Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (5): 857-873.doi: 10.3864/j.issn.0578-1752.2020.05.001

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

ABA Metabolism and Signaling and Their Molecular Mechanism Regulating Seed Dormancy and Germination

SONG SongQuan1,4,LIU Jun2,XU HengHeng2,LIU Xu3(),HUANG Hui4   

  1. 1 Institute of Botany, Chinese Academy of Sciences, Beijing 100093
    2 Agro-Biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou 510640
    3 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081
    4 Key Laboratory of Research and Utilization of Ethnomedicinal Plant Resources of Hunan Province, Huaihua University/College of Biological and Food Engineering, Huaihua 418008, Hunan
  • Received:2019-05-21 Accepted:2019-09-30 Online:2020-03-01 Published:2020-03-14
  • Contact: Xu LIU E-mail:liuxu01@caas.cn

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Abstract:

Seed dormancy is an adaptive characteristic to environmental changes acquired by many plants during long-term phylogenetic development, and is an effective way regulating the optimal spatiotemporal distribution of seed germination and seedling formation, and is also a selective strategy for the successful reproduction and propagation in species. Phytohormonal regulation of seed dormancy and germination may be a highly conserved mechanism, of which abscisic acid (ABA) plays a master role in dormancy release and germination, and gibberellin (GA) functions as stimulating seed germination after dormancy is released. The role of ABA in seed dormancy and germination is mainly regulated by its metabolism (biosynthesis and catabolism) and signaling pathways. Therefore, in this paper, we mainly summarize the research progresses of ABA metabolism and signaling, the effects of ABA on seed development, dormancy and germination as well as the relationships between DOG1 (DELAY OF GERMINATION1, a specific gene involved in seed dormancy) and ABA signaling components. The researches showed that C40 epoxycarotenoid is a precursor, and zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase are the principal regulatory enzymes in ABA biosynthesis. The ABA catabolism includes hydroxylation and conjugation with glucose. The hydroxylation of ABA at C-8' position is catalyzed by the CYP707A, which is an important step for ABA catabolism. In the core ABA signaling pathway, ABA binds to PYR/PYL/RCAR receptors and triggers a conformational change that allows receptor-ABA complex to bind to and inhibit type 2C protein phosphatase (PP2C) activity, which results in de-repression and activation of kinases such as sucrose non-fermenting1-related protein kinase 2 (SnRK2). These kinases then phosphorylate and activate transcription factors (TF), which bind to the target promoters and induce the expression of ABA response gene downstream. ABA accumulates in seeds during mid- and late-maturation stages, and ABA synthesized in zygotic tissues induces primary dormancy and promotes seed maturation. ABA content accumulated during development and preserved in dry seeds declines at the early stage of seed imbibition. ABA is a positive regulator of seed dormancy induction and maintenance, and is a negative regulator of seed germination. DOG1 expresses and functions during seed maturation, and its expression is regulated by alternative splicing and alternative polyadenylation. Antisense DOG1 is a repressor of seed dormancy, which negatively regulates DOG1 expression and seed dormancy by causing transcriptional interference and affecting transcription extension. Seed dormancy and germination are regulated not only by core ABA signaling pathway, but also by DOG1-AHG1 (ABA HYPERSENSITIVE GERMINATION1)/AHG3 pathway. DOG1 can bind to AHG1/AHG3 and cause seed dormancy by sequestrating those negative regulators of ABA signaling and increasing ABA sensitivity in seeds. Finally, we propose some scientific issues required for investigation further in the future. How do ABA 8'-hydroxylase, ABA glucosyltransferase and β-glucosidase and their genes respond to developmental and environmental changes to maintain the normal ABA levels in ABA catabolism? How do the important regulators in ABA physiology such as Ca 2+ or reactive oxygen species influence the core ABA signaling pathway? Which pathway is preferentially responded by PP2C, a downstream overlapping component of core ABA signaling pathway and DOG1-AHG1/AHG3 pathway, when it integrates physiological conditions or environmental signals, and how are these two pathways coordinated, and what new target components does PP2C have? This paper will provide a basis to further investigate the molecular mechanism regulating seed dormancy and germination by ABA.

