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Desiccation sensitivity and cell cycle aspects in seeds of Inga vera subsp. affinis

Published online by Cambridge University Press:  22 February 2007

José Marcio Rocha Faria
Affiliation:
Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, Wageningen, 6703 BD, The Netherlands Departamento de Ciências Florestais, Universidade Federal de Lavras, CP 37, Lavras, MG, CEP 37200-000, Brazil
André A.M. van Lammeren
Affiliation:
Laboratory of Plant Cell Biology, Wageningen University, Arboretumlaan 4, Wageningen, 6703 BD, The Netherlands
Henk W.M. Hilhorst*
Affiliation:
Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, Wageningen, 6703 BD, The Netherlands
*
*Correspondence Fax: +31 317 484740, Email: [email protected]

Abstract

The desiccation sensitivity of seeds of Inga vera Willd. subsp. affinis, a recalcitrant-seeded tree from Brazil, was analysed, focusing on water relations and cell-cycle aspects, including DNA content and the microtubular cytoskeleton. Seeds were collected at four developmental stages, dried to different moisture contents (MCs), assessed regarding water activity and set to germinate. Samples of fresh (non-dried) developing and mature seeds were used for assessment of DNA content by flow cytometry. Immunohistochemical detection of microtubules (MTs) was done in mature seeds at different MCs. Slight desiccation of immature seeds increased germination, but further drying resulted in a quick decline of germinability. During seed development the desiccation sensitivity decreased slightly, but DNA content of the embryonic axis cells remained constant, suggesting no relation between those two parameters. Embryonic axis cells of mature seeds showed abundant cortical microtubule arrays, which were not affected by mild desiccation, but broken down by further drying. It appeared that, upon rehydration, damaged cells were not able to reconstitute the microtubular cytoskeleton. The failure of germination of Inga vera seeds after drying could not be attributed to cellular damage to DNA synthesis and mitosis, since the radicle protruded by means of cell elongation, without a need for cell division. However, the breakdown of MTs during desiccation, and their subsequent inability to reassemble upon rehydration, may be related to the decreased germination, since MTs are required for cell elongation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2004

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References

Alberts, B., Bray, D., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P. (1998) Essential cell biology: An introduction to the molecular biology of the cell. New York, Garland Publishing.Google Scholar
Amaral, da and Silva, E.A. (2002) Coffee seed (Coffea arabica cv. Rubi) germination: mechanism and regulation. PhD Thesis, Wageningen University, The Netherlands.Google Scholar
Arumuganathan, K. and Earle, E.D. (1991) Estimation of nuclear DNA content of plants by flow cytometry. Plant Molecular Biology Reporter 9, 229241.CrossRefGoogle Scholar
Baskin, T.I., Busby, C.H., Fowke, L.C., Sammut, M. and Gubler, F. (1992) Improvements in immunostaining samples embedded in methacrylate: localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187, 405413.CrossRefGoogle ScholarPubMed
Berjak, P. and Pammenter, N.W. (1994) Recalcitrance is not an all-or-nothing situation. Seed Science Research 4, 263264.CrossRefGoogle Scholar
Berjak, P. and Pammenter, N.W. (2000) What ultrastructure has told us about recalcitrant seeds. Revista Brasileira de Fisiologia Vegetal 12, 2255.Google Scholar
Berjak, P., Pammenter, N.W. and Vertucci, C. (1992) Homoiohydrous (recalcitrant) seeds: developmental status, desiccation sensitivity and the state of water in axes of Landolphia kirkii Dyer. Planta 186, 249261.CrossRefGoogle ScholarPubMed
Berjak, P., Vertucci, C.W. and Pammenter, N.W. (1993) Effects of developmental status and dehydration rate on characteristics of water and desiccation-sensitivity in recalcitrant seeds of Camellia sinensis. Seed Science Research 3, 155166.Google Scholar
