Evolutionary ecophysiology of seed desiccation sensitivity
Alexandre Marques A , Gonda Buijs A , Wilco Ligterink A and Henk Hilhorst A B
+ Author Affiliations
- Author Affiliations
A Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700AA Wageningen, The Netherlands.
B Corresponding author. Email: henk.hilhorst@wur.nl
Functional Plant Biology 45(11) 1083-1095 https://doi.org/10.1071/FP18022
Submitted: 20 January 2018 Accepted: 11 May 2018 Published: 7 June 2018
Abstract
Desiccation sensitive (DS) seeds do not survive dry storage due to their lack of desiccation tolerance. Almost half of the plant species in tropical rainforests produce DS seeds and therefore the desiccation sensitivity of these seeds represents a problem for and long-term biodiversity conservation. This phenomenon raises questions as to how, where and why DS (desiccation sensitive)-seeded species appeared during evolution. These species evolved probably independently from desiccation tolerant (DT) seeded ancestors. They adapted to environments where the conditions are conducive to immediate germination after shedding, e.g. constant and abundant rainy seasons. These very predictable conditions offered a relaxed selection for desiccation tolerance that eventually got lost in DS seeds. These species are highly dependent on their environment to survive and they are seriously threatened by deforestation and climate change. Understanding of the ecology, evolution and molecular mechanisms associated with seed desiccation tolerance can shed light on the resilience of DS-seeded species and guide conservation efforts. In this review, we survey the available literature for ecological and physiological aspects of DS-seeded species and combine it with recent knowledge obtained from DT model species. This enables us to generate hypotheses concerning the evolution of DS-seeded species and their associated genetic alterations.
Additional keywords: dormancy, intermediate seeds, orthodox seeds, seed size.
References
Achard F, Eva HD, Stibig H-J, Mayaux P, Gallego J, Richards T, Malingreau J-P (2002) Determination of deforestation rates of the world’s humid tropical forests. Science 297, 999–1002.| Determination of deforestation rates of the world’s humid tropical forests.Crossref | GoogleScholarGoogle Scholar |
Alpert P, Oliver MJ (2002) Desiccation and survival in plants. In ‘ Desiccation and survival in plants: drying without dying’. (Eds M Black, HW Pritchard) pp. 3–43. (CABI Publishing: Wallingford, UK)
Andrade A, Cunha R, Souza A, Reis R, Almeida K (2003) Physiological and morphological aspects of seed viability of a neotropical savannah tree, Eugenia dysenterica DC. Seed Science and Technology 31, 125–137.
| Physiological and morphological aspects of seed viability of a neotropical savannah tree, Eugenia dysenterica DC.Crossref | GoogleScholarGoogle Scholar |
Ayongwa G, Stomph T, Belder P, Leffelaar P, Kuyper T (2011) Organic matter and seed survival of Striga hermonthica – mechanisms for seed depletion in the soil. Crop Protection 30, 1594–1600.
| Organic matter and seed survival of Striga hermonthica – mechanisms for seed depletion in the soil.Crossref | GoogleScholarGoogle Scholar |
Baskin CC, Baskin JM (2005) Seed dormancy in trees of climax tropical vegetation types. Tropical Ecology 46, 17–28.
Bateman R, DiMichele W (1994) Saltational evolution of form in vascular plants: a neoGoldschmidtian synthesis. In ‘Shape and form in plants and fungi’. pp. 63–102. In ‘Shape and form in plants and fungi’. (Eds DS Ingram, A Hudson) pp. 63–102. (Academic Press: London)
Bäumlein H, Miséra S, Luerßen H, Kölle K, Horstmann C, Wobus U, Müller AJ (1994) The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis. The Plant Journal 6, 379–387.
| The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis.Crossref | GoogleScholarGoogle Scholar |
Bazzaz FA (1991) Habitat selection in plants. American Naturalist 137, S116–S130.
| Habitat selection in plants.Crossref | GoogleScholarGoogle Scholar |
Beardmore T, Whittle C-A (2005) Induction of tolerance to desiccation and cryopreservation in silver maple (Acer saccharinum) embryonic axes. Tree Physiology 25, 965–972.
| Induction of tolerance to desiccation and cryopreservation in silver maple (Acer saccharinum) embryonic axes.Crossref | GoogleScholarGoogle Scholar |
Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 17042–17047.
| Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Berjak P, Pammenter NW (2008) From Avicennia to Zizania: seed recalcitrance in perspective. Annals of Botany 101, 213–228.
| From Avicennia to Zizania: seed recalcitrance in perspective.Crossref | GoogleScholarGoogle Scholar |
Berjak P, Pammenter NW (2013) Implications of the lack of desiccation tolerance in recalcitrant seeds. Frontiers in Plant Science 4, 478
| Implications of the lack of desiccation tolerance in recalcitrant seeds.Crossref | GoogleScholarGoogle Scholar |
Berjak P, Vertucci CW, Pammenter NW (2008) 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.
