Abstract
Cold stratification is commonly used for breaking seed dormancy in plants. However, the effects of cold stratification on dormancy release and its physiological characteristics are still unclear in rice. Dormancy release by different periods (6, 12, 18 and 24 days) of cold stratification (4 °C) was conducted using japonica Jiucaiqing (Oryza sativa L) in this study. Physiological characteristics, including hormones, antioxidant enzyme and α-amylase activities, were further estimated in imbibed seeds after 12 and 24 days cold stratification. Seed dormancy of Jiucaiqing was completely released by cold stratification for 18 and 24 days. The expressions of the hormones, including abscisic acid (ABA), gibberellin (GA) and indole acetic acid (IAA), metabolism related genes OsCYP707A5, OsCYP707A7, OsGA20ox1, OsGA20ox2, OsGH3-2, OsGH3-7 and OsGH3-8 were significantly increased while OsNCED3 and OsZEP significantly decreased in imbibed seeds by cold stratification, which resulted in the rapid decline of ABA and the increases of GA3 and IAA. The activities of antioxidant enzymes, including superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX), were significantly increased in imbibed seeds by cold stratification, which resulted in a slight increase of H2O2 level. The ratios of GA/ABA, GA/IAA and IAA/ABA and H2O2 level were gradually enhanced in imbibed seeds with cold stratification, which might contribute to the increase of α-amylase activity to promote dormancy release in rice.
Similar content being viewed by others
References
Ali-Rachedi S, Bouinot D, Wagner MH, Bonnet M, Sotta B, Grappin P (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
Bailly C, EI-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C R biol 331:806
Barba-Espín G, Diaz-Vivancos P, Clemente-Moreno MJ, Albacete A, Faize L, Faize M, Pérez-Alfocea F, Hernández JA (2010) Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant, Cell Environ 33:981–994
Barba-Espín G, Diaz-Vivancosn P, Job D, Belghazi M, Job C, Hernández JA (2011) Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant, Cell Environ 34:1907–1919
Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F (2009) Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol 150:1006
Bartel B (1997) Auxin biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 48:51
Bartel B, Fink GR (1995) ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268:1745
Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
Bialek K, Cohen JD (1992) Amide-linked indoleacetic acid conjugates may control levels of indoleacetic acid in germinating seedlings of Phaseolus vulgaris. Plant Physiol 100:2002–2007
Bialek K, Michalczuk L, Cohen JD (1992) Auxin biosynthesis during seed germination in Phaseolus vulgaris. Plant Physiol 100:509
Chen SY, Kuo SR, Chien CT (2008) Roles of gibberellins and abscisic acid in dormancy and germination of red bayberry (Myrica rubra) seeds. Tree Physiol 28:1431
Cheng JP, Wang L, Du WL, Lai YY, Huang X, Wang ZF, Zhang HS (2014) Dynamic quantitative trait locus analysis of seed dormancy at three development stages in rice. Mol Breeding 34:501–510
Cheng JP, He YQ, Yang B, Lai YY, Wang ZF, Zhang HS (2015) Association mapping of seed germination and seedling growth at three conditions in indica rice (Oryza sativa L.). Euphytica 206:103–115
De Gara L, de Pinto MC, Arrigoni O (1997) Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Plant Physiol 100:894–900
Debska K, Krasuska U, Budnicka K, Bogatek R, Gniazdowska A (2013) Dormancy removal of apple seeds by cold stratification is associated with fluctuation in H2O2, NO production and protein carbonylation level. J Plant Physiol 170:480–488
Diaz-Vivancos P, Barba-Espín G, Hernández JA (2013) Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Rep 32:1491–1502
Du WL, Cheng JP, Cheng YH, Wang L, He YQ, Wang ZF, Zhang HS (2015) Physiological characteristics and related gene expression of after-ripening on seed dormancy release in rice. Plant Biol 17:1156–1164
Eiji N, Masanori O, Kiyoshi T, Ryoichi Y, Mitsunori S, Yuji K (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci Res 20:55–67
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Fu J, Liu HB, Li Y, Yu HH, Li XH, Xiao JH, Wang SP (2011) Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol 155:589–602
Garcia-Fernandez A, Escudero A, Lara-Romero C, Iriondo JM (2015) Effects of the duration of cold stratification on early life stages of the Mediterranean alpine plant Silene ciliata. Plant Biol 17:344–350
Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ (2012) Molecular mechanisms of seed dormancy. Plant, Cell Environ 35:1769–1786
Hauvermale AL, Tuttle KM, Takebayashi Y, Seo M, Steber CM (2015) Loss of Arabidopsis thaliana seed dormancy is associated with increased accumulation of the GID1 GA hormone receptors. Plant Cell Physiol 56:1773–1785
He YQ, Cheng JP, Li XD, Zeng P, Yang B, Zhang HS, Wang ZF (2016) Acquisition of desiccation tolerance during seed development is associated with oxidative processes in rice. Botany 94:91–101
He YQ, Yang B, He YQ, Zhan CF, Cheng YH, Zhang JH, Zhang HS, Cheng JP, Wang ZF (2018) A quantitative trait locus, qSE3, promotes seed germination and seedling establishment under salinity stress in rice. Plant J 97(6):1089–1104
