Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): Both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit

Journal of Experimental Botany

Volumn 58, Issue 8, 2007, Pages 1947-1956

  Peters, Shaun ^a,b   Mundree, Sagadevan G ^a   Thomson, Jennifer A ^a   Farrant, Jill M ^a   Keller, Felix ^b  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Desiccation tolerance; Galactinol synthase; Raffinose family oligosaccharides; Resurrection plants

Indexed keywords

BIOACCUMULATION; ENZYME ACTIVITY; METABOLISM; OLIGOSACCHARIDES; SUGAR (SUCROSE);

DESICCATION TOLERANCE; GALACTINOL SYNTHASE; RAFFINOSE FAMILY OLIGOSACCHARIDES; RESURRECTION PLANTS;

PLANTS (BOTANY);

RAFFINOSE; SUCROSE; VEGETABLE PROTEIN; WATER;

AMINO ACID SEQUENCE; ANGIOSPERM; ARTICLE; CHEMISTRY; DNA SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PLANT LEAF; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANGIOSPERMS; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT PROTEINS; RAFFINOSE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; SUCROSE; WATER;

SELAGINELLA PILIFERA; XEROPHYTA VISCOSA;

EID: 34547661801     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erm056     Document Type: Article

References (57)

1. Albini FM, Murelli C, Patritti G, Rovati M, Zienna P, Finzi P. 1994. Low-molecular weight substances from the resurrection plant Sporobulus stapfianus. Phytochemistry 37, 137-142.
2. Arakawa T, Prestrelski SJ, Kenney WC, Carpenter JF. 1993. Factors affecting short term and long-term stability of proteins. Advanced Drug Delivery Reviews 10, 1-28.
3. Bachmann M, Matile P, Keller F. 1994. Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. Cold acclimation, translocation, and sink to source transition: discovery of chain elongation enzyme. Plant Physiology 105, 1335-1345.
4. Barrs HD, Weatherley PE. 1962. A re-examination of the relative turgidity techniques for estimating water deficits in leaves. Australian Journal of Biological Science 15, 413-428.
5. 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 Physiology 127, 1346-1353.
6. 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.
7. Black M, Corbineau F, Grzesik M, Guy P, Come D. 1996. Carbohydrate metabolism in the developing and maturing wheat embryo in relation to its desiccation tolerance. Journal of Experimental Botany 47, 161-169.
8. Brenac P, Horbowicz M, Downer SM, Dickerman AM, Smith ME, Obendorf RL. 1997. Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. Journal of Plant Physiology 150, 481-488.
9. Caffrey M, Fonseca V, Leopold AC. 1988. Lipid-sugar interactions: relevance to anhydrous biology. Plant Physiology 86, 754-758.
10. Carpenter JF, Crowe JH. 1989. An infrared spectroscopic study of the interactions of carbohydrates with dried proteins. Biochemistry 28, 3916-3922.
11. Cooper K, Farrant JM. 2002. Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. Journal of Experimental Botany 53, 1805-1813.
12. Cunningham SM, Nadeau P, Costanguay Y, Laberge S, Volenec JJ. 2003. Raffinose and stachyose accumulation, galactinol synthase expression, and winter injury of contrasting alfalfa germplasms. Crop Science 43, 562-570.
13. Downie B, Gurusinghe S, Dahal P, Thacker RR, Snyder JC, Nonogaki H, Yim K, Fukanaga K, Alvarado V, Bradford KJ. 2003. Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiology 131, 1347-1359.
14. Farrant JM. 2000. A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecology 151, 29-39.
15. Farrant JM. 2007. Mechanisms of desiccation tolerance in angiosperm resurrection plants. In: Jenks MA, Wood AJ, eds. Plant desiccation tolerance. Wallingford, UK: CAB International (in press).
16. Farrant JM, Bartsch S, Loffell D, Van der Willigen C, Whittaker A. 2003. An investigation into the effects of light on the desiccation of three resurrection plant species. Plant, Cell and Environment 26, 1275-1286.
17. Gaff DF. 1989. Responses of desiccation tolerant 'resurrection' plants to water stress. In: Kreeb KH, Richter H, Hinckley TM, eds. Structural and functional responses to environmental stress: water shortage. The Hague, The Netherlands: SPB Academic Publishers, 255-268.
18. Gaffney SH, Haslam E, Lilley TH, Ward TR. 1988. Homotactic and heterotactic interactions in aqueous-solutions containing some saccharides - experimental results and an empirical relationship between saccharide solvation and solute-solute interactions. Journal of the Chemical Society, Faraday Transactions 84, 2545-2552.
19. 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.
20. 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.
21. Handley LW, Pharr DM, McFeeters RF. 1983. Relationship between galactinol synthase activity and sugar composition of leaves and seeds of several crop species. Journal of the American Society of Horticultural Science 108, 600-605.
22. Hoekstra FA, Wolkers WF, Buitink J, Golovina EA, Crowe JH, Crowe LM. 1997. Membrane stabilization in the dry state. Comparitive Biochemistry and Physiology 117A, 335-341.
23. Horbowicz M, Obendorf RL. 1994. Seed desiccation tolerance and storability: dependence of flatulence-producing oligosaccharides and cyclitols. Review and survey. Seed Science Research 4, 385-405.
24. 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. Integrative and Comparative Biology 45, 771-787.
25. Inan Haab C, Keller F. 2002. Purification and characterization of the raffinose oligosaccharide chain elongation enzyme, galactan: galactan galactosyltransferase (GGT), from Ajuga reptans leaves. Physiologia Plantarum 114, 361-371.
