Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Ascorbate and glutathione metabolism during development and desiccation of orthodox and recalcitrant seeds of the genus Acer

Stanislawa Pukacka A B and Ewelina Ratajczak A
+ Author Affiliations
- Author Affiliations

A Seed Biochemistry Laboratory, Institute of Dendrology, Polish Academy of Sciences, 62-035 Kórnik, Poland.

B Corresponding author. Email: spukacka@man.poznan.pl

Functional Plant Biology 34(7) 601-613 https://doi.org/10.1071/FP07013
Submitted: 20 January 2007  Accepted: 4 April 2007   Published: 4 July 2007

Abstract

The ascorbate–glutathione system was studied during development and desiccation of seeds of two Acer species differing in desiccation tolerance: Norway maple (Acer platanoides L., orthodox) and sycamore (Acer pseudoplatanus L., recalcitrant). The results showed remarkable differences in the concentration and redox balance of ascorbate and glutathione between these two kinds of seeds during development, and a significant dependence between glutathione content and acquisition of desiccation tolerance in Norway maple seeds. There were relatively small differences between the species in the activities of enzymes of the ascorbate–glutathione cycle: ascorbate peroxidase (APX, EC 1.11.1.11), monodehydroascorbate reductase (MR, EC 1.6.5.4), dehydroascorbate reductase (DHAR, EC 1.8.5.1), and glutathione reductase (GR, EC 1.6.4.2). At the end of seed maturation, ascorbic acid content and the activities of the above enzymes was about the same in both species The electrophoretic pattern of APX isoenzymes was also similar for both species, and the intensity of the bands decreased at the end of seed maturation in both species. When sycamore seeds were desiccated to a moisture content of less than 26%, there was a marked decrease in seed viability and an increase in the production of reactive oxygen species. During desiccation, Norway maple seeds had a more active defence system, which was reflected in a higher glutathione content, a higher glutathione redox status, a higher ascorbate redox status, and higher activities of APX, MR, DHAR, GR and GPX (glutathione peroxidase). During desiccation, sulfhydryl-to-disulfide transition into proteins was more intense in Norway maple seeds than sycamore seeds. All of these results suggest that, in orthodox seeds, the ascorbate–glutathione cycle plays an important role in the acquisition of tolerance to desiccation, in protein maturation, and in protection from reactive oxygen species.

Additional keywords: ascorbic acid, ascorbate peroxidase, dehydroascorbate reducrase, glutathione reductase, monodehydroascorbate reductase, redox balance.


Acknowledgements

This study was supported by research funds of the Polish Ministry of Sciences and Education.


References


Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radical Biology & Medicine 23, 473–479.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Arrigoni O (1994) Ascorbate system in plant development. Journal of Bioenergetics and Biomembranes 26, 407–419.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Arrigoni O, De Gara L, Tommasi F, Liso R (1992) Changes in ascorbate system during seed development of Vicia faba L. Plant Physiology 99, 235–238.
PubMed |
open url image1

Bailly C (2004) Active oxygen species and antioxidants in seeds biology. Seed Science Research 14, 93–107.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bailly C, Audigier A, Ladonne F, Wagner MH, Coste F, Corbineau F, Côme D (2001) Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. Journal of Experimental Botany 52, 701–708.
PubMed |
open url image1

Bailly C , Leymarie J , Rousseau S , Côme D , Corbineau F (2003) Sunflower seed development as related to antioxidant enzyme activities. In ‘The biology of seeds: recent research advances’. (Eds G. Nicolas, K.J. Bradford, D. Côme, H.W. Prithard) pp. 69–75. (CABI Publishing: Wallingford, UK)

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

Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annual Review of Plant Biology 56, 187–220.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Daws MI, Cleland H, Chmielarz P, Gorian F, Leprince O, Mullins CE, Thanos CA, Vandvik V, Pritchard HW (2006) Variable desiccation tolerance in Acer pseudoplatanus seeds in relation to developmental conditions: a case of phenotypic recalcitrance? Functional Plant Biology 33, 59–66.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Gara L, de Pinto MC, Moliterni VMC, D’Egidio MG (2003) Redox regulation and storage processes during maturation in kernels of Triticum durum. Journal of Experimental Botany 54, 249–258.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

De Gara L, Paciolla C, De Tullio MC, Motto M, Arrigoni O (2000) Ascorbate-dependent hydrogen peroxide detoxification and ascorbate regeneration during germination of a highly productive maize hybrid: evidence of an improved detoxification mechanism against reactive oxygen species. Physiologia Plantarum 109, 7–13.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Tullio MC, Arrigoni O (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Science Research 13, 249–260.
Crossref | GoogleScholarGoogle Scholar | open url image1

Desikan R , Hancock JT , Neill SJ (2005) Reactive oxygen species as signalling molecules. In ‘Antioxidants and reactive oxygen species in plants’. (Ed. N. Smirnoff) pp. 169–197. (Blackwell Publishing: New York)

Dickie JB, May K, Morris SVA, Titley SE (1991) The effect of desiccation on seed survival in Acer platanoides L. and Acer pseudoplatanus L. Seed Science Research 1, 149–162. open url image1

