What is remarkable about resurrection plants is the ability of vegetative tissues (root, shoot, stem, leaves) to tolerate dehydration of the tissues and then return as functional units on rehydration. This phenomenon made resurrection plants exciting targets for molecular analysis of the poikilohydric ability and drought tolerance. The protective mechanisms of vegetative desiccation tolerance appear to involve three major components, sugars, proteins and antioxidants. According to the recent scientific consensus all three are postulated to be involved in maintaining cellular integrity during the drying phases. The aim of this review is to establish a provisional hierarchy among these stress avoiding mechanisms that are associated with desiccation tolerance. The main reason for ranking these signal metabolites and protective agents is their potential importance in practical applications. Although vegetative desiccation tolerance is a complex trait both genetically and physiologically, there are already examples where outcomes of targeted studies in resurrection plants are going to be directly utilized to engineer crop plants genetically. Here we also show that conventional genetic transformation techniques, via in vitro plant regeneration systems, still represent an unavoidable part of the high-throughput technology chain of molecular breeding.
Bae, H., Herman, E., Bailey, B., Bae, H. J., Sicher, R. (2005) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol. Plant. 125, 114–126.
Sicher R. , 'Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense ' (2005 ) 125 Physiol. Plant. : 114 -126 .
Baier, M., Dietz, K. J. (1997) The plant 2-cys peroxiredoxin BAS1 is a nuclear encoded chloroplast protein: its expression regulation, phylogenetic origin and implications for its specific physiological function in plants. Plant J. 12, 179–190
Dietz K. J. , 'The plant 2-cys peroxiredoxin BAS1 is a nuclear encoded chloroplast protein: its expression regulation, phylogenetic origin and implications for its specific physiological function in plants ' (1997 ) 12 Plant J. : 179 -190 .
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, 1346–1353.
Salamini F. , 'Desiccation tolerance in the resurrection plant Craterostigma plantagineum: a contribution to the study of drought tolerance at the molecular level ' (2001 ) 127 Plant Physiol. : 1346 -1353 .
Bent, A. F. (2000) Arabidopsis in planta transformation. Uses, mechanisms, and prospects for transformation of other species. Plant Physiol. 124, 1540–1547.
Bent A. F. , 'Arabidopsis in planta transformation ' (2000 ) 124 Uses, mechanisms, and prospects for transformation of other species. Plant Physiol. : 1540 -1547 .
Buitink, J., Leprince, O. (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48, 215–228.
Leprince O. , 'Glass formation in plant anhydrobiotes: survival in the dry state ' (2004 ) 48 Cryobiology : 215 -228 .
Chakrabortee, S., Boschetti, C., Walton, L. J., Sarkar, S., Rubinsztein, D. C., Tunnacliffe, A. (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc. Natl. Acad. Sci. USA 104, 18073–18078.
Tunnacliffe A. , 'Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function ' (2007 ) 104 Proc. Natl. Acad. Sci. USA : 18073 -18078 .
Crowe, J. H., Crowe, L. M., Carpenter, J. F., Rudolf, A. S., Wistrom, C. A., Spargo, B. J., Anchordoguy, T. J. (1988) Interaction of sugars with membranes. Biochimica et Biophysica Acta 947, 367–384.
Anchordoguy T. J. , 'Interaction of sugars with membranes ' (1988 ) 947 Biochimica et Biophysica Acta : 367 -384 .
Cuming, A. (1999) LEA proteins. In: Shewry, P. R., Casey, R. (eds) Seed Proteins. Kluwer Academic Publishers, Dordecht, The Netherlands, pp. 753–780.
Cuming A. , '', in Seed Proteins , (1999 ) -.
Cushman, M. A., Bufford, D., Fredrickson, M., Ray, A., Akselrod, I., Landrith, D., Stout, L., Maroco, J., Cushman, J. (1999) An expressed sequence tag (EST) database for the common ice plant Mesembryanthemum crystallinum. Plant Physiol. 120S, 145.
Cushman J. , 'An expressed sequence tag (EST) database for the common ice plant Mesembryanthemum crystallinum ' (1999 ) 120S Plant Physiol. : 145 -.
