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Cellular and Molecular Life Sciences

, Volume 69, Issue 19, pp 3175–3186 | Cite as

Molecular mechanisms of desiccation tolerance in resurrection plants

  • Tsanko S. Gechev
  • Challabathula Dinakar
  • Maria Benina
  • Valentina Toneva
  • Dorothea Bartels
Multi-author review

Abstract

Resurrection plants are a small but diverse group of land plants characterized by their tolerance to extreme drought or desiccation. They have the unique ability to survive months to years without water, lose most of the free water in their vegetative tissues, fall into anabiosis, and, upon rewatering, quickly regain normal activity. Thus, they are fundamentally different from other drought-surviving plants such as succulents or ephemerals, which cope with drought by maintaining higher steady state water potential or via a short life cycle, respectively. This review describes the unique physiological and molecular adaptations of resurrection plants enabling them to withstand long periods of desiccation. The recent transcriptome analysis of Craterostigma plantagineum and Haberlea rhodopensis under drought, desiccation, and subsequent rehydration revealed common genetic pathways with other desiccation-tolerant species as well as unique genes that might contribute to the outstanding desiccation tolerance of the two resurrection species. While some of the molecular responses appear to be common for both drought stress and desiccation, resurrection plants also possess genes that are highly induced or repressed during desiccation with no apparent sequence homologies to genes of other species. Thus, resurrection plants are potential sources for gene discovery. Further proteome and metabolome analyses of the resurrection plants contributed to a better understanding of molecular mechanisms that are involved in surviving severe water loss. Understanding the cellular mechanisms of desiccation tolerance in this unique group of plants may enable future molecular improvement of drought tolerance in crop plants.

Keywords

Drought stress Craterostigma plantagineum Haberlea rhodopensis Next generation sequencing Proteome Metabolome analysis 

Abbreviations

ABA

Abscisic acid

ELIP

Early light-inducible proteins

GABA

γ-Aminobutyric acid

LEA

Late embryogenesis abundant genes/proteins

RFOs

Raffinose family oligosaccharides

ROS

Reactive oxygen species

RWC

Relative water content

Notes

Acknowledgments

D.B. is a member of the COST action FA090 “Putting halophytes to work”. M.B., V.T., and T.G. acknowledge EC FP7 (project BioSupport, 245588).

