Regulators of auxin, jasmonic acid, brassinosteroid, and ethylene pathways in seed dormancy promotion or release.
Abstract
Seed dormancy is one of the most important adaptive mechanisms in plants, which protects seeds from precocious germination in the presence of the inappropriate conditions for growth continuation. Numerous environmental and molecular signals regulate seed dormancy. Maintenance or release of seed dormancy is dependent on light, temperature, and water availability. Precise response of seeds to environmental factors is mediated by different phytohormonal pathways. ABA is considered as a main phytohormone regulating seed dormancy induction and maintenance. ABA‐ and GA‐responsive components, ensure crosstalk between the GA and ABA pathways and enable seed response adequate to the environment. Phytohormonal regulation mechanism of seed dormancy is similar in dicot and monocot plants. Recently, it is suggested that other phytohormones, such as auxin, jasmonates, brassinosteroids, and ethylene, also take part in seed dormancy regulation. Auxin regulators, enhance ABA action and positively influence seed dormancy. However, jasmonates, brassinosteroids, and ethylene reduce seed dormancy level. Here, we describe recent advances in understanding the complex process of seed dormancy regulated by many phytohormonal pathways and their components. Seed dormancy studies can help obtain crop varieties producing seeds with the most desirable timing of germination.
Keywords
- seed dormancy
- germination
- abscisic acid
- gibberellic acid
- phytohormone crosstalk
1. Introduction
Seed dormancy is defined as the inability of seeds to germinate under favorable conditions. The quiescent stage of seeds enables their survival during the adverse period for further seedling development. The high level of seed dormancy is considered as a negative trait due to germination retardation and reduction in the length of the growing season. On the other hand, low level of seed dormancy leads to preharvest sprouting (PHS) and yield loss. Thus, the varieties with medium value of seed dormancy are the most desirable [1–4]. Seed dormancy is considered as a quantitative trait under the control of the genetic and environmental signals. The primary dormancy is induced during seed maturation, and its expression occurs mainly in freshly harvested seeds in order to prevent precocious seed germination. After‐ripening, which is dry seeds’ storage at room temperature, can reduce primary seed dormancy [1]. The secondary dormancy can be induced in the presence of unfavorable conditions even in initially nondormant seeds [5–7]. Environmental conditions such as cold or heat temperature (stratification), light, nitrate (NO3−), and nitric oxide (NO) can break the dormancy stage [1, 3, 6, 8, 9]. The level of seed dormancy depends on the season of a year. Deep dormancy is associated with sensing slow seasonal changes in winter. Shallow dormancy senses rapid condition changes in summer [10].
Induction and release of seed dormancy is mainly under the control of abscisic acid (ABA) and gibberellic acid (GA). ABA promotes seed dormancy and germination inhibition. Action of ABA is counteracted by GA, which promotes seed germination at appropriate time. The balance between ABA and GA is regulated by environmental conditions (light, temperature) and endogenous signals [4, 6, 7, 11]. Other phytohormones, such as auxin, brassinosteroids, and ethylene, modulate the interaction between ABA and GA in the regulation of seed dormancy [2, 4, 12].
Seed dormancy in cereals is established during seed development; however, the time of seed dormancy release can be different. Some varieties loose dormancy when the harvest maturity is reached. There are also varieties ready for germination after seed physiological maturity (fully developed, but not dried seeds). In cereals, such as barley (
Here, we discuss the genetic and molecular bases of seed dormancy entrance and breaking in Arabidopsis and monocot plants, considering the action of components belonging to ABA, GA, and other phytohormone pathways. Additionally, the influence of environmental cues on ABA‐ and GA‐related genes is described.
2. Role of ABA metabolism and signaling in maintaining seed dormancy
ABA is considered as a crucial phytohormone for seed dormancy establishment and maintenance. Many of the ABA metabolism‐ and signaling‐related genes play a crucial role in the control of seed dormancy.
2.1. ABA biosynthesis and catabolism activity in the regulation of seed dormancy
ABA produced in the embryo is fundamental for the promotion of seed dormancy. ABA synthesized in maternal tissues or ABA applied externally is not able to induce seed dormancy [13]. However, Kanno et al. [14] showed that ABA produced by maternal tissues can be transported to the embryo in order to take part in seed dormancy induction. ABA biosynthesis is catalyzed in several steps, and the rate‐limiting reaction is mediated by carotenoid cleavage dioxygenase (NCED) [15, 16].
Many ABA biosynthesis genes are implicated in the regulation of seed dormancy in Arabidopsis.
The regulation of ABA metabolism genes plays also a very important role in seed dormancy of monocot plants. In rice (
Barley seed dormancy is associated with the presence of glumellae (lemma and palea). It was shown that dehulled grains have no induction of
2.2. Regulation of seed dormancy via ABA signaling components
The core ABA signaling is mediated by pyrabactin resistance proteins/PYR‐like proteins/regulatory components of ABA receptor (PYR/PYL/RCAR), phosphatase 2C (PP2C), SNF1‐related protein kinase 2 (SnRK2), and abscisic acid responsive elements‐binding factor (AREB) basic leucine zipper (bZIP) transcription factors [34–36]. In Arabidopsis, ABA signaling genes are also implicated in seed dormancy regulation.
