title: 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.
authors.affiliation: Department of Plant Physiology and Plant Molecular Biology, University of Plovdiv, 24 Tsar Assen Str., Plovdiv, 4000, Bulgaria. tsangech@uni-plovdiv.bg
authors.forename: Tsanko S
authors.initials: TS
authors.lastname: Gechev
authors.forename: Maria
authors.initials: M
authors.lastname: Benina
authors.forename: Toshihiro
authors.initials: T
authors.lastname: Obata
authors.forename: Takayuki
authors.initials: T
authors.lastname: Tohge
authors.forename: Neerakkal
authors.initials: N
authors.lastname: Sujeeth
authors.forename: Ivan
authors.initials: I
authors.lastname: Minkov
authors.forename: Jacques
authors.initials: J
authors.lastname: Hille
authors.forename: Mohamed-Ramzi
authors.initials: MR
authors.lastname: Temanni
authors.forename: Andrew S
authors.initials: AS
authors.lastname: Marriott
authors.forename: Ed
authors.initials: E
authors.lastname: Bergström
authors.forename: Jane
authors.initials: J
authors.lastname: Thomas-Oates
authors.forename: Carla
authors.initials: C
authors.lastname: Antonio
authors.forename: Bernd
authors.initials: B
authors.lastname: Mueller-Roeber
authors.forename: Jos H M
authors.initials: JH
authors.lastname: Schippers
authors.forename: Alisdair R
authors.initials: AR
authors.lastname: Fernie
authors.forename: Valentina
authors.initials: V
authors.lastname: Toneva
mesh_terms: D000064:Acclimatization; D002374:Catalase / Q000235:genetics; D032181:Craterostigma / Q000235:genetics / Q000502:physiology*; D003890:Desiccation; D055864:Droughts; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D055442:Metabolome; D018384:Oxidative Stress; D010940:Plant Proteins / Q000235:genetics*; D014867:Water / Q000378:metabolism
chemical_list: D010940:Plant Proteins; D014867:Water; D002374:Catalase