References

  1. 1.
    Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  2. 2.
    Farrant J, Brandt W, Lidsey GG (2007) An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 1:72–84Google Scholar
  3. 3.
    Bartels D, Souer E (2003) Molecular responses of higher plants to dehydration. In: Hirt H, Shinozaki K (eds) Plant responses to abiotic stress. Springer, Berlin, pp 9–38CrossRefGoogle Scholar
  4. 4.
    Harb A, Krishnan A, Ambavaram MM, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271PubMedCrossRefGoogle Scholar
  5. 5.
    Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al Rasheid KA, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107:8023–8028PubMedCrossRefGoogle Scholar
  6. 6.
    Peters C, Li M, Narasimhan R, Roth M, Welti R, Wang X (2010) Nonspecific phospholipase C NPC4 promotes responses to abscisic acid and tolerance to hyperosmotic stress in Arabidopsis. Plant Cell 22:2642–2659PubMedCrossRefGoogle Scholar
  7. 7.
    Li M, Li Y, Li H, Wu G (2011) Overexpression of AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. Tree Physiol 31:349–357PubMedCrossRefGoogle Scholar
  8. 8.
    Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817PubMedCrossRefGoogle Scholar
  9. 9.
    Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430PubMedCrossRefGoogle Scholar
  10. 10.
    Olvera-Carrillo Y, Campos F, Reyes JL, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiol 154:373–390PubMedCrossRefGoogle Scholar
  11. 11.
    Martinelli T (2008) In situ localization of glucose and sucrose in dehydrating leaves of Sporobolus stapfianus. J Plant Physiol 165:580–587PubMedCrossRefGoogle Scholar
  12. 12.
    Farrant JM, Moore JP (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14:340–345PubMedCrossRefGoogle Scholar
  13. 13.
    Almeida-Rodriguez AM, Cooke JE, Yeh F, Zwiazek JJ (2010) Functional characterization of drought-responsive aquaporins in Populus balsamifera and Populus simonii X balsamifera clones with different drought resistance strategies. Physiol Plant 140:321–333PubMedCrossRefGoogle Scholar
  14. 14.
    Rae L, Lao NT, Kavanagh TA (2011) Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta 234:429–444PubMedCrossRefGoogle Scholar
  15. 15.
    Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24PubMedCrossRefGoogle Scholar
  16. 16.
    Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Hofer R, Schreiber L, Chory J, Aharoni A (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145:1345–1360PubMedCrossRefGoogle Scholar
  17. 17.
    Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, van de CB, De C, I, Chiwocha S, Fenske R, Prinsen E, Boerjan W, Genty B, Stubbs KA, Inzé D, Van Breusegem F (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell 22:2660-2679Google Scholar
  18. 18.
    Wang L, Shang H, Liu Y, Zheng M, Wu R, Phillips J, Bartels D, Deng X (2009) A role for a cell wall localized glycine-rich protein in dehydration and rehydration of the resurrection plant Boea hygrometrica. Plant Biol 11:837–848PubMedCrossRefGoogle Scholar
  19. 19.
    Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BW, Cushman JC (2011) A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23:1231–1248PubMedCrossRefGoogle Scholar
  20. 20.
    Alamillo J, Almoguera C, Bartels D, Jordano J (1995) Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol Biol 29:1093–1099PubMedCrossRefGoogle Scholar
  21. 21.
    Porembski S (2011) Evolution, diversity and habitats of poikilohydrous plants. In: Luttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Springer, Berlin, pp 139–156CrossRefGoogle Scholar
  22. 22.
    Martinelli T, Whittaker A, Masclaux-Daubresse C, Farrant JM, Brilli F, Loreto F, Vazzana C (2007) Evidence for the presence of photorespiration in desiccation-sensitive leaves of the C4 ‘resurrection’ plant Sporobolus stapfianus during dehydration stress. J Exp Bot 58:3929–3939PubMedCrossRefGoogle Scholar
  23. 23.
    Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation-tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci 182:29–41PubMedCrossRefGoogle Scholar
  24. 24.
    Phillips JR, Fischer E, Baron M, van den DN, Facchinelli F, Kutzer M, Rahmanzadeh R, Remus D, Bartels D (2008) Lindernia brevidens: a novel desiccation-tolerant vascular plant, endemic to ancient tropical rainforests. Plant J 54:938–948PubMedCrossRefGoogle Scholar
  25. 25.
    Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Compar Biol 45:696–701CrossRefGoogle Scholar
  26. 26.