Berjak, P., Kioko, J.I., Walker, M., Mycock, D.J., Wesley-Smith, J., Watt, P. and Pammenter, N.W. (1999) Cryopreservation: an elusive goal. pp. 96109in Marzalina, M., Khoo, K.C., Jayanthi, N., Tsan, F.Y. and Krishnapillay, B. (Eds) IUFRO seed symposium 1998. Recalcitrant seeds. Proceedings of the conference. Kuala Lumpur, Forest Research Institute Malaysia.Google Scholar
Bewley, J.D. and Black, M. (1994) Seeds. Physiology of development and germination (2nd edition). New York, Plenum Press.Google Scholar
Bilia, D.A.C., Marcos, Filho, J. and Novembre, A.D.C.L. (1999) Desiccation tolerance and seed storability of Inga uruguensis (Hook. et Arn.). Seed Science and Technology 27, 7789.Google Scholar
Bino, R.J., Lanteri, S., Verhoeven, H.A. and Kraak, H.L. (1993) Flow cytometric determination of nuclear replication stages in seed tissues. Annals of Botany 72, 181187.Google Scholar
Boubriak, I., Dini, M., Berjak, P. and Osborne, D.J. (2000) Desiccation and survival in the recalcitrant seeds of Avicennia marina: DNA replication, DNA repair and protein synthesis. Seed Science Research 10, 307315.CrossRefGoogle Scholar
Bouvier-Durand, M., Real, M., Côme, D. (1989) Changes in nuclear activity upon secondary dormancy induction by abscisic acid in apple embryos. Plant Physiology and Biochemistry 27, 511518.Google Scholar
Chin, H.F. (1989) Recalcitrant seeds. Extension Bulletin No. 288. Taipei City, Taiwan ASPAC: Food and Fertilizer Technology Center.Google Scholar
Chin, H.F., Krishnapillay, B. and Stanwood, P.C. (1989) Seed moisture: recalcitrant vs. orthodox seeds. pp. 1522in Stanwood, P.C. and McDonald, M.B. (Eds) Seed moisture. CSSA Special Publication No. 14. Madison, Wisconsin Crop Science Society of America.Google Scholar
Corbineau, F. and Côme, D. (1988) Storage of recalcitrant seeds of four tropical species. Seed Science and Technology 16, 97103.Google Scholar
Davide, A.C., Faria, J.M.R. and Botelho, S.A. (1995) Propagação de espécies florestais. Technical Bulletin. Belo Horizonte, Brazil, CEMIG/UFLA/FAEPE.Google Scholar
de Castro, R.D., Bino, R.J., Jing, H.C., Kieft, H. and Hilhorst, H.W.M. (2001) Depth of dormancy in tomato (Lycopersicon esculentum Mill.) seeds is related to the progression of the cell cycle prior to the induction of dormancy. Seed Science Research 11, 4554.CrossRefGoogle Scholar
Deltour, R. (1985) Nuclear activation during early germination of the higher plant embryo. Journal of Cell Science 75, 4383.Google Scholar
Dussert, S., Chabrillange, N., Engelmann, F. and Hamon, S. (1999) Quantitative estimation of seed desiccation sensitivity using a quantal response model: application to nine species of the genus Coffea L. Seed Science Research 9, 135144.Google Scholar
Dustin, P. (1978) Microtubules. Berlin, Springer-Verlag.Google Scholar
Ellis, R.H., Hong, T.D., Roberts., E.H. (1990) An intermediate category of seed storage behaviour? I. Coffee. Journal of Experimental Botany 41, 11671174.Google Scholar
Erdey, D.P., Pammenter, N.W., Finch-Savage, W.E. and Berjak, P. (2003) Physiological assessments of vigour enhancement by mild dehydration stress in recalcitrant seeds: effect of seed maturity. p. 16in Proceedings of the 4th international workshop on desiccation tolerance and sensitivity of seeds and vegetative plant tissues, August, Blouwaterbaai, South Africa.Google Scholar
Farnsworth, E. (2000) The ecology and physiology of viviparous and recalcitrant seeds. Annual Review of Ecology and Systematics 31, 107138.Google Scholar
Farrant, J.M., Berjak, P. and Pammenter, N.W. (1985) The effect of drying rate on viability retention of recalcitrant propagules of Avicennia marina. South African Journal of Botany 51, 432438.CrossRefGoogle Scholar
Farrant, J.M., Pammenter, N.W. and Berjak, P. (1993) Seed development in relation to desiccation tolerance: a comparison between desiccation-sensitive (recalcitrant) seeds of Avicennia marina and desiccation-tolerant types. Seed Science Research 3, 113.CrossRefGoogle Scholar
Finch-Savage, W.E. (1992) Embryo water status and survival in the recalcitrant species Quercus robur L.: evidence for a critical moisture content. Journal of Experimental Botany 43, 663669.Google Scholar
