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Protoplasma

, Volume 255, Issue 5, pp 1461–1475 | Cite as

Zygotic embryo cell wall responses to drying in three gymnosperm species differing in seed desiccation sensitivity

  • Wynston Ray Woodenberg
  • Sershen
  • Boby Varghese
  • Norman Pammenter
Original Article

Abstract

Plant cell walls (CWs) are dynamic in that they can change conformation during ontogeny and in response to various stresses. Though seeds are the main propagatory units of higher plants, little is known of the conformational responses of zygotic embryo CWs to drying. This study employed cryo-scanning electron microscopy to compare the effects of desiccation on zygotic embryo CW morphology across three gymnosperm species that were shown here to differ in seed desiccation sensitivity: Podocarpus henkelii (highly desiccation-sensitive), Podocarpus falcatus (moderately desiccation-sensitive), and Pinus elliottii (desiccation-tolerant). Fresh/imbibed (i.e. fresh Podocarpus at shedding and imbibed Pi. elliottii) embryos showed polyhedral cells with regular walls, typical of turgid cells with an intact plasmalemma. Upon desiccation to c. 0.05 g g−1 (dry mass basis), CWs assumed an undulating conformation, the severity of which appeared to depend on the amount and type of dry matter accumulated. After desiccation, intercellular spaces between cortical cells in all species were comparably enlarged relative to those of fresh/imbibed embryos. After rehydration, meristematic and cotyledonary CWs of P. henkelii and meristematic CWs of P. falcatus remained slightly undulated, suggestive of plasmalemma and/or CW damage, while those of Pi. elliottii returned to their original conformation. Cell areas in dried-rehydrated P. henkelii root meristem and cotyledon were also significantly lower than those from fresh embryos, suggesting incomplete recovery, even though embryo water contents were comparable between the two states. Electrolyte leakage measurements suggest that the two desiccation-sensitive species incurred significant plasmalemma damage relative to the tolerant species upon desiccation, in agreement with the CW abnormalities observed in these species after rehydration. Immunocytochemistry studies revealed that of the four CW epitopes common to embryos of all three species, an increase in arabinan (LM6) upon desiccation and rehydration in desiccation-tolerant Pi. elliottii was the only difference, although this was not statistically significant. Seed desiccation sensitivity in species like P. henkelii and P. falcatus may therefore be partly based on the inability of the plasmalemma and consequently CWs of dried embryos to regain their original conformation following rehydration.

Keywords

Cell wall Cryo-SEM Desiccation sensitivity Gymnosperm Seed Zygotic embryo 

Notes

Acknowledgements

We thank Vishal Bharuth and Nelisha Murugan of the Microscopy and Microanalysis Unit, University of KwaZulu-Natal, for the assistance with the cryo-SEM. Thanks are also due to Sappi Seed Centre for the donation of Pi. elliottii seeds and to Minoli Appalasamy for the assistance with the statistics.

