Variable desiccation tolerance in Acer pseudoplatanus seeds in relation to developmental conditions: a case of phenotypic recalcitrance?
Matthew I. Daws A H , Hazel Cleland A , Pawel Chmielarz B , Fabio Gorian C , Olivier Leprince D , Christopher E. Mullins E , Costas A. Thanos F , Vigdis Vandvik G and Hugh W. Pritchard AA Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex, RH17 6TN, UK.
B Polish Academy of Sciences, Institute of Dendrology, Parkowa 5, 62-035 Kórnik, Poland.
C State Forestry Service, National Centre for the Study and Conservation of Forest Biodiversity, via del Ponte, 256-37020 Peri, Verona, Italy.
D UMR Molecular Seed Physiology, INRA / INH / Université d’Angers, 16 Bd Lavoisier, F-49045 Angers, France.
E Department of Plant & Soil Science, University of Aberdeen, Aberdeen, AB24 3UU, UK.
F Department of Botany, University of Athens, Athens 15784, Greece.
G Department of Botany, University of Bergen, Allegaten 41, Bergen, N-5007 Norway.
H Corresponding author. Email: m.daws@rbgkew.org.uk
Functional Plant Biology 33(1) 59-66 https://doi.org/10.1071/FP04206
Submitted: 5 November 2004 Accepted: 12 August 2005 Published: 3 January 2006
Abstract
Nine seedlots of the widely planted southern and central European native tree species Acer pseudoplatanus L. were collected along a north–south gradient spanning 21° of latitude in Europe. We investigated how the heat sum during seed development influences seed maturity as assessed by physical, physiological and biochemical traits. Using principal component analysis we found predictable and consistent patterns in all traits, which correlated with heat sum. For example, compared with fruits from their native range (Italy and France, heat sum >3000°C d), fruits from the coldest location (Scotland; heat sum of 1873°C d) were shorter (c. 30 v. 42 mm), germinated over a narrower temperature range (5–20 v. 5–35°C) and had smaller embryos (28 v. > 70 mg) with a higher water content (c. 63 v. 48%), less negative solute potentials (c. –2.4 v. –4.1 MPa) and were more desiccation sensitive (critical water potential of –20.2 v. –55.4 to –60.7 MPa). The observed level of desiccation-tolerance for the French and Italian seedlots is more consistent with the intermediate category than the previous classification of A. pseudoplatanus as recalcitrant. Our results demonstrate that a lower heat sum causes fruits from northern Europe to be dispersed before maximum potential seed quality is achieved.
Keywords: climate change, heat sum, principal component analysis, recalcitrant seed.
Acknowledgments
The authors thank Emily Lydall and Kenneth Fuller for technical assistance and Dr Chris Wood for commenting on the manuscript. Financial support for this work from the Millennium Commission, the Wellcome Trust and Orange Plc. is gratefully acknowledged. The Royal Botanic Gardens, Kew is supported grant-in-aid from Defra.
Amma S, Watanabe A
(1985) Long-term storage of germplasm of tea (Camellia sinensis (L.) O. Kuntze). Japan Agricultural Research Quarterly 19, 196–201.
Berjak P,
Vertucci CW, Pammenter NW
(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, 155–166.
Boyer, JS (1995).
Cruden RW
(1974) The adaptive nature of seed germination in Nemophilia menziesii Aggr. Ecology 55, 1295–1305.
Daws MI,
Burslem DFRP,
Crabtree LM,
Kirkman P,
Mullins CE, Dalling JW
(2002) Differences in seed germination responses may promote coexistence of four sympatric Piper species. Functional Ecology 16, 258–267.
| Crossref | GoogleScholarGoogle Scholar |
Daws MI,
Lydall E,
Chmielarz P,
Leprince O,
Matthews S,
Thanos CA, Pritchard HW
(2004a) Developmental heat sum influences recalcitrant seed traits in Aesculus hippocastanum across Europe. New Phytologist 162, 157–166.
| Crossref | GoogleScholarGoogle Scholar |
Daws MI,
Gaméné CS,
Glidewell SM, Pritchard HW
(2004b) Seed mass variation potentially masks a single critical water content in recalcitrant seeds. Seed Science Research 14, 185–195.
| Crossref | GoogleScholarGoogle Scholar |
Dickie JB,
May K,
Morris SVA, Titley SE
(1991) The effects of desiccation on seed survival in Acer platanoides L. and Acer pseudoplatanus L. Seed Science Research 1, 149–162.
Dussert S,
Chabrillange N,
Rocquelin G,
Engelmann F,
Lopez M, Hamon S
(2001) Tolerance of coffee (Coffea spp.) seeds to ultra-low temperature exposure in relation to calorimetric properties of tissue water, lipid composition, and cooling procedure. Physiologia Plantarum 112, 495–504.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ellis RH,
Hong TD, Roberts EH
(1987) The development of desiccation tolerance and maximum seed quality during seed maturation in six grain legumes. Annals of Botany 59, 23–29.
Ellis RH,
Hong TD, Roberts EH
(1990) An intermediate category of seed storage behaviour? I. Coffee. Journal of Experimental Botany 41, 1167–1174.
Ellis RH,
Hong TD, Roberts EH
(1991a) Effect of storage temperature and moisture on the germination of papaya seeds. Seed Science Research 1, 69–72.
Ellis RH,
Hong TD, Roberts EH
(1991b) An intermediate category of seed storage behaviour? II. Effects of provenance, immaturity and imbibition on desiccation-tolerance in coffee. Journal of Experimental Botany 42, 653–657.
