Molecular mechanisms of desiccation tolerance in resurrection plants

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273 Farrant J, Brandt W, Lidsey GG (2007) An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 1:72–84 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 9–38 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 154:1254–1271 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 107:8023–8028 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 22:2642–2659 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 31:349–357 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 23:1805–1817 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 106:21425–21430 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 154:373–390 Martinelli T (2008) In situ localization of glucose and sucrose in dehydrating leaves of Sporobolus stapfianus. J Plant Physiol 165:580–587 Farrant JM, Moore JP (2011) Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr Opin Plant Biol 14:340–345 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 140:321–333 Rae L, Lao NT, Kavanagh TA (2011) Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta 234:429–444 Kranner I, Beckett RP, Wornik S, Zorn M, Pfeifhofer HW (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24 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 145:1345–1360 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 22:2660-2679 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 11:837–848 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 23:1231–1248 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 29:1093–1099 Porembski S (2011) Evolution, diversity and habitats of poikilohydrous plants. In: Luttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Springer, Berlin, pp 139–156 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 58:3929–3939 Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation-tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci 182:29–41 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 54:938–948 Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Compar Biol 45:696–701 Moore JP, Lindsey GG, Farrant JM, Brandt WF (2007) An overview of the biology of the desiccation-tolerant resurrection plant Myrothamnus flabellifolia. Ann Bot 99:211–217 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 38:457–469 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 26:843–853 Dell’Acqua G, Schweikert K (2011) Skin benefits of a myconoside-rich extract from resurrection plant Haberlea rhodopensis. Int J Cosm Sci 34:132–139 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 1:34–39 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 28:555–567 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 61:469–489 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 168:935–943 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 31:293–303 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 339–364 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 31:1813–1824 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 1797:1313–1326 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 160:1161–1170 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 11:2771–2778 Jones L, McQueen-Mason S (2004) A role for expansins in dehydration and rehydration of the resurrection plant Craterostigma plantagineum. FEBS Lett 559:61–65 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 120:229–239 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 3:102–104 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 141:651–662 Norwood M, Truesdale MR, Richter A, Scott P (2000) Photosynthetic carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. J Exp Bot 51:159–165 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 54:2313–2321 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 142:493–496 Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403 Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599 Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279 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 100:6849–6854 Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263 Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24 Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118 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 63:212–228 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 45:237–249 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 219:579–589 Mowla SB, Thomson JA, Farrant JM, Mundree SG (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 215:716–726 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 215:258–266 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 71:451–467 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 230:1155–1166 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 12:111–124 Villalobos MA, Bartels D, Iturriaga G (2004) Stress tolerance and glucose insensitive phenotypes in Arabidopsis overexpressing the CpMYB10 transcription factor gene. Plant Physiol 135:309–324 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 16:3599–3608 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 274:364–372 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 59:3885–3901 Garwe D, Thomson JA, Mundree SG (2006) XVSAP1 from Xerophyta viscosa improves osmotic-, salinity- and high-temperature-stress tolerance in Arabidopsis. Biotechnol J 1:1137–1146 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 54:191–201 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 53:1197–1205 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 100:4921–4926 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 8:3548–3560 Georgieva T, Christov N, Djilianov D (2012) Identification of desiccationregulated genes by cDNA-AFLP in Haberlea rhodopensis: a resurrection plant. Acta Physiol Plant 34:1055–1066 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 225:1405–1420 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 30:435–446 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 72:1273–1284 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 9:6561–6577 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 58:1947–1956 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 31:1917–1922 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 87:223–226 Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D (1991) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J 1:355–359 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 6:243–250 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 10:20 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 52:894–908 Gaff DF, McGregor GR (1979) The effect of dehydration and rehydration in the nitrogen content of various fractions from resurrection plants. Biol Plant 21:92–99 Tymms MJ, Gaff DF (1978) Proline accumulation during water stress in resurrection plants. J Exp Bot 30:165–168 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 385:301–308 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 13:767–776 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 179:877–887 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 176:90–98