D. et al. Key genes involved in desiccation tolerance and dormancy across life forms. Plant Sci. 251, 162–168 (2016).

    Google Scholar 

  38. Williams, B. et al. Trehalose accumulation triggers autophagy during plant desiccation. PLoS Genet. 11, 1–17 (2015).

    Google Scholar 

  39. Challabathula, D., Puthur, J. T. & Bartels, D. Surviving metabolic arrest: photosynthesis during desiccation and rehydration in resurrection plants. Ann. NY Acad. Sci. 1365, 89–99 (2015).

    Google Scholar 

  40. Todaka, D., Shinozaki, K. & Yamaguchi-Shinozaki, K. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front. Plant Sci. 6, 84 (2015).

    Google Scholar 

  41. Tunnacliffe, A. & Wise, M. J. The continuing conundrum of the LEA proteins. Naturwissenschaften 94, 791–812 (2007).

    Google Scholar 

  42. Wang, Y. et al. MCScanx: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012).

  43. Tuba, Z., Lichtenthaler, H. K., Maroti, I. & Csintalan, Z. Resynthesis of thylakoids and functional chloroplasts in the desiccated leaves of the poikilochlorophyllous plant Xerophyta scabrida upon rehydration. J. Plant Physiol. 142, 742–748 (1993).

    Google Scholar 

  44. Bajic, J. Exploring the longevity of dry Craterostigma wilmsii (homoiochlorophyllous) and Xerophyta humilis (poikolichlorophyllous) under simulated field conditions. PhD thesis, Univ. Cape Town (2006).

  45. Verdier, J. et al. A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiol. 163, 757–774 (2013).

    Google Scholar 

  46. Zinsmeister, J. et al. ABI5 is a regulator of seed maturation and longevity in legumes. Plant Cell 28, 2735–2754 (2016).

    Google Scholar 

  47. Mönke, G. et al. Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res. 40, 8240–8254 (2012).

    Google Scholar 

  48. Delahaie, J. et al. LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance. J. Exp. Bot. 64, 4559–4573 (2013).

    Google Scholar 

  49. Khandelwal, A. et al. Role of ABA and ABI3 in desiccation tolerance. Science 327, 546 (2010).

    Google Scholar 

  50. Griffiths, C. A. et al. Drying without senescence in resurrection plants. Front. Plant Sci. 5 (2014).

  51. Li, Z., Peng, J., Wen, X. & Guo, H. Gene network analysis and functional studies of senescence-associated genes reveal novel regulators of Arabidopsis leaf senescence. J. Integr. Plant Biol. 54, 526–539 (2012).

    Google Scholar 

  52. Reis, P. A. A. et al. The binding protein BiP attenuates stress-induced cell death in soybean via modulation of the N-rich protein-mediated signaling pathway. Plant Physiol. 157, 1853–1865 (2011).

    Google Scholar 

  53. Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).

    Google Scholar 

  54. English, A. C. et al. Mind the gap: upgrading genomes with pacific biosciences RS long-read sequencing technology. PLoS ONE 7, e47768 (2012).

    Google Scholar 

  55. Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).

    Google Scholar 

  56. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Google Scholar 

  57. Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).

    Google Scholar 

  58. Stanke, M. & Morgenstern, B. AUGUSTUS: A web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33, 465–467 (2005).

    Google Scholar 

  59. Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).

    Google Scholar 

  60. Hoff, K. J., Lange, S., Lomsadze, A., Borodovsky, M. & Stanke, M. BRAKER1: unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics 32, 767–769 (2016).

    Google Scholar 

  61. Harris, M. A. et al. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32, D258–D2261 (2004).

    Google Scholar 

  62. Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).

    Google Scholar 

  63. Smit, A. F. A., Hubley, R. & Green, P. RepeatMasker Open-3.0 (RepeatMasker, 2008); http://www.repeatmasker.org

  64. Lowe, T. M. & Eddy, S. R. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964 (1997).

    Google Scholar 

  65. Nawrocki, E. P. & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935 (2013).

    Google Scholar 

  66. Nawrocki, E. P. et al. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res. 43, D130–D137 (2015).

    Google Scholar 

  67. Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at https://arxiv.org/abs/1207.3907# (2012).

  68. Emms, D. M. & Kelly, S. Orthofinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).

    Google Scholar 

  69. Csuos, M. Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 26, 1910–1912 (2010).

    Google Scholar 

  70. Szinay, D. et al. High-resolution chromosome mapping of BACs using multi-colour FISH and pooled-BAC FISH as a backbone for sequencing tomato chromosome 6. Plant J. 56, 627–637 (2008).

    Google Scholar 

  71. Wan, C.-Y. & Wilkins, T. A. A modified hot borate method significantly enhances the yield of high quality RNA from cotton (Gossypium hirsutum L.). Anal. Biochem. 223, 7–12 (1994).

    Google Scholar 

  72. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).

    Google Scholar 

  73. Oliver, M. J. et al. A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23, 1231–1248 (2011).

    Google Scholar 

  74. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).

    Google Scholar 

  75. Finn, R. D. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279–D285 (2015).

    Google Scholar 

  76. Finn, R. D., Clements, J. & Eddy, S. R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39, W29–W37 (2011).

    Google Scholar 

  77. Freeman, T. C. et al. Construction, visualisation, and clustering of transcription networks from microarray expression data. PLoS Comput. Biol. 3, 2032–2042 (2007).

    Google Scholar 

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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 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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