Advertisement

Resurrection Plants: Physiology and Molecular Biology

  • Dorothea BartelsEmail author
  • Syed Sarfraz Hussain
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 215)

Abstract

The ability to survive desiccation is commonly found in seeds or pollen and it is widespread among bryophytes, but it is rarely present in vegetative tissues. A small group of vascular plants also known as resurrection plants exhibit tolerance to nearly complete desiccation of vegetative tissues. To date more than 300 angiosperm species have been identified that possess this kind of desiccation tolerance. The different problems associated with desiccation require specific mechanisms to be in place. Conservation of structure of membranes and macromolecules is correlated with the synthesis of large amounts of desiccation-induced protective proteins such as late embryogenesis abundant (LEA) proteins, sugars, and reactive oxygen scavengers. The desiccation-induced molecules may have different roles in cellular protection: (1) proteins may conserve structures of macromolecules and membranes, (2) the sugars may be effective in osmotic adjustment and they may stabilize membrane structures and proteins, (3) mechanical damage due to vacuole shrinkage in dehydrating cells is probably avoided by cell wall folding or by replacing the water in vacuoles with non-aqueous substances, and (4) oxidative stress, due to enhanced production of reactive oxygen species (ROS) especially by chloroplasts, is minimized through diverse ROS scavenging molecules. Photochemical activities of resurrection plants are inhibited with loss of water similar to those of non-tolerant plants; however, photosynthesis is rapidly reactivated during rehydration even when plants lost more than 95% water. In this chapter, we describe the molecular and biochemical mechanisms associated with desiccation tolerance as well as morphological and physiological adaptations of resurrection plants. Acquisition of desiccation tolerance requires the coordinated expression of diverse genes, which is achieved through a complex regulatory network. Many of the signalling pathways are mediated via the plant hormone abscisic acid (ABA), a key molecule in the process. Possible evolutionary mechanisms selecting for desiccation-tolerant plants are discussed.

Keywords

Late Embryogenesis Abundant Compatible Solute Vegetative Tissue Desiccation Tolerance Glycine Betaine 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ABA

Abscisic acid

LEA

Late embryogenesis abundant

ROS

Reactive oxygen species

Notes

Acknowledgements

We thank Prof. E. Fischer for advice on the geographical distribution of desiccation-tolerant species and for providing the information contained in Table 16.1. Work in the laboratory of D.B. was supported by grants from the German Research Council, by the European training network ADONIS and by an ERA-PG project. D.B. is a member of the European COST action INPAS (International Network of Plant Abiotic Stress). We thank C. Marikar for help with the manuscript preparation.

