Skip to main content
SpringerLink
Log in

What can cell cycle and ultrastructure tell us about desiccation tolerance in Leucaena leucocephala germinating seeds?

  • Original papers
  • Published:
Biologia Plantarum

Abstract

Desiccation tolerance (DT) is the ability to tolerate dehydration to levels below 0.1 g(H2O) g−1(dry mass) and subsequent rehydration without lethal damage. Here, it is proposed that Leucaena leucocephala, a tree species, has potential to be model tolerant species in seed research. Using flow cytometry and transmission electron microscopy, cytological changes related to loss of DT in Leucaena primary roots were followed during germination. Leucaena seeds lost their DT at the end of germination and this coincided with an increase in cellular 4C DNA content. A negative correlation between the 8C DNA content and the capacity of germinating Leucaena seeds to tolerate desiccation was also observed. Apparently, the seeds of Leucaena underwent extra cycles of endoreduplication and accumulated a high content of DNA — an event not previously linked to DT. The ultrastructural damage imposed by drying overcame Leucaena primary root cell resilience and their ability to resume normal growth. Nuclear DNA content may be used as indicator of progress of germination and loss of DT in Leucaena.

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

Similar content being viewed by others

Abbreviations

DT:

desiccation tolerance

TEM:

transmission electron microscopy

WC:

water content

References

  • Atif, R.M., Boulisset, F., Conreux, C., Thompson, R., Ochatt, S.J.: In vitro auxin treatment promotes cell division and delays endoreduplication in developing seeds of the model legume species Medicago truncatula. — Physiol. Plant. 148: 549–559, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Bailly, C.: Active oxygen species and antioxidants in seed biology. — Seed Sci Res. 14: 93–107, 2004.

    Article  CAS  Google Scholar 

  • Baskin, C.C., Baskin, J.M. (ed.): Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. - Academic Press, San Diego 1998.

    Google Scholar 

  • Berjak, P., Pammenter, N.W.: What ultrastructure has told us about recalcitrant seeds. — Rev. bras. Fisiol. veg. 12: 22–55, 2000.

    Google Scholar 

  • Berjak, P., Pammenter, N.W.: From Avicennia to Zizania: seed recalcitrance in perspective. — Ann Bot. 101: 213–228, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bewley, J.D., Black, M. (ed.): Seeds: Physiology of Development and Germination. - Plenum Press, New York 1994.

    Book  Google Scholar 

  • Bewley, J.D., Bradford, K., Hilhorst, H., Nonogaki, H.(ed.): Seeds: Physiology of Development, Germination and Dormancy. - Springer, New York 2013.

    Book  Google Scholar 

  • Bino, R.J., Lanteri, S., Verhoeven, H.A., Kraak, H.L.: Flow cytometric determination of nuclear replication stages in seed tissues. — Ann Bot. 72: 181–187, 1993.

    Article  Google Scholar 

  • Black, M., Corbineau, F., Gee, H., Come, D.: Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos. — Plant Physiol. 120: 463–472, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackman, S.A., Obendorf, R.L., Leopold, A.C.: Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. — Plant Physiol. 100: 225–230, 1992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruggink, T., Van der Toorn, P.: Induction of desiccation tolerance in germinated seeds. — Seed Sci Res. 5: 1–4, 1995.

    Article  Google Scholar 

  • Buitink, J., Leger, J.J., Guisle, I., Vu, B.L., Wuilleme, S., Lamirault, G., Le Bars, A., Le Meur, N., Becker, A., Kuster, H., Leprince, O.: Transcriptome profiling uncovers metabolic and regulatory processes occurring during the transition from desiccation-sensitive to desiccation-tolerant stages in Medicago truncatula seeds. — Plant J. 47: 735–750, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Buitink, J., Leprince, O.: Glass formation in plant anhydrobiotes: survival in the dry state. — Cryobiology 48: 215–228, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Buitink, J., Vu, B.L., Satour, P., Leprince, O.: The reestablishment of desiccation tolerance in germinated radicles of Medicago truncatula Gaertn. seeds. — Seed Sci Res. 13: 273–286, 2003.