Finch-Savage, W.E., Bergervoet, J.H.W., Bino, R.J., Clay, H.A. and Groot, S.P.C. (1998) Nuclear replication activity during seed development, dormancy breakage and germination in three tree species: Norway maple (Acer platanoides L.), sycamore (Acer pseudoplatanus L.) and cherry (Prunus avium L.). Annals of Botany 81, 519526.CrossRefGoogle Scholar
Goddard, R.H., Wick, S.M., Silflow, C.D. and Snustad, D.P. (1994) Microtubule components of the plant cell cytoskeleton. Plant Physiology 104, 16.CrossRefGoogle ScholarPubMed
Grabe, D.F. (1989) Measurement of seed moisture. pp. 6992in Stanwood, P.C. and McDonald, M.B. (Eds) Seed moisture. CSSA Special Publication No. 14. Madison, USA Crop Science Society of America.Google Scholar
Gumede, Z., Merhar, V. and Berjak, P. (2003) Effect of desiccation on the microfilament component of the cytoskeleton in zygotic embryonic axes of Trichilia dregeanai Sond. p. 22in Proceedings of the 4th international workshop on desiccation tolerance and sensitivity of seeds and vegetative plant tissues, August, Blouwaterbaai, South Africa.Google Scholar
Hong, T.D. and Ellis, R.H. (1990) A comparision of maturation drying, germination, and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytologist 116, 589596.Google Scholar
Hong, T.D. and Ellis, R.H. (1992) Optimum air-dry storage environments for arabica coffee. Seed Science and Technology 20, 547560.Google Scholar
Hong, T.D. and Ellis, R.H. (1996) A protocol to determine seed storage behaviour. IPGRI Technical Bulletin No. 1. Rome, International Plant Genetic Resources Institute.Google Scholar
ISTA (International Seed Testing Association). (1996) International rules for seed testing. Seed Science and Technology 24. (suppl.).Google Scholar
King, M.W. and Roberts, E.H. (1979) The storage of recalcitrant seeds: achievements and possible approaches. Rome, International Board for Plant Genetic Resources.Google Scholar
Köppen, W. (1936) Das geographische system der klimate. pp. 144in Köppen, W. and Geiger, R. (Eds) Handbuch der Klimatologie Vol. 1, part C. Berlin, Gebrüder Borntraeger.Google Scholar
Kumagai, F. and Hasezawa, S. (2001) Dynamic organization of microtubules and microfilaments during cell cycle progression in higher plant cells. Plant Biology 3, 416.Google Scholar
Leopold, A.C. and Vertucci, C.W. (1986) Physical attributes of desiccated seeds. pp. 2234in Leopold, A.C. (Eds) Membranes, metabolism and dry organisms. Ithaca, Comstock Publishing.Google Scholar
Liang, Y. and Sun, W.Q. (2000) Desiccation tolerance of recalcitrant Theobroma cacao embryonic axes: the optimal drying rate and its physiological basis. Journal of Experimental Botany 51, 19111919.Google Scholar
Lloyd, C. (1994) Why should stationary plant cells have such dynamic microtubules? Molecular Biology of the Cell 5, 12771280.Google Scholar
Mycock, D.J., Berjak, P., Finch-Savage, W.E. (2000) Effects of desiccation on the subcellular matrix of the embryonic axes of Quercus robur. pp. 197203in Black, M., Bradford, K.J. and Vazquez-Ramos, J. (Eds) Seed biology: Advances and applications. Wallingford, CABI Publishing.Google Scholar
Oliver, M.J. (1996) Desiccation tolerance in vegetative plant cells. Physiologia Plantarum 97, 779787.CrossRefGoogle Scholar
Pammenter, N.W. and Berjak, P. (1999) A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms. Seed Science Research 9, 1337.Google Scholar
Pammenter, N.W. and Berjak, P. (2000) Aspects of recalcitrant seed physiology. Revista Brasileira de Fisiologia Vegetal 12, 5669.Google Scholar
Pammenter, N.W., Vertucci, C.W. and Berjak, P. (1991) Homeohydrous (recalcitrant) seeds: dehydration, the state of water and viability characteristics in Landolphia kirkii. Plant Physiology 96, 10931098.Google Scholar
Pammenter, N.W., Berjak, P., Farrant, J.M., Smith, M.T. and Ross, G. (1994) Why do stored hydrated recalcitrant seeds die? Seed Science Research 4, 187191.Google Scholar
Pammenter, N.W., Greggains, V., Kioko, J.I., Wesley-Smith, J., Berjak, P., Finch-Savage, W.E. (1998) Effects of differential drying rates on viability retention of recalcitrant seeds of Ekebergia capensis. Seed Science Research 8, 463471.Google Scholar