Bewley JD (1979) Physiological aspects of desiccation tolerance. Annual Review of Plant Physiology 30, 195–238.
| Physiological aspects of desiccation tolerance.Crossref | GoogleScholarGoogle Scholar |
Bewley JD, Bradford K, Hilhorst H (2012) ‘Seeds: physiology of development, germination and dormancy.’ (Springer Science+Business Media: Berlin)
Bewley JD, Bradford KJ, Hilhorst HW, Nonogaki H (2013) Longevity, storage, and deterioration. In ‘Seeds’. pp. 341–376. (Springer: Berlin)
Born N, Behringer D, Liepelt S, Beyer S, Schwerdtfeger M, Ziegenhagen B, Koch M (2014) Monitoring plant drought stress response using terahertz time-domain spectroscopy. Plant Physiology 164, 1571–1577.
| Monitoring plant drought stress response using terahertz time-domain spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Buitink J, Vu BL, Satour P, Leprince O (2003) The re-establishment of desiccation tolerance in germinated radicles of Medigago truncatula Gaertn. Seed Science Research 13, 273–286.
| The re-establishment of desiccation tolerance in germinated radicles of Medigago truncatula Gaertn.Crossref | GoogleScholarGoogle Scholar |
Cerabolini B, Ceriani RM, Caccianiga M, De Andreis R, Raimondi B (2003) Seed size, shape and persistence in soil: a test on Italian flora from alps to mediterranean coasts. Seed Science Research 13, 75–85.
| Seed size, shape and persistence in soil: a test on Italian flora from alps to mediterranean coasts.Crossref | GoogleScholarGoogle Scholar |
Chatelain E, Hundertmark M, Leprince O, Le Gall S, Satour P, Deligny-Penninck S, Rogniaux H, Buitink J (2012) Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity. Plant, Cell & Environment 35, 1440–1455.
| Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity.Crossref | GoogleScholarGoogle Scholar |
Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root‐to‐shoot signalling of water shortage. The Plant Journal 52, 167–174.
| A hydraulic signal in root‐to‐shoot signalling of water shortage.Crossref | GoogleScholarGoogle Scholar |
Clerkx EJ, El-Lithy ME, Vierling E, Ruys GJ, Blankestijn-De Vries H, Groot SP, Vreugdenhil D, Koornneef M (2004a) Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiology 135, 432–443.
| Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population.Crossref | GoogleScholarGoogle Scholar |
Clerkx EJ, Vries BD, Ruys GJ, Groot SP, Koornneef M (2004b) Genetic differences in seed longevity of various Arabidopsis mutants. Physiologia Plantarum 121, 448–461.
| Genetic differences in seed longevity of various Arabidopsis mutants.Crossref | GoogleScholarGoogle Scholar |
Costa MC, Righetti K, Nijveen H, Yazdanpanah F, Ligterink W, Buitink J, Hilhorst HW (2015) A gene co-expression network predicts functional genes controlling the re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds. Planta 242, 435–449.
| A gene co-expression network predicts functional genes controlling the re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds.Crossref | GoogleScholarGoogle Scholar |
Crowe JH, Carpenter JF, Crowe LM, Anchordoguy TJ (1990) Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules. Cryobiology 27, 219–231.
| Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules.Crossref | GoogleScholarGoogle Scholar |
Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollination in angiosperms. Trends in Ecology & Evolution 17, 361–369.
| The evolution of wind pollination in angiosperms.Crossref | GoogleScholarGoogle Scholar |
Darwin C (1859) ‘On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life.’ (D. Appleton & Company: New York)
Daws MI, Pritchard HW (2008) The development and limits of freezing tolerance in Acer pseudoplatanus fruits across Europe is dependent on provenance. Cryo Letters 29, 189–198.