    Article  CAS  Google Scholar 

  • Carvalho, C.R., Clarindo, W.R., Praça, M.M., Araújo, F.S., Carels, N.: Genome size, base composition and karyotype of Jatropha curcas L., an important biofuel plant. — Plant Sci. 174: 613–617, 2008.

    Article  CAS  Google Scholar 

  • Cromarty, A.S., Ellis, R.H., Roberts, E.H. (ed.): Design of Seeds Storage Facilities for Genetic Conservation. - IPGRI, Rome 1985.

    Google Scholar 

  • Dante, R.A., Larkins, B.A., Sabelli, P.A.: Cell cycle control and seed development. — Front. Plant Sci. 5: 493, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • De Castro, R.D., Van Lammeren, Groot, S.P., Bino, R.J., Hilhorst, H.W.: Cell division and subsequent radicle protrusion in tomato seeds are inhibited by osmotic stress but DNA synthesis and formation of microtubular cytoskeleton are not. — Plant Physiol. 122: 327–336, 2000.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deltour, R. Nuclear activiation during early germination of the higher plant embryo. - J. Cell Sci. 75: 43–83, 1985.

    CAS  PubMed  Google Scholar 

  • Dinakar, C., Bartels, D.: Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. — Front. Plant Sci. 4: 482, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar, B.A., Zielke, N., Gutierrez, C.: Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. — Natur. Rev. mol. cell. Biol. 15: 197–210, 2014.

    Article  Google Scholar 

  • Elmaghrabi, A., Ochatt, S., Rogers, H., Francis, D.: Enhanced tolerance to salinity following cellular acclimation to increasing NaCl levels in Medicago truncatula. - Plant Cell Tissue Organ Cult. 114: 61–70, 2013.

    Article  CAS  Google Scholar 

  • Faria, J.M., Buitink, J., Van Lammeren, A.A., Hilhorst, H.W.: Changes in DNA and microtubules during loss and re-establishment of desiccation tolerance in germinating Medicago truncatula seeds. — J. exp Bot. 56: 2119–2130, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Farrant, J.: A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. — Plant Ecol. 151: 29–39, 2000.

    Article  Google Scholar 

  • Hundertmark, M., Buitink, J., Leprince, O., Hincha, D.K.: The reduction of seed-specific dehydrins reduces seed longevity in Arabidopsis thaliana. — Seed Sci Res. 21: 165–173, 2011.

    Article  CAS  Google Scholar 

  • Illing, N., Denby, K.J., Collett, H., Shen, A., Farrant, J.M.: The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. — Integr. Comp. Biol. 45: 771–787, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Koster, K.L., Leopold, A.C.: Sugars and desiccation tolerance in seeds. — Plant Physiol. 88: 829–832, 1988.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kranner, I., Birtic, S.: A modulating role for antioxidants in desiccation tolerance. — Integr. Comp. Biol. 45: 734–740, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Lemontey, C., Mousset-Déclas, C., Munier-Jolain, N., Boutin, J.P.: Maternal genotype influences pea seed size by controlling both mitotic activity during early embryogenesis and final endoreduplication level/cotyledon cell size in mature seed. — J. exp Bot. 51: 167–175, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Leopold, A.C., Vertucci, C.W.: Membranes, metabolism and dry organisms. - In Leopold, A.C. (ed.): Physical Attributes of Desiccated Seeds. Pp. 23–34, Comstock Publishing, London 1986.

    Google Scholar 

  • Maia, J., Dekkers, B.J., Provart, N.J., Ligterink, W., Hilhorst, H.W.: The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome. — PLoS ONE 6: e29123, 2011.

    Article  Google Scholar 

  • Maia, J., Dekkers, B.J.W., Dolle, M.J., Ligterink, W., Hilhorst, H.W.M.: Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. — New Phytol. 203: 81–93, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Moore, J.P., Vicre-Gibouin, M., Farrant, J.M., Driouich, A.: Adaptations of higher plant cell walls to water loss: drought vs desiccation. — Physiol Plant. 134: 237–245, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Ochatt, S.: Agroecological impact of an in vitro biotechnology approach of embryo development and seed filling in legumes. — Agron. Sustainable Develop. 35: 535–552, 2015.

