Skip to main content
SpringerLink
Log in

Cytological and physiological changes related to cryotolerance in orthodox maize embryos during seed development

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Cytological and physiological changes were studied in orthodox maize (Zea mays L.) embryos following the acquisition of cryotolerance to liquid nitrogen during seed development. It was found that the embryonic cells at radicle portion were hydrated at all stages investigated, but those at early stages contained fully functional organelles, which disappeared at last developmental stages, and reserve materials accumulated intensively during seed development. Total soluble sugar content in the embryos had a steady rise on fresh weight and moisture weight basis; meanwhile, soluble and heat-stable proteins increased progressively in their number and contents as embryos matured. These cytological and biochemical changes had good correspondence with acquisition of cryotolerance in maize embryos.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

DAP:

Days after pollination

W50FS :

The upper limit of moisture content allowing 50% postthaw embryos to survive

References

  • Bartels D, Singh M, Salamini F (1988) Onset of desiccation tolerance during development of the barley embryo. Planta 175:485–492. doi:10.1007/BF00393069

    Article  CAS  Google Scholar 

  • Berjak P, Pammenter NW (2008) From Avicennia to Zizania: seed recalcitrance in perspective. Ann Bot (Lond) 101:213–228. doi:10.1093/aob/mcm168

    Article  Google Scholar 

  • Bernac P, Horbowicz M, Downer SM, Dickerman AM, Smith ME, Obendore RL (1997) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. J Plant Physiol 150:481–488

    Google Scholar 

  • Bewley JD, Black M (1994) Seeds, physiology of development, germination. Plenum, New York

    Google Scholar 

  • Black M, Corbineau F, Gee H, Côme D (1999) Water content, raffinose and dehydrins in the induction of desiccation tolerance in immature wheat embryos. Plant Physiol 120:463–471. doi:10.1104/pp.120.2.463

    Article  PubMed  CAS  Google Scholar 

  • Blackman SA, Wettlaufer SH, Obendorf RL, Leopold AC (1991) Maturation proteins associated with desiccation tolerance in soybean. Plant Physiol 96:868–874. doi:10.1104/pp.96.3.868

    Article  PubMed  CAS  Google Scholar 

  • Blackman SA, Obendorf RL, Leopold AC (1992) Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiol 100:225–230. doi:10.1104/pp.100.1.225

    Article  PubMed  CAS  Google Scholar 

  • Bochicchio A, Vazzana C, Raschi A, Bartels D, Salamini F (1988) Effects of desiccation on isolated embryos of maize. Onset of desiccation tolerance during development. Agronomie 8:29–36. doi:10.1051/agro:19880104

    Article  Google Scholar 

  • Bochicchio A, Vazzana C, Velasco R, Singh M, Bartels D (1991) Exogenous ABA induces desiccation tolerance and leads to the synthesis of specific gen transcripts in immature embryos of maze. Maydica 39:11–16

    Google Scholar 

  • Bochicchio A, Vernieri P, Puliga S, Balducci F, Vazzana C (1994) Acquisition of desiccation tolerance by isolated maize embryos exposed to different conditions: the questionable role of endogenous abscisic acid. Physiol Plant 91:615–622. doi:10.1111/j.1399-3054.1994.tb02996.x

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  • Brown MJ, Hor YL, Greenwood JS (2001) Reserve accumulation and protein storage vacuole formation during development of recalcitrant seeds of Durio zibethinus L. Seed Sci Res 11:293–303

    CAS  Google Scholar 

  • Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228. doi:10.1016/j.cryobiol.2004.02.011

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Burris JS (1990) Role of carbohydrates in desiccation tolerance and membrane behaviour in maturing maize seed. Crop Sci 30:971–975

    CAS  Google Scholar 

  • Cordova-Tellez L, Burris JS (2002) Alignment of lipid bodies along the plasma membrane during the acquisition of desiccation tolerance in maize seed. Crop Sci 42:1982–1988

    Google Scholar 

  • Crèvecoeur M, Deltour R, Bronchart R (1976) Cytological study on water stress during germination of Zea mays. Planta 132:31–41. doi:10.1007/BF00390328