26. Ingram J, Chandler JW, Gallagher L, Salamini F, Bartels D. 1997. Analysis of cDNA clones encoding sucrose-phosphate synthase in relation to sugar interconversions associated with dehydration in the resurrection plant Craterostigma plantagineum Hochst. Plant Physiology 115, 113-121.
27. Keller F, Pharr DM. 1996. Metabolism of carbohydrates in sinks and sources: galactosyl-sucrose oligosaccharides. In: Zamski E, Schaffer AA, eds. Photoassimilate distribution in plants and crops: source-sink relationships. New York: Marcel Dekker, 157-183.
28. Koetsier P, Schorr J, Doerfler W. 1993. A rapid optimized protocol for downward alkaline Southern blotting of DNA. BioTechniques 15, 260-261.
29. Koster KL. 1991. Glass formation and desiccation tolerance in seeds. Plant Physiology 96, 302-304.
30. Koster KL, Leopold AC. 1988. Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829-832.
31. Koster KL, Bryant G. 2005. Dehydration in model membranes and protoplasts: contrasting effects at low, intermediate and high hydrations. In: Chen THH, Uemura M, Fujikawa S, eds. Cold hardiness in plants: molecular genetics, cell biology and physiology. Wallingford, UK: CAB International, 219-234.
32. Lin TP, Huang NH. 1994. The relationship between carbohydrate composition of some tree seeds and their longevity. Journal of Experimental Botany 45, 1289-1294.
33. Loewus FA, Murphy PPN. 2000. myo-Inositol metabolism in plants. Plant Science 150, 1-19.
34. Moore JP, Lindsey GG, Farrant JM, Brandt W. 2007. An overview of the biology of the desiccation tolerant resurrection plant Myrothamnus flabellifolia. Annals of Botany 99, 211-217.
35. Mowla S, Thomson JA, Farrant JM, Mundree SG. 2002. XvPer1, a novel antioxidant enzyme from the resurrection plant Xerophyta viscosa Baker. Planta 215, 716-726.
36. Müller J, Sprenger N, Bortlik K, Boller T, Wiemken A. 1997. Desiccation increases sucrose levels in Ramonda and Haberlea, two genera of resurrection plants in the Gesneriaceae. Physiologia Plantarum 100, 153-158.
37. Mundree SG, Farrant JM. 2000. Some physiological and molecular insights into the mechanisms of desiccation tolerance in the resurrection plant Xerophyta viscosa Baker. In: Cherry J, ed. Plant tolerance to abiotic stresses in agriculture: role of genetic engineering. Dordrecht, The Netherlands: Kluwer Academic Publishers, 201-222.
38. Mundree SG, Whittaker A, Thomson JA, Farrant JM. 2000. An aldose reductase homolog from the resurrection plant Xerophyta viscosa Baker. Planta 211, 693-700.
39. Ndima T, Farrant J, Thomson J, Mundree S. 2001. Molecular characterization of XVT8, a stress-responsive gene from the resurrection plant Xerophyta viscosa Baker. Plant Growth Regulation 35, 137-145.
40. Norwood M, Toldi O, Richter A, Scott P. 2003. Investigation into the ability of the roots of the poikilohydric plant Craterostigma plantigineum to survive dehydration stress. Journal of Experimental Botany 54, 2313-2321.
41. Pennycooke JC, Jones ML, Stushnoff C. 2003. Down-regulating α-galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiology 133, 901-909.
42. 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. Journal of Biological Chemistry 277, 194-200.
43. Prestrelski SJ, Tedeschi N, Arakawa T, Carpenter JF. 1993. Dehydration-induced conformational transitions in protein and their inhibition by stabilizers. Biophysical Journal 65, 661-671.
44. Proctor MCF, Pence VC. 2002. Vegetative tissues: bryophytes, vascular resurrection plants and vegetative propagules. In: Black M, Pritchard HW, eds. Desiccation and survival in plants: drying without dying. Wallingford, UK: CABI Publishing, 207-237.
45. Scott P. 2000. Resurrection plants and the secrets of eternal leaf. Annals of Botany 85, 159-166.
46. Sherwin HW, Farrant JM. 1996. Differences in rehydration of three different desiccation-tolerant species. Annals of Botany 78, 703-710.
47. Sherwin HW, Farrant JM. 1998. Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regulation 24, 203-210.
48. Sprenger N, Keller F. 2000. Allocation of raffinose family oligosaccharides to transport and storage pools in Ajuga reptans: the roles of two distinct galactinol synthases. The Plant Journal 21, 249-258.
49. Sun WQ, Irving TC, Leopold AC. 1994. The role of sugar, vitrification and membrane phase transition in seed desiccation tolerance. Physiologia Plantarum 90, 621-628.
50. Taji T, Oshumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. 2002. Important roles of drought and cold inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. The Plant Journal 29, 417-426.
51. 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.
52. Tuba Z, Proctor MCF, Csintalan Z. 1998. Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective. Plant Growth Regulation 24, 211-217.
53. Van der Willigen C, Mundree SG, Pammenter NW, Farrant JM. 2004. Mechanical stabilisation in desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does an alpha TIP and/or subcellular compartmentalization play a role? Journal of Experimental Botany 55, 651-661.
54. Vicre M, Farrant JM, Driouich A. 2004. Insights into the mechanisms of desiccation tolerance among resurrection plants. Plant, Cell and Environment 27, 1329-1340.
55. 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.
56. Zhao TY, Martin D, Meeley RB, Downie B. 2004. Expression of the maize GALACTINOL SYNTHASE gene family: (II) kernel abscission, environmental stress and myo-inositol influences accumulation of transcript in developing seeds and callus cells. Physiologia Plantarum 121, 647-655.
57. Zivkovic T, Quartacci MF, Stevanovic B, Marinone F, Navari-Izzo F. 2005. Low-molecular weight substances in the poikilohydric plant Ramonda serbica during dehydration and rehydration. Plant Science 168, 105-111.