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Plant function and evolutionary biology
RESEARCH ARTICLE

Protection mechanisms in the resurrection plant Xerophyta viscosa: cloning, expression, characterisation and role of XvINO1, a gene coding for a myo-inositol 1-phosphate synthase

Arnaud Lehner A C , Denis R. Chopera A , Shaun W. Peters B , Felix Keller B , Sagadevan G. Mundree A , Jennifer A. Thomson A and Jill M. Farrant A D
+ Author Affiliations
- Author Affiliations

A University of Cape Town, Department of Molecular and Cellular Biology, Private Bag, Rondebosch 7701, Cape Town, South Africa.

B University of Zürich, Institute of Plant Biology, Molecular Plant Physiology, Zollikerstrasse 107, Zürich, 8008, Switzerland.

C Present address: Université Paris 7, EA 3514 Electrophysiologie des Membranes, 2, place Jussieu, 75005 Paris, France.

D Corresponding author. Email: jill.farrant@uct.ac.za

Functional Plant Biology 35(1) 26-39 https://doi.org/10.1071/FP07142
Submitted: 8 June 2007  Accepted: 16 November 2007   Published: 25 January 2008

Abstract

We have used reverse transcription-PCR coupled with 5′- and 3′-RACE to isolate a full length INO1 cDNA (1692 bp with an ORF of 1530) from the resurrection plant Xerophyta viscosa Baker. XvINO1 encodes 510 amino acids, with a predicted MW of 56.7kD and contains four sequence motifs that are highly conserved in plant myo-inositol-1-phosphate synthases (MIPS, EC5.5.1.4), the enzyme that catalyses the first step in the formation of myo-inositol (Ino). Northern and western analyses show that the transcript and protein are constitutively present in leaves but their expression increases, temporarily, in response to both accumulative salt stress (~300 mM NaCl) and desiccation (to 5% relative water content). Leaf Ino concentration increases 40-fold during the first 6 h of salt stress, and levels of this and other carbohydrates (galactinol, sucrose, raffinose, stachyose and hexoses) remain elevated relative to control leaves for the duration of salt stress treatment. The timing and pattern of accumulation of these carbohydrates differ under desiccation stress and we propose that they perform different functions in the respective stresses. These are elaborated in discussion of our data.

Additional keywords: carbohydrates, desiccation tolerance.


References


Abreu EFM, Aragao FJL (2007) Isolation and characterization of myo-inositol-1-phosphate synthase gene from yellow passion fruit (Passiflora edulis f. flavicarpa) expressed during seed development and environmental stress. Annals of Botany 99, 285–292.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Adhikari J, Majumder AL, Bhaduri TJ, DasGupta S, Majumder AL (1987) Chloroplast as a locale of L-myo-inositol-1-phosphate synthase. Plant Physiology 85, 611–614.
PubMed |
open url image1

Altschul SF, Gish W, Miller W, Meyers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
PubMed |
open url image1

Ashraf M (1994) Breed for salinity tolerance in plants. Critical Reviews in Plant Sciences 166, 3–16. open url image1

Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress tolerance. Environmental and Experimental Botany 59, 206–216.
Crossref | GoogleScholarGoogle Scholar | open url image1

Avigad G , Dey PM (1997) Carbohydrate metabolism: storage carbohydrate. In ‘Plant biochemistry’. (Eds PM Dey, JB Harborne) pp. 143–204. (Academic Press: San Diego)

Balibrea ME, Rus-Alvarez AM, Bolarín MC, Pérez-Alfocea F (1997) Fast changes in soluble carbohydrates and proline contents in tomato seedlings in response to ionic and non-ionic iso-osmotic stresses. Journal of Plant Physiology 151, 221–226. open url image1

Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantigineum. a contribution to the study of drought tolerance at the molecular level. Plant Physiology 127, 1346–1353.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Berjak P (2006) Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Science Research 16, 1–15.
Crossref | GoogleScholarGoogle Scholar | open url image1