He YQ, Cheng JP, He Y, Yang B, Cheng YH, Yang C, Zhang HS, Wang ZF (2019) Influence of isopropylmalate synthase OsIPMS1 on seed vigour associated with amino acid and energy metabolism in rice. Plant Biotechnol J 17:322–337
Hoang HH, Sechet J, Bailly C, Leymarie J, 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 Environ 37:1393–1403
Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54
Hong YF, Ho TH, Wu CF, Ho SL, Yeh RH, Lu CA, Chen PW, Yu LC, Chao A, Yu SM (2012) Convergent starvation signals and hormone crosstalk in regulating nutrient mobilization upon germination in cereals. Plant Cell 24:2857–2873
Hong GL, Lee K, Seo PJ (2015) The Arabidopsis MYB96 transcription factor plays a role in seed dormancy. Plant Mol Biol 87:371–381
Huang YT, Zhang YC, Gao CH, Li Z, Guan YJ, Hu WM, Hu J (2018) The interactions of plant growth regulators and H2O2 during germination improvement of sweet corn seed through spermidine application. Plant Growth Regul 85:15–26
Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, Zheng SH, Yuasa T, Iwaya-Inoue M (2012) Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol 158:1705–1714
Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M (2004) Loss-of-function mutations of the rice GAMYB gene impair α-amylase expression in aleurone and flower development. Plant Cell 16:33–44
Kowalczyk M, Ljung K, Sandberg G, Bartel B (2004) A family of auxin-conjugate hydrolases that contributes to free indole-3-acetic acid levels during Arabidopsis germination. Plant Physiol 135:978–988
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656
Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant Mol Biol 52:133–146
Liu AH, Gao F, Kanno Y, Jordan MC, Kamiya Y, Seo M, Ayele BT (2013a) Regulation of wheat seed dormancy by after-ripening is mediated by specific transcriptional switches that induce changes in seed hormone metabolism and signaling. PLoS ONE 8:e56570
Liu XD, Zhang H, Zhao Y, Feng ZY, Li Q, Yang HQ, Luan S, Li JM, He ZH (2013b) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA 110:15485–15490
Liu Y, Muller K, El-Kassaby YA, Kermode AR (2015) Changes in hormone flux and signaling in white spruce (Picea glauca) seeds during the transition from dormancy to germination in response to temperature cues. BMC Plant Biol 15:292
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−△△C(T)) method. Methods 25:402–408
Ludwigmüller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773
Mittler R, Poulos TL (2008) Ascorbate peroxidase. In: Smirnoff N (ed) Antioxidant and reactive oxygen species in plants. Blackwell publishing, Oxford, pp 87–100
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Oracz K, Elmaarouf BH, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant Mol Biol 50:452
Pipinis E, Stampoulidis A, Milios E, Kitikidou K, Radoglou K (2017) Effects oF cold stratification and GA3 on germination of Arbutus unedo seeds of three provenances. Afr J Tradit Complem 14:318–323
Ravindran P, Verma V, Stamm P, Kumar PP (2017) A novel RGL2-DOF6 complex contributes to primary seed dormancy in Arabidopsis thaliana by regulating a GATA transcription factor. Mol Plant 10:1307–1320
Sahu B, Sahu AK, Chennareddy SR, Soni A, Naithani SC (2017) Insights on germinability and desiccation tolerance in developing neem seeds (Azadirachta indica): role of AOS, antioxidative enzymes and dehydrin-like protein. Plant Physiol Biochem 112:64–73
Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 134:1439–1449
Su L, Lan Q, Pritchard HW, Hua X, Wang X (2016) Reactive oxygen species induced by cold stratification promote germination of Hedysarum scoparium seeds. Plant Physiol Bioch 109:406
Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci USA 107:5792
Thornton B, Basu C (2015) Rapid and simple method of qPCR primer design. Methods Mol Biol 1275:173–179
Wang WB, Kim YH, Lee HS, Kim KY, Deng XP, Kwak SS (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577
Wang ZF, Wang JF, Bao YM, Wang FH, Zhang HS (2010) Quantitative trait loci analysis for rice seed vigor during the germination stage. J Zhejiang Univ Sci 11:958–964
Wang L, Cheng J, Lai Y, Du W, Huang X, Wang Z, Zhang H (2014) Identification of QTLs with additive, epistatic and QTL × development interaction effects for seed dormancy in rice. Planta 239:411–420
Xu Q, Truong TT, Barrero JM, Jacobsen JV, Hocart CH, Gubler F (2016) A role for jasmonates in the release of dormancy by cold stratification in wheat. J Exp Bot 67:3497–3508
Zentella R, Ho THD (2002) Molecular dissection of the gibberellin/abscisic acid signaling pathways by transiently expressed RNA interference in barley aleurone cells. Plant Cell 14:2289–2301
Zhou LJ, Ye Y, Zhao Q, Du XX, Zakari SA, Su D, Pan G, Cheng FM (2018) Suppression of ROS generation mediated by higher InsP3 level is critical for the delay of seed germination in lpa rice. Plant Growth Regul 85:411–424
Acknowledgements
This work was supported by the National Key R&D Program of China (2018YFD0100901), National Natural Science Foundation of China (31771889), and the Science and Technology Project of Jiangsu Province (BE2016380).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yang, B., Cheng, J., Wang, J. et al. Physiological characteristics of cold stratification on seed dormancy release in rice. Plant Growth Regul 89, 131–141 (2019). https://doi.org/10.1007/s10725-019-00516-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-019-00516-z