University of Groningen Molecular mechanisms of desiccation tolerance in the resurrection glacial relic

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 droughtinduced 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 c-aminobutyric acid during drought, as well Electronic supplementary material The online version of this article (doi:10.1007/s00018-012-1155-6) contains supplementary material, which is available to authorized users. T. S. Gechev and M. Benina contributed equally to this work. T. S. Gechev (&) M. Benina N. Sujeeth I. Minkov V. Toneva Department of Plant Physiology and Plant Molecular Biology, University of Plovdiv, 24 Tsar Assen Str. , Plovdiv 4000, Bulgaria e-mail: tsangech@uni-plovdiv.bg T. Obata T. Tohge C. Antonio B. Mueller-Roeber J. H. M. Schippers A. R. Fernie Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany N. Sujeeth J. Hille Molecular Biology of Plants, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Groningen, The Netherlands M. -R. Temanni ServiceXS B.V. , Plesmanlaan 1d, 2333 BZ Leiden, The Netherlands A. S. Marriott E. Bergström J. Thomas-Oates Department of Chemistry, University of York, Heslington, York YO10 5DD, UK B. Mueller-Roeber J. H. M. Schippers Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Haus 20, 14476 Potsdam-Golm, Germany T. S. Gechev M. Benina I. Minkov V. Toneva Genomics Research Center, Ruski Blvd. 105, Plovdiv 4000, Bulgaria Cell. Mol. Life Sci. (2013) 70:689–709 DOI 10.1007/s00018-012-1155-6 Cellular and Molecular Life Sciences