Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-03T01:15:44.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Fluctuating temperatures terminate dormancy in Cynara cardunculus seeds by turning off ABA synthesis and reducing ABA signalling, but not stimulating GA synthesis or signalling

Published online by Cambridge University Press:  09 May 2014

H. Roberto Huarte ,
Virginia Luna ,
Eduardo A. Pagano ,
Jorge A. Zavala  and
Roberto L. Benech-Arnold
H. Roberto Huarte*
Affiliation:
Facultad de Ciencias Agrarias, Universidad Católica Argentina, 183 Ramón Freire, 1426, CABA, Argentina
Virginia Luna
Affiliation:
Laboratorio de Fisiología Vegetal, Departamento de Ciencias Naturales, Universidad Nacional de Río Cuarto, 5800, Rio Cuarto, Argentina
Eduardo A. Pagano
Affiliation:
Cátedra de Bioquímica; Facultad de Agronomía, Universidad de Buenos Aires, 4453 San Martín Avenue, 1417DSE, CABA, Argentina
Jorge A. Zavala
Affiliation:
INBA/Cátedra de Bioquímica; Facultad de Agronomía, Universidad de Buenos Aires, 4453 San Martín Avenue, 1417DSE, CABA, Argentina
Roberto L. Benech-Arnold
Affiliation:
IFEVA/Cátedra de Cultivos Industriales/CONICET/Facultad de Agronomía, Universidad de Buenos Aires, 4453 San Martín Avenue, 1417DSE, CABA, Argentina
*
*Correspondence Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Fluctuating temperatures terminate seed dormancy in many species, including Cynara cardunculus (L.) var. sylvestris. Termination of physiological dormancy requires low ratios of abscisic acid (ABA)/gibberellins (GA). In a previous paper we have shown that physiological responses to fluctuating temperatures comprise a reduction of abscisic acid (ABA) content and sensitivity. However, a possible stimulation of GA synthesis was also suggested as part of the mechanism. That possible stimulation, as well as the identification of potential regulatory sites for ABA and GA metabolism and signalling involved in the termination of dormancy by fluctuating temperatures, are yet to be determined. In this study, we measured GA content and sensitivity in seeds incubated under constant and fluctuating temperatures. We also assessed the expression of several genes involved in ABA and GA metabolism and signalling. Our results show that fluctuating temperatures reduce ABA/GA ratios through a reduction in ABA accumulation during incubation but without altering GA synthesis as compared to that observed under constant temperatures. On the other hand, fluctuating temperatures did not increase sensitivity to GA. Fluctuating temperatures reduced the expression of CycaNCED and CycaABI5 (ABA synthesis and signalling genes) with a temporal pattern that coincides with the interruption of ABA accumulation that precedes germination of seeds incubated under fluctuating temperatures. However, fluctuating temperatures did not modify the expression of CycaCYP707A2 (ABA inactivation) as compared to that observed under constant temperatures. Consistent with our determinations of GA content and sensitivity, fluctuating temperatures did not modify the expression of GA synthesis (CycaGA3ox) and signalling genes (CycaRGL2 and CycaGAI) in relation to that observed at constant temperatures. These results show that fluctuating temperatures terminate dormancy in Cynara cardunculus seeds through an interruption in ABA accumulation and a reduction in ABA signalling exerted at the level of CycaNCED and CycaABI5 expression.

Keywords

abscisic aciddormancyfluctuating temperaturesgene expressiongibberellins
Type
Research Papers
Information
Seed Science Research , Volume 24 , Issue 2 , June 2014 , pp. 79 - 89
Copyright
Copyright © Cambridge University Press 2014 

