Skip to main content
Log in

The pivotal role of abscisic acid signaling during transition from seed maturation to germination

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Seed maturation and germination are two continuous developmental processes that link two distinct generations in spermatophytes; the precise genetic control of these two processes is, therefore, crucially important for the survival of the next generation. Pieces of experimental evidence accumulated so far indicate that a concerted action of endogenous signals and environmental cues is required to govern these processes. Plant hormone abscisic acid (ABA) has been suggested to play a predominant role in directing seed maturation and maintaining seed dormancy under unfavorable environmental conditions until antagonized by gibberellins (GA) and certain environmental cues to allow the commencement of seed germination when environmental conditions are favorable; therefore, the balance of ABA and GA is a major determinant of the timing of seed germination. Due to the advent of new technologies and system biology approaches, molecular studies are beginning to draw a picture of the sophisticated genetic network that drives seed maturation during the past decade, though the picture is still incomplete and many details are missing. In this review, we summarize recent advances in ABA signaling pathway in the regulation of seed maturation as well as the transition from seed maturation to germination, and highlight the importance of system biology approaches in the study of seed maturation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, Nicolás C (2011) Functional analysis in Arabidopsis of FsPTP1, a tyrosine phosphatase from beechnuts, reveals its role as a negative regulator of ABA signaling and seed dormancy and suggests its involvement in ethylene signaling modulation. Planta 234:589–597

    Article  PubMed  CAS  Google Scholar 

  • Angelovici R, Galili G, Fernie AR, Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15:211–218

    Article  CAS  PubMed  Google Scholar 

  • Ariizumi T, Hauvermale AL, Nelson SK, Hanada A, Yamaguchi S, Steber CM (2013) Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiol 162:2125–2139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrero JM, Millar AA, Griffiths J, Czechowski T, Scheible WR, Udvardi M, Reid JB, Ross JJ, Jacobsen JV, Gubler F (2010) Gene expression profiling identifies two regulatory genes controlling dormancy and ABA sensitivity in Arabidopsis seeds. Plant J 61:611–622

    Article  CAS  PubMed  Google Scholar 

  • Baud S, Boutin J-P, Miquel M, Lepiniec L, Rochat C (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40:151–160

    Article  CAS  Google Scholar 

  • Bentsink L, Koornneef M (2008) Seed dormancy and germination. In: The Arabidopsis Book, vol 6. vol 1. BioOne, pp 1-18

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou J-P, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7:e1002014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brocard-Gifford IM, Lynch TJ, Finkelstein RR (2003) Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol 131:78–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruijn SMd, Ooms JJJ, Karssen CM, Vreugdenhil D (1997) Effects of abscisic acid on reserve deposition in developing Arabidopsis seeds. Acta Bot Neerlandica 46:263–277

    Article  Google Scholar 

  • Cantoro R, Crocco CD, Benech-Arnold RL, Rodríguez MV (2013) In vitro binding of Sorghum bicolor transcription factors ABI4 and ABI5 to a conserved region of a GA 2-OXIDASE promoter: possible role of this interaction in the expression of seed dormancy. J Exp Bot 64:5721–5735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrasekaran U, Xu W, Liu A (2014) Transcriptome profiling identifies ABA mediated regulatory changes towards storage filling in developing seeds of castor bean (Ricinus communis L.). Cell Biosci 4:1–12

    Article  CAS  Google Scholar 

  • Chen H, Zhang J, Neff MM, Hong S-W, Zhang H, Deng X-W, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci 105:4495–4500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiang GCK, Barua D, Kramer EM, Amasino RM, Donohue K (2009) Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci 106:11661–11666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239

    Article  CAS  PubMed  Google Scholar 

  • De Bodt S, Hollunder J, Nelissen H, Meulemeester N, Inzé D (2012) CORNET 2.0: integrating plant coexpression, protein-protein interactions, regulatory interactions, gene associations and functional annotations. New Phytol 195:707–720

    Article  PubMed  CAS  Google Scholar 

  • Di Mauro MF, Iglesias MJ, Arce DP, Valle EM, Arnold RB, Tsuda K, K-i Yamazaki, Casalongué CA, Godoy AV (2012) MBF1s regulate ABA-dependent germination of Arabidopsis seeds. Plant Signal Behav 7:188–192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ding ZJ, Yan JY, Li GX, Wu ZC, Zhang SQ, Zheng SJ (2014) WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J 79:810–823

    Article  CAS  PubMed  Google Scholar 

  • Feng C-Z, Chen Y, Wang C, Kong Y-H, Wu W-H, Chen Y-F (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80:654–668