ABI4 is another ABA‐activated transcription factor with APETALA 2 (AP2) domain, expressed in seeds. It takes part in the regulation of abiotic stress responses and different aspects of plant development [47].
In monocot plants, the activation of ABA signaling is also associated with seed dormancy. The maize (
2.3. Environmental cues and epigenetic modifications in the regulation of the ABA pathway
The expression of Arabidopsis ABA metabolism and signaling genes is regulated through environmental factors. The red (R) light pulse irradiation applied to the far‐red (FR) light pulse pretreated, dark‐imbibed seeds inhibits and induces the expression of
The ABA metabolism and signaling genes are also regulated at epigenetic level during the establishment of seed dormancy. Kryptonite/SU(VAR) 3‐9 homolog 4 (KYP/SUVH4) is responsible for histone H3 lysine 9 dimethylation. Repression of
3. Gibberellins‐mediated control of seed dormancy release and germination
A high level of gibberellins (GA) is needed for the counteraction of ABA activity in seeds. GA promotes seed dormancy release and radical protrusion during seed germination. The activation of GA‐responsive genes induces cell wall–remodeling enzymes, such as endo‐β‐mannase, xyloglucan endotransglycolase, expansin, and β‐1,3‐mannase. Their activity leads to the weakening of the embryo‐surrounding layers. Additionally, GA ensures the high‐growth potential of the embryo [68].
3.1. Role of GA metabolism in seed dormancy break
GA biosynthesis takes place mainly in the radicle of the embryo, which in turn ensures germination progression [69]. Arabidopsis seed germination is associated with the regulation of GA metabolism genes. The highest expression of GA‐biosynthesis genes,
In barley and wheat, the expression of GA biosynthesis genes occurs during imbibition of nondormant seeds [31, 72]. The rapid increase in
GA metabolism genes are involved in seed dormancy regulation in other monocot species. In wheat, after‐ripening causes induction of
3.2. Action of GA signaling components in seed dormancy regulation
In Arabidopsis, GA signaling is mediated by GA insensitive dwarf1 (GID1) receptor. Overexpression of
3.3. The role of essential seed dormancy regulator, DOG1, in GA pathway regulation
4. ABA and GA crosstalk during seed dormancy
The seed dormancy maintenance or release and further promotion of the seed germination process are regulated by ABA and GA balance [1, 2, 12]. ABA‐mediated repression of GA biosynthesis enables the positive regulation of seed dormancy [60]. Many molecular interactions between ABA and GA pathways enable precise regulation of seed response according to environmental conditions.
4.1. Activity of ABA and GA metabolism genes ensures the ABA‐GA interaction
There is the relationship between ABA and GA biosynthesis in Arabidopsis. ABA‐deficient mutant,
4.2. ABA‐GA crosstalk depends on ABI transcription factors and DELLA proteins in seeds
ABA and GA signaling components are involved in the ABA‐GA crosstalk in Arabidopsis seeds. ABI4 exerts action on GA biosynthesis genes. In
Coat‐mediated dormancy is also related to RGL2 action. RGL2 promotes ABA biosynthesis in endosperm, then coat‐derived ABA is released to the embryo, where it ensures the expression of
The interaction between ABI transcription factors and GA catabolism genes was described in monocot plants. In sorghum, SbABI4 and SbABI5 are able to bind with coupling element 1 (CE1) and ABA responsive element (ABRE), respectively, that are present in
4.3. Seed dormancy regulators, MFT and DOG1, are a part of the ABA‐GA crosstalk
Mother of FT and TFL 1 (MFT) is one of the crucial regulators of seed dormancy enabling the interaction between ABA and GA signaling in Arabidopsis. MFT negatively regulates ABA signaling and seed dormancy, which in turn leads to germination. Its expression is repressed by ABI3 but promoted by RGL2. MFT also ensures a negative feedback loop in ABA signaling through the repression of
The role of DOG1, the GA‐related regulator of seed dormancy, was also described in ABA signaling in seeds.
5. The emerging role of auxin, jasmonates, brassinosteroids, and ethylene in seed dormancy regulation
ABA and GA are not the only phytohormonal regulators of seed dormancy establishment and release. Their action is modulated by other phytohormones, such as auxin, jasmonates (JA), brassinosteroids (BR), and ethylene.