Daskalova, E., Dontcheva, S., Yahubyan, G., Minkov, I., Toneva, V. (2010) Ecological characteristics and conservation of the protected resurrection species Haberlea rhodopensis Friv. as in vitro plants through a modified micropropagation system. Biotechnol. & Biotechnol. Eq. 24, 213–217.
Toneva V. , 'Ecological characteristics and conservation of the protected resurrection species Haberlea rhodopensis Friv. as in vitro plants through a modified micropropagation system ' (2010 ) 24 Biotechnol. & Biotechnol. Eq. : 213 -217 .
Djilianov, D., Genova, G., Parvanova, D., Zapryanova, N., Konstantinova, T., Atanasov, A. (2005) In vitro culture of the resurrection plant Haberlea rhodopensis. Plant Cell Tissue Organ Cult. 80, 115–118.
Atanasov A. , 'In vitro culture of the resurrection plant Haberlea rhodopensis ' (2005 ) 80 Plant Cell Tissue Organ Cult. : 115 -118 .
Djilianov, D., Ivanov, S., Georgieva, T., Moyankova, D., Berkov, S., Petrova, G., Mladenov, P., Christov, N., Hristozova, N., Preshev, D., Tchorbadjieva, M., Alexieva, V., Tosheva, A., Nikolova, M., Ionkova, I., van den Ende, W. (2009) A holistic approach to resurrection plants. Haberlea rhodopensis — a case study. Biotechnol. & Biotechnol. Eq. 23, 1414–1416.
Ende W. , 'A holistic approach to resurrection plants. Haberlea rhodopensis — a case study ' (2009 ) 23 Biotechnol. & Biotechnol. Eq. : 1414 -1416 .
Dontcheva, S., Daskalova, E., Yahubyan, G., Denev, I., Minkov, I., Toneva, V. (2009) Conservation of the protected resurrection species Ramonda serbica Panč. — habitat montana district, Bulgaria as in vitro plants through a modified micropropagation system. Biotechnol. & Biotechnol. Eq. 23, 369–372.
Toneva V. , 'Conservation of the protected resurrection species Ramonda serbica Panč. — habitat montana district, Bulgaria as in vitro plants through a modified micropropagation system ' (2009 ) 23 Biotechnol. & Biotechnol. Eq. : 369 -372 .
Fiehn, O. (2002) Metabolomics — the link between genotypes and phenotypes. Plant Mol. Biol. 48, 155–171.
Fiehn O. , 'Metabolomics — the link between genotypes and phenotypes ' (2002 ) 48 Plant Mol. Biol. : 155 -171 .
Furini, A., Koncz, C., Salamini, F., Bartels, D. (1994) Agrobacterium-mediated transformation of the desiccation-tolerant plant Craterostigma plantagineum. Plant Cell Rep. 14, 102–106.
Bartels D. , 'Agrobacterium-mediated transformation of the desiccation-tolerant plant Craterostigma plantagineum ' (1994 ) 14 Plant Cell Rep. : 102 -106 .
Goddijn, O. J. M., Verwoerd, T. C., Voogd, E., Krutwagen, R. W. H. H., de Graaf, P. T. H. M., Poels, J., van Dun, K., Ponstein, A. S., Damm, B., Pen, J. (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol. 113, 181–190.
Pen J. , 'Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants ' (1997 ) 113 Plant Physiol. : 181 -190 .
Goyal, K., Walton, L. J., Tunnacliffe, A. (2005) LEA proteins prevent protein aggregation due to water stress. Biochem. J. 388, 151–157.
Tunnacliffe A. , 'LEA proteins prevent protein aggregation due to water stress ' (2005 ) 388 Biochem. J. : 151 -157 .
Grill, E., Löffler, S., Winnacker, E. L., Zenk, M. H. (1989) Phytocelatins, the heavy-metal binding peptides of plants, are synthetised from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytocelatin synthase). Proc. Natl. Acad. Sci. USA 86, 6838–6842.
Zenk M. H. , 'Phytocelatins, the heavy-metal binding peptides of plants, are synthetised from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytocelatin synthase) ' (1989 ) 86 Proc. Natl. Acad. Sci. USA : 6838 -6842 .