Funding information

The National Research Foundation of South Africa and the Claude Leon Foundation, South Africa, funded this project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Albersheim P, Jones TM, English PD (1969) Biochemistry of the cell wall in relation to infective processes. Annu Rev Phytopathol 7:171–194CrossRefPubMedGoogle Scholar
  2. Baluška F, Šamaj J, Wojtaszek P, Volkmann D, Menzel D (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol 133:482–491CrossRefPubMedPubMedCentralGoogle Scholar
  3. Barnett JP, Vozzo JA (1985) Viability and vigour of slash and shortleaf pine seeds after 50 years of storage. For Sci 31:316–320Google Scholar
  4. Berjak P, Dini M, Pammenter NW (1984) Possible mechanisms underlying the differing dehydration responses in recalcitrant and orthodox seeds: desiccation-associated subcellular changes in propagules of Avicennia marina. Seed Sci Technol 12:365–384Google Scholar
  5. Bewley JD (1979) Physiological aspects of desiccation tolerance. Annu Rev Plant Physiol 30:195–238CrossRefGoogle Scholar
  6. Boudart G, Lafitte C, Barthe JP, Frasez D, Esquerré-Tugayé MT (1998) Differential elicitation of defense responses by pectic fragments in bean seedlings. Planta 206:86–94CrossRefGoogle Scholar
  7. 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
  8. Cardemil L, Riquelme A (1991) Expression of cell wall proteins in seeds and during early seedling growth of Araucaria araucana is a response to wound stress and is developmentally regulated. J Exp Bot 42:415–421CrossRefGoogle Scholar
  9. Carpita N, Ralph J, McCann MC (2000) The cell wall. In: Buchanan BB, Wilhelm G, Jones RL (eds) Biochemistry and molecular biology of plants. John Wiley and Sons, Hoboken, pp 45–109Google Scholar
  10. Dodd MC, Van Staden J, Smith MT (1989) Seed development in Podocarpus henkelii: an ultrastructural and biochemical study. Ann Bot 64:297–310CrossRefGoogle Scholar
  11. Ellis RH, Roberts EH (1980) Improved equations for the prediction of seed longevity. Ann Bot 45:13–30CrossRefGoogle Scholar
  12. Farrant JM (2000) A comparison of patterns of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecol 151:29–39CrossRefGoogle Scholar
  13. Farrant JM, Pammenter NW, Berjak P, Walters C (1997) Subcellular organization and metabolic activity during the development of seeds that attain different levels of desiccation tolerance. Seed Sci Res 7:135–144CrossRefGoogle Scholar
  14. Giarola V, Krey S, Driesch B, Bartels D (2016) The Craterostigma plantagineum glycine-rich protein CpGRP1 interacts with a cell wall-associated protein kinase 1 (CpWAK1) and accumulates in leaf cell walls during dehydration. New Phytol 210:535–550CrossRefPubMedGoogle Scholar
  15. Gomez LD, Steele-King CG, Jones L, Foster JM, Vuttipongchaikij S, McQueen-Mason SJ (2009) Arabinan metabolism during seed development and germination in Arabidopsis. Mol Plant 2:966–976CrossRefPubMedGoogle Scholar
  16. Humphrey TV, Bonetta DT, Goring DR (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytol 176:7–21CrossRefPubMedGoogle Scholar
  17. Jarvis MC (1998) Intercellular separation forces generated by intracellular pressure. Plant Cell Environ 21:1307–1310CrossRefGoogle Scholar
  18. Jarvis MC, Briggs SPH, Knox JP (2003) Intercellular adhesion and cell separation in plants. Plant Cell Environ 26:977–989CrossRefGoogle Scholar
  19. Merced A, Renzaglia K (2014) Developmental changes in guard cell wall structure and pectin composition in the moss Funaria: implications for function and evolution of stomata. Ann Bot 114:1001–1010CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 Physiol 141:651–662CrossRefPubMedPubMedCentralGoogle Scholar
  21. Moore JP, Nguema-Ona EE, Vicré-Gibouin M, Sørensen I, Willats WG, Driouich A, Farrant JM (2013) Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237:739–754CrossRefPubMedGoogle Scholar
  22. Mycock DJ, Berjak P, Finch-Savage WE (2000) Effects of desiccation on the subcellular matrix of the embryonic axes of Quercus robur. In: Bradford KJ, Chen F, Cooley MB et al (eds) Seed biology: advances and applications. CABI Publishing, Wallingford, pp 197–203Google Scholar