Berjak P , Farrant JM , Pammenter NW (2007) Seed desiccation tolerance mechanisms. In ‘Plant desiccation-tolerance’. (Eds MA Jenks, AJ Wood) pp. 151–192. (Blackwell Publishing: Oxford, UK)

Bernal-Lugo I, Leopold AC (1995) Seed stability during storage: raffinose content and seed glassy state. Seed Science Research 5, 75–80. open url image1

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 mechanism. In ‘Water and life: a comparative analysis of water relationships at the organismic, cellular and molecular levels’. (Eds GN Somero, CB Osmond, CL Bolis) pp. 141–160. (Springer: Berlin, Heidelberg, New York)

Bianchi G, Murelli C, Bochicchio A, Vazzana C (1991) Changes in low molecular weight substances in Boea hygroscopica in response to desiccation and rehydration. Phytochemistry 30, 461–466.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. The Plant Cell 7, 1099–1111.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boyer JS (1982) Plant productivity and environment. Science 218, 443–448.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boyer JS, Westgate ME (2004) Grain yields with limited water. Journal of Experimental Botany 55, 2385–2394.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Buitink J , Hoekstra FA , Leprince O (2002) Biochemistry and biophysics of tolerance systems. In ‘Desiccation and survival in plants. Drying without dying’. (Eds M Black, HW Pritchard) pp. 293–318. (CABI Publishing: Wallingford, Oxon)

Burke MJ (1986) The glassy state and survival of anhydrous biological systems. In ‘Membranes, metabolism and dry organisms’. (Ed. AC Leopold) pp. 358–363. (Cornell University Press: Ithaca, New York)

Caffrey M, Fonseca V, Leopold AC (1988) Lipid-sugar interactions. Plant Physiology 86, 754–758.
PubMed |
open url image1

Chiera JM, Streeter JG, Finer JJ (2006) Ononitol and pinitol production in transgenic soybean containing the inositol methyl transferase gene from Mesembryanthemum crystallinum. Plant Science 171, 647–654.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chun JA, Jin UH, Lee JW, Yi YB, Hyung NI , et al. (2003) Isolation and characterization of a myo-inositol-1-phosphate synthase cDNA from developing sesame (Sesamum indicum L.) seeds: functional and differential expression, and salt-induced transcription during germination. Planta 216, 874–880.
PubMed |
open url image1

Cosgrove DJ (1980) ‘Inositol phosphates: their chemistry, biochemistry and physiology.’ (Elsevier: Amsterdam)

Crowe JH, Crowe LM, Carpenter JF, Widstrom A (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. The Biochemical Journal 242, 1–10.
PubMed |
open url image1

Cushman JC (2001) Osmoregulation in plants: implications for agriculture. American Zoologist 41, 758–769.
Crossref | GoogleScholarGoogle Scholar | open url image1

Donahue TF, Henry SA (1981) Myo-inositol 1-phosphate synthase: characteristics of the enzyme and identification of its structural gene in yeast. The Journal of Biological Chemistry 256, 7077–7085.
PubMed |
open url image1

Farrant JM (2000) Comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plants. Plant Ecology 151, 29–39.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farrant JM, Brandt W, Lindsey GG (2007) An overview of mechanisms of desiccation tolerance in selected angiosperm resurrection plants. Plant Stress Journal 1, 72–84. open url image1

Flowers TJ (2004) Improving salt stress tolerance. Journal of Experimental Botany 55, 307–319.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gaff DF (1971) Desiccation tolerance flowering plants in southern Africa. Science 174, 1033–1034.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gaff DF (1989). Responses of desiccation tolerant ‘resurrection’ plants to water deficit. In ‘Adaptation of plants to water and high temperature stress’. (Eds KH Kreeb, H Richter, TM Hinckley) pp. 207–230. (Academic Publishing: The Hague, The Netherlands)

