Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-26T06:55:11.369Z Has data issue: false hasContentIssue false
  • English
  • Français

Sensitivity to hypoxia and microbial activity are instrumental in pericarp-imposed dormancy expression in sunflower (Helianthus annuus L.)

Published online by Cambridge University Press:  18 April 2019

Constanza P. Dominguez ,
María V. Rodríguez ,
Diego Batlla ,
Inés E. García de Salamone ,
Anita I. Mantese ,
Ana L. Andreani  and
Roberto L. Benech-Arnold
Constanza P. Dominguez*
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Producción Vegetal, Cátedra de Cultivos Industriales and Instituto de Fisiología y Ecología Vinculado a la Agricultura, Consejo Nacional de Investigaciones Científicas y Técnicas (IFEVA-CONICET), Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina
María V. Rodríguez
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Biología Aplicada y Alimentos, Cátedra de Fisiología Vegetal and Instituto de Fisiología y Ecología Vinculado a la Agricultura, Consejo Nacional de Investigaciones Científicas y Técnicas (IFEVA-CONICET), Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina
Diego Batlla
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Producción Vegetal, Cátedra de Cerealicultura and Instituto de Fisiología y Ecología Vinculado a la Agricultura, Consejo Nacional de Investigaciones Científicas y Técnicas (IFEVA-CONICET), Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina
Inés E. García de Salamone
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Biología Aplicada y Alimentos, Cátedra de Microbiología Agrícola, Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina
Anita I. Mantese
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Recursos Naturales y Ambiente, Cátedra de Botánica General, Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina
Ana L. Andreani
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Biología Aplicada y Alimentos, Cátedra de Fisiología Vegetal, Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina.
Roberto L. Benech-Arnold
Affiliation:
Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Producción Vegetal, Cátedra de Cultivos Industriales and Instituto de Fisiología y Ecología Vinculado a la Agricultura, Consejo Nacional de Investigaciones Científicas y Técnicas (IFEVA-CONICET), Av. San Martín 4453, C1417DSE, Ciudad de Buenos Aires, Argentina
*
Author for correspondence: Constanza P. Dominguez, cdomingu@agro.uba.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

We used two sunflower genotypes displaying pericarp-imposed dormancy at high incubation temperatures (i.e. 30°C) to investigate the role of the pericarp as a limitation to oxygen availability to the embryo (hypoxia), and its impact on embryo abscisic acid (ABA) content and sensitivity to ABA. Results showed that both genotypes displayed very different oxygen threshold values for inhibition of embryo germination when incubation was performed at 30°C. Expression of dormancy in one genotype was therefore related to exacerbated embryo sensitivity to hypoxia, whereas in the other genotype, the pericarp appeared to act as a more severe restraint to oxygen entry. Increased sensitivity to hypoxia was, in part, related to increased sensitivity to ABA, but not to alterations in ABA metabolism. The activity of pericarp-microbial communities (bacteria and fungi) at high temperatures was also assessed as a potential determinant of hypoxia to the embryo. Oxygen consumption in pericarps incubated at 30°C was attenuated with antibiotics, which concomitantly promoted achene germination. In agreement with the observed more severe oxygen deprivation to the embryo exerted by the pericarp, the bacterial load in the pericarp was significantly higher in the commercial hybrid than in the inbred line; however, the application of antibiotics strongly reduced the bacterial colony counts for each genotype. Different bacterial and fungal communities, assessed through their profiles of carbon-source utilization, were determined between genotypes and after treatment with antibiotics. This work highlights the relationship between enhancement of sensitivity to hypoxia with incubation temperature and seed dormancy expression, and suggests that microbial activity might be part of the mechanism through which hypoxia is imposed.