Key words: abscisic acid, dormancy, dormancy gene DOG1, germination, metabolism, signaling

Fig. 1

ABA biosynthetic and catabolic pathways (Modified from DEJONGHE et al.[13]) ABA precursor is synthesized from the methylerythritol phosphate (MEP) pathway. Enzymes are shown in red colour. ZEP: Zeaxanthin epoxidase; NSY: Neoxanthin synthase; NCED: 9-cis-epoxycarotenoid dioxygenase; XD: Xanthoxin dehydrogenase; ABAO: Abscisic aldehyde oxidase; CYP707A: ABA 8'-hydroxylase; ABH1: Phaseic acid reductase 1; ABAGT: ABA glucosyltransferase; βG: β-glucosidase. Enzyme inhibitors are shown in blue colour. (+)-9'-AABA: (+)-9'-acetylene-ABA; AHI4: ABA-8'-hydroxylase inhibitor 4; (+)-8'-MABA: (+)-8'-methylidyne-ABA; NDGA: Nordihydroguaiaretic acid; SLCCD13: Sesquiterpene-like carotenoid cleavage dioxygenase inhibitor 13"

Fig. 2

ABA-induced changes in receptor conformation (From CUTLER et al.[12]) In the absence of ABA, PYR/PYL (pyrabactin resistance 1/pyrabactin resistance 1-like) proteins possess an open conformation of the gate and latch loops (red and green, respectively) that flank the ABA-binding pocket. Binding of ABA induces closure of the gate and latch, which in turn creates the interaction surface that recruits docking of type 2C protein phosphatases (PP2C) onto the ABA-bound receptors. A conserved proline in the gate (which corresponds to the residue to proline 88 in PYR1 and is shown in blue) forms a direct contact with the PP2C at the docking site, which explains the PP2C-binding defect observed with PYR1P88"

Fig. 3

ABA signalling pathway and emerging model of seed dormancy regulated by DOG1 (Modified from NONOGAKI [19]) In the ABA perception and signaling pathway (left), ABA receptors (PYR/PYL/RCARs) bind to and inactivate the ABA INSENSITIVE1 (ABI1) subfamily protein phosphatases 2C (PP2Cs), including ABI1, ABI2, HYPERSENSITIVE TO ABA1 (HAB1) and HAB2, which results in de-repression and activation of kinases, such as sucrose nonfermenting1-related protein kinase 2 (SnRK2). These kinases then phosphorylate and activate transcription factors (TF), which bind to the target promoters (Pro), to induce ABA-responsive genes downstream. For seed dormancy regulation (right), DOG1 binds to ABA HYPERSENSITIVE GERMINATION1 (AHG1) and AHG3, PP2Cs primarily functioning in seeds. The DOG1 is thought to cause seed dormancy by sequestrating these negative regulators of ABA signaling and increasing ABA sensitivity in seeds"

Fig. 4

Regulation of DOG1 expression and function (From NONOGAKI[91]) A: Structures of the DOG1 gene. Top: DOG1 gDNA with exons (E1, E2, E3) and introns (I1, I2). Alternatively spliced regions are highlighted in pink and orange. Approximate positions of the dog1 mutations (T-DNAs in dog1-3, dog1-4, dog1-5 and a single-base deletion [-C] in dog1-1) are also indicated. Middle: Alternative DOG1 transcripts (α, β, γ, δ, ε) and the corresponding proteins. Note that DOG1-ε is not exactly an alternative splicing product. Bottom: Alternatively polyadenylated short DOG1 (shDOG1), which is identical to DOG1-ε and long (lgDOG1) transcripts, which comprises DOG1-α, -β, -γ and -δ. The transcriptional start (TSS) and termination (TTS) sites are indicated. Approximate position and the orientation of antisense DOG1 (asDOG1) are shown as a blue arrow. B: Possible mechanisms of asDOG1 function. Relatively stable asDOG1 RNA could function as a regulatory RNA, in a sequence-specific manner or through its secondary structure, for RNA-mediated chromatin remodeling (right panel, trans regulation). However, allele-specific asDOG1 expression has indicated that asDOG1 functions in cis (left panel). The “act” of transcription itself, rather than its product (RNA), exerts the negative effects of asDOG1 expression to DOG1 expression and dormancy. Antisense expression could cause transcriptional interference and affect transcription elongation, which is known to be important for DOG1 expression and seed dormancy while transcription-mediated chromatin remodeling is also possible. AS: Alternative splicing; APA: Alternative polyadenylation; Dist: Distal; Prox: Proximal; Prot: Protein; Tran: Transcription"

