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Stress–response relationships related to ageing and death of orthodox seeds: a study comparing viability and RNA integrity in soya bean (Glycine max) cv. Williams 82

Published online by Cambridge University Press:  15 September 2020

Christina Walters*
Affiliation:
USDA-ARS National Laboratory for Genetic Resources Preservation, 1111 S. Mason Street, Fort Collins, CO80521, USA
Margaret B. Fleming
Affiliation:
USDA-ARS National Laboratory for Genetic Resources Preservation, 1111 S. Mason Street, Fort Collins, CO80521, USA
Lisa M. Hill
Affiliation:
USDA-ARS National Laboratory for Genetic Resources Preservation, 1111 S. Mason Street, Fort Collins, CO80521, USA
Emma J. Dorr
Affiliation:
USDA-ARS National Laboratory for Genetic Resources Preservation, 1111 S. Mason Street, Fort Collins, CO80521, USA
Christopher M. Richards
Affiliation:
USDA-ARS National Laboratory for Genetic Resources Preservation, 1111 S. Mason Street, Fort Collins, CO80521, USA
*
Author for Correspondence: Christina Walters, E-mail: christina.walters@ars.usda.gov

Abstract

Characterizing non-lethal damage within dry seeds may allow us to detect early signs of ageing and accurately predict longevity. We compared RNA degradation and viability loss in seeds exposed to stressful conditions to quantify relationships between degradation rates and stress intensity or duration. We subjected recently harvested (‘fresh’) ‘Williams 82’ soya bean seeds to moisture, temperature and oxidative stresses, and measured time to 50% viability (P50) and rate of RNA degradation, the former using standard germination assays and the latter using RNA Integrity Number (RIN). RIN values from fresh seeds were also compared with those from accessions of the same cultivar harvested in the 1980s and 1990s and stored in the refrigerator (5°C), freezer (−18°C) or in vapour above liquid nitrogen (−176°C). Rates of viability loss (P50−1) and RNA degradation (RIN⋅d−1) were highly correlated in soya bean seeds that were exposed to a broad range of temperatures [holding relative humidity (RH) constant at about 30%]. However, the correlation weakened when fresh seeds were maintained at high RH (holding temperature constant at 35°C) or exposed to oxidizing agents. Both P50−1 and RIN⋅d−1 parameters exhibited breaks in Arrhenius behaviour near 50°C, suggesting that constrained molecular mobility regulates degradation kinetics of dry systems. We conclude that the kinetics of ageing reactions at RH near 30% can be simulated by temperatures up to 50°C and that RNA degradation can indicate ageing prior to and independent of seed death.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

Current address: Department of Plant Biology, 612 Wilson Road, Room 262, Michigan State University, East Lansing, MI 48824-1312, USA.