Gygi, S. P., Rochon, S. Y., Franza, B. R., Aebersold, R. (1999) Correlation between protein and mRNA abundance in yeast. Molecular and Cellular Biology 19, 1720–1730.
Aebersold R. , 'Correlation between protein and mRNA abundance in yeast ' (1999 ) 19 Molecular and Cellular Biology : 1720 -1730 .
Hoekstra, F. A., Wolkers, W. F., Buitink, J., Golovina, E. A., Crowe, J. H., Crowe, L. M. (1997) Membrane stabilization in the dry state. Comp. Biochem. Phys. 117A, 335–341.
Crowe L. M. , 'Membrane stabilization in the dry state ' (1997 ) 117A Comp. Biochem. Phys. : 335 -341 .
Ishianti, M., Xiong, I., Stevenson, B., Zhu, J. K. (1997) Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. Plant Cell 9, 1935–1949.
Zhu J. K. , 'Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways ' (1997 ) 9 Plant Cell : 1935 -1949 .
Iturriaga, G., Cushman, M. A. F., Cushman, J. C. (2006) An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Sci. 170, 1173–1184.
Cushman J. C. , 'An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes ' (2006 ) 170 Plant Sci. : 1173 -1184 .
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.
Deng X. , 'Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration ' (2007 ) 225 Planta : 1405 -1420 .
Kranner, I., Beckett, R. P., Wornik, S., Zorn, M., Pfeifhofer, H. W. (2002) Revival of a resurrection plant correlates with its antioxidant status. Plant J. 31, 13–24.
Pfeifhofer H. W. , 'Revival of a resurrection plant correlates with its antioxidant status ' (2002 ) 31 Plant J. : 13 -24 .
Lappartient, A. G., Touraine, B. (1996) Demand-driven control of root ATP sulfurylase activity and sulfate uptake in intact Canola. Plant Physiol. 111, 147–157.
Touraine B. , 'Demand-driven control of root ATP sulfurylase activity and sulfate uptake in intact Canola ' (1996 ) 111 Plant Physiol. : 147 -157 .
LePrince, O., Hendry, G. A. F., McKersie, B. D. (1993) The mechanism of desiccation tolerance in developing seeds. Seed Science Research 3, 231–246.
McKersie B. D. , 'The mechanism of desiccation tolerance in developing seeds ' (1993 ) 3 Seed Science Research : 231 -246 .
Liu, Y. B., Wang, G., Liu, J., Zhao, X., Tan, H. J., Li, X. R. (2007) Anatomical, morphological and metabolic acclimation in the resurrection plant Reaumuria soongorica during dehydration and rehydration. Journal of Arid Environments 70, 183–194.
Li X. R. , 'Anatomical, morphological and metabolic acclimation in the resurrection plant Reaumuria soongorica during dehydration and rehydration ' (2007 ) 70 Journal of Arid Environments : 183 -194 .
Marschall, M., Proctor, M. C. F., Smirnoff, N. (1998) Carbohydrate composition and invertase activity of the leafy liverwort Porella platyphylla. New Phytologist 138, 343–353.
Smirnoff N. , 'Carbohydrate composition and invertase activity of the leafy liverwort Porella platyphylla ' (1998 ) 138 New Phytologist : 343 -353 .
Moore, J. P., Westall, K. L., Ravenscroft, N., Farrant, J. M., Lindsey, G. G., Brandt, W. F. (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.
Brandt W. F. , '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 ' (2005 ) 385 Biochem. J. : 301 -308 .
Moore, J. P., Le, N. T., Brandt, W., Driouich, A., Farrant, J. (2009) Towards a system-based understanding of plant desiccation tolerance. Trends Plant Sci. 14, 112–117.
Farrant J. , 'Towards a system-based understanding of plant desiccation tolerance ' (2009 ) 14 Trends Plant Sci. : 112 -117 .
Mundree, S. G., Whittaker, A., Thomson, J. A., Farrant, J. M. (2000) An aldose reductase homolog from the resurrection plant Xerophyta viscosa Baker. Planta 211, 693–700.
