Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis

Tsanko S. Gechev, Maria Benina, Toshihiro Obata, Takayuki Tohge, Neerakkal Sujeeth, Ivan Minkov, Jacques Hille, Ramzi Temanni, Andrew S. Marriott, Ed Bergström, Jane Thomas-Oates, Carla Antonio, Bernd Mueller-Roeber, Jos H M Schippers, Alisdair R. Fernie, Valentina Toneva

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

Haberlea rhodopensis is a resurrection plant with remarkable tolerance to desiccation. Haberlea exposed to drought stress, desiccation, and subsequent rehydration showed no signs of damage or severe oxidative stress compared to untreated control plants. Transcriptome analysis by next-generation sequencing revealed a drought-induced reprogramming, which redirected resources from growth towards cell protection. Repression of photosynthetic and growth-related genes during water deficiency was concomitant with induction of transcription factors (members of the NAC, NF-YA, MADS box, HSF, GRAS, and WRKY families) presumably acting as master switches of the genetic reprogramming, as well as with an upregulation of genes related to sugar metabolism, signaling, and genes encoding early light-inducible (ELIP), late embryogenesis abundant (LEA), and heat shock (HSP) proteins. At the same time, genes encoding other LEA, HSP, and stress protective proteins were constitutively expressed at high levels even in unstressed controls. Genes normally involved in tolerance to salinity, chilling, and pathogens were also highly induced, suggesting a possible cross-tolerance against a number of abiotic and biotic stress factors. A notable percentage of the genes highly regulated in dehydration and subsequent rehydration were novel, with no sequence homology to genes from other plant genomes. Additionally, an extensive antioxidant gene network was identified with several gene families possessing a greater number of antioxidant genes than most other species with sequenced genomes. Two of the transcripts most abundant during all conditions encoded catalases and five more catalases were induced in water-deficient samples. Using the pharmacological inhibitor 3-aminotriazole (AT) to compromise catalase activity resulted in increased sensitivity to desiccation. Metabolome analysis by GC or LC-MS revealed accumulation of sucrose, verbascose, spermidine, and γ-aminobutyric acid during drought, as well as particular secondary metabolites accumulating during rehydration. This observation, together with the complex antioxidant system and the constitutive expression of stress protective genes suggests that both constitutive and inducible mechanisms contribute to the extreme desiccation tolerance of H. rhodopensis.

Original languageEnglish
Pages (from-to)689-709
Number of pages21
JournalCellular and Molecular Life Sciences
Volume70
Issue number4
DOIs
Publication statusPublished - Feb 2013
Externally publishedYes

Fingerprint

Desiccation
Genes
Fluid Therapy
Droughts
Catalase
Antioxidants
Heat-Shock Proteins
Embryonic Development
Craterostigma
Amitrole
Aminobutyrates
Plant Genome
Spermidine
Cytoprotection
Metabolome
Water
Gene Regulatory Networks
Salinity
Gene Expression Profiling
Growth

Keywords

  • Antioxidant genes
  • Catalase
  • Desiccation tolerance
  • Drought stress
  • Metabolome analysis
  • Resurrection plants

ASJC Scopus subject areas

  • Cell Biology
  • Molecular Biology
  • Molecular Medicine
  • Pharmacology
  • Cellular and Molecular Neuroscience

Cite this

Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. / Gechev, Tsanko S.; Benina, Maria; Obata, Toshihiro; Tohge, Takayuki; Sujeeth, Neerakkal; Minkov, Ivan; Hille, Jacques; Temanni, Ramzi; Marriott, Andrew S.; Bergström, Ed; Thomas-Oates, Jane; Antonio, Carla; Mueller-Roeber, Bernd; Schippers, Jos H M; Fernie, Alisdair R.; Toneva, Valentina.

In: Cellular and Molecular Life Sciences, Vol. 70, No. 4, 02.2013, p. 689-709.

Research output: Contribution to journalArticle

Gechev, TS, Benina, M, Obata, T, Tohge, T, Sujeeth, N, Minkov, I, Hille, J, Temanni, R, Marriott, AS, Bergström, E, Thomas-Oates, J, Antonio, C, Mueller-Roeber, B, Schippers, JHM, Fernie, AR & Toneva, V 2013, 'Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis', Cellular and Molecular Life Sciences, vol. 70, no. 4, pp. 689-709. https://doi.org/10.1007/s00018-012-1155-6
Gechev, Tsanko S. ; Benina, Maria ; Obata, Toshihiro ; Tohge, Takayuki ; Sujeeth, Neerakkal ; Minkov, Ivan ; Hille, Jacques ; Temanni, Ramzi ; Marriott, Andrew S. ; Bergström, Ed ; Thomas-Oates, Jane ; Antonio, Carla ; Mueller-Roeber, Bernd ; Schippers, Jos H M ; Fernie, Alisdair R. ; Toneva, Valentina. / Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. In: Cellular and Molecular Life Sciences. 2013 ; Vol. 70, No. 4. pp. 689-709.
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