References

  1. Aalen RB, Opsahl-Ferstad HG, Linnestad C, Olsen OA (1994) Transcripts encoding an oleosin and a dormancy-related protein are present in both the aleurone layer and the embryo of developing barley (Hordeum vulgare L.) seeds. Plant J 5:385–396PubMedCrossRefGoogle Scholar
  2. Abe S, Kurashima A, Yokohama Y, Tanaka J (2001) The cellular ability of desiccation tolerance in Japanese intertidal seaweeds. Bot Mar 44:125–131CrossRefGoogle Scholar
  3. Adamska I (1997) ELIPs. Light-induced stress proteins. Physiol Plant 100:794–805CrossRefGoogle Scholar
  4. Alamillo JM, Bartels D (1996) Light and stage of development influence the expression of desiccation-induced genes in the resurrection plant Craterostigma plantagineum. Plant Cell Environ 19:300–310CrossRefGoogle Scholar
  5. 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
  6. Alamillo J, Roncarati R, Heino P, Velasco R, Nelson D, Elster R, Brenacchia G, Furini A, Schwall G, Salamini F, Bartels D (1995) Molecular analysis of desiccation tolerance in barley embryos and in the resurrection plant Craterostigma plantagineum. Agronomie 2:161–167Google Scholar
  7. Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5–17CrossRefGoogle Scholar
  8. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small and rare. J Exp Biol 209:1575–1584PubMedCrossRefGoogle Scholar
  9. Angelovici R, Galili G, Fernie AR, Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15(4):211–218PubMedCrossRefGoogle Scholar
  10. Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Comp Biol 45:696–701PubMedCrossRefGoogle Scholar
  11. Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiol 127:1346–1353PubMedCrossRefGoogle Scholar
  12. Bartels D, Singh M, Salamini F (1988) Onset of desiccation tolerance during development of the barley embryo. Planta 175:485–492CrossRefGoogle Scholar
  13. Bartels D, Schneider K, Terstappen G, Piatkowski D, Salamini F (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181:27–34CrossRefGoogle Scholar
  14. 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
  15. Bartels D, Ditzer A, Furini A (2006) What can we learn from resurrection plants? In: Ribaut JM (ed) Drought adaptation in cereals. New York, Hayworth, pp 599–622Google Scholar
  16. 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
  17. Bernacchia G, Salamini F, Bartels D (1996) Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum. Plant Physiol 111:1043–1050PubMedGoogle Scholar
  18. Bewley JD (1979) Physiological aspects of desiccation tolerance. Ann Rev Plant Physiol 30:195–238CrossRefGoogle Scholar
  19. Bewley JD, Krochko JE (1982) Desiccation tolerance. In: Pirson A, Zimmermann MH (eds) Encyclopedia of plant physiology, vol 12b, New series. Springer, Heidelberg, pp 325–378Google Scholar
  20. Bewley JD, Oliver MJ (1992) Desiccation-tolerance in vegetative plant tissues and seeds: protein synthesis in relation to desiccation and a potential role for protection and repair mechanisms. In: Osmond CB, Somero G (eds) Water and life: a comparative analysis of water relationship at the organismic, cellular and molecular levels. Springer, Berlin, pp 141–160Google Scholar
  21. Bianchi G, Gamba A, Murelli C, Salamini F, Bartels D (1991) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. Plant J 1(3):355–359Google Scholar
  22. Bianchi G, Gamba A, Limiroli R, Pozzi N, Elste R, Salamini F, Bartels D (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87:223–226CrossRefGoogle Scholar
  23. Bockel C, Salamini F, Bartels D (1998) Isolation and characterization of genes expressed during early events of the dehydration process in the resurrection plant Craterostigma plantagineum. J Plant Physiol 152:158–166Google Scholar
  24. Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228PubMedCrossRefGoogle Scholar
  25. Chae HZ, Chung SJ, Rhee SG (1994) Thioredoxin-dependent peroxide reductase from yeast. J Biol Chem 269:27670–27678PubMedGoogle Scholar
