Advertisement

A comparison of partial dehydration and hydrated storage-induced changes in viability, reactive oxygen species production, and glutathione metabolism in two contrasting recalcitrant-seeded species

  • Anushka Moothoo-Padayachie
  • Boby Varghese
  • N. W. Pammenter
  • Patrick Govender
  • SershenEmail author
Original Article
  • 201 Downloads

Abstract

This study compared the responses of Avicennia marina and Trichilia dregeana seeds, both of which are recalcitrant, to partial dehydration and storage. Seeds of A. marina exhibited a faster rate of water and viability loss (± 50% viability loss in 4 days) during partial dehydration, compared with T. dregeana (± 50% viability loss in 14 days). In A. marina embryonic axes, reactive oxygen species (ROS) production peaked on 4 days of dehydration and was accompanied by an increase in the GSH:GSSG ratio; it appears that the glutathione system alone could not overcome dehydration-induced oxidative stress in this species. In A. marina, ROS and axis water content levels increased during hydrated storage and were accompanied by a decline in the GSH:GSSG ratio and rapid viability loss. In T. dregeana embryonic axes, ROS production (particularly hydrogen peroxide) initially increased and thereafter decreased during both partial dehydration and hydrated storage. Unlike in A. marina embryonic axes, this reduced ROS production was accompanied by a decline in the GSH:GSSG ratio. While T. dregeana seeds may have incurred some oxidative stress during storage, a delay in and/or suppression of the ROS-based trigger for germination may account for their significantly longer storage longevity compared with A. marina. Mechanisms of desiccation-induced seed viability loss may differ across recalcitrant-seeded species based on the rate and extent to which they lose water during partial drying and storage. While recalcitrant seed desiccation sensitivity and, by implication, storage longevity are modulated by redox metabolism, the specific ROS and antioxidants that contribute to this control may differ across species.

Keywords

Avicennia marina Partial dehydration Reactive oxygen species Recalcitrant Storage Trichilia dregeana 

Notes

Acknowledgements

We thank the National Research Foundation (NRF) of South Africa, and Deutscher Akademischer Austauschdienst, Germany, for their financial support to A. Moothoo-Padayachie, and to the NRF for a research grant awarded to Sershen.