[1] BEWLEY J D, BRADFORD K J , HILHORST H W M , NONOGAKI H . Physiology of Development, Germination and Dormancy. 3rd ed. New York: Springer, 2013.
[2] 邓志军, 宋松泉, 艾训儒, 姚兰 . 植物种子保存和检测的原理与技术. 北京: 科学出版社, 2019.
DENG Z J, SONG S Q, AI X R, YAO L. Principles and Techniques of Plant Seed Conservation and Test. Beijing: Science Press, 2019. ( in Chinese)
[3] FINKELSTEIN R, REEVES W, ARIIZUMI T, SREBER C . Molecular aspects of seed dormancy. Annual Review of Plant Biology, 2008,59:387-415.
[4] SHU K, LIU X D, XIE Q, HE Z H . Two faces of one seed: Hormonal regulation of dormancy and germination. Molecular Plant, 2016,9:34-45.
[5] 宋松泉 . 种子休眠//“10000个科学难题”农业科学编委会. 10000个科学难题. 北京: 科学出版社, 2011: 31-35.
SONG S Q. Seed dormancy//The Editorial Board of Agricultural Science for 10000 Selected Problems in Sciences, ed. 10000 Selected Problems in Sciences. Beijing: Science Press, 2011: 31-35. (in Chinese)
[6] GUBLER F, MILLER A A, JACOBSEN J V . Dormancy release, ABA and pre-harvest sprouting. Current Opinion in Plant Biology, 2005,8:183-187.
[7] NONOGAKI H . Seed dormancy and germination-emerging mechanism and new hypotheses. Frontiers in Plant Science, 2014,e5:233.
[8] CORBINEAU F, XIA Q, BAILLY C, EI-MAAROUF-BOUTEAU H . Ethylene, a key factor in the regulation of seed dormancy. Frontiers in Plant Science, 2014,5:539.
[9] KUCERA B, COHN M A, LEUBNER-METZGER G . Plant hormone interactions during seed dormancy release and germination. Seed Science Research, 2005,15:281-307.
[10] 徐恒恒, 黎妮, 刘树君, 王伟青, 王伟平, 张红, 程红焱, 宋松泉 . 种子萌发及其调控的研究进展. 作物学报, 2014,40:1141-1156.
XU H H, LI N, LIU S J, WANG W Q, WANG W P, ZHANG H, CHENG H Y, SONG S Q . Research progress in seed germination and its control. Acta Agronomica Sinica, 2014,40:1141-1156. (in Chinese)
[11] GRAEBER K, NAKABAYAYASHI K, MIATTON E, LEUBNER- METZGER G, SOPPE W J J . Molecular mechanisms of seed dormancy. Plant Cell and Environment, 2012,35:1769-1786.
[12] CUTLER S R, RODRIGUEZ P L, FINKELSTEIN R R, ABRAMS S R . Abscisic acid: Emergence of a core signaling network. Annual Review of Plant Biology, 2010,61:651-679.
[13] DEJONGHE W, OKAMOTO M, CUTLER S R . Small molecule probes of ABA biosynthesis and signaling. Plant Cell and Physiology, 2018,59:1490-1499.
[14] VISHWAKARMA K, UPADHYAY N, KUMAR N, YADAV G, SINGH J, MISHRA R K, KUMAR V, VERMA R, UPADHYAY R G, PANDEY M, SHARMA S . Abscisic acid signaling and abiotic stress tolerance in plants: A review on current knowledge and future prospects. Frontiers in Plant Science, 2017,8:161.
[15] GIANINETTI A, VERNIERI P . On the role of abscisic acid in seed dormancy of red rice. Journal of Experimental Botany, 2007,58:3449-3462.
[16] MILLAR A A, JACOBSEN J V, ROSS J J, HELLIWELL C A, POOLE A T, SCOFIELD G, REID J B, GUBLER F . Seed dormancy and ABA metabolism in Arabidopsis and barley: The role of ABA 8'-hydroxylase. The Plant Journal, 2006,45:942-954.
[17] NAMBARA E, OKAMOTO M, TATEMATSU K, YANO R, SEO M, KAMIYA Y . Abscisic acid and the control of seed dormancy and germination. Seed Science Research, 2010,20:55-67.
[18] NAMBARA E, MARION-POLL A . Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology, 2005,56:165-185.
[19] NONOGAKI H . Seed germination and dormancy - The classic story, new puzzles, and evolution. Journal of Integrative Plant Biology, 2019,61:541-563.
[20] HOLDSWORTH R, BENTSINK L, SOPPE W J J. Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytologist, 2008,179:33-54.
[21] LINKIES A, LEUBNER-METZGER G . Beyond gibberellins and abscisic acid: How ethylene and jasmonates control seed germination. Plant Cell Reports, 2012,31:253-270.
[22] FINKELSTEIN R . Abscisic acid synthesis and response. Arabidopsis Book, 2013,11:e0166.
[23] NORTH H M, ALMEIDA A D, BOUTIN J-P, FREY A, TO A, BOTRAN L, SOTTA B, MARION-POLL A . The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers. The Plant Journal, 2007,50:810-824.