    Article  CAS  Google Scholar 

  • Oliver, M.J., Tuba, Z., Mishler, B.D.: The evolution of vegetative desiccation tolerance in land plants. — Plant Ecol. 151: 85–100, 2000.

    Article  Google Scholar 

  • Öpik, H. The fine structure of some dry seed tissues observed after completely anhydrous chemical fixation. - Ann Bot. 56: 453–466, 1985.

    Google Scholar 

  • Pampurova, S., Van Dijck, P.: The desiccation tolerant secrets of Selaginella lepidophylla: what we have learned so far? — Plant Physiol. Biochem. 80: 285–290, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Phillips, J.R., Oliver, M.J., Bartels, D.: Molecular genetics of desiccation and tolerant systems. - In Black, M., Pritchard, H.W. (ed.): Desiccation and Survival in Plants: Drying without Dying. Pp 319–341. CABI Publishing, Wallingford 2002.

    Chapter  Google Scholar 

  • Potts, M.: Desiccation tolerance of prokaryotes. — Microbiol. Rev. 58: 755–805, 1994.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rolston, M.P.: Water impermeable seed dormancy. — Bot. Rev. 44: 365–396, 1978.

    Article  CAS  Google Scholar 

  • Saracco, F., Bino, R.J., Bergervoet, J.H.W., Lanteri, S.: Influence of priming-induced nuclear replication activity on storability of pepper (Capsicum annuum L.) seed. — Seed Sci. Res. 5: 25–29, 1995.

    Article  Google Scholar 

  • Setter, T.L., Flannigan, B.A.: Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. — J. exp Bot. 52: 1401–1408, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Skirycz, A., Claeys, H., De Bodt, S., Oikawa, A., Shinoda, S., Andriankaja, M., Maleux, K., Eloy, N.B., Coppens, F., Yoo, S-D., Saito, K., Inzé, D.: Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. — Plant Cell 23: 1876–1888, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sliwinska, E.: Nuclear DNA replication and seed quality. — Seed Sci Res. 19: 15–25, 2009.

    Article  CAS  Google Scholar 

  • Sliwinska, E.: Cell cycle and germination of fresh, dried and deteriorated sugarbeet seeds as indicators of optimal harvest time. — Seed Sci Res. 13: 131–138, 2003.

    Article  Google Scholar 

  • Sreedhar, L., Wolkers, W.F., Hoekstra, F.A., Bewley, J.D.: In vivo characterization of the effects of abscisic acid and drying protocols associated with the acquisition of desiccation tolerance in alfalfa (Medicago sativa L.) somatic embryos. — Ann Bot. 89: 391–400, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tunnacliffe, A., Wise, M.J.: The continuing conundrum of the LEA proteins. — Naturwissenschaften 94: 791–812, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Verdier, J., Lalanne, D., Pelletier, S., Torres-Jerez, I., Righetti, K., Bandyopadhyay, K., Leprince, O., Chatelain, E., Vu, B.L., Gouzy, J., Gamas, P., Udvardi, M.K., Buitink, J.: A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. — Plant Physiol. 163: 757–774, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira, C., Amaral da Silva, E., De Alvarenga, A., De Castro, E., Toorop, P.: Stress-associated factors increase after desiccation of germinated seeds of Tabebuia impetiginosa Mart. — Plant Growth Regul. 62: 257–263, 2010.

    Article  CAS  Google Scholar 

  • Wang, H., Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L., Fowke, L.C.: ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. — Plant J. 15: 501–510, 1998.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. São Paulo State University, FCA/UNESP, CEP 18610-307, Botucatu, SP, Brazil

    J. Maia & E. A. A. da Silva

  2. Departament of Forest Sciences, Federal University of Lavras, CEP 37200-000, Lavras, MG, Brazil

    C. C. Guimarães & J. M. R. Faria

Authors
  1. J. Maia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. C. Guimarães
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. A. A. da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. R. Faria
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Maia.

Additional information

Acknowledgments: This research was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maia, J., Guimarães, C.C., da Silva, E.A.A. et al. What can cell cycle and ultrastructure tell us about desiccation tolerance in Leucaena leucocephala germinating seeds?. Biol Plant 60, 320–328 (2016). https://doi.org/10.1007/s10535-016-0583-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0583-9

Additional key words

Search

Navigation