Garwe D, Thomson JA, Mundree SG (2003) Molecular characterization of XvSAP1, a stress-responsive gene from the resurrection plant Xerophyta viscosa Baker. Journal of Experimental Botany 54, 191–201.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ghasempour HR, Gaff DF, Williams RPW, Gianello RD (1998) Contents of sugars in leaves of drying desiccation tolerant flowering plants, particularly grasses. Plant Growth Regulation 24, 185–191.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44, 826–839.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Illing N, Denby K, 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. Integrative and Comparative Biology 45, 771–787.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377–403.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. The Plant Journal 9, 537–548.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Iyer R , Mundree SG , Rafudeen S , Thomson JA (2007) XvSAP1, a desiccation tolerance gene with potential in crop improvement. In ‘Plant desiccation tolerance’. (Eds MA Jenks, AJ Wood) pp. 283–296. (Blackwell Publishing: Oxford, UK)

Jin S, Chen CCS, Plant AL (2000) Regulation by ABA osmotic-stress induced changes in protein synthesis in tomato roots. Plant, Cell & Environment 23, 51–60.
Crossref | GoogleScholarGoogle Scholar | open url image1

Keller F, Ludlow MM (1993) Carbohydrate metabolism in drought-stressed leaves of pigeon pea (Cajanus cajan). Journal of Experimental Botany 44, 1351–1359.
Crossref | GoogleScholarGoogle Scholar | open url image1

Keller F , Pharr DM (1996) Metabolism of carbohydrates in sinks and source: galactosyl-sucrose oligosaccharides. In ‘Photoassimilate distribution in plants and crops: source-sink relationships’. (Eds E Zamski, AA Schaffer) pp. 157–183. (Marcel-Dekker: New York)

Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A (2007) Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. Journal of Experimental Botany 58, 415–424.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Klages K, Boldingh H, Smith GS (1999) Accumulation of myo-inositol in Actinidia seedlings subjected to salt stress. Annals of Botany 84, 521–527.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kleiger G, Eisenberg D (2002) GXXXG and GXXXA motifs stabilize FAD and NAD(P)-binding Rossmann folds through C-alpha-H.O hydrogen bonds and van der Waals interactions. Journal of Molecular Biology 323, 69–76.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koster KL , Bryant G (2005) Dehydration in model membranes and protoplasts: contrasting effects at low, intermediate and high hydrations. In ‘Cold hardiness in plants: molecular genetics, cell biology and physiology’. (Eds THH Chen, M Uemura, S Fujikawa) pp. 219–234. (CAB International: Wallingford, UK)

Leopold AC, Sun WQ, Bernard-Lugo I (1994) The glassy state in seed: analysis and function. Seed Science Research 4, 267–274. open url image1

Leprince O, Walters-Vertucci C (1995) A calorimetric study of glass transition behaviors in axes of bean with relevance to storage ability. Plant Physiology 109, 1471–1481.
PubMed |
open url image1

Loewus FA, Loewus MW (1983) Myo-inositol: its biosynthesis and metabolism. Annual Review of Plant Physiology 34, 137–161.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loewus FA, Murthy PPN (2000) Myo-inositol metabolism in plants. Plant Science 150, 1–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Posteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. The Journal of Biological Chemistry 279, 28539–28552.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Majumder AL, Dattagupta S, Goldwasser P, Donahue TF, Henry SA (1981) The mechanism of interallelic complementation at the ino-1 locus in yeast: immunological analysis of mutants. Molecular & General Genetics 184, 347–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Majumder AL, Chatterjee A, Dastidar KG, Majee M (2003) Diversification and evolution of L-myo-inositol 1-phosphate synthase. FEBS Letters 553, 3–10.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Marais S, Thomson JA, Farrant JM, Mundree SG (2004) VATP1XV- a novel stress responsive V-ATPase subunit c homologue isolated from the resurrection plant Xerophyta viscosa Baker. Physiologia Plantarum 122, 54–61.
Crossref | GoogleScholarGoogle Scholar | open url image1