    Article  CAS  PubMed  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5:765–771

    Article  Google Scholar 

  • Finkelstein RR (2010) The role of hormones during seed development and germination. In: Plant hormones. Springer, pp 549–573

  • Finkelstein R (2013) Abscisic acid synthesis and response. The Arabidopsis Book, p e0166

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  CAS  PubMed  Google Scholar 

  • Footitt S, Douterelo-Soler I, Clay H, Finch-Savage WE (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc Natl Acad Sci 108:20236–20241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frey A, Godin B, Bonnet M, Sotta B, Marion-Poll A (2004) Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta 218:958–964

    Article  CAS  PubMed  Google Scholar 

  • Fuchs S, Tischer SV, Wunschel C, Christmann A, Grill E (2014) Abscisic acid sensor RCAR7/PYL13, specific regulator of protein phosphatase coreceptors. Proc Natl Acad Sci 111:5741–5746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez L, Van Wuytswinkel O, Castelain M, Bellini C (2007) Combined networks regulating seed maturation. Trends Plant Sci 12:294–300

    Article  CAS  PubMed  Google Scholar 

  • Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Heß B, Macháčková I, Fischer U, Leubner-Metzger G (2007) 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.): a comparative study of fruits and seeds. J Exp Bot 58:3047–3060

    Article  CAS  PubMed  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Feng C-Z, Ye Q, Wu W-H, Chen Y-F (2016) Arabidopsis WRKY6 transcription factor acts as a positive regulator of abscisic acid signaling during seed germination and early seedling development. PLoS Genet 12:e1005833

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560

    Article  CAS  PubMed  Google Scholar 

  • Jiang S, Kumar S, Eu Y-J, Jami SK, Stasolla C, Hill RD (2012) The Arabidopsis mutant, fy-1, has an ABA-insensitive germination phenotype. J Exp Bot 63:2693–2703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T (2005a) Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol 46:300–311

    Article  CAS  PubMed  Google Scholar 

  • Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T (2005b) LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol 46:399–406

    Article  CAS  PubMed  Google Scholar 

  • Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M (2010) Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol 51:1988–2001

    Article  CAS  PubMed  Google Scholar 

  • Karssen CM, Brinkhorst-van der Swan DLC, Breekland AE, Koornneef M (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta 157:158–165

    Article  CAS  PubMed  Google Scholar 

  • Kendall SL, Hellwege A, Marriot P, Whalley C, Graham IA, Penfield S (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. Plant Cell 23:2568–2580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DH, Yamaguchi S, Lim S, Oh E, Park J, Hanada A, Kamiya Y, Choi G (2008) SOMNUS, a CCCH-type zinc finger protein in Arabidopsis, negatively regulates light-dependent seed germination downstream of PIL5. Plant Cell 20:1260–1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Hwang H, Hong J-W, Lee Y-N, Ahn IP, Yoon IS, Yoo S-D, Lee S, Lee SC, Kim B-G (2012) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63:1013–1024

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Y-h Cho, Ryu H, Kim Y, Kim T-H, Hwang I (2013a) BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis. Plant J 75:755–766

    Article  CAS  PubMed  Google Scholar 

  • Kim W, Lee Y, Park J, Lee N, Choi G (2013b) HONSU, a protein phosphatase 2C, regulates seed dormancy by inhibiting ABA signaling in Arabidopsis. Plant Cell Physiol 54:555–572

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh. Theor Appl Genet 61:385–393

    CAS  PubMed  Google Scholar 

  • Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plantarum 61:377–383

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee K, Seo PJ (2015) Coordination of seed dormancy and germination processes by MYB96. Plant Signal Behav 10:e1056423

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee KH, Piao HL, Kim H-Y, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee I-J, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120

    Article  CAS  PubMed  Google Scholar 

  • Lee KP, Piskurewicz U, Turečková V, Strnad M, Lopez-Molina L (2010) A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proc Natl Acad Sci 107:19108–19113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HG, Lee K, Seo PJ (2015a) The Arabidopsis MYB96 transcription factor plays a role in seed dormancy. Plant Mol Biol 87:371–381

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Lee HG, Yoon S, Kim HU, Seo PJ (2015b) The Arabidopsis MYB96 transcription factor is a positive regulator of ABSCISIC ACID-INSENSITIVE4 in the control of seed germination. Plant Physiol 168:677–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-Poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45:309–319

    Article  CAS  PubMed  Google Scholar 

  • Léon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JAD, Koornneef M (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661