    Moore JP, Lindsey GG, Farrant JM, Brandt WF (2007) An overview of the biology of the desiccation-tolerant resurrection plant Myrothamnus flabellifolia. Ann Bot 99:211–217PubMedCrossRefGoogle Scholar
  27. 27.
    Lohr G, Beikler T, Podbielski A, Standar K, Redanz S, Hensel A (2011) Polyphenols from Myrothamnus flabellifolia Welw. inhibit in vitro adhesion of Porphyromonas gingivalis and exert anti-inflammatory cytoprotective effects in KB cells. J Clin Periodontol 38:457–469PubMedCrossRefGoogle Scholar
  28. 28.
    Kamng’ona A, Moore JP, Lindsey G, Brandt W (2011) Inhibition of HIV-1 and M-MLV reverse transcriptases by a major polyphenol (3,4,5-tri-O-galloylquinic acid) present in the leaves of the South African resurrection plant, Myrothamnus flabellifolia. J Enzyme Inhib Med Chem 26:843–853PubMedCrossRefGoogle Scholar
  29. 29.
    Dell’Acqua G, Schweikert K (2011) Skin benefits of a myconoside-rich extract from resurrection plant Haberlea rhodopensis. Int J Cosm Sci 34:132–139CrossRefGoogle Scholar
  30. 30.
    Popov B, Georgieva S, Gadjeva V, Petrov V (2011) Radioprotective, anticlastogenic and antioxidant effects of total extract of Haberlea rhodopensis on rabbit blood samples exposed to gamma radiation in vitro. Revue Med Vet 1:34–39Google Scholar
  31. 31.
    Kirch HH, Nair A, Bartels D (2001) Novel ABA- and dehydration-inducible aldehyde dehydrogenase genes isolated from the resurrection plant Craterostigma plantagineum and Arabidopsis thaliana. Plant J 28:555–567PubMedCrossRefGoogle Scholar
  32. 32.
    Deng X, Phillips J, Brautigam A, Engstrom P, Johannesson H, Ouwerkerk PB, Ruberti I, Salinas J, Vera P, Iannacone R, Meijer AH, Bartels D (2006) A homeodomain leucine zipper gene from Craterostigma plantagineum regulates abscisic acid responsive gene expression and physiological responses. Plant Mol Biol 61:469–489PubMedCrossRefGoogle Scholar
  33. 33.
    Wu H, Shen Y, Hu Y, Tan S, Lin Z (2011) A phytocyanin-related early nodulin-like gene, BcBCP1, cloned from Boea crassifolia enhances osmotic tolerance in transgenic tobacco. J Plant Physiol 168:935–943PubMedCrossRefGoogle Scholar
  34. 34.
    Hilbricht T, Salamini F, Bartels D (2002) CpR18, a novel SAP-domain plant transcription factor, binds to a promoter region necessary for ABA mediated expression of the CDeT27-45 gene from the resurrection plant Craterostigma plantagineum Hochst. Plant J 31:293–303PubMedCrossRefGoogle Scholar
  35. 35.
    Bartels D, Hussain SS (2011) Resurrection plants: physiology and molecular biology. In: Luttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Springer, Berlin, pp 339–364CrossRefGoogle Scholar
  36. 36.
    Ingle RA, Collett H, Cooper K, Takahashi Y, Farrant JM, Illing N (2008) Chloroplast biogenesis during rehydration of the resurrection plant Xerophyta humilis: parallels to the etioplast-chloroplast transition. Plant Cell Environ 31:1813–1824PubMedCrossRefGoogle Scholar
  37. 37.
    Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326PubMedCrossRefGoogle Scholar
  38. 38.
    Alamillo JM, Bartels D (2001) Effects of desiccation on photosynthesis pigments and the ELIP-like dsp 22 protein complexes in the resurrection plant Craterostigma plantagineum. Plant Sci 160:1161–1170PubMedCrossRefGoogle Scholar
  39. 39.
    Bartels D, Hanke C, Schneider K, Michel D, Salamini F (1992) A desiccation-related Elip- like gene from the resurrection plant Craterostigma plantagineum is regulated by light and ABA. EMBO J 11:2771–2778PubMedGoogle Scholar
  40. 40.
    Jones L, McQueen-Mason S (2004) A role for expansins in dehydration and rehydration of the resurrection plant Craterostigma plantagineum. FEBS Lett 559:61–65PubMedCrossRefGoogle Scholar
  41. 41.
    Vicre M, Lerouxel O, Farrant J, Lerouge P, Driouich A (2004) Composition and desiccation-induced alterations of the cell wall in the resurrection plant Craterostigma wilmsii. Physiol Plant 120:229–239PubMedCrossRefGoogle Scholar
  42. 42.
    Moore JP, Farrant JM, Driouich A (2008) A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal Behav 3:102–104PubMedCrossRefGoogle Scholar
  43. 43.
    Moore JP, Nguema-Ona E, Chevalier L, Lindsey GG, Brandt W, Lerouge P, Farrant J, Driouich A (2006) Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus flabellifolius. Plant Physiol 141:651–662PubMedCrossRefGoogle Scholar
  44. 44.
    Norwood M, Truesdale MR, Richter A, Scott P (2000) Photosynthetic carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. J Exp Bot 51:159–165PubMedCrossRefGoogle Scholar
  45. 45.