References

Agacka, M, Laskowska, D, Doroszewska, T, Hay, FR and Börner, A (2014) Longevity of Nicotiana seeds conserved at low temperatures in ex situ genebanks. Seed Science and Technology 42, 355362.CrossRefGoogle Scholar
Angell, CA (1995) Formation of glasses from liquids and biopolymers. Science 267, 19241935.CrossRefGoogle ScholarPubMed
Ballesteros, D and Walters, C (2011) Detailed characterization of mechanical properties and molecular mobility within dry seed glasses: relevance to the physiology of dry biological systems. Plant Journal 68, 607619.CrossRefGoogle ScholarPubMed
Ballesteros, D, Hill, LM, Lynch, RT, Pritchard, HW and Walters, C (2019) Longevity of preserved germplasm: the temperature dependency of aging reactions in glassy matrices of dried fern spores. Plant and Cell Physiology 60, 376392. https://doi.org/10.1093/pcp/pcy217CrossRefGoogle ScholarPubMed
Bhattacharya, S and Suryanarayanan, R (2009) Local mobility in amorphous pharmaceuticals - characterization and implications on stability. Journal of Pharmacological Sciences 98, 29352953.CrossRefGoogle ScholarPubMed
Buitink, J and Leprince, O (2008) Intracellular glasses and seed survival in the dry state. Comptes Rendus Biologies 331, 788795.Google ScholarPubMed
Chang, LL and Pikal, MJ (2009) Mechanisms of protein stabilization in the solid state. Journal of Pharmacological Science 98, 28862908.Google ScholarPubMed
Clerkx, EJ, El-Lithy, ME, Vierling, E, Ruys, GJ, Blankestijn-De Vries, H, Groot, SP, Vreugdenhil, D and Koornneef, M (2004) 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, 432443.Google ScholarPubMed
Conger, AD and Randolph, ML (1968) Is age-dependent genetic damage in seeds caused by free radicals? Radiation Botany 8, 193196.CrossRefGoogle Scholar
Crawley, MJ (2007) The R Book. Chichester, Wiley.Google Scholar
Dirk, LM and Downie, AB (2018) An examination of Job's rule: protection and repair of the proteins of the translational apparatus in seeds. Seed Science Research 28, 168181.CrossRefGoogle Scholar
Ellis, RH and Roberts, EH (1980) Improved equations for the prediction of seed longevity. Annals of Botany 45, 1330.CrossRefGoogle Scholar
Ellis, RH, Hong, TD and Roberts, EH (1988) A low-moisture-content limit to logarithmic relations between seed moisture content and longevity. Annals of Botany 61, 405408.CrossRefGoogle Scholar
Ferrio, JP, Alonso, N, Voltas, J and Araus, JL (2004) Estimating grain weight in archaeological cereal crops: a quantitative approach for comparison with current conditions. Journal of Archaeological Science 31, 16351642.CrossRefGoogle Scholar
Fleming, MB, Richards, CM and Walters, C (2017) Decline in RNA integrity of dry-stored soybean seeds correlates with loss of germination potential. Journal of Experimental Botany 68, 22192230.Google ScholarPubMed
Fleming, MB, Patterson, EL, Reeves, PA, Richards, CM, Gaines, TA and Walters, C (2018a) Exploring the fate of mRNA in aging seeds: protection, destruction, or slow decay? Journal of Experimental Botany 69, 43094321. https://doi.org/10.1093/jxb/ery215.CrossRefGoogle Scholar
Fleming, MB, Hill, LM and Walters, C (2018b) The kinetics of aging in dry-stored seeds: a comparison of viability loss and RNA degradation in unique ‘legacy’ seed collections. Annals of Botany 123, 11331146. https://doi.org/10.1093/aob/mcy217.CrossRefGoogle Scholar
Fundo, JF, Quintas, MA and Silva, CL (2015) Molecular dynamics and structure in physical properties and stability of food systems. Food Engineering Reviews 7, 384392.CrossRefGoogle Scholar
Glenister, PH and Lyon, MF (1986) Long-term storage of eight-cell mouse embryos at −196°C. Journal of In Vitro Fertilization and Embryo Transfer 3, 2027.CrossRefGoogle ScholarPubMed
Groot, SPC, Surki, AA, De Vos, RCH and Kodde, J (2012) Seed storage at elevated partial pressure of oxygen, a fast method for analysing seed ageing under dry conditions. Annals of Botany 110, 11491159.CrossRefGoogle ScholarPubMed