[24] TAN B C, JOSEPH L M, DENG W T, LIU L, LI Q B, CLINE K , McCARTY D R. Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. The Plant Journal, 2003,35:44-56.
[25] CHENG W H, ENDO A, ZHOU L, PENNEY J, CHEN H C, ARROYO A, LEON P, NAMBARA E, ASAMI T, SEO M, KOSHIBA T, SHEEN J . A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. The Plant Cell, 2002,14:2723-2743.
[26] GONZÁLEZ-GUZMÁ M, APOSTOLOVA N, BELLÉS J M, BARRERO J M, PIQUERAS P, PONCE M R, MICOL J L, SERRANO R, RODRÍGUEZ P . The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. The Plant Cell, 2002,14:1833-1846.
[27] XIONG L, ISHITANI M, LEE H, ZHU J K . The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. The Plant Cell, 2001,13:2063-2083.
[28] GAMBLE P E, MULLET J E . Inhibition of carotenoid accumulation and abscisic acid biosynthesis in fluridone-treated dark-grown barley. European Journal of Biochemistry, 1986,160:117-121.
[29] CREELMAN R A, BELL E, MULLET J E . Involvement of a lipoxygenase-like enzyme in abscisic acid biosynthesis. Plant Physiology, 1992,99:1258-1260.
[30] MÉRIGOUT P, KÉPÈS F, PERRET A M, SATIAT-JEUNEMAITRE B, MOREAU P . Effects of brefeldin A and nordihydroguaiaretic acid on endomembrane dynamics and lipid synthesis in plant cells. FEBS Letters, 2002,518:88-92.
[31] HAN S Y, KITAHATA N, SEKIMATA K, SAITO T, KOBAYASHI M, NAKASHIMA K, YAMAGUCHI-SHINOZAKI K, SHINOZAKI K, YOSHIDA S, ASAMI T . A novel inhibitor of 9-cis-epoxycarotenoid dioxygenase in abscisic acid biosynthesis in higher plants. Plant Physiology, 2004,135:1574-1582.
[32] KITAHATA N, HAN S Y, NOJI N, SAITO T, KOBAYASHI M, NAKANO T, KUCHITSU K, SHINOZAKI K, YOSHIDA S, MATSUMOTO S . A 9-cis-epoxycarotenoid dioxygenase inhibitor for use in the elucidation of abscisic acid action mechanisms. Bioorganic and Medicinal Chemistry, 2006,14:5555-5561.
[33] BOYD J, GAI Y, NELSON K M, LUKIWSKI E, TALBOT J, LOEWEN M K, OWEN S, ZAHARIA L I, CUTLER A J, ABRAMS S R, LOEWEN M C . Sesquiterpene-like inhibitors of a 9-cis- epoxycarotenoid dioxygenase regulating abscisic acid biosynthesis in higher plants. Bioorganic and Medicinal Chemistry, 2009,17:2902-2912.
[34] KUSHIRO T, OKAMOTO M, NAKABAYASHI K, YAMAGISHI K, KITAMURA S, ASAMI T, 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.
[35] SAITO S, HIRAI N, MATSUMOTO C, OHIGASHI H, OHTA D, SAKATA K, MIZUTANI M . Arabidopsis CYP707As encode (+)-abscisic acid 8'-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiology, 2004,134:1439-1449.
[36] HANADA K, HASE T, TOYODA T, SHIONZAKI K, OKAMOTO M . Origin and evolution of genes related to ABA metabolism and its signaling pathways. Journal of Plant Research, 2011,124:455-465.
[37] OKAMOTO M, KUWAHARA A, SEO M, KUSHIRO T, ASAMI T, HIRAI N, KAMIYA Y, KOSHIBA T, NAMBARA E . CYP707A1 and CYP707A2, which encode ABA 8'-hydroxylases, are indispensable for a proper control of seed dormancy and germination in Arabidopsis. Plant Physiology, 2006,141:97-107.
[38] OKAMOTO M, TANAKA Y, ABRAMS S R, KAMIYA Y, SEKI M, NAMBARA E . High humidity induces abscisic acid 8'-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiology, 2009,149:825-834.
[39] KEPKA M, BENSON C L, GONUGUNTA V K, NELSON K M, CHRISTMANN A, GRILL E, ABRAMA S R . Action of natural abscisic acid precursors and catabolites on abscisic acid receptor complexes. Plant Physiology, 2011,157:2108-2119.
[40] WENG J K, YE M, LI B, NOEL J P . Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell, 2016,166:881-893.
[41] KITAHATA N, SAITO S, MIYAZAWA Y, UMEZAWA T, SHIMADA Y, MIN Y K, MIZUTANI M, HIRAI N, SHINOZAKI K, YOSHIDA S . Chemical regulation of abscisic acid catabolism in plants by cytochrome P450 inhibitors. Bioorganic and Medicinal Chemistry, 2005,13:4491-4498.