    Article  Google Scholar 

  • Crowe JH, Crowe LM, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipids bilayers and proteins by sugars. Biochem J 242:1–10

    PubMed  CAS  Google Scholar 

  • Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599. doi:10.1146/annurev.ph.54.030192.003051

    Article  PubMed  CAS  Google Scholar 

  • Daws MI, Pritchard HW (2008) The development and limits of freezing tolerance in Acer pseudoplatanus fruits across Europe is dependent on provenance. Cryo Lett 29:189–198

    CAS  Google Scholar 

  • Dodd MC, van Staden JV, Smith MT (1989) Seed development in Podocarpus henelii: an ultrastructural and biochemical study. Ann Bot (Lond) 64:297–310

    Google Scholar 

  • Fairbairn NJ (1953) A modified anthrone reagent. Chem Ind 31:72–86

    Google Scholar 

  • Farrant JM, Walters C (1998) Ultrastructural and biophysical changes in developing embryos of Aesculus hippocastanum in relation to the acquisition of tolerance to drying. Physiol Plant 104:513–524. doi:10.1034/j.1399-3054.1998.1040401.x

    Article  CAS  Google Scholar 

  • Huang H (2008) Analysis on reactive oxygen species scavenging enzymes and proteome associated with changes of desiccation tolerance of maize seeds. Ph.D. thesis of Graduate School, Chinese Academy of Sciences, Beijing, China

  • Iljin WS (1957) Drought resistance in plants and physiological processes. Annu Rev Plant Physiol 8:257–274. doi:10.1146/annurev.pp 08.060157.001353

    Article  CAS  Google Scholar 

  • Isaaca C, Mycock D (1999) Ultrastructural effects of early imbibition and cryostorage on Zea mays L. root meristems. Cryo Lett 20:183–192

    Google Scholar 

  • Jitsuyama Y, Suzuki T, Fujikawa S (2002) Sucrose incubation increases freezing tolerance of asparagus (Asparagus officinalis L.) embryogenic cell suspensions. Cryo Lett 23:103–112

    CAS  Google Scholar 

  • Klein S, Pollock B (1968) Cell fine structure of developing lima bean seeds related to seed desiccation. Am J Bot 55:658–672. doi:10.2307/2440523

    Article  Google Scholar 

  • Leprince O, Bronchart R, Deltour R (1990) Changes in starch and soluble sugars in relation to the acquisition of desiccation tolerance during maturation of Brassica campestris seed. Plant Cell Environ 13:539–546. doi:10.1111/j.1365-3040.1990.tb01070.x

    Article  CAS  Google Scholar 

  • Lin C, Guo W, Everson E, Thomashow MF (1990) Cold acclimation in Arabidopsis and wheat. A response associated with expression of related genes encoding ‘boiling-stable’ polypeptides. Plant Physiol 94:1078–1083. doi:10.1104/pp.94.3.1078

    Article  PubMed  CAS  Google Scholar 

  • Nagao M, Arakawa K, Takezawa D, Fujikawa S (2008) Long- and short-term freezing induce different types of injury in Arabidopsis thaliana leaf cells. Planta 227:477–489. doi:10.1007/s00425-007-0633-9

    Article  PubMed  CAS  Google Scholar 

  • Ooms JJJ, Wilmer JA, Karssen CM (1994) Carbohydrates are not the sole factor determining desiccation tolerance in seeds of Arabidopsis thaliana. Physiol Plant 90:431–436. doi:10.1111/j.1399-3054.1994.tb08798.x

    Article  CAS  Google Scholar 

  • Pammenter NW, Berjak P (1999) A review of recalcitrant seed physiology in relation to desiccation- tolerance mechanisms. Seed Sci Res 9:13–37

    Google Scholar 

  • Perdomo A, Burris JS (1998) Histochemical, physiological and ultrastructural changes in the maize embryo during artificial drying. Crop Sci 38:1236–1244

    Google Scholar 

  • Pomeroy MK, Siminovitch D (1971) Seasonal cytological changes in secondary phloem parenchyma cells in Robinia pseudoacacia in relation to cold hardiness. Can J Bot 49:787–800. doi:10.1139/b71-118