Daws MI, Garwood NC, Pritchard HW (2006) Prediction of desiccation sensitivity in seeds of woody species: a probabilistic model based on two seed traits and 104 species. Annals of Botany 97, 667–674.
| Prediction of desiccation sensitivity in seeds of woody species: a probabilistic model based on two seed traits and 104 species.Crossref | GoogleScholarGoogle Scholar |
de Souza TV, Torres IC, Steiner N, Paulilo MTS (2015) Seed dormancy in tree species of the tropical Brazilian Atlantic Forest and its relationships with seed traits and environmental conditions. Brazilian Journal of Botany 38, 243–264.
| Seed dormancy in tree species of the tropical Brazilian Atlantic Forest and its relationships with seed traits and environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122, 403–414.
| Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Dekkers BJ, Costa MCD, Maia J, Bentsink L, Ligterink W, Hilhorst HW (2015) Acquisition and loss of desiccation tolerance in seeds: from experimental model to biological relevance. Planta 241, 563–577.
| Acquisition and loss of desiccation tolerance in seeds: from experimental model to biological relevance.Crossref | GoogleScholarGoogle Scholar |
Delahaie J, Hundertmark M, Bove J, Leprince O, Rogniaux H, Buitink J (2013) LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance. Journal of Experimental Botany 64, 4559–4573.
| LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance.Crossref | GoogleScholarGoogle Scholar |
Delmas F, Sankaranarayanan S, Deb S, Widdup E, Bournonville C, Bollier N, Northey JG, McCourt P, Samuel MA (2013) ABI3 controls embryo degreening through Mendel’s I locus. Proceedings of the National Academy of Sciences of the United States of America 110, E3888–E3894.
| ABI3 controls embryo degreening through Mendel’s I locus.Crossref | GoogleScholarGoogle Scholar |
dePamphilis CW, Palmer JD (1990) Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 348, 337–339.
| Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant.Crossref | GoogleScholarGoogle Scholar |
Dickie JB, Pritchard HW (2002) Systematic and evolutionary aspects of desiccation tolerance in seeds. In ‘Desiccation and survival in plants: drying without dying’. (Eds M Black, HW Pritchard) pp. pp. 239–259. (CABI Publishing: Wallingford, UK)
Donohue K, Rubio de Casas R, Burghardt L, Kovach K, Willis CG (2010) Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology Evolution and Systematics 41, 293–319.
| Germination, postgermination adaptation, and species ecological ranges.Crossref | GoogleScholarGoogle Scholar |
Ellis R, Hong T, Roberts E (1990) An intermediate category of seed storage behaviour? I. Coffee. Journal of Experimental Botany 41, 1167–1174.
| An intermediate category of seed storage behaviour? I. Coffee.Crossref | GoogleScholarGoogle Scholar |
Ellis R, Hong T, Roberts E (1991) 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.
| An intermediate category of seed storage behaviour? II. Effects of provenance, immaturity, and imbibition on desiccation-tolerance in coffee.Crossref | GoogleScholarGoogle Scholar |
Faria JM, Buitink J, van Lammeren AA, Hilhorst HW (2005a) Changes in DNA and microtubules during loss and re-establishment of desiccation tolerance in germinating Medicago truncatula seeds. Journal of Experimental Botany 56, 2119–2130.
| Changes in DNA and microtubules during loss and re-establishment of desiccation tolerance in germinating Medicago truncatula seeds.Crossref | GoogleScholarGoogle Scholar |
Faria JM, Buitink J, van Lammeren AA, Hilhorst HWM (2005b) Changes in DNA and microtubules during loss and re-establishment of desiccation tolerance in germinating Medicago truncatula seeds. Journal of Experimental Botany 56, 2119–2130.
| Changes in DNA and microtubules during loss and re-establishment of desiccation tolerance in germinating Medicago truncatula seeds.Crossref | GoogleScholarGoogle Scholar |
Farnsworth E (2000) The ecology and physiology of viviparous and recalcitrant seeds. Annual Review of Ecology and Systematics 31, 107–138.
| The ecology and physiology of viviparous and recalcitrant seeds.Crossref | GoogleScholarGoogle Scholar |
Farnsworth E, Farrant J (1998) Reductions in abscisic acid are linked with viviparous reproduction in mangroves. American Journal of Botany 85, 760
| Reductions in abscisic acid are linked with viviparous reproduction in mangroves.Crossref | GoogleScholarGoogle Scholar |
Farrant JM, Berjak P, Cutting J, Pammenter N (1993) The role of plant growth regulators in the development and germination of the desiccation-sensitive (recalcitrant) seeds of Avicennia marina. Seed Science Research 3, 55–63.
| The role of plant growth regulators in the development and germination of the desiccation-sensitive (recalcitrant) seeds of Avicennia marina.Crossref | GoogleScholarGoogle Scholar |
Fenner M (2000) ‘Seeds: the ecology of regeneration in plant communities.’ (CABI Publishing: Wallingford, UK)
Ferrandis P, Bonilla M, Osorio LdC (2011) Germination and soil seed bank traits of Podocarpus angustifolius (Podocarpaceae): an endemic tree species from Cuban rain forests. Revista de Biología Tropical 59, 1061–1069.