Keywords

abscisic aciddormancyHelianthus annuus L.hypoxiamicrobial activitypericarptemperature
Type
Research Paper
Information
Seed Science Research , Volume 29 , Issue 2 , June 2019 , pp. 85 - 96
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrade, A, Riera, N, Lindstrom, L, Alemano, S, Alvarez, D, Abdala, G and Vigliocco, A (2015) Pericarp anatomy and hormone profiles of cypselas in dormant and non-dormant inbred sunflower lines. Plant Biology 17, 351–360. doi: 10.1111/plb.12244Google Scholar
Anton, GF, Joiţa-Păcureanu, M and Cucerevii, A (2015) Diversification of sunflower germplasm for different economically important characteristics. Scientific Papers. Series A. Agronomy LVIII, 123–127.Google Scholar
Barret, M, Briand, M, Bonneau, S, Préveaux, A, Valière, S, Bouchez, O, Hunault, G, Simoneau, P and Jacques, M-A (2015) Emergence shapes the structure of the seed microbiota. Applied and Environmental Microbiology 81, 1257–1266. doi: 10.1128/AEM.03722-14Google Scholar
Bazin, J, Batlla, D, Dussert, S, El-Maarouf-Bouteau, H and Bailly, C (2011) Role of relative humidity, temperature, and water status in dormancy alleviation of sunflower seeds during dry after-ripening. Journal of Experimental Botany 62, 627–640. doi: 10.1093/jxb/erq314Google Scholar
Benech-Arnold, RL (2004) Inception, maintenance, and termination of dormancy in grain crops: Physiology, genetics, and environmental control, pp. 169–198 in Benech-Arnold, RL and Sánchez, R (eds), Handbook of Seed Physiology: Applications to Agriculture. New York, USA: Food Products Press.Google Scholar
Benech-Arnold, R, Sánchez, R, Forcella, F, Kruk, B and Ghersa, C (2000) Environmental control of dormancy in weed seed banks in soil. Field Crops Reseach 67, 105–122. doi: 10.1016/S0378-4290(00)00087-3Google Scholar
Benech-Arnold, RL, Gualano, N, Leymarie, J, Côme, D and Corbineau, F (2006) Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. Journal of Experimental Botany 57, 1423–1430. doi: 10.1093/jxb/erj122Google Scholar
Bewley, JD (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066. doi: 10.1105/tpc.9.7.1055Google Scholar
Black, M, Bewley, JD and Halmer, P (2006) The Encyclopedia of Seeds: Science, Technology and Uses. Cambridge, USA: CAB International.Google Scholar
Bodrone, MP, Rodríguez, MV, Arisnabarreta, S and Batlla, D (2017) Maternal environment and dormancy in sunflower: the effect of temperature during fruit development. European Journal of Agronomy 82, 93–103. doi: 10.1016/j.eja.2016.10.007Google Scholar
Corbineau, F and Côme, D (1995) Control of seed germination and dormancy by the gaseous environment, pp. 397–424 in Kigel, J and Galili, G (eds), Seed Development and Germination. CRC Press.Google Scholar
Corbineau, F, Bagniol, S and Côme, D (1990) Sunflower (Helianthus annuus L.) seed dormancy and its regulation by ethylene. Israel Journal of Botany 39, 313–325. doi: 10.1080/0021213X.1990.10677156Google Scholar
Cutler, AJ, Rose, PA, Squires, TM, Loewen, MK, Shaw, AC, Quail, JW, Krochko, JE and Abrams, SR (2000) Inhibitors of abscisic acid 8’-hydroxylase. Biochemistry 39, 13614–13624.Google Scholar
Di Rienzo, JA, Casanoves, F, Balzarini, MG, Gonzalez, L, Tablada, M and Robledo, CW (2014) InfoStat versión 2014. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina.Google Scholar
Di Salvo, LP, Ferrando, L, Fernández-Scavino, A and García de Salamone, IE (2018) Microorganisms reveal what plants do not: wheat growth and rhizosphere microbial communities after Azospirillum brasilense inoculation and nitrogen fertilization under field conditions. Plant and Soil. doi: 10.1007/s11104-017-3548-7Google Scholar
Di Salvo, LP and García de Salamone, IE (2012) Evaluation of soil-microbial communities by their CLPP. Standardization of a laboratory technique to replace commercial available microplates. Ecología Austral 22, 129–136.Google Scholar