[42] SAITO S, OKAMOTO M, SHINODA S, KUSHIRO T, KOSHIBA T, KAMIYA Y, HIRAI N, TODOROKI Y, SAKATA K, NAMBARA E, MIZUTANI M . A plant growth retardant, uniconazole, is a potent inhibitor of ABA catabolism in Arabidopsis. Bioscience Biotechnology and Biochemistry, 2006,70:1731-1739.
[43] RADEMACHER W . Growth retardants: Effects on gibberellin biosynthesis and other metabolic pathways. Annual Review of Plant Physiology and Plant Molecular Biology, 2000,51:501-531.
[44] TAKEUCHI J, OKAMOTO M, MEGA R, KANNO Y, OHNISHI T, SEO M, TODOROKI Y . Abscinazole-E3M, a practical inhibitor of abscisic acid 8'-hydroxylase for improving drought tolerance. Scientific Reports, 2016,6:37060.
[45] BENSON C L, KEPKA M, WUNSCHEL C, RAJAGOPALAN N, NELSON K M, CHRISTMANN A, ABRAMS S R, GRILL E, LOEWEN M . Abscisic acid analogs as chemical probes for dissection of abscisic acid responses in Arabidopsis thaliana. Phytochemistry, 2015,113:96-107.
[46] ARAKI Y, MIYAWAKI A, MIYASHITA T, MIZUTANI M, HIRAI N, TODOROKI Y . A new non-azole inhibitor of ABA 8'-hydroxylase: Effect of the hydroxyl group substituted for geminal methyl groups in the six-membered ring. Bioorganic and Medicinal Chemistry Letters, 2006,16:3302-3305.
[47] MA Y, SZOSTKIEWICZ I, KORTE A, MOES D, YANG Y, CHRISTMANN A, GRILL E . Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 2009,324:1064-1068.
[48] NISHIMURA N, TSUCHIYA W, MORESCO J J, HAYASHI Y, SATOH K, KAIWA N, IRISA T, KINOSHITA T, SCHROEDER J I, YATES J R, HIRAYAMA T, YAMAZAKI T . Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nature Communication, 2018,9:2132.
[49] PARK S Y, FUNG P, NISHIMURA N, JENSEN D R, FUJII H, ZHAO Y, LUMBA S, SANTIAGO J, RODRIGUES A, CHOW T F, ALFRED S E, BONETTA D, FINKELSTEIN R, PROVART N J, DESVEAUX D, RODRIGUEZ P L, McCOURT P, ZHU J K, SCHROEDER J I, VOLKMAN B F, CUTLER S R . Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 2009,324:1068-1071.
[50] MELCHER K, NG L M, ZHOU X E, SOON F-F, XU Y, SUINO-POWELL K M, PARK S Y, WEINER J J, FUJII H, CHINNUSAMY V, KOVACH A, LI J, WANG Y, LI J, PERTERSON F C, JENSEN D R, YONG E L, VOLKMAN B F, CUTLER S R, ZHU J K, XU H E. A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature, 2009,462:602-608.
[51] SANTIAGO J, DUPEUX F, ROUND A, ANTONI R, PARK S Y, JAMIN M, CUTLER S R, RODRIGUEZ P L, MÁRQUEZ J A. The abscisic acid receptor PYR1 in complex with abscisic acid. Nature, 2009,462:665-668.
[52] YIN P, FAN H, HAO Q, YUAN X, WU D, PANG Y, YAN C, LI W, WANG J, YAN N . Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nature Structural and Molecular Biology, 2009,16:1230-1236.
[53] FUJII H, ZHU J K . Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proceedings of the National Academy of Sciences of the United States of America, 2009,106:8380-8385.
[54] SOON F F, NG L M, ZHOU X E, WEST G M, KOVACH A, TAN M H E, SUINO-POWELL K M, HE Y, XU Y, CHALMERS M J, BRUNZELLE J S, ZHANG H, YANG H, JIANG H, LI J, YONG E L, CUTLER S, ZHU J K, GRIFFIN P R, MELCHER K, XU H E. Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science, 2012,335:85-88.
[55] NAKAMURA S, LYNCH T J, FINKELSTEIN R R . Physical interactions between ABA response loci of Arabidopsis. The Plant Journal, 2001,26:627-635.
[56] HAUSER F, WAADT R, SCHROEDER J I . Evolution of abscisic acid synthesis and signaling mechanisms. Current Biology, 2011,21:R346-R355.
[57] BOWMAN J L, KOHCHI T, YAMATO K T, JENKINS J, SHU S, ISHIZAKI K, YAMAOKA S, NISHIHAMA R, NAKAMURA Y, BERGER F, ADAM C, AKI S S, ALTHOFF F, ARAKI T, ARTEAGA-VAZQUEZ M A, BALASUBRMANIAN S, BARRY K, BAYER D, SCHMUTZ J. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell, 2017,171:287-304.
[58] TISCHER S V, WUNSCHEL C, PAPACEK M, KLEIGREWE K, HOFMANN T, CHRISTMANN A, GRILL E . Combinatorial interaction network of abscisic acid receptors and coreceptors from Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 2017,114:10280-10285.