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.
| Seed dormancy and the control of germination.Crossref | GoogleScholarGoogle Scholar |
Freeling M (2008) The evolutionary position of subfunctionalization, downgraded. In ‘Plant genomes. Vol. 4’. pp. 25–40. (Karger Publishers: Basel, Switzerland)
Funes G, Basconcelo S, Díaz S, Cabido M (1999) Seed size and shape are good predictors of seed persistence in soil in temperate mountain grasslands of Argentina. Seed Science Research 9, 341–345.
| Seed size and shape are good predictors of seed persistence in soil in temperate mountain grasslands of Argentina.Crossref | GoogleScholarGoogle Scholar |
Gaff DF, Oliver M (2013) The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Functional Plant Biology 40, 315
| The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon.Crossref | GoogleScholarGoogle Scholar |
Garello G, Page‐Degivry MT (1995) Desiccation‐sensitive Hopea odorata seeds: sensitivity to abscisic acid, water potential and inhibitors of gibberellin biosynthesis. Physiologia Plantarum 95, 45–50.
| Desiccation‐sensitive Hopea odorata seeds: sensitivity to abscisic acid, water potential and inhibitors of gibberellin biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Garwood NC (1989) Tropical soil seed banks: a review. Ecology of Soil Seed Banks 149, 210
González-Morales SI, Chávez-Montes RA, Hayano-Kanashiro C, Alejo-Jacuinde G, Rico-Cambron TY, de Folter S, Herrera-Estrella L (2016) Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 113, E5232–E5241.
| Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
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.
| Putative desiccation tolerance mechanisms in orthodox and recalcitrant seeds of the genus Acer.Crossref | GoogleScholarGoogle Scholar |
Gubler F, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and pre-harvest sprouting. Current Opinion in Plant Biology 8, 183–187.
| Dormancy release, ABA and pre-harvest sprouting.Crossref | GoogleScholarGoogle Scholar |
Hamilton KN, Offord CA, Cuneo P, Deseo MA (2013) A comparative study of seed morphology in relation to desiccation tolerance and other physiological responses in 71 Eastern Australian rainforest species. Plant Species Biology 28, 51–62.
| A comparative study of seed morphology in relation to desiccation tolerance and other physiological responses in 71 Eastern Australian rainforest species.Crossref | GoogleScholarGoogle Scholar |
Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends in Plant Science 10, 472–477.
| Genetic analysis of seed coat development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
He H, de Souza Vidigal D, Snoek LB, Schnabel S, Nijveen H, Hilhorst H, Bentsink L (2014) Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. Journal of Experimental Botany 65, 6603–6615.
| Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Hill JP, Edwards W, Franks PJ, Leishman M (2012) Size is not everything for desiccation-sensitive seeds. Journal of Ecology 100, 1131–1140.
| Size is not everything for desiccation-sensitive seeds.Crossref | GoogleScholarGoogle Scholar |
Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends in Plant Science 6, 431–438.
| Mechanisms of plant desiccation tolerance.Crossref | GoogleScholarGoogle Scholar |
Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology & Evolution 4, 131–135.
| Evolution of thermal sensitivity of ectotherm performance.Crossref | GoogleScholarGoogle Scholar |
Jaganathan GK, Dalrymple SE, Liu B (2015) Towards an understanding of factors controlling seed bank composition and longevity in the alpine environment. Botanical Review 81, 70–103.
| Towards an understanding of factors controlling seed bank composition and longevity in the alpine environment.Crossref | GoogleScholarGoogle Scholar |
Jaramillo MA, Kramer EM (2007) Molecular evolution of the petal and stamen identity genes, APETALA3 and PISTILLATA, after petal loss in the Piperales. Molecular Phylogenetics and Evolution 44, 598–609.
| Molecular evolution of the petal and stamen identity genes, APETALA3 and PISTILLATA, after petal loss in the Piperales.Crossref | GoogleScholarGoogle Scholar |
Jayasuriya KG, Baskin JM, Baskin CC (2009) Sensitivity cycling and its ecological role in seeds with physical dormancy. Seed Science Research 19, 3–13.
