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Nitrate controls testa rupture and water content during release of physiological dormancy in seeds of Sisymbrium officinale (L.) Scop.

Published online by Cambridge University Press:  09 January 2015

Peter E. Toorop
Peter E. Toorop*
Affiliation:
Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex, RH17 6TN, United Kingdom
*
*Correspondence E-mail: p.toorop@kew.org
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Abstract

Seeds of Sisymbrium officinale display physiological dormancy and require nitrate to germinate. Rupture of the testa precedes radicle protrusion through the endosperm (germination sensu stricto). While both endosperm rupture and testa rupture (TR) required nitrate, endosperm rupture was fully inhibited by abscisic acid (ABA) but TR was not inhibited. The gibberellic acid (GA)-synthesis inhibitor paclobutrazol prevented TR, which was reverted by exogenous GA4 but not by nitrate. The orientation of TR was transverse, which prompted the question whether seeds elongate prior to radicle protrusion, concurrent with an increase in water content. Between 9 h and 1 d no increase in length or water content was observed. During incubation in ABA the length of imbibed seeds without TR did not increase between 1 and 5 d, whereas nitrate added to ABA induced TR and a 94% increase in length. At the same time the water content of seeds without TR increased by 18%, while the water content of seeds with TR increased by 38%. Length and water content were correlated in a single-seed analysis for seeds with TR, but not for seeds without TR. Increased length was also observed in Arabidopsis seeds with nitrate-induced TR. These results indicate that prior to endosperm rupture dormancy release by nitrate is accompanied by TR, seed elongation and an increase in water content. A new multiphasic model is proposed for the imbibition curve, where the second phase of the classical triphasic curve is split into three sub-phases, of which phases IIB and IIC are associated with TR.

Keywords

Arabidopsisimbibition phasesnitratephysiological dormancyseed imbibitionSisymbrium officinale
Type
Research Papers
Information
Seed Science Research , Volume 25 , Special Issue 2: Seed Dormancy , June 2015 , pp. 138 - 146
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Copyright
Copyright © Cambridge University Press 2015 