5.1. Action of auxin pathway components in seeds
Auxin promotes seed dormancy release and germination. Constitutive induction of auxin biosynthesis in
Phytohormonal pathway | Regulator | Function | Role in seed dormancy regulation | References |
---|---|---|---|---|
Auxin | ARF10 ARF16 |
Auxin‐related transcription factors | Promotion of |
[93] |
TaIAR3 TaARF2 TaAXR1 TaRUB1 |
Releasing auxin from conjugates Auxin‐related transcription factor Aux/IAA proteasome degradation‐associated protein Ubiquitin pathway‐associated protein |
Seed dormancy release | [93] | |
Jasmonic Acid | TaAOS TaKAT3 TaLOX5 |
JA biosynthesis | Seed dormancy release | [93] |
TaAOC TaAOS |
JA biosynthesis | Seed dormancy release via repression of |
[96] [97] |
|
Brassinosteroids | TaBIN2 | Negative regulator of BR signaling with kinase activity | Seed dormancy promotion via ABI5 activation | [99, 100] |
TaDET2 TaDWF4 TaBSK2 |
BR biosynthesis Positive regulator of BR signaling with kinase activity |
Seed dormancy release | [100] | |
Ethylene | ACO ETR1 EIN2 |
Ethylene biosynthesis Ethylene receptors |
Seed dormancy release Seed dormancy release through the regulation of ABA metabolism genes |
[101] [104] |
5.2. Dual role of jasmonic acid in seed dormancy regulation
The role of JA (Jasmonic Acid) in seed dormancy is ambiguous. The increased JA content was detected in nondormant Arabidopsis seeds. Probably, the decrease of JA content during imbibition in nondormant seeds is associated with germination promotion [94]. Application of JA precursor, 12‐oxo‐phytodienoic acid (OPDA) promotes the expression of
5.3. Brassinosteroids promote seed germination via repression of ABA signaling
Brassinosteroids (BR) act opposite to ABA signaling in the regulation of seed dormancy and germination. In Arabidopsis, the crucial regulator of seed dormancy,
5.4. Ethylene represses ABA accumulation and promotes seed dormancy release
Ethylene (ET) is positively related to seed dormancy release and germination promotion. In Arabidopsis, the expression of ET biosynthesis gene,
6. Conclusions
Proper regulation of seed dormancy is crucial for appropriate timing of germination. Many environmental factors, including light and temperature, exert action on switch from dormancy to germination stage. Their action is mediated by phytohormones: ABA and GA. ABA is a master player for the entrance to and the establishment of seed dormancy. Many ABA‐related genes are necessary for the quiescent stage of seeds. Contrary to ABA, GA‐mediated pathway promotes germination under favorable conditions. Similar mechanism of seed dormancy regulation exists in monocot plants. The seed response is dependent on the ABA and GA balance. The ABA‐GA crosstalk ensures the precise seed response according to developmental stage, environmental factors, and seasons. Many components of the ABA and GA pathway, for example ABI3, ABI4, ABI5, RGL2, MFT, and DOG1, are responsible for the proper regulation of seed dormancy. Additionally, auxin, jasmonic acid, brassinosteroids, and ethylene modulate the ABA pathway in seeds. Furthermore, epigenetic control of dormancy‐related components also occurs. Therefore, seed dormancy regulation appears to be a very elaborate process. In monocot plants, a part of the seed dormancy regulatory mechanism acts in a different manner. Action of MFT and JA pathway seems to be reverse in comparison to dicot plants. A better understanding of precise phytohormonal regulation of seed response of cereals can help in obtaining new varieties with the appropriate seed dormancy level.
References
- 1.
Finch‐Savage WE, Leubner‐Metzger G. Seed dormancy and the control of germination. New Phytologist. 2006; 171 :501-523. DOI: 10.1111/j.1469‐8137.2006.01787.x - 2.
Finkelstein R, Reeves W, Ariizumi T, Steber C. Molecular aspects of seed dormancy. Plant Biology. 2008; 59 :387. DOI: 10.1146/annurev.arplant.59.032607.092740 - 3.
Graeber K, Nakabayashi K, Miatton E, Leubner‐Metzger G, Soppe WJJ. Molecular mechanisms of seed dormancy. Plant, Cell & Environment. 2012; 35 :1769-1786. DOI: 10.1111/j.1365‐3040.2012.02542.x - 4.
Shu K, Liu XD, Xie Q, He ZH. Two faces of one seed: Hormonal regulation of dormancy and germination. Molecular Plant. 2016; 9 :34-45. DOI: 10.1016/j.molp.2015.08.010 - 5.
Holdsworth MJ, Bentsink L, Soppe WJJ. Molecular networks regulating Arabidopsis seed maturation, after‐ripening, dormancy and germination. New Phytologist. 2008; 179 :33-54. DOI: 10.1111/j.1469‐8137.2008.02437.x - 6.
Gao F, Ayele BT. Functional genomics of seed dormancy in wheat: Advances and prospects. Frontiers in Plant Science. 2014; 5 :458. DOI: 10.3389/fpls.2014.00458 - 7.
Rodríguez MV, Barrero JM, Corbineau F, Gubler F, Benech‐Arnold RL. Dormancy in cereals (not too much, not so little): About the mechanisms behind this trait. Seed Science Research. 2015; 25 :99-119. DOI: 10.1017/S0960258515000021 - 8.
Liu Y, Shi L, Ye N, Liu R, Jia W, Zhang J. Nitric oxide-induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytologist. 2009; 183 :1030-1042. DOI: 10.1111/j.1469‐8137.2009.02899.x - 9.
Matakiadis T, Alboresi A, Jikumaru Y, Tatematsu K, Pichon O, Renou JP, Yuji Kamiya Y, Nambara E, Truong HN. The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiology. 2009; 149 :949-960. DOI: 10.1104/pp.108.126938 - 10.
Footitt S, Douterelo‐Soler I, Clay H, Finch‐Savage WE. Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone‐signaling pathways. Proceedings of the National Academy of Sciences. 2011; 108 :20236-20241. DOI: 10.1073/pnas.1116325108 - 11.