Groot, SP, de Groot, L, Kodde, J and van Treuren, R (2015) Prolonging the longevity of ex situ conserved seeds by storage under anoxia. Plant Genetic Resources 3, 1826.CrossRefGoogle Scholar
Halliwell, B and Chirico, S (1993) Lipid peroxidation: its mechanism, measurement, and significance. The American Journal of Clinical Nutrition 57, 715725.CrossRefGoogle ScholarPubMed
Halliwell, B and Gutteridge, JM (2015) Free radicals in biology and medicine. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Harman, D (2006) Free radical theory of aging: an update. Annals of the New York Academy of Sciences 1067, 1021.CrossRefGoogle ScholarPubMed
Hay, FR, Mead, A, Manger, K and Wilson, FJ (2003) One-step analysis of seed storage data and the longevity of Arabidopsis thaliana seeds. Journal of Experimental Botany 54, 9931011.CrossRefGoogle ScholarPubMed
Hay, FR, Valdez, R, Lee, JS, Cruz, S and Pompe, C (2018) Seed longevity phenotyping: recommendations on research methodology. Journal of Experimental Botany 70, 425434.Google Scholar
Kato, KL and Cameron, RE (1999) A review of the relationship between thermally-accelerated ageing of paper and hornification. Cellulose 6, 2340.CrossRefGoogle Scholar
Khan, MM, Hendry, GA, Atherton, NM and Vertucci-Walters, CW (1996) Free radical accumulation and lipid peroxidation in testas of rapidly aged soybean seeds: a light-promoted process. Seed Science Research 6, 101107.CrossRefGoogle Scholar
Kranner, I, Minibayeva, FV, Beckett, RP and Seal, CE (2010) What is stress? Concepts, definitions and applications in seed science. New Phytologist 188, 655673.CrossRefGoogle ScholarPubMed
Levitt, J (1980) Responses of plants to environmental stress. Vol. 1: Chilling, Freezing, and High Temperature Stresses. New York, Academic Press.Google Scholar
Li, CS, Shao, GS, Wang, L, Wang, ZF, Mao, YJ, Wang, XQ and Zhang, HS (2017) QTL identification and fine mapping for seed storability in rice (Oryza sativa L.). Euphytica 213, 127.Google Scholar
Lindsey, BE III, Rivero, L, Calhoun, CS, Grotewold, E and Brkljacic, J (2017) Standardized method for high-throughput sterilization of Arabidopsis seeds. Journal of Visualized Experiments JoVE 128, 56587. https://doi.org/10.3791/56587Google Scholar
Menart, E, De Bruin, G and Strlič, M (2011) Dose–response functions for historic paper. Polymer Degradation and Stability 96, 20292039.CrossRefGoogle Scholar
Meryman, HT (1974) Freezing injury and its prevention in living cells. Annual Review of Biophysics and Bioengineering 3, 341363.CrossRefGoogle ScholarPubMed
Mira, S, González-Benito, ME, Hill, LM and Walters, C (2010) Characterization of volatile production during storage of lettuce (Lactuca sativa) seed. Journal of Experimental Botany 61, 39153924.CrossRefGoogle ScholarPubMed
Nagel, M, Kranner, I, Neumann, K, Rolletschek, H, Seal, CE, Colville, L and Börner, A (2015) Genome-wide association mapping and biochemical markers reveal that seed ageing and longevity are intricately affected by genetic background and developmental and environmental conditions in barley. Plant, Cell and Environment 38, 10111022.Google ScholarPubMed
Navarro, E, Fabrègue, O, Scorretti, R, Reboulet, J, Simonet, P, Dawson, L and Demanèche, S (2015) RisaAligner software for aligning fluorescence data between Agilent 2100 Bioanalyzer chips: application to soil microbial community analysis. BioTechniques 59, 347358.Google ScholarPubMed
Nelson, DL, Lehninger, AL and Cox, MM (2008) Lehninger principles of biochemistry. New York, MacMillan.Google Scholar
Nyström, T (2005) Role of oxidative carbonylation in protein quality control and senescence. EMBO Journal 24, 13111317.CrossRefGoogle ScholarPubMed
Ohlrogge, JB and Kernan, TP (1982) Oxygen-dependent aging of seeds. Plant Physiology 70, 791794.Google ScholarPubMed
Priestley, DA, Werner, BG and Leopold, AC (1985) The susceptibility of soybean seed lipids to artificially-enhanced atmospheric oxidation. Journal of Experimental Botany 36, 16531659.CrossRefGoogle Scholar