Moore JP, Nguema-Ona E, Chevalier L, Lindsey GG, Brandt WF, Lerouge P, Farrant JM, Driouich A (2006) Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus flabellifolius. Plant Physiology 141, 651–662.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moore JP, Hearshaw M, Ravenscroft N, Lindsey GG, Farrant JM, Brandt WF (2007) Desiccation-induced ultrastructural and biochemical changes in the leaves of the resurrection plants Myrothamnus flabellifolia. Australian Journal of Botany in press , open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mundree SG , Farrant JM (2000) Some physiological and molecular insights into the mechanisms of desiccation tolerance in the resurrection plant Xerophyta viscosa Baker. In ‘Plant tolerance to abiotic stresses in agriculture: role of genetic engineering’. (Eds JH Cherry, RD Locy, A Rychter) pp. 201–222. (Kluwer Academic Publishers: The Netherlands)

Mundree SG, Whittaker A, Thomson JA, Farrant JM (2000) An aldose reductase homolog from the resurrection plant Xerophyta viscosa Baker. Planta 211, 693–700.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mundree SG, Baker B, Mowla S, Peters S, Marais S, Vander Willigen C, Govender K, Maredza A, Farrant JM, Thomson JA (2002) Physiological and molecular insights into drought tolerance. African Journal of Biotechnology 1, 28–38. open url image1

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Munns R (2005) Genes and salt tolerance: bringing them together. The New Phytologist 167, 645–663.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ndima T, Farrant JM, Thomson JA, Mundree S (2001) Molecular and characterization of XVT8, a stress-responsive gene from the resurrection plant Xerophyta viscosa baker. Plant Growth Regulation 35, 137–145.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nelson DE, Rammesmayer G, Bohnert HJ (1998) Regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. The Plant Cell 10, 753–764.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10, 1–6.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Norwood M, Truesdale MR, Richter A, Scott P (2000) Photosynthetic carbohydrate metabolism in the resurrection plant Craterostigma plantigineum. Journal of Experimental Botany 51, 159–165.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Norwood M, Toldi O, Richter A, Scott P (2003) Investigation into the ability of roots of the poikilohydric plant Craterostrigma plantigineum to survive dehydration stress. Journal of Experimental Botany 54, 2313–2321.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Obendorf RL (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Science Research 7, 61–74. open url image1

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 Regulation 24, 193–201.
Crossref | GoogleScholarGoogle Scholar | open url image1

Peterbauer T, Puschenreiter M, Richter A (1998) Metabolism of galactosylononitol in seeds of Vigna umbellata. Plant & Cell Physiology 39, 334–341. open url image1

Peterbauer T, Richter A (2001) Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Science Research 11, 185–197. open url image1

Peters SW, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanism in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose oligosaccharides (RFOs) accumulate in leaves in response to water deficit. Journal of Experimental Botany 58, 1947–1956.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant, Cell & Environment 25, 141–151.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

RayChaudhuri A, Majumder AL (1996) Salinity-induced enhancement of L-myo-inositol 1-phosphate synthase in rice (Oryza sativa L.). Plant, Cell & Environment 19, 1437–1442.
Crossref | GoogleScholarGoogle Scholar | open url image1

RayChaudhuri A, Hait NC, DasGupta S, Bhaduri TJ, Deb R, Majumder AL (1997) L-myo-inositol-1-phosphate synthase from plant source. Characteristics of the chloroplastic and cytosolic enzymes. Plant Physiology 115, 727–736.
PubMed |
open url image1

Sambrook J , Fritsch EF , Maniatis T (1989) ‘Molecular cloning: a laboratory manual.’ 2nd edn. (Cold Spring Harbour Laboratory Press: New York)