Farrant J. M. , 'An aldose reductase homolog from the resurrection plant Xerophyta viscosa Baker ' (2000 ) 211 Planta : 693 -700 .
Murashige, T., Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plantarum 15, 473–497.
Skoog F. , 'A revised medium for rapid growth and bioassays with tobacco tissue cultures ' (1962 ) 15 Physiol. Plantarum : 473 -497 .
Noctor, G., Arisi, A. C. M., Jouanin, L., Kunert, K. J., Rennenberg, H., Foyer, C. H. (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J. Exp. Bot. 49, 623–647.
Foyer C. H. , 'Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants ' (1998 ) 49 J. Exp. Bot. : 623 -647 .
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.
Scott P. , 'Investigation into the ability of roots of the poikilohydric plant Craterostigma plantagineum to survive dehydration stress ' (2003 ) 54 J. Exp. Bot. : 2313 -2321 .
Oliver, M. J., Tuba, Z., Mishler, B. D. (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 151, 85–100.
Mishler B. D. , 'The evolution of vegetative desiccation tolerance in land plants ' (2000 ) 151 Plant Ecol. : 85 -100 .
Păcurar, D. I. (2009) Model organisms — a journey from the dawn of biological research to the postgenomic era. Romanian Biotechnological Letters 14, 4087–4094.
Păcurar D. I. , 'Model organisms — a journey from the dawn of biological research to the postgenomic era ' (2009 ) 14 Romanian Biotechnological Letters : 4087 -4094 .
Peterbauer, T., Mucha, J., Mach, L., Richter, A. (2002) Chain elongation of raffinose in pea seeds — isolation, characterization, and molecular cloning of a multifunctional enzyme catalyzing the synthesis of stachyose and verbascose. J. Biol. Chem. 277, 194–200.
Richter A. , 'Chain elongation of raffinose in pea seeds — isolation, characterization, and molecular cloning of a multifunctional enzyme catalyzing the synthesis of stachyose and verbascose ' (2002 ) 277 J. Biol. Chem. : 194 -200 .
Peters, S., Mundree, S. G., Thomson, J. A., Farrant, J. M., Keller, F. (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose familiy oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J. Exp. Bot. 58, 1947–1956.
Keller F. , 'Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose familiy oligosaccharides (RFOs) accumulate in leaves in response to water deficit ' (2007 ) 58 J. Exp. Bot. : 1947 -1956 .
Sabovljevic, A., Sabovljevic, M., Rakic T., Stevanovic, B. (2008) Establishment of procedures for in vitro maintenance, plant regeneration, and protoplast transfection of the resurrection plant Ramonda serbica. Belg. J. Bot. 141, 178–184
Stevanovic B. , 'Establishment of procedures for in vitro maintenance, plant regeneration, and protoplast transfection of the resurrection plant Ramonda serbica ' (2008 ) 141 Belg. J. Bot. : 178 -184 .
Schiraldi, C., Di Lernia, I., De Rosa, M. (2002) Trehalose production: exploiting novel approaches. Trends Biotech. 20, 420–425.
Rosa M. , 'Trehalose production: exploiting novel approaches ' (2002 ) 20 Trends Biotech. : 420 -425 .
Smith-Espinoza, C., Bartels, D., Phillips, J. (2007) Analysis of a LEA gene promoter via Agrobacterium-mediated transformation of the desiccation tolerant plant Lindernia brevidens. Plant Cell Rep. 26, 1681–1688.
Phillips J. , 'Analysis of a LEA gene promoter via Agrobacterium-mediated transformation of the desiccation tolerant plant Lindernia brevidens ' (2007 ) 26 Plant Cell Rep. : 1681 -1688 .
Suzuki, T., Imamura, K., Yamamoto, K., Satoh, K., Okazaki, M. (1997) Thermal stabilisation of freeze-dried enzymes by sugars. J. Chem. Eng. Jpn. 30, 609–613.
Okazaki M. , 'Thermal stabilisation of freeze-dried enzymes by sugars ' (1997 ) 30 J. Chem. Eng. Jpn. : 609 -613 .