Shu K, Meng YJ, Shuai HW, Liu WG, Du JB, Liu J, Yang WY. Dormancy and germination: How does the crop seed decide? Plant Biology. 2015; 17 :1104-1112. DOI: 10.1111/plb.12356 - 12.
Kucera B, Cohn MA, Leubner‐Metzger G. Plant hormone interactions during seed dormancy release and germination. Seed Science Research. 2005; 15 :281-307. DOI: 10.1079/SSR2005218 - 13.
Nambara E, Marion‐Poll A. ABA action and interactions in seeds. Trends in Plant Science. 2003; 8 :213-217. DOI: 10.1016/S1360‐1385(03)00060‐8 - 14.
Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M. Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant and Cell Physiology. 2010; 51 :1988-2001. DOI: 10.1093/pcp/pcq158 - 15.
Mehrotra R, Bhalothia P, Bansal P, Basantani MK, Bharti V, Mehrotra S. Abscisic acid and abiotic stress tolerance—different tiers of regulation. Journal of Plant Physiology. 2014; 171 :486-496. DOI: 10.1016/j.jplph.2013.12.007 - 16.
Sah SK, Reddy KR, Li J. Abscisic acid and abiotic stress tolerance in crop plants. Frontiers in Plant Science. 2016; 7 :571. DOI: 10.3389/fpls.2016.00571 - 17.
Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A. Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. The Plant Journal. 2006; 45 :309-319. DOI: 10.1111/j.1365‐313X.2005.02622.x - 18.
Martínez‐Andújar C, Ordiz MI, Huang Z, Nonogaki M, Beachy RN, Nonogaki H. Induction of 9‐cis‐epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proceedings of the National Academy of Sciences. 2011; 108 :17225-17229. DOI: 10.1073/pnas.1112151108 - 19.
Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A. Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. The Plant Journal. 2012; 70 :501-512. DOI: 10.1111/j.1365‐313X.2011.04887.x - 20.
González‐Guzmán M, Abia D, Salinas J, Serrano R, Rodríguez PL. Two new alleles of the abscisic aldehyde oxidase 3 gene reveal its role in abscisic acid biosynthesis in seeds. Plant Physiology. 2004; 135 :325-333. DOI: 10.1104/pp.103.036590 - 21.
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Nobuhiro Hirai N, Koshiba T, Kamiya Y, Nambara E. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: Key enzymes in ABA catabolism. The EMBO Journal. 2004; 23 :1647-1656. DOI: 10.1038/sj.emboj.7600121 - 22.
Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E. CYP707A1 and CYP707A2, which encode abscisic acid 8′‐hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiology. 2006; 141 :97-107. DOI: 10.1104/pp.106.079475 - 23.
Matilla AJ, Carrillo‐Barral N, del Carmen Rodríguez‐Gacio M. An update on the role of NCED and CYP707A ABA metabolism genes in seed dormancy induction and the response to after‐ripening and nitrate. Journal of Plant Growth Regulation. 2015; 34 :274-293. DOI: 10.1007/s00344‐014‐9464‐7 - 24.
Liu Y, Fang J, Xu F, Chu J, Yan C, Schläppi MR, Wang Y, Chu C. Expression patterns of ABA and GA metabolism genes and hormone levels during rice seed development and imbibition: A comparison of dormant and non‐dormant rice cultivars. Journal of Genetics and Genomics. 2014; 41 :327-338. DOI: 10.1016/j.jgg.2014.04.004 - 25.
Chono M, Honda I, Shinoda S, Kushiro T, Kamiya Y, Nambara E, Kawakami N, Kaneko S, Watanabe Y. Field studies on the regulation of abscisic acid content and germinability during grain development of barley: Molecular and chemical analysis of pre‐harvest sprouting. Journal of Experimental Botany. 2006; 57 :2421-2434. DOI: 10.1093/jxb/erj215 - 26.
Leymarie J, Robayo‐Romero ME, Gendreau E, Benech‐Arnold RL, Corbineau F. Involvement of ABA in induction of secondary dormancy in barley ( Hordeum vulgare L.) seeds. Plant and Cell Physiology. 2008;49 :1830-1838. DOI: 10.1093/pcp/pcn164 - 27.
Sreenivasulu N, Radchuk V, Alawady A, Borisjuk L, Weier D, Staroske N, Fuchs J, Miersch O, Strickert M, Usadel B, Wobus U, Grimm B, Weber H, Weschke W. De-regulation of abscisic acid contents causes abnormal endosperm development in the barley mutant seg8 . The Plant Journal. 2010;64 :589-603. DOI: 10.1111/j.1365‐313X.2010.04350.x - 28.
Mendiondo GM, Leymarie J, Farrant JM, Corbineau F, Benech‐Arnold RL. 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. 2010;20 : 69-77. DOI: 10.1017/S0960258509990262 - 29.
Hoang HH, Bailly C, Corbineau F, Leymarie J. Induction of secondary dormancy by hypoxia in barley grains and its hormonal regulation. Journal of Experimental Botany. 2013a; 64 :2017-2025. DOI: 10.1093/jxb/ert062 - 30.