  26. Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257PubMedCrossRefGoogle Scholar
  27. Child GF (1960) Brief notes on the ecology of the resurrection plant Myrothamnus flabellifolia with mention of its water-absorbing abilities. J S Afr Bot 26:1–8Google Scholar
  28. Clegg JS (2005) Desiccation tolerance in encysted embryos of the animal extremophile, Artemia. Integr Comp Biol 45:715–724PubMedCrossRefGoogle Scholar
  29. Collett H, Butowt R, Smith J, Farrant JM, Illing N (2003) Photosynthetic genes are differentially transcripted during the dehydration-rehydration cycle in the resurrection plant, Xerophyta humilis. J Exp Bot 54:2593–2595PubMedCrossRefGoogle Scholar
  30. Cooper K, Farrant JM (2002) Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. J Exp Bot 53:1805–1813PubMedCrossRefGoogle Scholar
  31. Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38:109–124PubMedCrossRefGoogle Scholar
  32. Crowe JH, Crowe LM (1992) Membrane integrity in anhydrobiotic organisms: towards a mechanism for stabilizing dry cells. In: Somero GN, Osmond CB, Bolin CL (eds) Water and life. A comparative analysis of water relationships at the organismic, cellular and molecular levels. Springer, Berlin, pp 87–113Google Scholar
  33. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Plant Physiol 60:73–103Google Scholar
  34. Dalla Vecchia F, Asmar TE, Calamassi R, Rascio N, Vazzana C (1998) Morphological and ultrastructural aspects of dehydration and rehydration in leaves of Sporobolus stapfianus. Plant Growth Reg 24:219–228CrossRefGoogle Scholar
  35. Deng X, Phillips J, Meijer AH, Salamini F, Bartels D (2002) Characterization of five novel dehydrationresponsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 49:601–610PubMedCrossRefGoogle Scholar
  36. Dickie JB, Pritchard HW (2002) Systematic and evolutionary aspects of desiccation tolerance in seeds. In: Black M, Pritchard HW (eds) Desiccation and survival of plants – drying without dying. CABI, Wallingford, pp 239–259CrossRefGoogle Scholar
  37. Ditzer A, Bartels D (2006) Identification of stress-responsive promoter elements and isolation of corresponding DNA binding proteins for the LEA gene CpC2 promoter. Plant Mol Biol 61:643–663PubMedCrossRefGoogle Scholar
  38. Farrant JM (2000) A comparation of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecol 151:29–39CrossRefGoogle Scholar
  39. Farrant JM, Kruger LA (2001) Longevity of dry Myrothamnus flabellifolius in simulated field conditions. Plant Growth Reg 35:109–120CrossRefGoogle Scholar
  40. Farrant JM, Sherwin HW (1997) Mechanisms of desiccation tolerance in seeds and resurrection plants. In: Taylor AG, Huang XL (eds) Progress in seed research. Proceedings of the second international conference on seed science and technology. Communication Services of the New York State Agricultural Experimental Station, Geneva, NY, pp 109–120Google Scholar
  41. Farrant JM, Vander Willigen C, Loffell DA, Bartsch S, Whittaker A (2003) An investigation into the role of light during desiccation of three angiosperm resurrection plants. Plant Cell Environ 26:1275–1286CrossRefGoogle Scholar
  42. Farrant JM, Brandt W, Lindsey GG (2007) An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress 1(1):72–84Google Scholar
  43. Feder ME, Hofmann GE (1999) Heat shock proteins, evolutionary and ecological physiology. Ann Rev Physiol 61:243–282CrossRefGoogle Scholar
  44. Fischer E (1992) Systematik der afrikanischen Lindernieae (Scrophulariaceae). Tropische und subtropische Pflanzenwelt 81:1–365Google Scholar
  45. Fischer E (1995) Revision of the Lindernieae (Scrophulariaceae) in Madagascar. 1. The genera Lindernia Allioni and Crepidorhopalon E. Fischer. Bull Mus Natl Hist Nat Paris 4e sér., 17, section B, Adansonia: 227–257Google Scholar
  46. Frank W, Phillips JR, Salamini F, Bartels D (1998) Two dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant J 15:413–421PubMedCrossRefGoogle Scholar
  47. 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 J16:3599–3608Google Scholar
