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

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.

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Abbreviations

AT:

3-Aminotriazole

ELIP:

Early light-inducible genes/proteins

GABA:

γ-Aminobutyric acid

HSP:

Heat shock genes/proteins

LEA:

Late embryogenesis abundant genes/proteins

NGS:

Next-generation sequencing

RFO:

Raffinose family oligosaccharides

ROS:

Reactive oxygen species

RWC:

Relative water content

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Acknowledgments

The authors are grateful to N. Mehterov and V. Baev for technical support. This work was financially supported by National Science Fund of Bulgaria (grant DO02-071) and EC FP7 (project BioSupport, 245588); ASM gratefully acknowledges studentship support from the UK BBSRC. Author contributions are as follows: TG designed the research; TG, MB, TO, TT, SN, IM, RT, AM, EB, JTO, CA, JS, BMR, ARF, and VT performed the research and/or analyzed the data; TG, TO, JH, BMR, and ARF wrote the paper.

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Correspondence to Tsanko S. Gechev.

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T. S. Gechev and M. Benina contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

18_2012_1155_MOESM1_ESM.xlsx

Supplementary material 1 (XLSX 25301 kb) Supplemental Table 1 List of all expressed sequence contigs (ESC) and their sequences as obtained by NGS and the expression of all ESC in unstressed controls, drought-stressed, desiccated, and rehydrated plants

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Supplementary material 2 (XLS 50 kb) Supplemental Table 2 QRT-PCR verification of the expression pattern of selected genes chosen from the NGS analysis

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Supplementary material 3 (XLSX 11 kb) Supplemental Table 3 Expression patterns of the 25 most abundant H. rhodopensis transcripts under normal conditions, drought stress, desiccation, and rehydration

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Supplementary material 4 (XLSX 51 kb) Supplemental Table 4 Genes highly regulated by drought, desiccation, and rehydration

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Supplementary material 5 (XLS 75 kb) Supplemental Table 5 Expression pattern of Haberlea rhodopensis antioxidant genes under normal conditions, drought stress, desiccation, and rehydration

18_2012_1155_MOESM6_ESM.xls

Supplementary material 6 (XLS 124 kb) Supplemental Table 6 Metabolites in Haberlea rhodopensis during water deficiency and subsequent rehydration

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Supplementary material 7 (PDF 15 kb) Supplemental Fig. 1 Cluster analysis of the four growth conditions based on the next-generation sequence (NGS) transcriptome data. T1, unstressed controls; T2, drought stress; T3, desiccation; T4, rehydration. The intensity of the color corresponds to similarity in gene expression. Unstressed controls cluster with rehydrated plants (T1 and T4) while drought-stressed and desiccated plants cluster together (T2 and T3)

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Supplementary material 8 (PDF 75 kb) Supplemental Fig. 2 Principal component analysis (PCA) of the abundance of Haberlea rhodopensis metabolites identified in the four growth conditions. Red, well-watered controls; green, mild drought stress; light blue, severe desiccation; dark blue, rehydration. Unstressed controls group with rehydrated plants while drought-stressed and desiccated plants group together

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Supplementary material 9 (TIFF 16469 kb) Supplemental Fig. 3 Heat map of 72 secondary metabolites identified in Haberlea rhodopensis grown under optimal condition (unstressed control), drought stress, desiccation, and rehydration. The data are normalized by dry weight. Blue and red colors indicate decrease and increase in metabolite abundances, respectively. Data are means from six biological replicates

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Gechev, T.S., Benina, M., Obata, T. et al. Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis . Cell. Mol. Life Sci. 70, 689–709 (2013). https://doi.org/10.1007/s00018-012-1155-6

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Keywords

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