Millar AA, Jacobsen JV, Ross JJ, Helliwell CA, Poole AT, Scofield G, Reid J, Gubler F. Seed dormancy and ABA metabolism in Arabidopsis and barley: The role of ABA 8′‐hydroxylase. The Plant Journal. 2006; 45 :942-954. DOI: 10.1111/j.1365‐313X.2006. 02659.x - 31.
Gubler F, Hughes T, Waterhouse P, Jacobsen J. Regulation of dormancy in barley by blue light and after‐ripening: Effects on abscisic acid and gibberellin metabolism. Plant Physiology. 2008; 147 :886-896. DOI: 10.1104/pp.107.115469 - 32.
Barrero JM, Talbot MJ, White RG, Jacobsen JV, Gubler F. Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiology. 2009; 150 :1006-1021. DOI: 10.1104/pp.109.137901 - 33.
Barrero JM, Jacobsen JV, Talbot MJ, White RG, Swain SM, Garvin DF, Gubler F. Grain dormancy and light quality effects on germination in the model grass Brachypodium distachyon . New Phytologist. 2012;193 :376-386. DOI: 10.1111/j.1469‐8137.2011.03938.x - 34.
Nakashima K, Yamaguchi‐Shinozaki K. ABA signaling in stress‐response and seed development. Plant Cell Reports. 2013; 32 :959-970. DOI: 10.1007/s00299‐013‐1418‐1 - 35.
Yoshida T, Mogami J, Yamaguchi‐Shinozaki K. ABA‐dependent and ABA‐independent signaling in response to osmotic stress in plants. Current Opinion in Plant Biology. 2014; 21 :133-139. DOI: 10.1016/j.pbi.2014.07.009 - 36.
Daszkowska‐Golec A. The role of abscisic acid in drought stress: How ABA helps plants to cope with drought stress. Hossain MA, Wani SH, Bhattachajee S, Burritt DJ, Tran LSP, editors. In: Drought Stress Tolerance in Plants. Vol. 2. Cham: Springer International Publishing; 2016. pp. 123-151. DOI: 10.1007/978‐3‐319‐32423‐4_5 - 37.
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi‐Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K. Type 2C protein phosphatases directly regulate abscisic acid‐activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences. 2009; 106 :17588-17593. DOI: 10.1073/pnas.0907095106 - 38.
Karssen CM, Hilhorst HWM, Koornneef M. The benefit of biosynthesis and response mutants to the study of the role of abscisic acid in plants. In: Pharis RP, Rood SB, editors. Plant Growth Substances 1988. Berlin, Heidelberg: Springer; 1990. pp. 23-31. DOI: 10.1007/978‐3‐642‐74545‐4_3 - 39.
Kim W, Lee Y, Park J, Lee N, Choi G. HONSU, a protein phosphatase 2C, regulates seed dormancy by inhibiting ABA signaling in Arabidopsis. Plant and Cell Physiology. 2013; 54 :555-572. DOI: 10.1093/pcp/pct017 - 40.
Lee KP, Piskurewicz U, Turečková V, Strnad M, Lopez‐Molina L. 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 Sciences. 2010; 107 :19108-19113. DOI: 10.1073/pnas.1012896107 - 41.
Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Chunyan Liu C, Feng Y, Cao X, Xie Q. ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genetics. 2013; 9 :e1003577. DOI: 10.1371/journal.pgen.1003577 - 42.
Skubacz A, Daszkowska‐Golec A, Szarejko I. The role and regulation of ABI5 (ABA‐insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Frontiers in Plant Science. 2016; 7 :1884. DOI: 10.3389/fpls.2016.01884 - 43.
Parcy F, Valon C, Raynal M, Gaubier‐Comella P, Delseny M, Giraudat J. Regulation of gene expression programs during Arabidopsis seed development: Roles of the ABI3 locus and of endogenous abscisic acid. The Plant Cell. 1994; 6 :1567-1582. DOI: 10.1105/tpc.6.11.1567 - 44.
Parcy F, Valon C, Kohara A, Miséra S, Giraudat J. The ABSCISIC ACID‐INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. The Plant Cell. 1997; 9 :1265-1277. DOI: 10.1105/tpc.9.8.1265 - 45.
Nambara E, Naito S, McCourt P. A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. The Plant Journal. 1992;2 :435-441. DOI: 10.1111/j.1365‐313X.1992.00435.x - 46.
Ding ZJ, Yan JY, Li GX, Wu ZC, Zhang SQ, Zheng SJ. WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. The Plant Journal. 2014; 79 :810-823. DOI: 10.1111/tpj.12597 - 47.
Wind JJ, Peviani A, Snel B, Hanson J, Smeekens SC. ABI4: Versatile activator and repressor. Trends in Plant Science. 2013; 18 :125-132. DOI: 10.1016/j.tplants.2012.10.004 - 48.
Lee K, Seo PJ. Coordination of seed dormancy and germination processes by MYB96. Plant Signaling & Behavior. 2015; 10 :e1056423. DOI: 10.1080/15592324.2015.1056423 - 49.