  48. Gaff DF (1971) Desiccation-tolerant flowering plants in southern Africa. Science 174:1033–1034PubMedCrossRefGoogle Scholar
  49. Gaff DF (1977) Desiccation tolerant vascular plants of southern Africa. Oecologia 31:95–109CrossRefGoogle Scholar
  50. Gaff DF (1980) Protoplasmic tolerance of extreme water stress. In: Turner NC, Kramer PJ (eds) Adaptation of plants to water and high temperature stress. Wiley, New York, pp 207–230Google Scholar
  51. Gaff DF (1986) Desiccation tolerant “resurrection” grasses from Kenya and West Africa. Oecologia 70:118–120CrossRefGoogle Scholar
  52. Gaff DF (1989) Responses of desiccation-tolerant “resurrection” plants to water stress. SPB Academic, The HagueGoogle Scholar
  53. Gaff DF, Churchill DM (1976) Borya nitida Labill. – an Australian species in the Liliaceae with desiccation-tolerant leaves. Aust J Bot 24:209–224CrossRefGoogle Scholar
  54. Gaff DF, Ellis RP (1974) Southern African grasses with foliage that revives after dehydration. Bothalia 11:305–308Google Scholar
  55. Gaff DF, Latz PK (1978) The occurrence of resurrection plants in the Australian flora. Aust J Bot 26:485–492CrossRefGoogle Scholar
  56. Gaff DF, Loveys BR (1984) Abscisic-acid content and effects during dehydration of detached leaves of desiccation tolerant plants. J Exp Bot 35:1350–1358CrossRefGoogle Scholar
  57. Gaff DF, Zee S-Y, O’Brien TP (1976) The fine structure of dehydrated and reviving leaves of Borya nitida Labill. – a desiccation-tolerant plant. Aust J Bot 24:225–236CrossRefGoogle Scholar
  58. 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
  59. Ghasempour HR, Gaff DF, Williams RPW, Gianello RD (1998) Contents of sugars in leaves of drying desiccation-tolerant flowering plants, particularly grasses. Plant Growth Reg 24:185–191CrossRefGoogle Scholar
  60. Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157PubMedCrossRefGoogle Scholar
  61. Hare PD, Cress WA, Van Staden J (1998) Dissecting the role of osmolyte accumulation during stress. Plant Cell Environ 21:535–553CrossRefGoogle Scholar
  62. Haslekas C, Stacy RAP, Nygaard V, Culianez-Macia FA, Aalen RB (1998) The expression of a peroxiredoxin antioxidant gene, AtPer1, in Arabidopsis thaliana is seed-specific and related to dormancy. Plant Mol Biol 36:833–845PubMedCrossRefGoogle Scholar
  63. Hellwege EM, Dietz KJ, Volk OH, Hartung W (1994) Abscisic acid and the induction of desiccation tolerance in the extremely xerophilic liverwort Exormotheca holstii. Planta 194:525–531CrossRefGoogle Scholar
  64. Hetherington SE, Smillie RM, Hallam ND (1982) Humidity-sensitive degreening and regreening of leaves of Borya nitida Labill. as followed by changes in chlorophyll fluorescence. Aust J Plant Physiol 9:587–599CrossRefGoogle Scholar
  65. 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
  66. 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
  67. Hoekstra FA (2005) Differential longevities in desiccated anhydrobiotic plant systems. Integr Comp Biol 45:725–733PubMedCrossRefGoogle Scholar
  68. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation-tolerance. Trends Plant Sci 6:431–438PubMedCrossRefGoogle Scholar
  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. Iljin WS (1957) Drought-resistance in plants and physiological processes. Annu Rev Plant Physiol 3:341–363Google Scholar
  71. Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45:771–787PubMedCrossRefGoogle Scholar
  72. 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
  73. Ingram J, Bartels D (1996) The molecular basis of dehydration-tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403PubMedCrossRefGoogle Scholar
  74. Iturriaga G, Leyns L, Villegas A, Gharaibeh R, Salamini F, Bartels D (1996) A family of novel myb-related genes from the resurrection plant Craterostigma plantagineum are specifically expressed in callus and roots in response to ABA or desiccation. Plant Mol Biol 32:707–716PubMedCrossRefGoogle Scholar