Tausz, M., Šircelj, H., Grill, D. (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J. Exp. Bot. 55, 1955–1962.
Grill D. , 'The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid ' (2004 ) 55 J. Exp. Bot. : 1955 -1962 .
Toldi, O., Norwood, M., Tóth, S., Scott, P. (2000) The susceptibility to Agrobacterium-mediated transformation in the desiccation-tolerant plant Craterostigma plantagineum is determined by in vitro preinduction of vir genes of the bacterial Ti plasmid. Plant Physiology and Biochemistry 38S, 97.
Scott P. , 'The susceptibility to Agrobacterium-mediated transformation in the desiccation-tolerant plant Craterostigma plantagineum is determined by in vitro preinduction of vir genes of the bacterial Ti plasmid ' (2000 ) 38S Plant Physiology and Biochemistry : 97 -.
Toldi, O., Tóth, S., Ponyi, T., Scott, P. (2002) An effective and reproducible transformation protocol for the model resurrection plant Craterostigma plantagineum Hochst. Plant Cell Rep. 21, 63–69.
Scott P. , 'An effective and reproducible transformation protocol for the model resurrection plant Craterostigma plantagineum Hochst ' (2002 ) 21 Plant Cell Rep. : 63 -69 .
Toldi, O., Djilianov, D., Scott, P. (2006) Transgenic Approach for Functional Analysis of Genes Associated with Desiccation Tolerance in Resurrection Plants. In: Teixeira da Silva, J. A. (ed.) Floriculture, Ornamental and Plant Biotechnology. Vol. III. Global Science Book, UK, pp. 209–217.
Scott P. , '', in Floriculture, Ornamental and Plant Biotechnology , (2006 ) -.
Toldi, O., Tuba, Z., Scott, P. (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci. 176, 187–199.
Scott P. , 'Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? ' (2009 ) 176 Plant Sci. : 187 -199 .
Toldi, O., Tuba, Z., Scott, P. (2010) Can lessons learned from resurrection plants extended over crop plant species? Romanian Biotechnological Letters 15, 3–11.
Scott P. , 'Can lessons learned from resurrection plants extended over crop plant species? ' (2010 ) 15 Romanian Biotechnological Letters : 3 -11 .
Tóth, S., Scott, P., Sorvari, S., Toldi, O. (2004) Effective and reproducible protocols for in vitro culturing and plant regeneration of the physiological model plant Ramonda myconi (L.) Rchb. Plant Sci. 166, 1027–1034.
Toldi O. , 'Effective and reproducible protocols for in vitro culturing and plant regeneration of the physiological model plant Ramonda myconi (L.) Rchb ' (2004 ) 166 Plant Sci. : 1027 -1034 .
Tóth, S., Kiss, C., Scott, P., Kovács, G., Sorvari, S., Toldi, O. (2006) Agrobacterium-mediated genetic transformation of the desiccation tolerant resurrection plant Ramonda myconi (L.) Rchb. Plant Cell Rep. 25, 442–449.
Toldi O. , 'Agrobacterium-mediated genetic transformation of the desiccation tolerant resurrection plant Ramonda myconi (L.) Rchb ' (2006 ) 25 Plant Cell Rep. : 442 -449 .
Voinnet, O. V., Pinto, Y. M., Baulcombe, D. C. (1999) Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. Proc. Natl. Acad. Sci. USA 96, 14147–14152.
Baulcombe D. C. , 'Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants ' (1999 ) 96 Proc. Natl. Acad. Sci. USA : 14147 -14152 .
Watson, B. S., Asirvatham, V. S., Wang, L., Sumner, L. W. (2003) Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiol. 131, 1104–1123.
Sumner L. W. , 'Mapping the proteome of barrel medic (Medicago truncatula) ' (2003 ) 131 Plant Physiol. : 1104 -1123 .
Wise, M. J., Tunnacliffe, A. (2004) POPP the question: what do LEA proteins do? Trends Plant Sci. 9, 13–17.
Tunnacliffe A. , 'POPP the question: what do LEA proteins do? ' (2004 ) 9 Trends Plant Sci. : 13 -17 .