| Sensitivity cycling and its ecological role in seeds with physical dormancy.Crossref | GoogleScholarGoogle Scholar |
Joët T, Ourcival J-M, Capelli M, Dussert S, Morin X (2016) Explanatory ecological factors for the persistence of desiccation-sensitive seeds in transient soil seed banks: Quercus ilex as a case study. Annals of Botany 117, 165–176.
| Explanatory ecological factors for the persistence of desiccation-sensitive seeds in transient soil seed banks: Quercus ilex as a case study.Crossref | GoogleScholarGoogle Scholar |
Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M (2010) Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant & Cell Physiology 51, 1988–2001.
| Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions.Crossref | GoogleScholarGoogle Scholar |
Kermode AR, Finch-Savage BE (2002) Desiccation sensitivity in orthodox and recalcitrant seeds in relation to development. In ‘Desiccation and survival in plants: drying without dying’. (Eds M Black, HW Pritchard) pp.149–184. (CABI Publishing: Wallingford, UK)
Kew RBG (2017) Seed information database – SID. Release 7.1. Available at http://data.kew.org/sid/ [Verified 18 May 2018]
Khandelwal A, Cho S, Marella H, Sakata Y, Perroud P-F, Pan A, Quatrano R (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327, 546
| Role of ABA and ABI3 in desiccation tolerance.Crossref | GoogleScholarGoogle Scholar |
Kimura M, Ohta T (1971) ‘Theoretical aspects of population genetics.’ (Princeton University Press: Princeton, NJ, USA)
Koonin EV (2009) Darwinian evolution in the light of genomics. Nucleic Acids Research 37, 1011–1034.
| Darwinian evolution in the light of genomics.Crossref | GoogleScholarGoogle Scholar |
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Current Opinion in Plant Biology 5, 33–36.
| Seed dormancy and germination.Crossref | GoogleScholarGoogle Scholar |
Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281–307.
| Plant hormone interactions during seed dormancy release and germination.Crossref | GoogleScholarGoogle Scholar |
Le Tam V, Hong T, Ellis R, Ngoc-Tam B (2004) Seed storage of Avicennia alba Bl. Seed Science and Technology 32, 531–536.
| Seed storage of Avicennia alba Bl.Crossref | GoogleScholarGoogle Scholar |
Leck MA (2012) ‘Ecology of soil seed banks.’ (Elsevier: New York)
Levins R (1968) ‘Evolution in changing environments: some theoretical explorations.’ (Princeton University Press: Princeton, NJ, USA)
Levitt J (1980) ‘Responses of plants to environmental stress. Vol. 1: Chilling, freezing, and high temperature stresses’. (Academic Press: New York)
Li DZ, Pritchard HW (2009) The science and economics of ex situ plant conservation. Trends in Plant Science 14, 614–621.
| The science and economics of ex situ plant conservation.Crossref | GoogleScholarGoogle Scholar |
Long RL, Panetta FD, Steadman KJ, Probert R, Bekker RM, Brooks S, Adkins SW (2008) Seed persistence in the field may be predicted by laboratory-controlled aging. Weed Science 56, 523–528.
| Seed persistence in the field may be predicted by laboratory-controlled aging.Crossref | GoogleScholarGoogle Scholar |
Long RL, Gorecki MJ, Renton M, Scott JK, Colville L, Goggin DE, Commander LE, Westcott DA, Cherry H, Finch‐Savage WE (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews of the Cambridge Philosophical Society 90, 31–59.
| The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise.Crossref | GoogleScholarGoogle Scholar |
Lynch M, Gabriel W (1987) Environmental tolerance. American Naturalist 129, 283–303.
| Environmental tolerance.Crossref | GoogleScholarGoogle Scholar |
Maia J, Dekkers BJ, Provart NJ, Ligterink W, Hilhorst HW (2011) The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome. PLoS One 6, e29123
| The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome.Crossref | GoogleScholarGoogle Scholar |
Maia J, Dekkers BJ, Dolle MJ, Ligterink W, Hilhorst HW (2014) Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. New Phytologist 203, 81–93.
| Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar |
Marella HH, Sakata Y, Quatrano RS (2006) Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3‐like genes from Physcomitrella patens. The Plant Journal 46, 1032–1044.
| Characterization and functional analysis of ABSCISIC ACID INSENSITIVE3‐like genes from Physcomitrella patens.Crossref | GoogleScholarGoogle Scholar |
McNeal JR, Kuehl JV, Boore JL, de Pamphilis CW (2007) Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta. BMC Plant Biology 7, 57
| Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus Cuscuta.Crossref | GoogleScholarGoogle Scholar |
Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. Journal of Ecology 92, 372–383.