Schramm G, Bruchhaus I, Roeder T (2000) A simple and reliable 5′-RACE approach. Nucleic Acids Research 28, e96.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Serraj R, Sinclair TR (2002) Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant, Cell & Environment 25, 333–341.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Serrano R, Mulet JM, Rios G, Marquez JA, de Larrinoa IF , et al. (1999) A glimpse of the mechanisms of ion homeostasis during salt stress. Journal of Experimental Botany 50, 1023–1036.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sherwin HW, Farrant JM (1996) Differences in rehydration of three desiccation-tolerant angiosperm species. Annals of Botany 78, 703–710.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sherwin HW, Farrant JM (1998) Protection mechanism against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regulation 24, 203–210.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiology 115, 1211–1219.
PubMed |
open url image1

Smart CC, Fleming AJ (1993) A plant gene with homology to D-myo-inositol-3-phosphate synthase is rapidly and spatially up-regulated during an abscissic-acid-induced morphogenic response in Spirodela polyrrhiza. The Plant Journal 4, 279–293.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smirnoff N (1998) Plant resistance to environmental stress. Current Opinion in Biotechnology 9, 214–219.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sprenger N, Keller F (2000) Allocation of raffinose family oligosaccharides to transport and storage pools in Ajuga reptans: the role of two distinct galactinol synthases. The Plant Journal 21, 249–258.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sun WQ (1997) Glassy state and seed storage stability: the WLF kinetics of seed viability loss at T greater than T-g and the plasticization effect of water on storage stability. Annals of Botany 79, 291–297.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stein AJ, Geiger JH (2002) The crystal structure and mechanism of 1-L-myo-inositol-1-phosphate synthase. The Journal of Biological Chemistry 277, 9484–9491.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis micro-array. Plant Physiology 135, 1697–1709.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tapernoux-Lüthi EM, Böhm A, Keller F (2004) Cloning, functional expression, and characterization of the raffinose oligosaccharide chain elongation enzyme, galactan: galactan galactosyltransferase, from common bugle leaves. Plant Physiology 134, 1377–1387.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plant. Current Opinion in Plant Biology 9, 189–195.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vernon DM, Bohnert HJ (1992) A novel methyl transferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. The EMBO Journal 11, 2077–2085.
PubMed |
open url image1

Vertucci CW , Farrant JM (1995) Acquisition and loss of desiccation tolerance. In ‘Seed development and germination’. (Eds J Kigel, G Galilli) pp. 237–271. (Marcel Dekker: New York)

Vicre M, Farrant JM, Gibouin D, Driouich A (2003) Resurrection plants: how to cope with desiccation? Recent Research Developments in Plant Biology 3, 69–93. open url image1

Vicre M, Farrant JM, Driouich A (2004) Insights into the mechanisms of desiccation tolerance among resurrection plants. Plant, Cell & Environment 27, 1329–1340.
Crossref | GoogleScholarGoogle Scholar | open url image1

Walters C (1998) Understanding the mechanisms and kinetics of seed aging. Seed Science Research 8, 223–244. open url image1

Walford SA, Thomson JA, Farrant JM, Mundree SG (2004) Isolation and characterisation of a novel dehydration-induced Grp94 homologue from the resurrection plant Xerophyta viscosa. South African Journal of Botany 70, 741–750. open url image1

Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures towards genetic engineering for stress tolerance. Planta 218, 1–14.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Whittaker A, Bochicchio A, Vazzana C, Lindsey G, Farrant J (2001) Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. Journal of Experimental Botany 52, 961–969.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Whittaker A, Martinelli T, Bochicchio A, Vazzana C, Farrant J (2004) Comparison of sucrose metabolism during the rehydration of desiccation-tolerant and desiccation-sensitive leaf material of Sporobolus stapfianus. Physiologia Plantarum 122, 11–20.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein in pollen that stabilizes glasses in vitro. Biochimica et Biophysica Acta 1544, 196–206.
PubMed |
open url image1

Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell & Environment 25, 131–139.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. The Journal of Experimental Biology 208, 2819–2830.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology 53, 247–273. open url image1