  75. Iturriaga G, Cushman MAF, Cushman JC (2006) An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Sci 170:1173–1184CrossRefGoogle Scholar
  76. 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
  77. Kappen L, Valladares F (1999) Opportunistic growth and desiccation tolerance: the ecological success of poikilohydrous autotrophs. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. Marcel Dekker, New York, pp 10–80Google Scholar
  78. Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B Biol Sci 150:149–191PubMedCrossRefGoogle Scholar
  79. 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(5):555–567PubMedCrossRefGoogle Scholar
  80. Kleines M, Elster RC, Rodrigo MJ, Blervacq AS, Salamini F, Bartels D (1999) Isolation and expression analysis of two stress-responsive sucrose-synthase genes from the resurrection plant Craterostigma plantagineum (Hochst.). Planta 209:13–24PubMedCrossRefGoogle Scholar
  81. Kozak CA (1999) Genetic mapping of six mouse peroxiredoxin genes and fourteen peroxiredoxin related sequences. Mamm Genome 10:1017–1019PubMedCrossRefGoogle Scholar
  82. Kranner I, Birtić S (2005) A modulating role for antioxidants in desiccation tolerance. Integr Comp Biol 45:734–740PubMedCrossRefGoogle Scholar
  83. Kranner I, Lutzoni F (1999) Evolutionary consequences of transition to a lichen symbiotic state and physiological adaptation to oxidative damage associated with poikilohydry. In: Lerner HR (ed) Plant responses to environmental stress. From phytohormones to genome reorganization. Marcel Dekker, New York, pp 591–628Google Scholar
  84. Kranner I, Beckett RP, Wornik S, Zorn M, Pfeinhofer W (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J 31:13–24PubMedCrossRefGoogle Scholar
  85. Król M, Ivanov MG, Jansson S, Kloppstech K, Huner NPA (1999) Greening under high light or cold temperature affects the level of xanthophyllcycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the chlorina f2 mutant. Plant Physiol 120:193–203PubMedCrossRefGoogle Scholar
  86. Le TN (2005) Genetics of desiccation tolerance in the resurrection plant Sporobolus stapfianus. PhD thesis. Monash University, Melbourne, AustraliaGoogle Scholar
  87. Levitt J (1980) Responses of plants to environmental stresses, vol 2, Water, radiation, salt and other stresses. Academic, New YorkGoogle Scholar
  88. Lewis ML, Miki K, Veda T (2000) FePer1, a gene encoding an evolutionary conserved 1-Cys peroxiredoxin in buckwheat (Fagopyrum esculentum Moench), is expressed in a seed-specific manner and induced during seed germination. Gene 246:81–91PubMedCrossRefGoogle Scholar
  89. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought and low temperature responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406PubMedCrossRefGoogle Scholar
  90. Lu ZJ, Neumann PM (1998) Water stressed maize, barley and rice seedlings show species diversity in mechanisms of leaf growth inhibition. J Exp Bot 49:1945–1952CrossRefGoogle Scholar
  91. Liu Y, Tengguo Z, Li X, Wang J (2007) Protective mechanisms of desiccation tolerance in Reaumuria soongorica. Sci China Ser C-Life Sci 50:15–21Google Scholar
  92. Marais S, Thomson JA, Farrant JM, Mundree SG (2004) XV VHA-C”-1 a novel stress responsive V-ATPhase Subnit C” homologue isolated from the resurrection plant Xerophyta viscosa. Plant Physiol 122:54–64CrossRefGoogle Scholar
  93. Mariaux JB, Bockel C, Salamini F, Bartels D (1998) Desiccationand abscisic acid-responsive genes encoding major intrinsic proteins (MIP) from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 38:1089–1099PubMedCrossRefGoogle Scholar
  94. Maurel C, Chrispeels MJ (2001) Aquaporins. A Molecular entry into plant water relations. Plant Physiol 125:135–138PubMedCrossRefGoogle Scholar
  95. Maurel C, Kado RT, Guern J, Chrispeels MJ (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP. EMBO J 14:3028–3035PubMedGoogle Scholar