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

Alvarado, V. and Bradford, K.J. (2005) Hydrothermal time analysis of seed dormancy in true (botanical) potato seeds. Seed Science Research 15, 77–88.Google Scholar
Arana, M.V., De Miguel, L.C. and Sánchez, R.A. (2006) A phytochrome-dependent embryonic factor modulates gibberellin responses in the embryo and micropylar endosperm of Datura ferox seeds. Planta 223, 847–857.Google Scholar
Argyris, J., Dahal, P., Hayashi, E., Still, D.W. and Bradford, K.J. (2008) Genetic variation for lettuce seed thermoinhibition is associated with temperature-sensitive expression of abscisic acid, gibberellin, and ethylene biosynthesis, metabolism, and response genes. Plant Physiology 148, 926–947.CrossRefGoogle ScholarPubMed
Baskin, J.M. and Baskin, C.C. (2007) A classification system for seed dormancy. Seed Science Research 14, 1–16.Google Scholar
Benech-Arnold, R.L., Sánchez, R.A., Forcella, F., Kruk, B.C. and Ghersa, C.M. (2000) Environmental control of dormancy in weed seed banks in soil. Field Crops Research 67, 105–122.Google Scholar
Bewley, J.D. (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1994) Seeds: Physiology of development and germination. New York, Plenum Press.Google Scholar
Chen, H., Zhang, J., Neff, M.M., Hong, S.W., Zhang, H., Deng, X.W. and Xiong, L. (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proceedings of the National Academy of Sciences of the USA 105, 4495–4500.Google Scholar
Finch-Savage, W.E. and Footitt, S. (2012) To germinate or not to germinate: a question of dormancy relief not germination stimulation. Seed Science Research 22, 243–248.Google Scholar
Finch-Savage, W.E. and Leubner-Metzger, G. (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.CrossRefGoogle ScholarPubMed
Finkelstein, R., Reeves, W., Ariizumi, T. and Steber, C. (2008) Molecular aspects of seed dormancy. Annual Review of Plant Biology 59, 387–415.CrossRefGoogle ScholarPubMed
Foley, M.E. and Chao, W.S. (2008) Growth regulators and chemicals stimulate germination of Leafy Spurge (Euphorbia esula) seeds. Weed Science 56, 516–522.Google Scholar
Foley, M.E., Chao, W.S., Dogramaci, M., Horvath, D.P. and Anderson, J.V. (2012) Changes in the transcriptome of dry leafy spurge (Euphorbia esula) seeds imbibed at a constant and alternating temperature. Weed Science 60, 48–56.CrossRefGoogle Scholar
Footitt, S., Douterelo-Soler, I., Clay, H. and Finch-Savage, W.E. (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences of the USA 108, 20236–20241.Google Scholar
Ghersa, C.M., Benech-Arnold, R.L. and Martinez-Ghersa, M.A. (1992) The role of fluctuating temperatures in germination and establishment of S. halepense (L.) Pers. II. Regulation of germination at increasing depths. Functional Ecology 6, 460–468.CrossRefGoogle Scholar
Graeber, K., Nakabayashi, K., Miatton, E., Leubner-Metzger, G. and Soppe, W.J.J. (2012) Molecular mechanisms of seed dormancy. Plant, Cell and Environment 35, 1769–1786.Google Scholar
Gummerson, R.J. (1986) The effect of constant temperatures and osmotic potentials on the germination of sugar beet. Journal of Experimental Botany 37, 729–741.CrossRefGoogle Scholar
Hartweck, L.M. (2008) Gibberellin signaling. Planta 229, 1–13.CrossRefGoogle ScholarPubMed
Hilhorst, H.M. (1995) A critical update on seed dormancy I. Primary dormancy. Seed Science Research 5, 61–73.Google Scholar
Holdsworth, M.J., Bentsink, L. and Soppe, W.J.J. (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytologist 179, 33–54.Google Scholar
Hu, X.W., Huang, X.H. and Wang, Y.R. (2012) Hormonal and temperature regulation of seed dormancy and germination in Leymus chinensis . Plant Growth Regulation 67, 199–207.Google Scholar
Huarte, H.R. and Benech-Arnold, R.L. (2010) Hormonal nature of seed responses to fluctuating temperatures in Cynara cardunculus (L.). Seed Science Research 20, 39–45.CrossRefGoogle Scholar
Huarte, R. and Benech-Arnold, R.L. (2005) Incubation under fluctuating temperatures reduces mean base water potential for seed germination in several non-cultivated species. Seed Science Research 15, 89–97.Google Scholar
Huo, H., Dahal, P., Kunusoth, K., McCallum, C.M. and Bradford, K.J. (2013) Expression of 9-cis-epoxycarotenoid dioxygenase 4 is essential for thermoinhibition of lettuce seed germination but not for seed development or stress tolerance. The Plant Cell 25, 884–900.CrossRefGoogle ScholarPubMed
Kucera, B., Cohn, M.A. and Leubner-Metzger, G. (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281–307.Google 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
Lopez-Molina, L., Mongrand, S. and Chua, N.H. (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis . Proceedings of the National Academy of Sciences of the USA 98, 4782–4787.CrossRefGoogle ScholarPubMed
Lopez-Molina, L., Mongrand, S., McLachlin, D.T., Chait, B.T. and Chua, N.H. (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant Journal 32, 317–328.Google Scholar
Lopez-Molina, L., Mongrand, S., Kinoshita, N. and Chua, N.H. (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes & Development 17, 410–418.CrossRefGoogle ScholarPubMed