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References

Ali-Rachedi, S., Bouinot, D., Wagner, M.-H., Bonnet, M., Sotta, B., Grappin, P. and Julien, M. (2004) Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana . Planta 219, 479–488.Google Scholar
Baskin, C.C. and Baskin, J.M. (1998) Seeds; Ecology, biogeography and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Benech-Arnold, R.L., Sánchez, R.A., Forcella, F., Kruk, B.C. and Ghersha, C.M. (2000) Environmental control of dormancy in weed seed banks in soil. Field Crops Research 67, 105–122.Google Scholar
Bewley, J.D. and Black, M. (1994) Seeds: Physiology of development and germination (2nd edition). New York, Plenum Press.Google Scholar
Bouwmeester, H.J., Derks, L., Keizer, J.J. and Karssen, C.M. (1994) Effects of endogenous nitrate content of Sisymbrium officinale seeds on germination and dormancy. Acta Botanica Neerlandica 43, 39–50.CrossRefGoogle Scholar
Cadman, C.S.C., Toorop, P.E., Hilhorst, H.W.M. and Finch-Savage, W.E. (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. The Plant Journal 46, 805–822.Google Scholar
Carrillo-Barral, N., Matilla, A.J., Iglesias-Fernández, R. and Rodríguez-Gacio, M.C. (2013) Nitrate-induced early transcriptional changes during imbibition in non-after-ripened Sisymbrium officinale seeds. Physiologia Plantarum 148, 560–573.CrossRefGoogle ScholarPubMed
Carrillo-Barral, N., Matilla, A.J., Rodríguez-Gacio, M.C. and Iglesias-Fernández, R. (2014) Nitrate affects sensu-stricto germination of after-ripened Sisymbrium officinale seeds by modifying expression of SoNCED5, SoCYP707A2 and SoGA3ox2 genes. Plant Science 217–218, 99–108.CrossRefGoogle Scholar
da Silva, E.A.A., Toorop, P.E., van Aelst, A.C. and Hilhorst, H.W.M. (2004) Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Coffea arabica cv. Rubi) seed germination. Planta 220, 251–261.Google Scholar
da Silva, E.A.A., Toorop, P.E., van Lammeren, A.A.M. and Hilhorst, H.W.M. (2008) ABA inhibits embryo cell expansion and early cell division events during coffee (Coffea arabica ‘Rubi’) seed germination. Annals of Botany 102, 425–433.Google Scholar
Dekkers, B.J.W., Pearce, S., van Bolderen-Veldkamp, R.P., Marshall, A., Widera, P., Gilbert, J., Drost, H.-G., Bassel, G.W., Müller, K., King, J.R., Wood, A.T.A., Grosse, I., Quint, M., Krasnogor, N., Leubner-Metzger, G., Holdsworth, M.J. and Bentsink, L. (2013) Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiology 163, 205–215.CrossRefGoogle ScholarPubMed
Finch-Savage, W.E., Cadman, C.S.C., Toorop, P.E., Lynn, J.R. and Hilhorst, H.W.M. (2007) Seed dormancy release in Arabidopsis Cvi by dry afterripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. The Plant Journal 51, 60–78.Google Scholar
Hepher, A. and Roberts, J.A. (1985) The control of seed germination in Trollius ledebouri: the breaking of dormancy. Planta 166, 314–320.Google Scholar
Hilhorst, H.W.M. (1995) A critical update on seed dormancy. I. Primary dormancy. Seed Science Research 5, 61–73.CrossRefGoogle Scholar
Hilhorst, H.W.M. and Karssen, C.M. (1989) Nitrate reductase independent stimulation of seed germination in Sisymbrium officinale L. (hedge mustard) by light and nitrate. Annals of Botany 63, 131–137.Google Scholar
Hilhorst, H.W.M., Smitt, A.I. and Karssen, C.M. (1986) Gibberellin-biosynthesis and -sensitivity mediated stimulation of seed germination of Sisymbrium officinale by red light and nitrate. Physiologia Plantarum 67, 285–290.CrossRefGoogle Scholar
Iglesias-Fernandez, R. and Matilla, A. (2009) After-ripening alters the gene expression pattern of oxidases involved in the ethylene and gibberellin pathways during early imbibition of Sisymbrium officinale L. seeds. Journal of Experimental Botany 60, 1645–1661.Google Scholar
Iglesias-Fernandez, R. and Matilla, A. (2010) Genes involved in ethylene and gibberellins metabolism are required for endosperm-limited germination of Sisymbrium officinale L. seeds. Planta 231, 653–664.Google Scholar
Iglesias-Fernandez, R., Matilla, A.J., Pulgar, I. and de la Torre, F. (2007) Ripe fruits of Sisymbrium officinale L. contain heterogeneous endospermic seeds with different germination rates. Seed Science and Biotechnology 1, 18–24.Google Scholar
Karssen, C.M. (1976) Uptake and effect of abscisic acid during induction and progress of radicle growth in seeds of Chenopodium album . Physiologia Plantarum 36, 259–263.Google Scholar
Krock, B., Schmidt, S., Hertweck, C. and Baldwin, I.T. (2002) Vegetation-derived abscisic acid and four terpenes enforce dormancy in seeds of the post-fire annual, Nicotiana attenuata . Seed Science Research 12, 239–252.Google Scholar
Lee, K.P., Piskurewicz, U., Turečková, V., Strnad, M. and Lopez-Molina, L. (2010) A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proceedings of the National Academy of Science, USA 107, 19108–19113.Google Scholar
Leubner-Metzger, G., Fründt, C., Vögeli-Lange, R. and Meins, F. Jr (1995) Class I β-1,3-glucanases in the endosperm of tobacco during germination. Plant Physiology 109, 751–759.CrossRefGoogle Scholar
Linkies, A. and Leubner-Metzger, G. (2012) Beyond gibberellins and abscisic acid: how ethylene and jasmonates control seed germination. Plant Cell Reports 31, 253–270.Google Scholar
Liu, P.P., Koizuka, N., Homrichhausen, T.M., Hewitt, J.R., Martin, R.C. and Nonogaki, H. (2005) Large-scale screening of Arabidopsis enhancer-trap lines for seed germination-associated genes. The Plant Journal 41, 936–944.Google Scholar