  96. Mayee MB, Mundree SG, Majumder AL (2005) Molecular cloning, bacterial overexpression and characterization of L-myo-inositol 1-Phosphate Synthase from a monocotyledonous resurrection plant, Xerophyta viscosa. J Plant Biochem Biotechnol 14:95–98Google Scholar
  97. McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls – analysis of wall hydrolysis, stress-relaxation, and binding. Plant Physiol 107:87–100PubMedGoogle Scholar
  98. Meissner RC, Jin H, Cominelli E, Denekamp M, Fuertes A, Greco R, Kranz HD, Penfield S, Petronik K, Urzainqui A, Martin C, Paz-Ares J, Smeekens S, Tonelli C, Weisshaar B, Baumann E, Klimyuk V, Marillonnet S, Patel S, Speulman E, Tissier AF, Bouchez D, Jones JDG, Periera A, Wisman E, Bevan M (1999) Function search in a large transcription factor gene family in Arabidopsis assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes. Plant Cell 11:1827–1840PubMedCrossRefGoogle Scholar
  99. Montané MH, Dreyer S, Triantaphylides C, Kloppstech K (1997) Early light-inducible proteins during long-term acclimation of barley to photooxidative stress caused by light and cold: high level of accumulation by posttranscriptional regulation. Planta 202:293–302CrossRefGoogle Scholar
  100. Moon BY, Higashi S, Gombos Z, Murata N (1995) Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc Natl Acad Sci USA 92(14):6219–6223PubMedCrossRefGoogle Scholar
  101. Moore JP, Lindsey FJM, GG BWF (2005) The South African and Namibian populations of the resurrection plant Myrothamnus flabellifolius are genetically distinct and display variation in their galloquinic acid composition. J Chem Ecol 31:2823–2834PubMedCrossRefGoogle Scholar
  102. Moore JP, Lindsey GG, Farrant JM, Brandt WG (2007) An overview of the biology of desiccation tolerant resurrection plant Myrothamnus flabellifolia. Ann Bot 99:211–217PubMedCrossRefGoogle Scholar
  103. Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 134:237–245PubMedCrossRefGoogle Scholar
  104. Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparecio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352CrossRefGoogle Scholar
  105. 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
  106. Mtwisha L, Farrant J, Brandt W, Lindsey GG (2006) Protection mechanisms against water deficit stress: desiccation tolerance in seeds as a study case. In: Ribaut J (ed) Drought adaptation in cereals. Haworth, New York, pp 531–549Google Scholar
  107. Mundree SG, Whittaker A, Thomson JA, Farrant JM (2000) An aldose reductase homolog from the resurrection plant Xerophyta viscose Baker. Planta 211:693–700PubMedCrossRefGoogle Scholar
  108. Mundree SG, Baker B, Mowla S, Peters S, Marais S, Vander Willigen C, Govender K, Maredza A, Muyanga S, Farrant JM, Thomson JA (2002) Physiological and molecular insights into drought tolerance. Afr J Biotechnol 1:28–38Google Scholar
  109. Munns R, Passioura JB, Guo JM, Chazen O, Cramer GR (2000) Water relations and leaf expansion: importance of time scale. J Exp Bot 51:1495–1504PubMedCrossRefGoogle Scholar
  110. Murelli C, Adamo V, Finzi PV, Albini FM, Bochicchio A, Picco AM (1996) Sugar biotransformations by fungi on leaves of the resurrection plant Sporobolus stapfianus. Phytochemistry 43:741–745CrossRefGoogle Scholar
  111. Navari-Izzo F, Ricci F, Vazzana C, Quartacci MF (1995) Unusual composition of thylakoid membranes of the resurrection plant Boea hygroscopica: changes in lipids upon dehydration and rehydration. Physiol Plant 94:135–142CrossRefGoogle Scholar
  112. Navari-Izzo F, Quartacci MF, Pinzino C, Rascio N, Vazzana C, Sgherri C (2000) Protein dynamics in thylakoids of the desiccation-tolerant plant Boea hygroscopica during dehydration and rehydration. Plant Physiol 124:1427–1436PubMedCrossRefGoogle Scholar
  113. Ndima T, Farrant JM, Thomson J, Mundree S (2001) Molecular characterization of XVT8, a stress-responsive gene from the resurrection plant Xerophyta viscosa Baket. Plant Growth Reg 35:137–145CrossRefGoogle Scholar