    Norwood M, Toldi O, Richter A, Scott P (2003) Investigation into the ability of roots of the poikilohydric plant Craterostigma plantagineum to survive dehydration stress. J Exp Bot 54:2313–2321PubMedCrossRefGoogle Scholar
  46. 46.
    Drennan PM, Smith MT, Goldsworthy D, van Staden J (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. J Plant Physiol 142:493–496CrossRefGoogle Scholar
  47. 47.
    Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403PubMedCrossRefGoogle Scholar
  48. 48.
    Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599PubMedCrossRefGoogle Scholar
  49. 49.
    Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279PubMedCrossRefGoogle Scholar
  50. 50.
    Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6849–6854PubMedCrossRefGoogle Scholar
  51. 51.
    Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263PubMedCrossRefGoogle Scholar
  52. 52.
    Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24PubMedCrossRefGoogle Scholar
  53. 53.
    Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118PubMedCrossRefGoogle Scholar
  54. 54.
    Rodriguez MC, Edsgard D, Hussain SS, Alquezar D, Rasmussen M, Gilbert T, Nielsen BH, Bartels D, Mundy J (2010) Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J 63:212–228PubMedCrossRefGoogle Scholar
  55. 55.
    Saavedra L, Svensson J, Carballo V, Izmendi D, Welin B, Vidal S (2006) A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J 45:237–249PubMedCrossRefGoogle Scholar
  56. 56.
    Rodrigo MJ, Bockel C, Blervacq AS, Bartels D (2004) The novel gene CpEdi-9 from the resurrection plant C. plantagineum encodes a hydrophilic protein and is expressed in mature seeds as well as in response to dehydration in leaf phloem tissues. Planta 219:579–589PubMedCrossRefGoogle Scholar
  57. 57.
    Mowla SB, Thomson JA, Farrant JM, Mundree SG (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 215:716–726PubMedCrossRefGoogle Scholar
  58. 58.
    Phillips JR, Hilbricht T, Salamini F, Bartels D (2002) A novel abscisic acid- and dehydration-responsive gene family from the resurrection plant Craterostigma plantagineum encodes a plastid-targeted protein with DNA-binding activity. Planta 215:258–266PubMedCrossRefGoogle Scholar
  59. 59.
    Zhu Y, Wang Z, Jing Y, Wang L, Liu X, Liu Y, Deng X (2009) Ectopic over-expression of BhHsf1, a heat shock factor from the resurrection plant Boea hygrometrica, leads to increased thermotolerance and retarded growth in transgenic Arabidopsis and tobacco. Plant Mol Biol 71:451–467PubMedCrossRefGoogle Scholar
  60. 60.
    Wang Z, Zhu Y, Wang L, Liu X, Liu Y, Phillips J, Deng X (2009) A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230:1155–1166PubMedCrossRefGoogle Scholar
  61. 61.
    Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12:111–124PubMedGoogle Scholar
  62. 62.
    Villalobos MA, Bartels D, Iturriaga G (2004) Stress tolerance and glucose insensitive phenotypes in Arabidopsis overexpressing the CpMYB10 transcription factor gene. Plant Physiol 135:309–324PubMedCrossRefGoogle Scholar
  63. 63.
    Furini A, Koncz C, Salamini F, Bartels D (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO J 16:3599–3608PubMedCrossRefGoogle Scholar
  64. 64.
    Smith-Espinoza CJ, Phillips JR, Salamini F, Bartels D (2005) Identification of further Craterostigma plantagineum cdt mutants affected in abscisic acid mediated desiccation tolerance. Mol Genet Genomics 274:364–372PubMedCrossRefGoogle Scholar
  65. 65.
    Mulako I, Farrant JM, Collett H, Illing N (2008) Expression of Xhdsi-1VOC, a novel member of the vicinal oxygen chelate (VOC) metalloenzyme superfamily, is upregulated in leaves and roots during desiccation in the resurrection plant Xerophyta humilis (Bak) Dur and Schinz. J Exp Bot 59:3885–3901PubMedCrossRefGoogle Scholar
  66. 66.
    Garwe D, Thomson JA, Mundree SG (2006) XVSAP1 from Xerophyta viscosa improves osmotic-, salinity- and high-temperature-stress tolerance in Arabidopsis. Biotechnol J 1:1137–1146PubMedCrossRefGoogle Scholar
  67. 67.
    Garwe D, Thomson JA, Mundree SG (2003) Molecular characterization of XVSAP1, a stress-responsive gene from the resurrection plant Xerophyta viscosa Baker. J Exp Bot 54:191–201PubMedCrossRefGoogle Scholar
  68. 68.
    Zeng Q, Chen X, Wood AJ (2002) Two early light-inducible protein (ELIP) cDNAs from the resurrection plant Tortula ruralis are differentially expressed in response to desiccation, rehydration, salinity, and high light. J Exp Bot 53:1197–1205PubMedCrossRefGoogle Scholar
  69. 69.
    Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100:4921–4926PubMedCrossRefGoogle Scholar