  23. Negash L (1992) In vitro methods for the rapid germination of seeds of Podocarpus falcatus. SINET Ethiopian J Sci 15:85–97Google Scholar
  24. Pammenter NW, Berjak P (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Sci Res 9:13–38CrossRefGoogle Scholar
  25. Perán R, Pammenter NW, Naicker J, Berjak P (2004) The influence of rehydration technique on the response of recalcitrant seed embryos to desiccation. Seed Sci Res 14:179–184CrossRefGoogle Scholar
  26. Reiter WD (2002) Biosynthesis and properties of the plant cell wall. Curr Opin Plant Biol 5:536–542CrossRefPubMedGoogle Scholar
  27. Roberts EH (1973) Predicting the viability of seeds. Seed Sci Technol 1:499–514Google Scholar
  28. Sacandé M, Golovina EA, van Aelst AC, Hoekstra FA (2001) Viability loss of neem (Azadirachta indica) seeds associated with membrane phase behaviour. J Exp Bot 52:919–931CrossRefPubMedGoogle Scholar
  29. Sarkar P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot 60:3615–3635CrossRefPubMedGoogle Scholar
  30. Sershen BP, Pammenter NW, Wesley-Smith J (2012) Rate of dehydration, state of subcellular organisation and nature of cryoprotection are critical factors contributing to the variable success of cryopreservation: studies on recalcitrant zygotic embryos of Haemanthus montanus. Protoplasma 249:171–186CrossRefPubMedGoogle Scholar
  31. 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 18:433–444CrossRefPubMedGoogle Scholar
  32. Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459CrossRefGoogle Scholar
  33. Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Mol Struct Res 26:31–43CrossRefGoogle Scholar
  34. Tetteroo FA, Hoekstra FA, Karssen CM (1995) Induction of complete desiccation tolerance in carrot (Daucus carota) embryoids. J Plant Physiol 145:349–356CrossRefGoogle Scholar
  35. Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862CrossRefPubMedGoogle Scholar
  36. Vertucci CW, Farrant JM (1995) Acquisition and loss of desiccation-tolerance. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, New York, pp 237–271Google Scholar
  37. Wakabayashi K, Hoson T, Kamisaka S (1997) Osmotic stress suppresses cell wall stiffening and the increase in cell wall-bound ferulic and diferulic acids in wheat coleoptiles. Plant Physiol 113:967–973CrossRefPubMedPubMedCentralGoogle Scholar
  38. Walters C (2015) Orthodoxy, recalcitrance and in-between: describing variation in seed storage characteristics using threshold responses to water loss. Planta 242:397–406CrossRefPubMedGoogle Scholar
  39. Walters C, Farrant JM, Pammenter NW, Berjak P (2002) Desiccation stress and damage. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, pp 263–291CrossRefGoogle Scholar
  40. Webb MA, Arnott HJ (1982) Cell wall conformation in dry seeds in relation to the preservation of structural integrity during desiccation. Am J Bot 69:1657–1668CrossRefGoogle Scholar
  41. Weiser RL, Wallner SJ, Waddell JW (1990) Cell wall and extensin mRNA changes during cold acclimation of pea seedlings. Plant Physiol 93:1021–1026CrossRefPubMedPubMedCentralGoogle Scholar
  42. Willats WG, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1→ 5)-α-L-arabinan. Carbohydr Res 308:149–152CrossRefPubMedGoogle Scholar
  43. Woodenberg WR, Berjak P, Pammenter NW, Farrant JM (2014) Development of cycad ovules and seeds. 2. Histological and ultrastructural aspects of ontogeny of the embryo in Encephalartos natalensis (Zamiaceae). Protoplasma 251:797–816CrossRefPubMedGoogle Scholar
  44. Woodenberg WR, Pammenter NW, Farrant JM, Driouich A, Berjak P (2015) Embryo cell wall properties in relation to development and desiccation in the recalcitrant-seeded Encephalartos natalensis (Zamiaceae) Dyer and Verdoorn. Protoplasma 252:245–258CrossRefPubMedGoogle Scholar
  45. Zwiazek JJ (1991) Cell wall changes in white spruce (Picea glauca) needles subjected to repeated drought stress. Physiol Plant 82:513–518CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Wynston Ray Woodenberg
    • 1
  • Sershen
    • 1
  • Boby Varghese
    • 1
  • Norman Pammenter
    • 1
  1. 1.School of Life SciencesUniversity of KwaZulu-NatalDurbanSouth Africa

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