References

  1. Berjak P, Pammenter NW (2008) From Avicennia to Zizania: seed recalcitrance in perspective. Ann Bot 101:213–228CrossRefGoogle Scholar
  2. Berjak P, Pammenter NW (2013) Implications of the lack of desiccation tolerance in recalcitrant seeds. Front Plant Sci 4(478):1–9.  https://doi.org/10.3389/fpls.2013.00478 CrossRefGoogle Scholar
  3. Calistru C, Mclean M, Pammenter NW, Berjak P (2000) The effects of mycofloral infection on the viability and ultrastructure of wet-stored recalcitrant seeds of Avicennia marina (Forssk.) Vierh. Seed Sci Res 10:341–353CrossRefGoogle Scholar
  4. Chaitanya KSK, Naithani SC (1994) Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn. f. New Phytol 126:623–627CrossRefGoogle Scholar
  5. Connor KF, Bonner FT, Vozzo JA (1996) Effects of desiccation on temperate recalcitrant seeds: differential scanning calorimetry, gas chromatography, electron microscopy, and moisture studies on Quercus nigra and Quercus alba. Can J For Res 26:1813–1821CrossRefGoogle Scholar
  6. Ellis RH, Roberts EH (1981) The quantification of ageing and survival in orthodox seeds. Seed Sci Technol 9:373–409Google Scholar
  7. Farrant JM, Pammenter NW, Berjak P (1986) The increasing desiccation sensitivity of recalcitrant Avicennia marina seeds with storage time. Physiol Plant 67:291–298CrossRefGoogle Scholar
  8. Farrant JM, Pammenter NW, Berjak P (1989) Germination-associated events and the desiccation sensitivity of recalcitrant seeds—a study on three unrelated species. Planta 178:189–198CrossRefGoogle Scholar
  9. Farrant JM, Berjak P, Pammenter NW (1993) Studies on the development of the desiccation-sensitive (recalcitrant) seeds of Avicennia marina (Forssk.)Vierh.: the acquisition of germinability and response to storage and dehydration. Ann Bot 71:405–410CrossRefGoogle Scholar
  10. Finch-Savage WE (1992) Seed development in the recalcitrant species Quercus robur L: germinability and desiccation tolerance. Seed Sci Res 2:17–22CrossRefGoogle Scholar
  11. Finch-Savage WE, Pramanik SK, Bewley JD (1994) The expression of dehydrin proteins in desiccation-sensitive (recalcitrant) seeds of temperate trees. Planta 193:478–485CrossRefGoogle Scholar
  12. Garnczarska M (2008) Ascorbate and glutathione metabolism in embryo axes and cotyledons of germinating lupine seeds. Biol Plant 52:681–686CrossRefGoogle Scholar
  13. Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220CrossRefGoogle Scholar
  14. Goveia M, Kioko JI, Berjak P (2004) Developmental status is a critical factor in the selection of excised recalcitrant axes as explants for cryopreservation: a study on Trichilia dregeana Sond. Seed Sci Res 14:241–248CrossRefGoogle Scholar
  15. Kioko JI, Berjak P, Pammenter NW (2006) Viability and ultrastructural responses of seeds and embryonic axes of Trichilia emetica to different dehydration and storage conditions. S Afr J Bot 72:167–176CrossRefGoogle Scholar
  16. Kranner I, Grill D (1993) Content of low-molecular-weight thiols during the imbibition of pea seeds. Physiol Plant 88:557–562CrossRefGoogle Scholar
  17. Kranner I, Birtic S, Anderson KM, Pritchard HW (2006) Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radic Biol Med 40:2155–2165CrossRefGoogle Scholar
  18. Leprince O, Buitink J, Hoekstra FA (1999) Axes and cotyledons of recalcitrant seeds of Castanea sativa Mill. exhibit contrasting responses of respiration to drying in relation to desiccation sensitivity. J Exp Bot 338:1515–1524CrossRefGoogle Scholar
  19. Li C, Sun WQ (1999) Desiccation sensitivity and activities of free radical-scavenging enzymes in recalcitrant Theobroma cacao seeds. Seed Sci Res 9:209–217CrossRefGoogle Scholar
  20. Lin T, Chen M (1995) Biochemical characteristics associated with the development of the desiccation-sensitive seeds of Machilus thunbergii Sieb. & Zucc. Ann Bot 76:381–387CrossRefGoogle Scholar
  21. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175Google Scholar
  22. Moothoo-Padayachie A, Varghese B, Pammenter NW, Govender P, Sershen (2016) Germination associated ROS production and glutathione redox capacity in two recalcitrant-seeded species differing in seed longevity. Botany 94:1103–1114CrossRefGoogle Scholar
  23. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49(249–279):49Google Scholar
  24. Normah MN, Ramiya SD, Gintangga M (1997) Desiccation sensitivity of recalcitrant seeds—a study on tropical fruit species. Seed Sci Res 7:179–184CrossRefGoogle Scholar
  25. Oracz K, Bouteau HE, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50:452–465CrossRefGoogle Scholar
  26. Pammenter NW, Berjak P (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Sci Res 9:13–38CrossRefGoogle Scholar
  27. Pammenter NW, Berjak P, Farrant JM, Smith MT, Ross G (1994) Why do stored hydrated recalcitrant seeds die? Seed Sci Res 4:187–191CrossRefGoogle Scholar
  28. Pammenter NW, Greggains V, Kioko JI, Wesley-Smith J, Berjak P, Finch-Savage WE (1998) Effects of differential drying rates on viability retention of recalcitrant seeds of Ekebergia capensis. Seed Sci Res 8:463–471CrossRefGoogle Scholar
  29. Pukacka S, Ratajczak E (2006) Antioxidative response of ascorbate–glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds. J Plant Physiol 163:1259–1266CrossRefGoogle Scholar
  30. Roach T, Ivanova M, Beckett RP, Minibayeva FV, Green I, Pritchard HW, Kranner I (2008) An oxidative burst of superoxide in embryonic axes of recalcitrant sweet chestnut seeds as induced by excision and desiccation. Physiol Plant 133:131–139CrossRefGoogle Scholar
  31. Roach T, Beckett RP, Minibayeva FV, Colville L, Whitaker C, Chen H, Bailly C, Kranner I (2010) Extracellular superoxide production, viability and redox poise in response to desiccation in recalcitrant Castanea sativa seeds. Plant Cell Environ 33:59–75PubMedGoogle Scholar
  32. Roberts EH (1973) Predicitng the storage life of seeds. Seed Sci Technol 1:499–514Google Scholar
  33. Sershen Varghese B, Naidoo C, Pammenter NW (2016) The use of plant stress biomarkers in assessing the effects of desiccation in zygotic embryos from recalcitrant seeds: challenges and considerations. Plant Biol 18:433–444CrossRefGoogle Scholar
  34. Tommasi F, Paciolla C, De Pinto MC, De Gara L (2001) A comparative study of glutathione and ascorbate metabolism during germination of Pinus pinea L. seeds. J Exp Bot 52:1647–1654CrossRefGoogle Scholar
  35. Tommasi F, Paciolla C, de Pinto MC, De Gara L (2006) Effects of storage temperature on viability, germination and antioxidant metabolism in Ginkgo biloba L. seeds. Plant Physiol Biochem 44:359–368CrossRefGoogle Scholar
  36. Varghese B, Naithani SC (2002) Desiccation-induced changes in lipid peroxidation, superoxide level and antioxidant enzymes activity in neem (Azadirachta indica A. Juss) seeds. Acta Physiol Plant 24:79–87CrossRefGoogle Scholar
  37. Varghese B, Sershen A, Berjak P, Varghese D, Pammenter NW (2011) Differential drying rates of recalcitrant Trichilia dregeana embryonic axes: a study of survival and oxidative stress metabolism. Physiol Plant 142:326–338CrossRefGoogle Scholar
  38. Woodenberg WR, Berjak P, Pammenter NW (2010) Development of cycad ovules and seeds. 1. Implication of the ER in primary cellularisation of the megagametophyte in Encephalartos natalensis Dyer and Verdoorn. J Plant Growth Regul 62:265–278CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of KwaZulu-NatalDurbanSouth Africa

Personalised recommendations