Yano R, Kanno Y, Jikumaru Y, Nakabayashi K, Kamiya Y, Nambara E. CHOTTO1, a putative double APETALA2 repeat transcription factor, is involved in abscisic acid‐mediated repression of gibberellin biosynthesis during seed germination in Arabidopsis. Plant Physiology. 2009; 151 :641-654. DOI: 10.1104/pp.109.142018 - 50.
Yamagishi K, Tatematsu K, Yano R, Preston J, Kitamura S, Takahashi H, McCourt P, Kamiya Y, Nambara E. CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant and Cell Physiology. 2009; 50 :330-340. DOI: 10.1093/pcp/pcn201 - 51.
Finkelstein RR. Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. The Plant Journal. 1994;5 :765-771. DOI: 10.1046/j.1365‐313X.1994.5060765.x - 52.
Holman TJ, Jones PD, Russell L, Medhurst A, Tomás SÚ, Talloji P, Marquez J, Schmuths H, Tung S, Taylor I, Footitt S, Bachmair A, Theodoulou FL, Holdsworth MJ. The N‐end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proceedings of the National Academy of Sciences. 2009; 106 :4549-4554. DOI: 10.1073/pnas.0810280106 - 53.
Cantoro R, Crocco CD, Benech‐Arnold RL, Rodríguez MV. In vitro binding of Sorghum bicolor transcription factors ABI4 and ABI5 to a conserved region of aGA 2‐OXIDASE promoter: Possible role of this interaction in the expression of seed dormancy. Journal of Experimental Botany. 2013;64 :5721-5735. DOI: 10.1093/jxb/ert347 - 54.
Dekkers BJ, He H, Hanson J, Willems LA, Jamar DC, Cueff G, Rajjou L, Hilhorst HWM, Bentsink L. The Arabidopsis DELAY OF GERMINATION 1 gene affects ABSCISIC ACID INSENSITIVE 5 (ABI5) expression and genetically interacts with ABI3 during Arabidopsis seed development. The Plant Journal. 2016; 85 :451-465. DOI: 10.1111/tpj.13118 - 55.
Robichaud C, Sussex IM. The response of viviparous‐1 and wild type embryos of Zea mays to culture in the presence of abscisic acid. Journal of Plant Physiology. 1986;126 :235-242. DOI: 10.1016/S0176‐1617(86)80025‐6 - 56.
Huang T, Qu B, Li HP, Zuo DY, Zhao ZX, Liao YC. A maize viviparous 1 gene increases seed dormancy and preharvest sprouting tolerance in transgenic wheat. Journal of Cereal Science. 2012; 55 :166-173. DOI: 10.1016/j.jcs.2011.11.003 - 57.
Fan J, Niu X, Wang Y, Ren G, Zhuo T, Yang Y, Lu B, Liu Y. Short, direct repeats (SDRs)‐mediated post‐transcriptional processing of a transcription factor gene OsVP1 in rice (Oryza sativa ). Journal of Experimental Botany. 2007;58 :3811-3817. DOI: 10.1093/jxb/erm231 - 58.
Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, Yano M. Molecular cloning of Sdr4 , a regulator involved in seed dormancy and domestication of rice. Proceedings of the National Academy of Sciences. 2010;107 :5792-5797. DOI: 10.1073/pnas.0911965107 - 59.
Rodríguez MV, Mendiondo GM, Maskin L, Gudesblat GE, Iusem ND, Benech‐Arnold RL. Expression of ABA signalling genes and ABI5 protein levels in imbibed Sorghum bicolor caryopses with contrasting dormancy and at different developmental stages. Annals of Botany. 2009;104 :975-985. DOI: 10.1093/aob/mcp184 - 60.
Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, North H, Marion‐Poll A, Sun T, Koshiba T, Kamiya Y, Yamaguchi S, Nambara E. Regulation of hormone metabolism in Arabidopsis seeds: Phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. The Plant Journal. 2006; 48 :354-366. DOI: 10.1111/j.1365‐313X.2006.02881.x - 61.
Hoang HH, Sechet J, Bailly C, Leymarie J, Corbineau F. Inhibition of germination of dormant barley ( Hordeum vulgare L.) grains by blue light as related to oxygen and hormonal regulation. Plant, Cell & Environment. 2014;37 :1393-1403. DOI: 10.1111/pce.12239 - 62.
Barrero JM, Downie AB, Xu Q, Gubler F. A role for barley CRYPTOCHROME1 in light regulation of grain dormancy and germination. The Plant Cell. 2014; 26 :1094-1104. DOI: 10.1105/tpc.113.121830 - 63.
Hofmann N. Cryptochromes and seed dormancy: The molecular mechanism of blue light inhibition of grain germination. The Plant Cell. 2014; 26 :846. DOI: 10.1105/tpc.114.124727 - 64.
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, Kawakami N. High temperature‐induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiology. 2008; 146 :1368-1385. DOI: 10.1104/pp.107.113738 - 65.
Gibbs DJ, Bacardit J, Bachmair A, Holdsworth MJ. The eukaryotic N‐end rule pathway: Conserved mechanisms and diverse functions. Trends in Cell Biology. 2014; 24 :603-611. DOI: 10.1016/j.tcb.2014.05.001 - 66.