| Seedling survival and seed size: a synthesis of the literature.Crossref | GoogleScholarGoogle Scholar |
Murdoch AJ, Ellis RH (1992) Longevity, viability and dormancy. In ‘Seeds: the ecology of regeneration in plant communities’. (Ed. M Fenner) pp. 193–229. (CABI Publishing: Wallingford, UK)
Nambara E, Naito S, McCourt P (1992) A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. The Plant Journal 2, 435–441.
| A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele.Crossref | GoogleScholarGoogle Scholar |
Nesi N, Delourme R, Brégeon M, Falentin C, Renard M (2008) Genetic and molecular approaches to improve nutritional value of Brassica napus L. seed. Comptes Rendus Biologies 331, 763–771.
| Genetic and molecular approaches to improve nutritional value of Brassica napus L. seed.Crossref | GoogleScholarGoogle Scholar |
Nguyen TP, Keizer P, van Eeuwijk F, Smeekens S, Bentsink L (2012) Natural variation for seed longevity and seed dormancy are negatively correlated in Arabidopsis. Plant Physiology 160, 2083–2092.
| Natural variation for seed longevity and seed dormancy are negatively correlated in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Obroucheva N, Antipova O (2004) The role of water uptake in the transition of recalcitrant seeds from dormancy to germination. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 51, 848–856.
| The role of water uptake in the transition of recalcitrant seeds from dormancy to germination.Crossref | GoogleScholarGoogle Scholar |
Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530, 331–335.
| The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea.Crossref | GoogleScholarGoogle Scholar |
Ooms JJ, Veen R, Karssen CM (1994) Abscisic acid and osmotic stress or slow drying independently induce desiccation tolerance in mutant seeds of Arabidopsis thaliana. Physiologia Plantarum 92, 506–510.
| Abscisic acid and osmotic stress or slow drying independently induce desiccation tolerance in mutant seeds of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Orozco-Segovia A, Vazquez-Yanes C (1990) Effect of moisture on longevity in seeds of some rain forest species. Biotropica 22, 215–216.
| Effect of moisture on longevity in seeds of some rain forest species.Crossref | GoogleScholarGoogle Scholar |
Pammenter N, Berjak P (2000) Evolutionary and ecological aspects of recalcitrant seed biology. Seed Science Research 10, 301–306.
| Evolutionary and ecological aspects of recalcitrant seed biology.Crossref | GoogleScholarGoogle Scholar |
Pan J, Han H, Jiang X, Zhang W, Zhao N, Song S, Li X, Li X (2012) Desiccation, moisture content and germination of Zostera marina L. seed. Restoration Ecology 20, 311–314.
| Desiccation, moisture content and germination of Zostera marina L. seed.Crossref | GoogleScholarGoogle Scholar |
Piña-Rodrigues F, Figliolia M (2005) Embryo immaturity associated with delayed germination in recalcitrant seeds of Virola surinamensis (Rol.) Warb.(Myristicaceae). Seed Science and Technology 33, 375–386.
| Embryo immaturity associated with delayed germination in recalcitrant seeds of Virola surinamensis (Rol.) Warb.(Myristicaceae).Crossref | GoogleScholarGoogle Scholar |
Pritchard HW, Daws MI, Fletcher BJ, Gaméné CS, Msanga HP, Omondi W (2004) Ecological correlates of seed desiccation tolerance in tropical African dryland trees. American Journal of Botany 91, 863–870.
| Ecological correlates of seed desiccation tolerance in tropical African dryland trees.Crossref | GoogleScholarGoogle Scholar |
Pukacka S, Ratajczak E (2006) Antioxidative response of ascorbate–glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds. Journal of Plant Physiology 163, 1259–1266.
| Antioxidative response of ascorbate–glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds.Crossref | GoogleScholarGoogle Scholar |
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiology 133, 1755–1767.
| Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.Crossref | GoogleScholarGoogle Scholar |
Rajjou L, Debeaujon I (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. Comptes Rendus Biologies 331, 796–805.
| Seed longevity: survival and maintenance of high germination ability of dry seeds.Crossref | GoogleScholarGoogle Scholar |
Rees M (1994) Delayed germination of seeds: a look at the effects of adult longevity, the timing of reproduction, and population age/stage structure. American Naturalist 144, 43–64.
| Delayed germination of seeds: a look at the effects of adult longevity, the timing of reproduction, and population age/stage structure.Crossref | GoogleScholarGoogle Scholar |
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9, 981–993.
| Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions.Crossref | GoogleScholarGoogle Scholar |
Roach T, Beckett RP, Minibayeva FV, Colville L, Whitaker C, Chen H, Bailly C, Kranner I (2010) Extracellular superoxide production, viability and redox poise in response to desiccation in recalcitrant Castanea sativa seeds. Plant, Cell & Environment 33, 59–75.