    Article  Google Scholar 

  • Pritchard HW, Grout BWW, Short KC (1986a) Osmotic stress as a pregrowth procedure for cryopreservation. 1. Growth and ultrastructure of sycamore and soybean cell suspensions. Ann Bot (Lond) 57:41–48

    Google Scholar 

  • Pritchard HW, Grout BWW, Short KC (1986b) Osmotic stress as a pregrowth procedure for cryopreservation. 3. Cryobiology of sycamore and soybean cell suspensions. Ann Bot (Lond) 57:379–387

    Google Scholar 

  • Rinne P, Welling A, Kaikuranta P (1998) Onset of freezing tolerance in birch (Betula pubescens Ehrh.) involves LEA proteins and osmoregulation and is impaired in an ABA-deficient genotype. Plant Cell Environ 21:601–611. doi:10.1046/j.1365-3040.1998.00306.x

    Article  CAS  Google Scholar 

  • Roberts EH (1973) Predicting the storage life of seeds. Seed Sci Technol 1:499–514

    Google Scholar 

  • Rosenberg LA, Rinne R (1988) Protein synthesis during natural and precocious soybean seed (Glycine max [L.] Merr.) maturation. Plant Physiol 87:474–478. doi:10.1104/pp.87.2.474

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg LA, Rinne RW (1989) Protein synthesis during rehydration, germination and seedling growth of naturally and precociously matured soybean seeds (Glycine max). Ann Bot (Lond) 64:77–86

    CAS  Google Scholar 

  • Sargent JA, Sen Mandi S, Osborne DJ (1981) The loss of desiccation tolerance during germination: an ultrastructural and biochemical approach. Protoplasma 105:225–239. doi:10.1007/BF01279221

    Article  Google Scholar 

  • Steadman KJ, Pritchard HW, Dey PM (1996) Tissue-specific soluble sugars in seeds as indicators of storage category. Ann Bot (Lond) 77:667–674. doi:10.1006/anbo.1996.0083

    Article  CAS  Google Scholar 

  • Still DW, Kovach DA, Bradford KJ (1994) Development of desiccation tolerance during embryogenesis in rice (Oryza sativa) and wild rice (Zizania palustris). Dehydrin expression, abscisic content and sucrose accumulation. Plant Physiol 104:431–438

    PubMed  CAS  Google Scholar 

  • Sun WQ, Leopold AC (1994) Glassy state and seed storage stability: a viability equation analysis. Ann Bot (Lond) 74:601–604. doi:10.1006/anbo.1994.1160

    Article  Google Scholar 

  • Thierry C, Florin B, Pétiard V (1999) Changes in protein metabolism during the acquisition of tolerance to cryopreservation of carrot somatic embryos. Plant Physiol Biochem 37:145–154. doi:10.1016/S0981-9428(99)80076-X

    Article  CAS  Google Scholar 

  • Thomann EB, Sollinger J, White C, Rivin CJ (1992) Accumulation of group 3 late embryogenesis abundant proteins in Zea mays embryos. Plant Physiol 99:607–614. doi:10.1104/pp.99.2.607

    Article  PubMed  CAS  Google Scholar 

  • 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 237–271

    Google Scholar 

  • 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, Wallingford, pp 263–291

    Google Scholar 

  • Wen B, Song SQ (2007a) Acquisition of cryotolerance in maize embryos during seed development. Cryo Lett 28:109–118

    Article  CAS  Google Scholar 

  • Wen B, Song SQ (2007b) Acquisition and loss of cryotolerance in Livistona chinensis embryos during seed development. Cryo Lett 28:291–302

    Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (No. 30571526) and the President’s Foundation of the Chinese Academy of Sciences.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Xishuangbanna Tropical Botanical Garden, The Chinese Academy of Sciences, Mengla, Yunnan, 666303, China

    Bin Wen, Ruling Wang & Songquan Song

Authors
  1. Bin Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruling Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Songquan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bin Wen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wen, B., Wang, R. & Song, S. Cytological and physiological changes related to cryotolerance in orthodox maize embryos during seed development. Protoplasma 236, 29–37 (2009). https://doi.org/10.1007/s00709-009-0044-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-009-0044-9

Keywords

Search

Navigation