  70. 70.
    Röhrig H, Colby T, Schmidt J, Harzen A, Facchinelli F, Bartels D (2008) Analysis of desiccation-induced candidate phosphoproteins from Craterostigma plantagineum isolated with a modified metal oxide affinity chromatography procedure. Proteomics 8:3548–3560PubMedCrossRefGoogle Scholar
  71. 71.
    Georgieva T, Christov N, Djilianov D (2012) Identification of desiccationregulated genes by cDNA-AFLP in Haberlea rhodopensis: a resurrection plant. Acta Physiol Plant 34:1055–1066CrossRefGoogle Scholar
  72. 72.
    Jiang G, Wang Z, Shang H, Yang W, Hu Z, Phillips J, Deng X (2007) Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225:1405–1420PubMedCrossRefGoogle Scholar
  73. 73.
    Ingle RA, Schmidt UG, Farrant JM, Thomson JA, Mundree SG (2007) Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa. Plant Cell Environ 30:435–446PubMedCrossRefGoogle Scholar
  74. 74.
    Oliver MJ, Jain R, Balbuena TS, Agrawal G, Gasulla F, Thelen JJ (2011) Proteome analysis of leaves of the desiccation-tolerant grass, Sporobolus stapfianus, in response to dehydration. Phytochemistry 72:1273–1284PubMedCrossRefGoogle Scholar
  75. 75.
    Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L, Xie Y, Wang T, Yan X, Dai S (2010) Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res 9:6561–6577PubMedCrossRefGoogle Scholar
  76. 76.
    Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J Exp Bot 58:1947–1956PubMedCrossRefGoogle Scholar
  77. 77.
    Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D (1992) Low molecular weight solutes in desiccated and ABA-treated calli and leaves of Craterostigma plantagineum. Phytochemistry 31:1917–1922CrossRefGoogle Scholar
  78. 78.
    Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F, Bartels D (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87:223–226CrossRefGoogle Scholar
  79. 79.
    Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D (1991) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J 1:355–359CrossRefGoogle Scholar
  80. 80.
    Alcazar R, Bitrian M, Bartels D, Koncz C, Altabella T, Tiburcio AF (2011) Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum. Plant Signal Behav 6:243–250PubMedCrossRefGoogle Scholar
  81. 81.
    Renault H, Roussel V, El AA, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol 10:20PubMedCrossRefGoogle Scholar
  82. 82.
    Renault H, El AA, Palanivelu R, Updegraff EP, Yu A, Renou JP, Preuss D, Bouchereau A, Deleu C (2011) GABA accumulation causes cell elongation defects and a decrease in expression of genes encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant Cell Physiol 52:894–908PubMedCrossRefGoogle Scholar
  83. 83.
    Gaff DF, McGregor GR (1979) The effect of dehydration and rehydration in the nitrogen content of various fractions from resurrection plants. Biol Plant 21:92–99CrossRefGoogle Scholar
  84. 84.
    Tymms MJ, Gaff DF (1978) Proline accumulation during water stress in resurrection plants. J Exp Bot 30:165–168CrossRefGoogle Scholar
  85. 85.
    Moore JP, Westall KL, Ravenscroft N, Farrant J, Lindsey GG, Brandt W (2005) The predominant polyphenol in the leaves of the resurrection plant Myrothamnus flabellifolius, 3,4,5-tri-O-galloylquinic acid, protects membranes against desiccation and free radical-induced oxidation. Biochem J 385:301–308PubMedCrossRefGoogle Scholar
  86. 86.
    Djilianov D, Ivanov S, Moyankova D, Miteva L, Kirova E, Alexieva V, Joudi M, Peshev D, Van den Ende W (2011) Sugar ratios, glutathione redox status and phenols in the resurrection species Haberlea rhodopensis and the closely related non-resurrection species Chirita eberhardtii. Plant Biol 13:767–776PubMedCrossRefGoogle Scholar
  87. 87.
    Hilbricht T, Varotto S, Sgaramella V, Bartels D, Salamini F, Furini A (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol 179:877–887PubMedCrossRefGoogle Scholar
  88. 88.
    Liu X, Wang Z, Wang L, Wu R, Phillips J, Deng X (2009) LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Sci 176:90–98CrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2012

Authors and Affiliations

  • Tsanko S. Gechev
    • 1
    • 2
  • Challabathula Dinakar
    • 3
  • Maria Benina
    • 1
    • 2
  • Valentina Toneva
    • 1
    • 2
  • Dorothea Bartels
    • 3
  1. 1.Department of Plant Physiology and Plant Molecular BiologyUniversity of PlovdivPlovdivBulgaria
  2. 2.Genomics Research CenterPlovdivBulgaria
  3. 3.Institute of Molecular Physiology and Biotechnology of PlantsUniversity of BonnBonnGermany

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