  114. Neale AD, Blomstedt CK, Bronson P, Le TN, Guthridge K, Evand D, Gaff DF, Hamill JD (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant Cell Environ 23:265–277CrossRefGoogle Scholar
  115. 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
  116. Oliver MJ (1996) Desiccation-tolerance in vegetative plant cells. Physiol Plant 97:779–787CrossRefGoogle Scholar
  117. Oliver MJ, Bewley JD (1984) Desiccation and ultrastructure in bryophytes. Adv Bryology 2:91–131Google Scholar
  118. Oliver MJ, Bewley JD (1997) Desiccation-tolerance in plant tissues. A mechanistic overview. Hortic Rev 18:171–214Google Scholar
  119. Oliver MJ, Wood AJ, O’Mahony P (1998) “To dryness and beyond” – preparation for the dried state and rehydration in vegetative desiccation tolerant plants. Plant Growth Reg 24:193–201CrossRefGoogle Scholar
  120. Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100CrossRefGoogle Scholar
  121. Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799PubMedCrossRefGoogle Scholar
  122. 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 oligosacharides (RFOs) accumulate in leaves in response to water deficit. J Exp Bot 58(8):1947–1956PubMedCrossRefGoogle Scholar
  123. 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
  124. Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597PubMedCrossRefGoogle Scholar
  125. Phillips JR, Fischer E, Baron M, van den Dries N, 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
  126. Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol 151:19–28CrossRefGoogle Scholar
  127. Proctor MCF, Pence VC (2002) Vegetative tissues: bryophytes, vascular resurrection plants, and vegetative propogules. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI, Wallingford, Oxon, pp 207–237CrossRefGoogle Scholar
  128. Provart NJ, Gil P, Chen W, Han B, Chang HS, Wang X, Zhu T (2003) Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures. Plant Physiol 132:893–906PubMedCrossRefGoogle Scholar
  129. Quartacci MF, Forli M, Rascio N, DallaVecchia F, Bochicchio A, Navari-Izzo F (1997) Desiccation-tolerant Sporobolus stapfianus: lipid composition and cellular ultrastructure during dehydration and rehydration. J Exp Bot 48:1269–1279CrossRefGoogle Scholar
  130. Quartacci MF, Glisic O, Stevanovic B, Navari-Izzo F (2002) Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration. J Exp Bot 53:2159–2166PubMedCrossRefGoogle Scholar
  131. Rahmanzadeh R, Müller K, Fischer E, Bartels D, Borsch T (2005) The Linderniaceae and Gratiolaceae are further lineages distinct from the Scrophulariaceae (Lamiales). Plant Biol 7:1–12CrossRefGoogle Scholar
  132. Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25:141–151PubMedCrossRefGoogle Scholar
  133. Rascio N, La Rocca N (2005) Resurrection plants: the puzzle of surviving extreme vegetative desiccation. Crit Rev Plant Sci 24:209–225CrossRefGoogle Scholar
  134. Reynolds TL, Bewley JD (1993) Abasicic acid enhances the ability of the desiccation tolerant fern Polypodium virginianum to withstand drying. J Exp Bot 44:1771–1779CrossRefGoogle Scholar
  135. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedCrossRefGoogle Scholar
  136. Rodriguez M, Edsgard D, Hussain SS, Alquezar A, Rasmussen M, Gilbert T, Nielsen B, Bartels D, Mundy J (2010) Transcriptomes of the desiccation tolerant resurrection plant Craterostigma plantagineum. Plant J 63:212–228PubMedCrossRefGoogle Scholar
  137. Savenstrand H, Olofsson M, Samuelsson M, Strid A (2004) Induction of early-inducible protein gene expression in Pisum sativum after exposure to low levels of UV-B radiation and other environmental stresses. Plant Cell Rep 22:532–536PubMedCrossRefGoogle Scholar
  138. Schiller P, Heilmeier H, Hartung W (1997) Absisic acid (ABA) relations in the aquatic resurrection plant Chamaegigas intrepidus under naturally fluctuating environmental conditions. New Phytol 136:603–611CrossRefGoogle Scholar