Pammenter, N.W., Berjak, P. and Walters, C. (2000) The effect of drying rate on recalcitrant seeds: ‘lethal water contents’, causes of damage, and quantification of recalcitrance. pp. 215221in Black, M., Bradford, K.J. and Vazquez-Ramos, J. (Eds) Seed biology: Advances and applications. Wallingford, CABI Publishing.Google Scholar
Pennington, T.D. (1997) The genus Inga: Botany. Richmond, The Royal Botanic Gardens.Google Scholar
Poulsen, K.M. and Eriksen, E.N. (1992) Physiological aspects of recalcitrance in embryonic axes of Quercus robur L. Seed Science Research 2, 215221.Google Scholar
Pritchard, H.W. (1991) Water potential and embryonic axis viability in recalcitrant seeds of Quercus rubra. Annals of Botany 67, 4349.Google Scholar
Pritchard, H.W., Haye, A.J., Wright, W.J. and Steadman, K.J. (1995) A comparative study of seed viability in Inga species: desiccation tolerance in relation to the physical characteristics and chemical composition of the embryo. Seed Science and Technology 23, 85100.Google Scholar
Probert, R.J. and Longley, P.L. (1989) Recalcitrant seed storage physiology in three aquatic grasses (Zizania palustris, Spartina anglica and Porteresia coarctata). Annals of Botany 63, 5363.Google Scholar
Roberts, E.H. (1973) Predicting the storage life of seeds. Seed Science and Technology 1, 499514.Google Scholar
Roberts, E.H. and Ellis, R.H. (1989) Water and seed survival. Annals of Botany 63, 3952.Google Scholar
Sacandé, M. (2000) Stress, storage and survival of neem seed. PhD Thesis, Wageningen Agricultural University, The Netherlands.Google Scholar
Saracco, F., Bino, R.J., Bergervoet, J.H.W. and Lanteri, S. (1995) Influence of priming-induced nuclear replication activity on storability of pepper (Capsicum annuum L.) seed. Seed Science Research 5, 2529.Google Scholar
Sargent, J.A., Sen Mandi, S. and Osborne, D.J. (1981) The loss of desiccation tolerance during germination: an ultrastructural and biochemical approach. Protoplasma 105, 225239.Google Scholar
Sun, W.Q. (2002) Methods for the study of water relations under desiccation stress. pp. 4791in Black, M. and Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.Google Scholar
Sun, W.Q. and Gouk, S.S. (1999) Preferred parameters and methods for studying moisture content of recalcitrant seeds. pp. 404430in Marzalina, M., Khoo, K.C., Jayanthi, N., Tsan, F.Y. and Krishnapillay, B. (Eds) IUFRO seed symposium 1998. Recalcitrant seeds. Proceedings of the conference. Kuala Lumpur, Forest Research Institute Malaysia.Google Scholar
Tompsett, P.B. (1984) Desiccation studies in relation to the storage of Araucaria seed. Annals of Applied Biology 105, 581586.Google Scholar
Uniyal, R.C. and Nautiyal, A.R. (1996) Physiology of seed development in Aesculus indica, a recalcitrant seed. Seed Science and Technology 24, 419424.Google Scholar
Vantard, M., Cowling, R. and Delichère, C. (2000) Cell cycle regulation of the microtubular cytoskeleton. Plant Molecular Biology 43, 691703.CrossRefGoogle ScholarPubMed
Vazquez-Ramos, J.M. and Sanchez, M.D. (2003) The cell cycle and seed germination. Seed Science Research 13, 113130.Google Scholar
Vertucci, C.W. and Leopold, A.C. (1987a) The relationship between water binding and desiccation tolerance in tissues. Plant Physiology 85, 232238.CrossRefGoogle ScholarPubMed
Vertucci, C.W. and Leopold, A.C. (1987b) Water binding in legume seeds. Plant Physiology 85, 224231.Google Scholar
Walters, C., Farrant, J.M., Pammenter, N.W. and Berjak, P. (2002) Desiccation stress and damage. pp. 263291in Black, M. and Pritchard, H.W. (Eds) Desiccation and survival in plants: Drying without dying. Wallingford, CABI Publishing.Google Scholar
Wesley-Smith, J., Pammenter, N.W., Berjak, P. and Walters, C. (2001) The effects of two drying rates on the desiccation tolerance of embryonic axes of recalcitrant jackfruit (Artocarpus heterophyllus Lamk.) seeds. Annals of Botany 88, 653664.Google Scholar
Yuan, M., Shaw, P.J., Warn, R.M. and Lloyd, C.W. (1994) Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proceedings of the National Academy of Sciences, USA 91, 60506053Google Scholar