Manz, B., Müller, K., Kucera, B., Volke, F. and Leubner-Metzger, G. (2005) Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant Physiology 138, 1538–1551.Google Scholar
Matakiadis, T., Alboresi, A., Jikumaru, Y., Tatematsu, K., Pichon, O., Renou, J.-P., Kamiya, Y., Nambara, E. and Truong, H.-N. (2009) The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiology 149, 949–960.CrossRefGoogle Scholar
Müller, K., Tintelnot, S. and Leubner-Metzger, G. (2006) Endosperm-limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana . Plant and Cell Physiology 47, 864–877.Google Scholar
Ni, B.-R. and Bradford, K. (1993) Germination and dormancy of abscisic acid-deficient and gibberellin-deficient mutant tomato (Lycopersicon esculentum) seeds. Sensitivity of germination to abscisic acid, gibberellin, and water potential. Plant Physiology 101, 607–617.Google Scholar
Ogawa, M., Hanada, A., Yamauchi, Y., Kuwahara, A., Kamiya, Y. and Yamaguchi, S. (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. The Plant Cell 15, 1591–1604.Google Scholar
Penfield, S., Li, Y., Gilday, A.D., Graham, S. and Graham, I.A. (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. The Plant Cell 18, 1887–1899.Google Scholar
Petruzelli, L., Müller, K., Hermann, K. and Leubner-Metzger, G. (2003) Distinct expression patterns of β-1,3-glucanases and chitinases during the germination of Solanaceous seeds. Seed Science Research 13, 139–153.Google Scholar
Pinto, L.V.A., da Silva, E.A.A., Davide, A.C., Mendes de Jesus, V.A., Toorop, P.E. and Hilhorst, H.W.M. (2007) Mechanism and control of Solanum lycocarpum seed germination. Annals of Botany 100, 1175–1187.Google Scholar
Piskurewicz, U. and Lopez-Molina, L. (2009) The GA-signaling repressor RGL3 represses testa rupture in response to changes in GA and ABA levels. Plant Signaling and Behavior 4, 63–65.Google Scholar
Piskurewicz, U., Jikumaru, Y., Kinoshita, N., Nambara, E., Kamiya, Y. and Lopez-Molina, L. (2008) The gibberellic acid signaling repressor RGL2 Inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. The Plant Cell 20, 2729–2745.Google Scholar
Queiroz, S.E.E., da Silva, E.A.A., Davide, A.C., José, A.C., Silva, A.T., Fraiz, A.C.R., Faria, J.M.R. and Hilhorst, H.W.M. (2012) Mechanism and control of Genipa americana seed germination. Physiologia Plantarum 144, 263–276.Google Scholar
Robert, C., Noriega, A., Tocino, A. and Cervantes, E. (2008) Morphological analysis of seed shape in Arabidopsis thaliana reveals altered polarity in mutants of the ethylene signaling pathway. Journal of Plant Physiology 165, 911–919.Google Scholar
Sanchez, R.A., De Miguel, L. and Mercuri, O. (1986) Phytochrome control of cellulase activity in Datura ferox L. seeds and its relationship with germination. Journal of Experimental Botany 37, 1574–1580.Google Scholar
Schopfer, P. and Plachy, C. (1984) Control of seed germination by abscisic acid. II. Effect on embryo water uptake in Brassica napus L. Plant Physiology 76, 155–160.CrossRefGoogle ScholarPubMed
Schopfer, P. and Plachy, C. (1985) Control of seed germination by abscisic acid. III. Effect on embryo growth potential (minimum turgor pressure) and growth coefficient (cell wall extensibility) in Brassica napus L. Plant Physiology 77, 676–686.Google Scholar
Serrato-Valenti, G., Cornara, L., Modenesi, P., Piana, M. and Mariotti, M.G. (2000) Structure and histochemistry of embryo envelope tissues in the mature dry seed and early germination of Phacelia tanacetifolia . Annals of Botany 85, 625–634.CrossRefGoogle Scholar
Sliwinska, E., Bassel, G.W. and Bewley, J.D. (2009) Germination of Arabidopsis thaliana seeds is not completed as a result of elongation of the radicle but of the adjacent transition zone and lower hypocotyl. Journal of Experimental Botany 60, 3587–3594.Google Scholar
Sliwinska, E., Mathur, J. and Bewley, J.D. (2012) Synchronously developing collet hairs in Arabidopsis thaliana provide an easily accessible system for studying nuclear movement and endoreduplication. Journal of Experimental Botany 63, 4165–4178.Google Scholar
Toorop, P.E., Van Aelst, A.C. and Hilhorst, H.W.M. (2000) The second step of the biphasic endosperm cap weakening that mediates tomato (Lycopersicon esculentum) seed germination is under control of ABA. Journal of Experimental Botany 51, 1371–1379.Google Scholar
Toorop, P.E., Cuerva, R.C., Begg, G.S., Locardi, B., Squire, G.R. and Iannetta, P.P.M. (2012) Co-adaptation of seed dormancy and flowering time in the arable weed Capsella bursa-pastoris (shepherd's purse). Annals of Botany 109, 481–489.CrossRefGoogle ScholarPubMed
Watkins, J.T. and Cantliffe, D.J. (1983) Mechanical resistance of the seed coat and endosperm during germination of Capsicum annuum at low temperature. Plant Physiology 72, 146–150.Google Scholar
Weitbrecht, K., Müller, K. and Leubner-Metzger, G. (2011) First off the mark: early seed germination. Journal of Experimental Botany 62, 3289–3309.CrossRefGoogle ScholarPubMed
Welbaum, G.E., Muthui, W.J., Wilson, J.H., Grayson, R.L. and Fell, R.D. (1995) Weakening of muskmelon (Cucumis melo L.).V. Water relations of imbibition and germination. Journal of Experimental Botany 46, 391–400.Google Scholar
Yamauchi, Y., Ogawa, M., Kuwahara, A., Hanada, A., Kamiya, Y. and Yamaguchi, S. (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. The Plant Cell 16, 367–378.Google Scholar