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.Google Scholar
Millar, A.A., Jacobsen, J.V., Ross, J.J., Helliwell, C.A., Poole, A.T., Scofield, G., Reid, J.B. and Gubler, F. (2006) Seed dormancy and ABA metabolism in Arabidopsis and barley: The role of ABA 8′-hydroxylase. Plant Journal 45, 942–954.CrossRefGoogle ScholarPubMed
Nambara, E. and Marion-Poll, A. (2005) Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165–185.Google Scholar
Nambara, E., Okamoto, M., Tatematsu, K., Yano, R., Seo, M. and Kamiya, Y. (2010) Abscisic acid and the control of seed dormancy and germination. Seed Science Research 20, 55–67.Google Scholar
Ni, B.R. and Bradford, K.J. (1992) Quantitative models characterizing seed germination responses to abscisic acid and osmoticum. Plant Physiology 98, 1057–1068.Google Scholar
Ni, B.R. and Bradford, K.J. (1993) Germination and dormancy of abscisic acid- and gibberellin-deficient mutant tomato (Lycopersicon esculentum) seeds: sensitivity of germination to abscisic acid, gibberellin, and water potential. Plant Physiology 101, 607–617.CrossRefGoogle ScholarPubMed
Piskurewicz, U., Jikumaru, Y., Kinoshita, N., Nambara, E., Kamiya, Y., Lopez-Molina, L. and Gene, D. (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
Raghavendra, A.S., Gonugunta, V.K., Christmann, A. and Grill, E. (2010) ABA perception and signalling. Trends in Plant Science 15, 395–401.Google Scholar
Sawada, Y., Aoki, M., Nakaminami, K., Mitsuhashi, W. and Tatematsu, K. (2008a) Phytochrome and gibberellin-mediated regulation of abscisic acid metabolism during germination of lettuce seeds. Plant Physiology 146, 1386–1396.Google Scholar
Sawada, Y., Aoki, M., Nakaminami, K., Mitsuhashi, W., Tatematsu, K., Kushiro, T., Koshiba, T., Kamiya, Y., Inoue, Y., Nambara, E. and Toyomasu, T. (2008b) Phytochrome and gibberellin-mediated regulation of abscisic acid metabolism during germination of photoblastic lettuce seeds. Plant Physiology 146, 1386–1396.Google Scholar
Sawada, Y., Katsumata, T., Kitamura, J., Kawaide, H., Nakajima, M. and Asami, T.B. (2008c) Germination of photoblastic lettuce seeds is regulated via the control of endogenous physiologically active gibberellin content, rather than of gibberellin responsiveness. Journal of Experimental Botany 59, 3383–3393.CrossRefGoogle ScholarPubMed
Seo, M., Hanada, A., Kuwahara, A., Endo, A., Okamoto, M., Yamauchi, Y., North, H., Marion-Poll, A., Sun, T.P., Koshiba, T., Kamiya, Y., Yamaguchi, S. and Nambara, E. (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant Journal 48, 354–366.CrossRefGoogle ScholarPubMed
Seo, M., Nambara, E., Choi, G. and Yamaguchi, S. (2009) Interaction of light and hormone signals in germinating seeds. Plant Molecular Biology 69, 463–472.Google Scholar
Stone, S.L., Williams, L.A., Farmer, L.M., Vierstra, R.D. and Callis, J. (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. The Plant Cell 18, 3415–3428.Google Scholar
Thompson, K. and Grime, J.P. (1983) A comparative study of responses to diurnally fluctuating temperatures. Journal of Applied Ecology 20, 141–156.Google Scholar
Toh, S., Imamura, A., Watanabe, A., Nakabayashi, K., Okamoto, M., Jikumaru, Y., Hanada, A., Aso, Y., Ishiyama, K., Tamura, N., Iuchi, S., Kobayashi, M., Yamaguchi, S., Kamiya, Y., Nambara, E. and Kawakami, N. (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiology 146, 1368–1385.CrossRefGoogle ScholarPubMed
Toyomasu, T., Tsuji, H., Yamane, H., Nakayama, M., Yamaguchi, I., Murofushi, N., Takahashi, N. and Inoue, Y. (1993) Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds. Journal of Plant Growth Regulation 12, 85–90.Google Scholar
Toyomasu, T., Yamane, H., Murofushi, N. and Nick, P. (1994) Phytochrome inhibits the effectiveness of gibberellins to induce cell elongation in rice. Planta 194, 256–263.Google Scholar
Toyomasu, T., Kawaide, H., Mitsuhashi, W., Inoue, Y. and Kamiya, Y. (1998) Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. Plant Physiology 118, 1517–1523.CrossRefGoogle ScholarPubMed
Umezawa, T., Okamoto, M., Kushiro, T., Nambara, E., Oono, Y. and Seki, M. (2006) CYP707A3 a major ABA 8′-hydroxylase involved in dehydration and rehydration response in Arabidopsis thaliana . Plant Journal 46, 171–182.Google Scholar
Yamaguchi, S. (2008) Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59, 225–251.Google Scholar
Yamaguchi, S., Kamiya, Y. and Nambara, E. (2007) Regulation of ABA and GA levels during seed development and germination in Arabidopsis . pp. 224–247 in Bradford, K.J.; Nonogaki, H. (Eds) Seed development, dormancy and germination. Oxford, Blackwell Publishing.Google Scholar
Yamauchi, Y., Takeda-Kamiya, N., Hanada, A., Ogawa, M., Kuwahara, A., Seo, M., Kamiya, Y. and Yamaguchi, S. (2007) Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant and Cell Physiology 48, 555–561.Google Scholar
Supplementary material: File

Roberto Huarte Supplementary Material

Figure S1

Download Roberto Huarte Supplementary Material(File)
File 17.5 KB
Supplementary material: File

Roberto Huarte Supplementary Material

Table S1

Download Roberto Huarte Supplementary Material(File)
File 22 KB