  139. Schneider K, Wells B, Schmelzer E, Salamini F, Bartels D (1993) Desiccation leads to the rapid accumulation of both cytosol and chloroplast proteins in the resurrection plant Craterostigma plantagineum Hochst. Planta 189:120–131CrossRefGoogle Scholar
  140. Scott P (2000) Resurrection plants and the secrets of eternal leaf. Ann Bot 85:159–166CrossRefGoogle Scholar
  141. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302PubMedCrossRefGoogle Scholar
  142. Shen-Miller J, Mudgett MB, Schopf JW, Clarke S, Berger R (1995) Exceptional seed longevity and robust growth – ancient sacred lotus from China. Am J Bot 82:1367–1380CrossRefGoogle Scholar
  143. Sherwin HW, Farrant JM (1996) Differences in rehydration of three desiccation tolerant angiosperm species. Ann Bot 78:703–710CrossRefGoogle Scholar
  144. Sherwin HW, Farrant JM (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Reg 24:203–210CrossRefGoogle Scholar
  145. Shigyo M, Haseba M, Ito M (2006) Molecular evolution of the AP2 subfamily. Gene 366:256–265PubMedCrossRefGoogle Scholar
  146. 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 Gen Genom 274:364–372CrossRefGoogle Scholar
  147. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cisacting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040PubMedCrossRefGoogle Scholar
  148. Thomson WW, Platt KA (1997) Conservation of cell order in desiccated mesophyll of Selaginella lepidophylla ([Hook and Grev.] Spring). Ann Bot 79:439–447CrossRefGoogle Scholar
  149. Trainor FR, Gladych R (1995) Survival of algae in a desiccated soil: a 35-year study. Phycologia 34:191–192CrossRefGoogle Scholar
  150. Tuba Z, Proctor MCF, Csintalan Z (1998) Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation-tolerant plants: a comparison and an ecological perspective. Plant Growth Reg 24:211–217CrossRefGoogle Scholar
  151. Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812PubMedCrossRefGoogle Scholar
  152. Vander Willigen C, Farrant JM, Pammenter NW (2001) Anomalous pressure volume curves of resurrection plants do not suggest negative turgor. Ann Bot 88:537–543CrossRefGoogle Scholar
  153. Vander Willigen C, Pammenter CNW, Jaffer MA, Mundree SG, Farrant JM (2003) An ultrastructural study using anhydrous fixation of Eragrostis nindensis, a resurrection grass with both desiccation-tolerant and sensitice tissues. Funct Plant Biol 30:1–10CrossRefGoogle Scholar
  154. Vander Willigen C, Pammenter NW, Mundree SG, Farrant JM (2004) Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP 3;1 and/or compartimentation of subcellular components and metabolites play a role? J Exp Bot 397:651–661CrossRefGoogle Scholar
  155. Vicré M, Sherwin HW, Driouich A, Jaffer MA, Farrant JM (1999) Cell wall characteristics and structure of hydrated and dry leaves of the resurrection plant Craterostigma wilmsii, a microscopical study. J Plant Physiol 155:719–726Google Scholar
  156. Vicré 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
  157. 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
  158. Wang L, Shang H, Liu X, Wu R, Zheng M, Phillips J, Bartels D, Deng X (2009) A cell wall localised glycine-rich protein plays a role in dehydration tolerance in the resurrection plant Boea hygrometrica. Plant Biol 12:1–13Google Scholar
  159. Wehmeyer N, Hernandez LD, Finkelstein RR, Vierling E (1996) Synthesis of small heat shock proteins is part of the developmental program of late seed maturation. Plant Physiol 112:747–757PubMedCrossRefGoogle Scholar
  160. Willige B, Kutzer M, Tebartz F, Bartels D (2009) Subcellular localization and enzymatic properties of differentially expressed transketolase genes isolated from the desiccation tolerant resurrection plant Craterostigma plantagineum. Planta 229:659–666PubMedCrossRefGoogle Scholar
  161. Yamaguchi-Shinozaki K, Shinozaki K (1993) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25PubMedGoogle Scholar
  162. 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Institute of Molecular Plant Physiology and Plant BiotechnologyUniversity of BonnBonnGermany

Personalised recommendations