Farrant JM, Walters C
(1998) Ultrastructural and biophysical changes in developing embryos of Aesculus hippocastanum in relation to the acquisition of tolerance to drying. Physiologia Plantarum 104, 513–524.
| Crossref | GoogleScholarGoogle Scholar |
Fenner M
(1991) The effects of the parent environment on seed germinability. Seed Science Research 1, 75–84.
Finch-Savage WE,
Clay HA,
Blake PS, Browning G
(1992) Seed development in the recalcitrant species Quercus robur L. — water status and endogenous abscisic acid levels. Journal of Experimental Botany 43, 671–679.
Greggains V,
Finch-Savage WE,
Quick WP, Atherton NM
(2000) Putative desiccation tolerance mechanisms in orthodox and recalcitrant seeds of the genus Acer. Seed Science Research 10, 317–327.
Gutterman, Y (2000). Maternal effects on seeds during development. In ‘Seeds: the ecology of regeneration in plant communities. 2nd edn’. pp. 59–84. (CABI Publishing: Wallingford)
Hong TD, Ellis RH
(1990) A comparison of maturation drying, germination, and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytologist 116, 589–596.
Hong TD, Ellis RH
(2002) Optimum moisture status for the exceptional survival of seeds of arabica coffee (Coffea arabica L.) in medium-term storage at –20 degrees C. Seed Science and Technology 30, 131–136.
Hu J,
Guo CG, Shi SX
(1993) Partial drying and post-thaw preconditioning improve the survival and germination of cryopreserved seeds of tea (Camellia sinensis). Plant Genetic Resources Newsletter 93, 1–4.
International Seed Testing Association
(1999) International rules for seed testing. Seed Science and Technology
,
Jackson DA
(1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74, 2204–2214.
Jones EW
(1945) Biological flora of the British Isles: Acer pseudo-platanus L. Journal of Ecology 32, 220–237.
Kermode AR, Bewley JD
(1985) Developing seeds of Ricinus communis L., when detached and maintained in an atmosphere of high relative humidity, switch to a germinative mode without the requirement for complete desiccation. Plant Physiology 90, 702–707.
McCune, B ,
and
Mefford, MJ (1997). Multivariate analysis of ecological data. Version 3.17. (MjM Software: Gleneden Beach, OR)
Pammenter NW,
Vertucci CW, Berjak P
(1991) Homeohydrous (recalcitrant) seeds — dehydration, the state of water and viability characteristics in Landolphia kirkii. Plant Physiology 96, 1093–1098.
Poulsen, K (1996). Case study: neem (Azadiracta indica A. Juss.) seed research. In ‘Intermediate / recalcitrant tropical forest tree seeds’. pp. 14–26. (International Plant Genetic Resources Institute: Rome)
Pritchard, HW (2004). Classification of seed storage ‘types’ for ex situ conservation in relation to temperature and moisture. In ‘ plant conservation. Supporting species survival in the wild’. pp. 139–161. (Island Press: Washington, DC)
Pritchard HW,
Tompsett PB, Manger KR
(1996) Development of a thermal time model for the quantification of dormancy loss in Aesculus hippocastanum. Seed Science Research 6, 127–135.
Pritchard HW,
Steadman KJ,
Nash JV, Jones C
(1999) Kinetics of dormancy release and the high temperature germination response in Aesculus hippocastanum seeds. Journal of Experimental Botany 50, 1507–1514.
| Crossref | GoogleScholarGoogle Scholar |
Sacandé M
(2000)
Sacandé M,
Hoekstra FA,
van Pijlen JG, Groot SPC
(1998) A multifactorial study of conditions influencing longevity of neem (Azadirachta indica) seeds. Seed Science Research 8, 473–482.
St. Clair SB, Lynch JP
(2004) Photosynthetic and antioxidant enzyme responses of sugar maple and red maple seedlings to excess manganese in contrasting light environments. Functional Plant Biology 31, 1005–1014.
| Crossref | GoogleScholarGoogle Scholar |
Sun WQ, Liang Y
(2001) Discrete levels of desiccation sensitivity in various seeds as determined by the equilibrium dehydration method. Seed Science Research 11, 317–323.
Suszka B, Tylkowski T
(1980) Storage of acorns of the English oak (Quercus robur L.) over 1–5 winters. Arboretum Kornickie 25, 199–229.
Thompson PA
(1975) Characterisation of germination responses of Silene dioica L. populations from Europe. Annals of Botany 39, 1–19.
Tompsett PB, Pritchard HW
(1993) Water status changes during development in relation to the germination and desiccation tolerance of Aesculus hippocastanum L. seeds. Annals of Botany 71, 107–116.
| Crossref | GoogleScholarGoogle Scholar |
Tompsett PB, Pritchard HW
(1998) The effect of chilling and moisture status on the germination, desiccation tolerance and longevity of Aesculus hippocastanum L. seeds. Annals of Botany 82, 249–261.
| Crossref | GoogleScholarGoogle Scholar |
Underwood, AJ (1997).
Warr SJ
(1986) Factors affecting fruit development, fruit production and seedling survival of sycamore (Acer pseudoplatanus L.). M. Phil Thesis
(University of Lancaster:
UK)
Webb DP, Wareing PF
(1972) Seed dormancy in Acer pseudoplatanus L.: the role of covering structures. Journal of Experimental Botany 23, 813–829.
Welbaum GE, Bradford KJ
(1989) Water relations of seed development and germination in muskmelon (Cucumis melo L.). II. Development of germinability, vigour and desiccation tolerance. Journal of Experimental Botany 40, 1355–1362.