[59] ANTONI R, GONZALEZ-GUZMAN M, RODRIGUEZ L, RODRIGUES A, PIZZIO G A, RODRIGUEZ P L . Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiology, 2012,158:970-980.
[60] NISHIMURA N, YOSHIDA T, KITAHATA N, ASAMI T, SHINOZAKI K, HIRAYAMA T . ABA-HYPERSENSITIVE GERMINATION1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. The Plant Journal, 2007,50:935-949.
[61] FUJITA Y, NAKASHIMA K, YOSHIDA T, KATAGIRI T, KIDOKORO S, KANAMORI N, UMEZAWA T, FUJITA M, MARUYAMA K, ISHIYAMA K, KOBAYASHI M, NAKASONE S, YAMADA K, ITO T, SHINOZAKI K . Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant and Cell Physiology, 2009,50:2123-2132.
[62] NAKASHIMA K, FUJITA Y, KANAMORI N, KATAGIRI T, UMEZAWA T, KIDOKORO S, MARUYAMA K, YOSHIDA T, ISHIYAMA K, KOBAYASHI M, SHINOZAKI K, YAMAGUCHI- SHINOZAKI K . Three Arabidopsis SnRK2 protein kinases, SRK2D/ SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant and Cell Physiology, 2009,50:1345-1363.
[63] 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 of the United states of America, 2009,106:17588-17593.
[64] KLINE K G, BARRETT-WILT G A, SUSSMAN M R. In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proceedings of the National Academy of Sciences of the United States of America, 2010,107:15986-15991.
[65] UMEZAWA T, SUGIYAMA N, TAKAHASHI F, ANDERSON J C, ISHIHAMA Y, PECK S C, SHINOZAKI K. Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Science Signaling, 2013, 6:1rs8.
[66] WANG P, XUE L, BATELLI G, LEE S, HOU Y J, VAN OOSTEN M J, ZHANG H, TAO W A, ZHU J K. Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proceedings of the National Academy of Sciences of the United states of America, 2013,110:11205-11210.
[67] DING S, ZHANG B, QIN F . Arabidopsis RZFP34/CHYR1, an ubiquitin E3 ligase, regulates stomatal movement and drought tolerance via SnRK2.6-mediated phosphorylation. The Plant Cell, 2015,27:3228-3244.
[68] BELDA-PALAZON B, RODRIGUEZ L, FERNANDEZ M A, CASTILLO M C, ANDERSON E A, GAO C, GONZALEZ- GUZMAN M, PEIRATS-LLOBET M, ZHAO Q, DE WINNE N, GEVEERT K, DE JAEGER G, JIANG L, LEÒN J, MULLEN R T, RODRIGUEZ P L. FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. The Plant Cell, 2016,28:2291-2311.
[69] WU Q, ZHANG X, PEIRATS-LLOBET M, BELDA-PALAZON B, WANG X, CUI S, YU X, RODRIGUEZ P L, AN C . Ubiquitin ligases RGLG1 and RGLG5 regulate abscisic acid signaling by controlling the turnover of phosphatase PP2CA. The Plant Cell, 2016,28:2178-2196.
[70] YU F, WU Y, XIE Q . Ubiquitin-proteasome system in ABA signaling: From perception to action. Molecular Plant, 2016,9:21-33.
[71] ZHAO J, ZHAO L, ZHANG M, ZAFAR S, FANG J, LI M, ZHANG W, LI X . Arabidopsis E3 ubiquitin ligases PUB22 and PUB23 negatively regulate drought tolerance by targeting ABA receptor PYL9 for degradation. International Journal of Molecular Science, 2017,18:1841.
[72] KARSSEN C M, BRINKHORST-VAN DER SWAN D L C, BREEKLAND A E, KOORNNEEF M. Induction of dormancy during seed development by endogenous abscisic acid: Studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta, 1983,157:158-165.
[73] FREY A, GODIN B, BONNET M, SOTTA B, MARION-POLL A . Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta, 2004,218:958-964.
[74] KOORNNEEF M, HANHART C J, HILHORST H W M, KARSSEN C M. In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiology, 1989,90:463-469.
[75] CADMAN C S, TOOROP P E, HILHORST H W M, FINCH- SAVAGE W E. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. The Plant Journal, 2006,46:805-822.
[76] 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 synthesised in the endosperm is involved in the induction of seed dormancy. The Plant Journal, 2006,45:309-319.
[77] NAKABAYASHI K, OKAMOTO M, KOSHIBA T, KAMIYA Y, NAMBARA E . Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: Epigenetic and genetic regulation of transcription in seed. The Plant Journal, 2005,41:697-709.