Roberts EH (1973) Predicting the storage life of seeds. Seed Science and Technology 1, 499–514.
Roberts EH, Ellis RH (1989) Water and seed survival. Annals of Botany 63, 39
| Water and seed survival.Crossref | GoogleScholarGoogle Scholar |
Sano N, Rajjou L, North HM, Debeaujon I, Marion-Poll A, Seo M (2016) Staying alive: molecular aspects of seed longevity. Plant & Cell Physiology 57, 660–674.
| Staying alive: molecular aspects of seed longevity.Crossref | GoogleScholarGoogle Scholar |
Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. The Plant Journal 54, 608–620.
| Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Sattler SE, Gilliland LU, Magallanes-Lundback M, Pollard M, DellaPenna D (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. The Plant Cell 16, 1419–1432.
| Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination.Crossref | GoogleScholarGoogle Scholar |
Seed Information Database Kew (2008) Release 7.1. http://data.kew.org/sid/
Shu K, Chen Q, Wu Y, Liu R, Zhang H, Wang P, Li Y, Wang S, Tang S, Liu C (2016) ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels. The Plant Journal 85, 348–361.
| ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels.Crossref | GoogleScholarGoogle Scholar |
Silverstone AL, Ciampaglio CN, Sun T-p (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. The Plant Cell 10, 155–169.
| The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway.Crossref | GoogleScholarGoogle Scholar |
Silvertown JW (1981) Seed size, life span, and germination date as coadapted features of plant life history. American Naturalist 118, 860–864.
| Seed size, life span, and germination date as coadapted features of plant life history.Crossref | GoogleScholarGoogle Scholar |
Silvertown J, Charlesworth D (2009) ‘Introduction to plant population biology.’ (John Wiley & Sons: Chichester, UK)
Steinbach HS, Benech-Arnold R, Kristof G, Sánchez R, Marcucci-Poltri S (1995) Physiological basis of pre-harvest sprouting resistance in Sorghum bicolor (L.) Moench. ABA levels and sensitivity in developing embryos of sprouting-resistant and-susceptible varieties. Journal of Experimental Botany 46, 701–709.
| Physiological basis of pre-harvest sprouting resistance in Sorghum bicolor (L.) Moench. ABA levels and sensitivity in developing embryos of sprouting-resistant and-susceptible varieties.Crossref | GoogleScholarGoogle Scholar |
Sussex I (1975) Growth and metabolism of the embryo and attached seedling of the viviparous mangrove, Rhizophora mangle. American Journal of Botany 62, 948–953.
| Growth and metabolism of the embryo and attached seedling of the viviparous mangrove, Rhizophora mangle.Crossref | GoogleScholarGoogle Scholar |
Terrasson E, Buitink J, Righetti K, Ly Vu B, Pelletier S, Zinsmeister J, Lalanne D, Leprince O (2013) An emerging picture of the seed desiccome: confirmed regulators and newcomers identified using transcriptome comparison. Frontiers in Plant Science 4, 497
| An emerging picture of the seed desiccome: confirmed regulators and newcomers identified using transcriptome comparison.Crossref | GoogleScholarGoogle Scholar |
Thompson K, Band S, Hodgson J (1993) Seed size and shape predict persistence in soil. Functional Ecology 7, 236–241.
| Seed size and shape predict persistence in soil.Crossref | GoogleScholarGoogle Scholar |
Thompson K, Bakker JP, Bekker RM (1997) ‘The soil seed banks of North West Europe: methodology, density and longevity.’ (Cambridge University Press: Cambridge, UK)
To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. The Plant Cell 18, 1642–1651.
| A network of local and redundant gene regulation governs Arabidopsis seed maturation.Crossref | GoogleScholarGoogle Scholar |
Tucker SC (2001) The ontogenetic basis for missing petals in Crudia (Leguminosae: Caesalpinioideae: Detarieae). International Journal of Plant Sciences 162, 83–89.