Doke N (1983) Generation of superoxide anion by potato tuber protoplasts during the hypersensitive response to hyphal wall components of Phytophthora infestans and specific inhibition of the reaction by suppressors of hypersensitivity. Physiological Plant Pathology 23, 359–367. open url image1

Esterbauer H, Grill D (1978) Seasonal variation of glutathione and glutathione reductase in needles of Picea abies. Plant Physiology 61, 119–121.
PubMed |
open url image1

Foyer CH, Noctor G (2003) Redox sensing and signaling associated with reactive oxygen in chloroplast, peroxisomes and mitochondria. Physiologia Plantarum 119, 355–364.
Crossref | GoogleScholarGoogle Scholar | open url image1

Foyer CH, Descouvrières P, Kunert KJ (1997) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant, Cell & Environment 1717, 507–523. open url image1

Greggains V, Finch-Savage WE, Quick WP, Atherton NM (2000) Putative desiccation tolerance mechanisms in orthodox and recalcitrant seeds of the genus Acer. Seed Science Research 10, 317–327. open url image1

Helmerhorst E, Stokes GB (1980) Microcentrifuge desalting: a rapid, quantitative method for desalting small amounts of protein. Analytical Biochemistry 104, 130–135.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hong TD, Ellis RH (1990) A comparison of maturation drying, germination and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytologist 116, 589–596.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jahnel H (1955) The stratification of forest seed. Angewante Botany 29, 139–141. open url image1

Kampfenkel K, Van Montagu M, Inzé D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225, 165–167.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kobrehel K, Wong JH, Balogh A, Kiss F, Yee BC, Buchanan BB (1992) Specific reduction of wheat storage proteins by thioredoxin h. Plant Physiology 99, 919–924.
PubMed |
open url image1

Kranner I, Grill D (1993) Content of low-molecular weight thiols during the imbibition of pea seeds. Physiologia Plantarum 88, 557–562.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kranner I, Birtić S, Anderson KM, Pritchard HW (2006) Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radical Biology & Medicine 40, 2155–2165.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Science 159, 75–85.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leprince O, Hendry GAF, McKersie BD (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Science Research 3, 231–246. open url image1

Liso R, Calabrese G, Bitonti MB, Arrigoni O (1984) Relationship between ascorbic acid and cell division. Experimental Cell Research 150, 314–320.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880. open url image1

Nagalakshmi N, Prasad MNV (2001) Responses of glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Science 160, 291–299.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Paciolla C, De Tullio MC, Chiappetta A, Innocenti AM, Bitonti MB, Liso R, Arrigoni O (2001) Short- and long-term effects of dehydroascorbate on Lupinus albus and Allium cepa roots. Plant & Cell Physiology 42, 857–863.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Padh H (1990) Cellular function of ascorbic acid. Biochemistry and Cell Biology 68, 1166–1173.
PubMed |
open url image1

Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ, Noctor G, Foyer CH (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. The Plant Cell 15, 939–951.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Potters G, De Gara L, Asrad H, Horemans N (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537–548.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pukacka S (1998) The characteristics of the seed development of Norway maple (Acer platanoides L.) and sycamore (Acer pseudoplatanus L.). Arboretum Kórnickie [in polish] 43, 97–104. open url image1

Pukacka S, Czubak A (1998) The effect of desiccation on viability and membrane lipid composition of Acer pseudoplatanus seeds. Acta Societatis Botanicorum Poloniae 67, 249–252. open url image1

Pukacka S, Pukacki PM (1997) Changes in soluble sugars in relation to desiccation tolerance and effect of dehydration on freezing characteristics of Acer platanoides and Acer pseudoplatanus seeds. Acta Physiologiae Plantarum 19, 147–154.
Crossref |
open url image1

Pukacka S, Wójkiewicz E (2002) Carbohydrate metabolism in Norway maple and sycamore seeds in relation to desiccation tolerance. Journal of Plant Physiology 159, 273–279.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pukacka S, Wójkiewicz E (2003) The effect of temperature of drying on viability and some factors affecting storability of Fagus sylvatica seeds. Acta Physiologiae Plantarum 25, 163–169.
Crossref |
open url image1

Pukacka S, Ratajczak E (2006) Antioxidative response of ascorbate-glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds. Journal of Plant Physiology 163, 1259–1266.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sagisaka S (1976) The occurrence of peroxide in a perennial plant Populus gelrica. Plant Physiology 57, 308–309.
PubMed |
open url image1

Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and non-protein sulfhydryl groups in tissue by Ellman’s reagent. Analytical Biochemistry 25, 192–205.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schafer FQ, Beuttner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biology & Medicine 30, 1191–1212.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith I (1985) Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiology 79, 1044–1047.
PubMed |
open url image1

Tommasi F, Paciolla C, Arrigoni O (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiologia Plantarum 105, 193–198.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Zhang J, Kirkham MB (1996) Enzymatic response of the ascorbate-glutathione cycle to drought in sorghum and sunflower plants. Plant Science 113, 139–147.
Crossref | GoogleScholarGoogle Scholar | open url image1