[78] FINCH-SAVAGE W E, LEUBNER-METZGER G . Seed dormancy and the control of germination. New Phytologist, 2006,171:501-523.
[79] 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.
[80] JACOBSEN J V, BARRERO J M, HUGHES T, JULKOWSKA M, TAYLOR J M, XU Q, GUBLER F . Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat (Triticum aestivum L.) grain. Planta, 2013,238:121-138.
[81] LIU A, GAO F, KANNO Y, JORDAN M C, KAMIYA Y, SEO M, AYELE B T . 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.
[82] BARRERO J M, TALBOT M J, WHITE R G, JACOBSEN J V, 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.
[83] 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.
[84] 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.
[85] MATAKIADIS T, ALBORESI A, JIKUMARU Y, TATEMATSU K, PICHON O, RENOU J P, SOTTA B, KAMIYA Y, NAMBARA E, TROUNG H N . The Arabidopsis abscisic acid catabolism gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiology, 2009,149:949-960.
[86] 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 ABA biosynthesis and its role in the inhibition of GA action in Arabidopsis seeds. Plant Physiology, 2008,146:1368-1385.
[87] BENECH-ARNOLD R L, GUALANO N, LEYMARIE J, CÔME D, CORBINEAU F . Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. Journal of Experimental Botany, 2006,57:1423-1430.
[88] TOOROP P E, BEWLEY J D, HILHORST H W M. Endo-β-isoforms are present in the endosperm and embryo of tomato seeds, but are not essentially linked to germination. Planta, 1996,200:153-158.
[89] MÜLLER K, TINTELNOT S, LEUBNER-METZGER G . 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, 2006,47:864-877.
[90] MÜLLER K, CARSTENS A C, LINKIES A, TORRES M A, LEUBNER-METZGER G . The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytologist, 2009,184:885-897.
[91] NONOGAKI H . Seed biology updates-highlights and new discoveries in seed dormancy and germination research. Frontiers in Plant Science, 2017,8:524.
[92] NÉE G, KRAMER K, NAKABAYASHI K, YUAN B, XIANG Y, MIATTON E, FINKEMEIER I, SOPPE W J . DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nature Communication, 2017,8:72.
[93] ALONSO-BLANCO C, BENTSINK L, HANHART C J, VRIES H B D, KOORNNEEF M . Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics, 2003,164:711-729.
[94] BENTSINK L, HANSON J, HANHART C J, BLANKESTIJN-DE VRIES H, COLTRANE C, KEIZER P, EL-LITHY M, ALONSO-BLANCO C, DE ANDRÉS M T, REYMOND M, VAN EEUWIJK F, SMEEKENS S, KOORNNEEF M. Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways. Proceedings of the National Academy of Sciences of the United States of America , 2010,107:4264-4269.
[95] BENTSINK L, JOWETT J, HANHART C J, KOORNNEEF M . Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 2006,103:17042-17047.
[96] NAKABAYASHI K, BARTSCH M, XIANG Y, MIATTON E, PELLENGAHR S, YANO R, SEO M, SOPPE W J J. The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. The Plant Cell, 2012,24:2826-2838.
[97] NAKABAYASHI K, BARTSCH M, DING J, SOPPE W J . Seed dormancy in Arabidopsis requires self-binding ability of DOG1 protein and the presence of multiple isoforms generated by alternative splicing. PLoS Genetics, 2015,11:e1005737.
[98] CYREK M, FEDAK H, CIESIELSKI A, GUO Y W, SLIWA A, BRZEZNIAK L, KRZYCZMONIK K, PIETRAS Z, KACZANOWSKI S, LIU F, SWIEZEWSKI S . Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1. Plant Physiology, 2016,170:947-955.
[99] DOLATA J, GUO Y, KOŁOWERZO A, SMOLIŃSKI D, BRZYŻEK G, JARMOŁOWSKI A, ŚWIEŻEWSKI S. NTR1 is required for transcription elongation checkpoints at alternative exons in Arabidopsis. The EMBO Journal, 2015,34:544-558.
[100] LIU Y, KOORNNEEF M, SOPPE W J . The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. The Plant Cell, 2007,19:433-444.