Pritchard, HW and Dickie, JB (2003) Predicting seed longevity: the use and abuse of seed viability equations, pp. 653722 in Smith, RD; Dickie, JB; Linington, SH; Pritchard, HW; Probert, RJ (Eds) Seed conservation: turning science into practice, London, Royal Botanic Gardens Kew.Google Scholar
Probert, RJ, Daws, MI and Hay, FR (2009) Ecological correlates of ex situ seed longevity: a comparative study on 195 species. Annals of Botany 104, 5769.Google ScholarPubMed
Rajjou, L, Lovigny, Y, Groot, SP, Belghazi, M, Job, C and Job, D (2008) Proteome-wide characterization of seed aging in Arabidopsis: a comparison between artificial and natural aging protocols. Plant Physiology 148, 620641.CrossRefGoogle ScholarPubMed
RBG Kew (Royal Botanic Gardens Kew) (2018) Seed Information Database (SID). Version 7.1. Available from: http://data.kew.org/sid/ (accessed 15 December 2018).Google Scholar
R Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Sano, N, Rajjou, L, North, HM, Debeaujon, I, Marion-Poll, A and Seo, M (2016) Staying alive: molecular aspects of seed longevity. Plant and Cell Physiology 57, 660674.Google ScholarPubMed
Sattler, SE, Gilliland, LU, Magallanes-Lundback, M, Pollard, M and DellaPenna, D (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16, 14191432.CrossRefGoogle ScholarPubMed
Schroeder, A, Mueller, O, Stocker, S, Salowsky, R, Leiber, M, Gassmann, M and Ragg, T (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Molecular Biology 7, 3. https://doi.org/10.1186/1471-2199-7-3Google ScholarPubMed
Schwember, AR and Bradford, KJ (2010) Quantitative trait loci associated with longevity of lettuce seeds under conventional and controlled deterioration storage conditions. Journal of Experimental Botany 61, 44234436.CrossRefGoogle ScholarPubMed
Singh, B and Sharma, N (2008) Mechanistic implications of plastic degradation. Polymer Degradation and Stability 93, 561584.Google Scholar
Sun, WQ and Leopold, AC (1994) Glassy state and seed storage stability: a viability equation analysis. Annals of Botany 74, 601604.Google Scholar
Threadgold, J and Brown, TA (2003) Degradation of DNA in artificially charred wheat seeds. Journal of Archaeological Science 30, 10671076.CrossRefGoogle Scholar
Vertucci, CW, Roos, EE and Crane, J (1994) Theoretical basis of protocols for seed storage III. Optimum moisture contents for pea seeds stored at different temperatures. Annals of Botany 74, 531540.CrossRefGoogle Scholar
Walters, C (1998) Understanding the mechanisms and kinetics of seed aging. Seed Science Research 8, 223244.CrossRefGoogle Scholar
Walters, C (2015) Orthodoxy, recalcitrance and in-between: describing variation in seed storage characteristics using threshold responses to water loss. Planta 242, 397406.CrossRefGoogle ScholarPubMed
Walters, C, Farrant, JM, Pammenter, NW and Berjak, P (2002) Desiccation stress and damage, pp. 263291 in Black, M; Pritchard, H (Eds) Desiccation and survival in plants: drying without dying. Wallingford, CAB International.Google Scholar
Walters, C, Wheeler, L and Stanwood, PC (2004) Longevity of cryogenically stored seeds. Cryobiology 48, 229244.CrossRefGoogle ScholarPubMed
Walters, C, Wheeler, LM and Grotenhuis, JM (2005) Longevity of seeds stored in a genebank: species characteristics. Seed Science Research 15, 120.CrossRefGoogle Scholar
Walters, C, Ballesteros, D and Vertucci, VA (2010) Structural mechanics of seed deterioration: standing the test of time. Plant Science 179, 565573.CrossRefGoogle Scholar
Wurtmann, EJ and Wolin, SL (2009) RNA under attack: cellular handling of RNA damage. Critical Reviews in Biochemistry and Molecular Biology 44, 3449.Google ScholarPubMed
Yoshioka, S and Aso, Y (2007) Correlations between molecular mobility and chemical stability during storage of amorphous pharmaceuticals. Journal of Pharmacological Sciences 96, 960–81.CrossRefGoogle ScholarPubMed
Zheng, GH, Jing, XM and Tao, KL (1998) Ultra dry seed storage cuts cost of gene bank. Nature 393, 223.Google Scholar
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