Zheng J, Chen F, Wang Z, Cao H, Li X, Deng X, Soppe WJJ, Li Y, Liu Y. A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytologist. 2012; 193 :605-616. DOI: 10.1111/j.1469‐8137.2011.03969.x - 67.
Zhao M, Yang S, Liu X, Wu K. Arabidopsis histone demethylases LDL1 and LDL2 control primary seed dormancy by regulating DELAY OF GERMINATION 1 and ABA signaling‐related genes. Frontiers in Plant Science. 2014; 6 :159. DOI: 10.3389/fpls.2015.00159 - 68.
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S. Gibberellin biosynthesis and response during Arabidopsis seed germination. The Plant Cell. 2003; 15 :1591-1604. DOI: 10.1105/tpc.011650 - 69.
Yamaguchi S, Kamiya Y, Sun TP. Distinct cell-specific expression patterns of early and late gibberellin biosynthetic genes during Arabidopsis seed germination. The Plant Journal. 2001; 28 :443-453. DOI: 10.1046/j.1365‐313X.2001.01168.x - 70.
Debeaujon I, Koornneef M. Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiology. 2000; 122 :415-424. DOI: 10.1104/pp.122.2.415 - 71.
Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S. Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. The Plant Cell. 2004;16 :367-378. DOI: 10.1105/tpc.018143 - 72.
Liu A, Gao F, Kanno Y, Jordan MC, Kamiya Y, Seo M, Ayele B. 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. 2013; 8 :e56570. DOI: 10.1371/journal.pone.0056570 - 73.
Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA. Cold and light control seed germination through the bHLH transcription factor SPATULA. Current Biology. 2005; 15 :1998-2006. DOI: 10.1016/j.cub.2005.11.010 - 74.
Gabriele S, Rizza A, Martone J, Circelli P, Costantino P, Vittorioso P. The Dof protein DAG1 mediates PIL5 activity on seed germination by negatively regulating GA biosynthetic gene AtGA3ox1 . The Plant Journal. 2010;61 :312-323. DOI: 10.1111/j.1365‐313X.2009.04055.x - 75.
Hoang HH, Sotta B, Gendreau E, Bailly C, Leymarie J, Corbineau F. Water content: A key factor of the induction of secondary dormancy in barley grains as related to ABA metabolism. Physiologia Plantarum. 2013b; 148 :284-296. DOI: 10.1111/j.1399‐3054.2012.01710.x - 76.
Rodríguez MV, Mendiondo GM, Cantoro R, Auge GA, Luna V, Masciarelli O, Benech‐Arnold RL. Expression of seed dormancy in grain sorghum lines with contrasting pre‐harvest sprouting behavior involves differential regulation of gibberellin metabolism genes. Plant and Cell Physiology. 2012; 53 :64-80. DOI: 10.1093/pcp/pcr154 - 77.
Hauvermale AL, Tuttle KM, Takebayashi Y, Seo M, Steber CM. Loss of Arabidopsis thaliana seed dormancy is associated with increased accumulation of the GID1 GA hormone receptors. Plant and Cell Physiology. 2015; 56 :1773-1785. DOI: 10.1093/pcp/pcv084 - 78.
Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP. DELLA proteins and gibberellin‐regulated seed germination and floral development in Arabidopsis. Plant Physiology. 2004; 135 :1008-1019. DOI: 10.1104/pp.104.039578 - 79.
Steber CM, Cooney SE, McCourt P. Isolation of the GA‐response mutant sly1 as a suppressor of ABI1‐1 in Arabidopsis thaliana . Genetics. 1998;149 :509-521 - 80.
Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, Graham I, Baker A, Holdsworth M. Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. The EMBO Journal. 2002; 21 :2912-2922. DOI: 10.1093/emboj/cdf300 - 81.
Cao D, Hussain A, Cheng H, Peng J. Loss of function of four DELLA genes leads to light‐and gibberellin‐independent seed germination in Arabidopsis. Planta. 2005; 223 :105-113. DOI: 10.1007/s00425‐005‐0057‐3 - 82.
Richards DE, King KE, Ait‐Ali T, Harberd NP. How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signaling. Annual Review of Plant Biology. 2001; 52 :67-88. DOI: 10.1146/annurev.arplant.52.1.67 - 83.
Bentsink L, Jowett J, Hanhart CJ, Koornneef M. Cloning of DOG1 , a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences. 2006;103 :17042-17047. DOI: 10.1073/pnas.0607877103 - 84.
Graeber K, Linkies A, Steinbrecher T, Mummenhoff K, Tarkowská D, Turečková V, Ignatz M, Sperber K, Voegele A, de Jong H, Urbanová T, Strnad M, Leubner‐Metzger G. DELAY OF GERMINATION 1 mediates a conserved coat‐dormancy mechanism for the temperature‐and gibberellin‐dependent control of seed germination. Proceedings of the National Academy of Sciences. 2014; 111 :E3571‐E3580. DOI: 10.1073/pnas.1403851111 - 85.
Seo M, Kanno Y, Frey A, North HM, Marion‐Poll A. Dissection of Arabidopsis NCED9 promoter regulatory regions reveals a role for ABA synthesized in embryos in the regulation of GA‐dependent seed germination. Plant Science. 2016; 246 :91-97. DOI: 10.1016/j.plantsci.2016.02.013 - 86.
Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez‐Molina L. The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. The Plant Cell. 2008; 20 :2729-2745. DOI: 10.1105/tpc.108.061515 - 87.
Yuan K, Rashotte AM, Wysocka‐Diller JW. ABA and GA signaling pathways interact and regulate seed germination and seedling development under salt stress. Acta Physiologiae Plantarum. 2011; 33 :261-271. DOI: 10.1007/s11738‐010‐0542‐6 - 88.
Liu X, Hu P, Huang M, Tang Y, Li Y, Li L, Hou X. The NF‐YC‐RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nature Communications. 2016; 7 :12768. DOI: 10.1038/ncomms12768 - 89.
Vaistij FE, Gan Y, Penfield S, Gilday AD, Dave A, He Z, Josse E, Choi G, Halliday KJ, Graham IA. Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proceedings of the National Academy of Sciences. 2013; 110 :10866-10871. DOI: 10.1073/pnas.1301647110 - 90.
Ibarra SE, Tognacca RS, Dave A, Graham IA, Sánchez RA, Botto JF. Molecular mechanisms underlying the entrance in secondary dormancy of Arabidopsis seeds. Plant, Cell & Environment. 2016; 39 :213-221. DOI: 10.1111/pce.12607 - 91.
Xi W, Liu C, Hou X, Yu H. MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. The Plant Cell. 2010; 22 :1733-1748. DOI: 10.1105/tpc.109.07 3072 - 92.
Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Taiichi Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H. A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. The Plant Cell. 2011; 23 :3215-3229. DOI: 10.1105/tpc.111.088492 - 93.
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF‐mediated ABI3 activation in Arabidopsis. Proceedings of the National Academy of Sciences. 2013; 110 :15485-15490. DOI: 10.1073/pnas.1304651110 - 94.
Preston J, Tatematsu K, Kanno Y, Hobo T, Kimura M, Jikumaru Y, Yano R, Kamiya Y, Nambara E. Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: A comparative study on dormant and non‐dormant accessions. Plant and Cell Physiology. 2009; 50 :1786-1800. DOI: 10.1093/pcp/pcp121 - 95.
Dave A, Vaistij FE, Gilday AD, Penfield SD, Graham IA. Regulation of Arabidopsis thaliana seed dormancy and germination by 12‐oxo‐phytodienoic acid. Journal of Experimental Botany. 2016; 67 :2277-2284. DOI: 10.1093/jxb/erw028 - 96.
Jacobsen JV, Barrero JM, Hughes T, Julkowska M, Taylor JM, Xu Q, Gubler F. Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain ( Triticum aestivum L.). Planta. 2013;238 :121-138. DOI: 10.1007/s00425‐013‐1878‐0 - 97.
Xu Q, Truong TT, Barrero JM, Jacobsen JV, Hocart CH, Gubler F. A role for jasmonates in the release of dormancy by cold stratification in wheat. Journal of Experimental Botany. 2016; 67 :3497-3508. DOI: 10.1093/jxb/erw172 - 98.
Xi W, Yu H. MOTHER OF FT AND TFL1 regulates seed germination and fertility relevant to the brassinosteroid signaling pathway. Plant Signaling & Behavior. 2010; 5 :1315-1317. DOI: 10.4161/psb.5.10.13161 - 99.
Hu Y, Yu D. BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. The Plant Cell. 2014; 26 :4394-4408. DOI: 10.1105/tpc.114.130849 - 100.
Chitnis VR, Gao F, Yao Z, Jordan MC, Park S, Ayele BT. After‐ripening induced transcriptional changes of hormonal genes in wheat seeds: The cases of brassinosteroids, ethylene, cytokinin and salicylic acid. PloS One. 2014; 9 :e87543. DOI: 10.1371/journal.pone.0087543 - 101.
Narsai R, Law SR, Carrie C, Xu L, Whelan J. In‐depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiology. 2011; 157 :1342-1362. DOI: 10.1104/pp.111.183129 - 102.
Beaudoin N, Serizet C, Gosti F, Giraudat J. Interactions between abscisic acid and ethylene signaling cascades. The Plant Cell. 2000; 12 :1103-1115. DOI: 10.1105/tpc.12.7.1103 - 103.
Chiwocha SD, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross AR, Kermode AR. The etr1‐2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. The Plant Journal. 2005;42 :35-48. DOI: 10.1111/j.1365‐313X.2005.02359.x - 104.
Cheng WH, Chiang MH, Hwang SG, Lin PC. Antagonism between abscisic acid and ethylene in Arabidopsis acts in parallel with the reciprocal regulation of their metabolism and signaling pathways. Plant Molecular Biology. 2009; 71 :61-80. DOI: 10.1007/s11103‐009‐9509‐7 - 105.
Wang Z, Cao H, Sun Y, Li X, Chen F, Carles A, Li Y, Ding M, Zhang C, Deng X, Soppe WJ, Yong‐Xiu Liu YX. Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid‐ethylene antagonism mediated by histone deacetylation. The Plant Cell. 2013; 25 :149-166. DOI: 10.1105/tpc.112.108191