[101] LIU Y, GEYER R, VAN ZANTEN M, CARLES A, LI Y, HÖROLD A, VAN NOCKER S, SOPPE W J J. Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy. PLoS ONE, 2011,6:e22241.
[102] MORTENSEN S A, GRASSER K D . The seed dormancy defect of Arabidopsis mutants lacking the transcript elongation factor TFIIS is caused by reduced expression of the DOG1 gene. FEBS Letters, 2014,588:47-51.
[103] DI GIAMMARTINO D C, NISHIDA K, MANLEY J L . Mechanisms and consequences of alternative polyadenylation. Molecular Cell, 2011,43:853-866.
[104] FEDAK H, PALUSINSKA M, KRZYCZMONIK K, BRZEZNIAK L, YATUSEVICH R, PIETRAS Z, KACZANOWSKI S, SWIEZEWSKI S . Control of seed dormancy in Arabidopsis by a cis-acting non- coding antisense transcript. Proceedings of the National Academy of Sciences of the United States of America, 2016,113:E7846-E7855.
[105] ARCHACKI R, YATUSEVICH R, BUSZEWICZ D, KRZYCZMONIK K, PATRYN J, IWANICKA-NOWICKA R, BIECEK P, WILCZYNSKI B, KOBLOWSKA M, JERZMANOWSKI A, SWIEZEWSKI S . Arabidopsis SWI/SNF chromatin remodeling complex binds both promoters and terminators to regulate gene expression. Nucleic Acids Research, 2016,45:3116-3129.
[106] LIN S, ZHANG L, LUO W, ZHANG X . Characteristics of antisense transcript promoters and the regulation of their activity. International Journal of Molecular Sciences, 2015,17:1-17.
[107] KORNIENKO A E, GUENZL P M, BARLOW D P, PAULER F M . Gene regulation by the act of long non-coding RNA transcription. BMC Biology, 2013,11:59.
[108] PELECHANO V, STEINMETZ L M . Non-coding RNA gene regulation by antisense transcription. Nature Review of Genetics, 2013,14:880-893.
[109] QUINN J J, CHANG H Y . Unique features of long non-coding RNA biogenesis and function. Nature Review Genetics, 2016,17:47-62.
[110] SHEARWIN K E, CALLEN B P, EGAN J B . Transcriptional interference - a crash course. Trends in Genetics, 2005,21:339-345.
[111] HONGAY C F, GRISAFI P L, GALITSKI T, FINK G R . Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell, 2006,127:735-745.
[112] NÉE G, XIANG Y, SOPPE W J . The release of dormancy, a wake-up call for seeds to germinate. Current Opinion in Plant Biology, 2016,35:8-14.
[113] YOSHIDA T, NISHIMURA N, KITAHATA N, KUROMORI T, ITO T, ASAMI T, SHINOZAKI K, HIRAYAMA T . ABA-HYPERSENSITIVE GERMINATION3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiology, 2005,140:115-126.
[114] LI T, BONKOVSKY H L, GUO J . Structural analysis of heme proteins: Implications for design and prediction. BMC Structural Biology, 2011,11:13.
[115] ALBERTOS P, ROMERO-PUERTAS M C, TATEMATSU K, MATEOS I, SANCHEZ-VICENTE I, NAMBARA E, LORENZO O, SÁNCHEZ-VICENTE I, NAMBARA E, LORENZO O. S- Nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nature Communication, 2015,6:1-10.
[116] OHKUMA K, LYON J L, ADDICOTT F T, SMITH O E . Abscisin II, an abscission-accelerating substance from young cotton fruit. Science, 1963,142:1592-1593.
[117] WANG Y G, FU F L, YU H Q, HU T, ZHANG Y Y, TAO Y, ZHU J K, ZHAO Y, LI W C . Interaction network of core ABA signaling components in maize. Plant Molecular Biology, 2018,96:245-263.
[118] LIU S J, SONG S H, WANG W Q, SONG S Q . De novo assembly and characterization of germinating lettuce seed transcriptome using Illumina paired-end sequencing. Plant Physiology and Biochemistry, 2015,96:154-162.
[119] WANG W Q, SONG B Y, DENG Z J, WANG Y, LIU S J, MØLLER I M, SONG S Q . Proteomic analysis of Lactuca sativa seed germination and thermoinhibition by sampling of individual seeds at germination and removal of storage proteins by PEG fractionation. Plant Physiology, 2015,167:1332-1350.
[120] XU H H, LIU S J, SONG S H, WANG W Q, MØLLER I X, SONG S Q . Proteome changes associated with dormancy release of Dongxiang wild rice seeds. Journal of Plant Physiology, 2016,206:68-86.
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