Dominguez, CP, Batlla, D, Rodríguez, MV, Windauer, LB, Gerbaldo, M and Benech-Arnold, RL (2016) Pericarp-imposed dormancy in sunflower: physiological basis, impact on crop emergence, and removal at an industrial scale. Crop Science 56, 716–726. doi: 10.2135/cropsci2015.06.0335Google Scholar
Edelstein, M and Welbaum, GE (2011) Seed O2 uptake and germination of cold-tolerant and cold-intolerant cultivars of muskmelon. Crop Science 51, 810–817. doi: 10.2135/cropsci2010.05.0285Google Scholar
Edelstein, M, Corbineau, F, Kigel, J and Nerson, H (1995) Seed coat structure and oxygen availability control low-temperature germination of melon (Cucumis melo) seeds. Physiologia Plantarum 93, 451–456. doi: 10.1111/j.1399-3054.1995.tb06842.xGoogle Scholar
Esau, K (1977) Anatomy of Seed Plants (2nd edn). New York, USA: John Wiley & Sons, Inc.Google Scholar
Finch-Savage, WE and Leubner-Metzger, G (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523. doi: 10.1111/j.1469-8137.2006.01787.xGoogle Scholar
Gay, G, Corbineau, F and Côme, D (1991) Effects of temperature and oxygen on seed germination and seedling growth in sunflower (Helianthus annuus L.). Environmental and Experimental Botany 31, 193–200.Google Scholar
Heydecker, W and Chetram, RS (1971) Water relations of beetroot seed germination. I. Microbial factors, with special reference to laboratory germination. Annals of Botany 35, 17–29.Google Scholar
Hoang, HH, Bailly, C, Corbineau, F and Leymarie, J (2013) Induction of secondary dormancy by hypoxia in barley grains and its hormonal regulation. Journal of Experimental Botany 64, 2017–2025. doi: 10.1093/jxb/ert062Google Scholar
Hoang, HH, Sechet, J, Bailly, C, Leymarie, J and Corbineau, F (2014) Inhibition of germination of dormant barley (Hordeum vulgare L.) grains by blue light as related to oxygen and hormonal regulation. Plant, Cell and Environment 37, 1393–1403. doi: 10.1111/pce.12239Google Scholar
Ishibashi, Y, Tawaratsumida, T, Zheng, S, Yuasa, T and Iwaya-Inoue, M (2010) NADPH oxidases act as key enzyme on germination and seedling growth in barley (Hordeum vulgare L.). Plant Production Science 13, 45–52. doi: 10.1626/pps.13.45Google Scholar
Johansen, DA (1940) Plant Microtechnique. New York, USA: McGraw-Hill.Google Scholar
Krochko, JE, Abrams, GD, Loewen, MK, Abrams, SR and Cutler, AJ (1998) (+)-Abscisic acid 8´-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiology 118, 849–860.Google Scholar
Kutschera, U (2002) Bacterial colonization of sunflower cotyledons during seed germination. Journal of Applied Botany-Angewandte Botanik 76, 96–98.Google Scholar
Le Page-Degivry, MT and Garello, G (1992) In situ abscisic acid synthesis. Plant Physiology 98, 1386–1390. doi: 10.1104/pp.98.4.1386Google Scholar
Lenoir, C, Corbineau, F and Côme, D (1986) Barley (Hordeum vulgare) seed dormancy as related to glumella characteristics. Physiologia Plantarum 68, 301–307.Google Scholar
Mendiondo, GM, Leymarie, J, Farrant, JM, Corbineau, F and Benech-Arnold, RL (2010) Differential expression of abscisic acid metabolism and signalling genes induced by seed-covering structures or hypoxia in barley (Hordeum vulgare L.) grains. Seed Science Research 20, 69–77. doi: 10.1017/S0960258509990262Google Scholar
Miransari, M and Smith, DL (2014) Plant hormones and seed germination. Environmental and Experimental Botany 99, 110–121. doi: 10.1016/j.envexpbot.2013.11.005Google Scholar
Motulsky, HJ (2003) GraphPad Prism 4.0 Statistics Guide – Statistical Analyses for Laboratory and Clinical Researchers. GraphPad Software Inc., San Diego, CA, USA.Google Scholar
Nasreen, S, Khan, MA, Zia, M, Ishaque, M, Uddin, S, Arshad, M and Rizvi, ZF (2015) Response of sunflower to various pre-germination techniques for breaking seed dormancy. Pakistan Journal of Botany 47, 413–416.Google Scholar