| The ontogenetic basis for missing petals in Crudia (Leguminosae: Caesalpinioideae: Detarieae).Crossref | GoogleScholarGoogle Scholar |
Tweddle JC, Dickie JB, Baskin CC, Baskin JM (2003) Ecological aspects of seed desiccation sensitivity. Journal of Ecology 91, 294–304.
| Ecological aspects of seed desiccation sensitivity.Crossref | GoogleScholarGoogle Scholar |
Van Tienderen PH (1991) Evolution of generalists and specialist in spatially heterogeneous environments. Evolution 45, 1317–1331.
| Evolution of generalists and specialist in spatially heterogeneous environments.Crossref | GoogleScholarGoogle Scholar |
Vaz TA, Davide AC, Rodrigues-Junior AG, Nakamura AT, Tonetti OA, da Silva EA (2016) Swartzia langsdorffii Raddi: morphophysiological traits of a recalcitrant seed dispersed during the dry season. Seed Science Research 26, 47–56.
| Swartzia langsdorffii Raddi: morphophysiological traits of a recalcitrant seed dispersed during the dry season.Crossref | GoogleScholarGoogle Scholar |
Vázquez-Yanes C, Orozco-Segovia A (1993) Patterns of seed longevity and germination in the tropical rainforest. Annual Review of Ecology and Systematics 24, 69–87.
| Patterns of seed longevity and germination in the tropical rainforest.Crossref | GoogleScholarGoogle Scholar |
Verdier J, Lalanne D, Pelletier S, Torres-Jerez I, Righetti K, Bandyopadhyay K, Leprince O, Chatelain E, Vu BL, Gouzy J, Gamas P, Udvardi MK, Buitink J (2013) A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiology 163, 757–774.
| A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds.Crossref | GoogleScholarGoogle Scholar |
Villiers T (1974) Seed aging: chromosome stability and extended viability of seeds stored fully imbided. Plant Physiology 53, 875–878.
| Seed aging: chromosome stability and extended viability of seeds stored fully imbided.Crossref | GoogleScholarGoogle Scholar |
Vu BL, Satour P, Leprince O (2003) The re-establishment of desiccation tolerance in germinated radicles of Medicago truncatula Gaertn. seeds. Seed Science Research 13, 273–286.
| The re-establishment of desiccation tolerance in germinated radicles of Medicago truncatula Gaertn. seeds.Crossref | GoogleScholarGoogle Scholar |
Walters C, Berjak P, Pammenter N, Kennedy K, Raven P (2013) Preservation of recalcitrant seeds. Science 339, 915–916.
| Preservation of recalcitrant seeds.Crossref | GoogleScholarGoogle Scholar |
West MA, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. The Plant Cell 6, 1731–1745.
| LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
White CN, Proebsting WM, Hedden P, Rivin CJ (2000) Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways. Plant Physiology 122, 1081–1088.
| Gibberellins and seed development in maize. I. Evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways.Crossref | GoogleScholarGoogle Scholar |
Whitmore TC (1990) ‘An introduction to tropical rain forests.’ (Clarendon Press: Wotton-under-Edge, UK)
Wright S (1986) ‘Evolution: selected papers.’ (University of Chicago Press: Chicago, IL, USA)
Wyse SV, Dickie JB (2017) Predicting the global incidence of seed desiccation sensitivity. Journal of Ecology 105, 1082–1093.
| Predicting the global incidence of seed desiccation sensitivity.Crossref | GoogleScholarGoogle Scholar |
Zeng Y, Kermode AR (2004) A gymnosperm ABI3 gene functions in a severe abscisic acid-insensitive mutant of Arabidopsis (abi3-6) to restore the wild-type phenotype and demonstrates a strong synergistic effect with sugar in the inhibition of post-germinative growth. Plant Molecular Biology 56, 731–746.
| A gymnosperm ABI3 gene functions in a severe abscisic acid-insensitive mutant of Arabidopsis (abi3-6) to restore the wild-type phenotype and demonstrates a strong synergistic effect with sugar in the inhibition of post-germinative growth.Crossref | GoogleScholarGoogle Scholar |
Zinsmeister J, Lalanne D, Terrasson E, Chatelain E, Vandecasteele C, Vu BL, Dubois-Laurent C, Geoffriau E, Le Signor C, Dalmais M (2016) ABI5 is a regulator of seed maturation and longevity in legumes. The Plant Cell 28, 2735–2754.
| ABI5 is a regulator of seed maturation and longevity in legumes.Crossref | GoogleScholarGoogle Scholar |