Nelson, EB, Simoneau, P, Barret, M, Mitter, B and Compant, S (2018) Editorial special issue: the soil, the seed, the microbes and the plant. Plant and Soil 422, 1–5. doi: 10.1007/s11104-018-3576-yGoogle Scholar
Oracz, K, El-Maarouf-Bouteau, H, Bogatek, R, Corbineau, F and Bailly, C (2008) Release of sunflower seed dormancy by cyanide: cross-talk with ethylene signalling pathway. Journal of Experimental Botany 59, 2241–2251. doi: 10.1093/jxb/ern089Google Scholar
Paparella, S, Araújo, SS, Rossi, G, Wijayasinghe, M, Carbonera, D and Balestrazzi, A (2015) Seed priming: state of the art and new perspectives. Plant Cell Reports 34, 1281–1293. doi: 10.1007/s00299-015-1784-yGoogle Scholar
Preston-Mafham, J, Boddy, L and Randerson, PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles – a critique. FEMS Microbiology Ecology 42, 1–14. doi: 10.1111/j.1574-6941.2002.tb00990.xGoogle Scholar
Quarrie, SA, Whitford, PN, Appleford, NEJ, Wang, TL, Cook, SK, Henson, IE and Loveys, BR (1988) A monoclonal antibody to (S)-abscisic acid: its characterisation and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173, 330–339. doi: 10.1007/BF00401020Google Scholar
Rodríguez, MV, Toorop, PE and Benech-Arnold, RL (2011) Challenges facing seed banks and agriculture in relation to seed quality, pp. 17–40 in Kermode, AR (ed), Seed Dormancy: Methods in Molecular Biology. New York, USA: Humana Press.Google Scholar
Rolletschek, H, Borisjuk, L, Sánchez-García, A, Gotor, C, Romero, LC, Martínez-Rivas, JM and Mancha, M (2007) Temperature-dependent endogenous oxygen concentration regulates microsomal oleate desaturase in developing sunflower seeds. Journal of Experimental Botany 58, 3171–3181. doi: 10.1093/jxb/erm154Google Scholar
Roselló, PL, Vigliocco, AE, Andrade, AM, Riera, NV, Calafat, M, Molas, ML and Alemano, SG (2016) Differential hormonal and gene expression dynamics in two inbred sunflower lines with contrasting dormancy level. Plant Physiology and Biochemistry 102, 133–140. doi: 10.1016/j.plaphy.2016.02.021Google Scholar
Schauer, S and Kutschera, U (2008) Methylotrophic bacteria on the surfaces of field-grown sunflower plants: a biogeographic perspective. Theory in Biosciences 127, 23–29. doi: 10.1007/s12064-007-0020-xGoogle Scholar
Seiler, GJ (1997) Anatomy and morphology of sunflower, pp. 67–111 in Schneiter, AA (ed), Sunflower Technology and Production. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America. Madison, Wisconsin, USA.Google Scholar
Sperber, K, Steinbrecher, T, Graeber, K, Scherer, G, Clausing, S, Wiegand, N, Hourston, JE, Kurre, R, Leubner-Metzger, G and Mummenhoff, K (2017) Fruit fracture biomechanics and the release of Lepidium didymum pericarp-imposed mechanical dormancy by fungi. Nature Communications 8, 1868. doi: 10.1038/s41467-017-02051-9Google Scholar
Steinbach, HS, Benech-Arnold, RL, Kristof, G, Sánchez, RA and 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. doi: 10.1093/jxb/46.6.701Google Scholar
Subrahmanyam, SVR, Kumar, SSR and Ranganatha, ARG (2002) Genotypic differences for seed dormancy in sunflower (Helianthus annuus L.). Seed Research (New Delhi) 30, 325–327.Google Scholar
Truyens, S, Weyens, N, Cuypers, A and Vangronsveld, J (2014) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environmental Microbiology Reports 7, 40–50. doi: 10.1111/1758-2229.12181Google Scholar
Viswanathan, R (1996) Seed mycoflora composition in sunflower. Indian Phytopathology 49, 286–289.Google Scholar
Supplementary material: Image

Dominguez et al. supplementary material

Figure S2

Download Dominguez et al. supplementary material(Image)
Image 13.2 MB
Supplementary material: Image

Dominguez et al. supplementary material

Figure S1

Download Dominguez et al. supplementary material(Image)
Image 7.6 MB