    Article  PubMed  Google Scholar 

  • Levi M, Brusa P, Chiatante D, Sparvoli E (1993) Cell cycle reactivation in cultured pea embryo axes. Effect of abscisic acid. In Vitro Cell Develop Biol Plant 29:47–50

    Article  Google Scholar 

  • Lim S, Park J, Lee N, Jeong J, Toh S, Watanabe A, Kim J, Kang H, Kim DH, Kawakami N, Choi G (2013) ABA-INSENSITIVE3, ABA-INSENSITIVE5, and DELLAs interact to activate the expression of SOMNUS and other high-temperature-inducible genes in imbibed seeds in Arabidopsis. Plant Cell 25:4863–4878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linkies A, Müller K, Morris K, Turečková V, Wenk M, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, Leubner-Metzger G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linkies A, Graeber K, Knight C, Leubner-Metzger G (2010) The evolution of seeds. New Phytol 186:817–831

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Bergervoet JHW, Vos CHR, Hilhorst HWM, Kraak HL, Karssen CM, Bino RJ (1994) Nuclear replication activities during imbibition of abscisic acid- and gibberellin-deficient tomato (Lycopersicon esculentum Mill.) seeds. Planta 194:368–373

    Article  CAS  Google Scholar 

  • Liu Y, Fang J, Xu F, Chu J, Yan C, Schläppi MR, Wang Y, Chu C (2014) 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. J Genet Genom 41:327–338

    Article  CAS  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua N-H (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Mansfield SG, Briarty LG (1992) Cotyledon cell development in Arabidopsis thaliana during reserve deposition. Can J Bot 70:151–164

    Article  Google Scholar 

  • Martínez-Andújar C, Ordiz MI, Huang Z, Nonogaki M, Beachy RN, Nonogaki H (2011) Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proc Natl Acad Sci 108:17225–17229

    Article  PubMed  PubMed Central  Google Scholar 

  • Meurs C, Basra AS, Karssen CM, van Loon LC (1992) Role of abscisic acid in the induction of desiccation tolerance in developing seeds of Arabidopsis thaliana. Plant Physiol 98:1484–1493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci 106:5418–5423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M (2013) Structure and function of abscisic acid receptors. Trends Plant Sci 18:259–266

    Article  CAS  PubMed  Google Scholar 

  • Mönke G, Seifert M, Keilwagen J, Mohr M, Grosse I, Hähnel U, Junker A, Weisshaar B, Conrad U, Bäumlein H, Altschmied L (2012) Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res 40:8240–8254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709

    Article  CAS  PubMed  Google Scholar 

  • Nakamura S, Toyama T (2001) Isolation of a VP1 homologue from wheat and analysis of its expression in embryos of dormant and non-dormant cultivars. J Exp Bot 52:875–876

    Article  CAS  PubMed  Google Scholar 

  • 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 (2009) 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 Cell Physiol 50:1345–1363

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, Kamiya Y, Naito S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220:412–423

    Article  CAS  PubMed  Google Scholar 

  • Nasmyth K, Hunt T (1993) Cell cycle. Dams and sluices. Nature 366:634–635

    Article  CAS  PubMed  Google Scholar 

  • Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T (2007) ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J 50:935–949

    Article  CAS  PubMed  Google Scholar 

  • Nonogaki M, Sall K, Nambara E, Nonogaki H (2014) Amplification of ABA biosynthesis and signaling through a positive feedback mechanism in seeds. Plant J 78:527–539

    Article  CAS  PubMed  Google Scholar 

  • Oh E, Yamaguchi S, Kamiya Y, Bae G, Chung W-I, Choi G (2006) Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J 47:124–139

    Article  CAS  PubMed  Google Scholar 

  • Oh E, Yamaguchi S, Hu J, Yusuke J, Jung B, Paik I, Lee HS, Sun T, Kamiya Y, Choi G (2007) PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19:1192–1208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh E, Kang H, Yamaguchi S, Park J, Lee D, Kamiya Y, Choi G (2009) Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21:403–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-Hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka M, Endo TA, Mochizuki Y, Toyoda T, Kamiya Y, Shinozaki K, Nambara E, Seki M (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62:39–51

    Article  CAS  PubMed  Google Scholar 

  • Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, T-fF Chow, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins. Science 324:1068–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park J, Lee N, Kim W, Lim S, Choi G (2011) ABI3 and PIL5 collaboratively activate the expression of SOMNUS by directly binding to its promoter in imbibed Arabidopsis seeds. Plant Cell 23:1404–1415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penfield S, Josse E-M, Kannangara R, Gilday AD, Halliday KJ, Graham IA (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol 15:1998–2006

    Article  CAS  PubMed  Google Scholar 

  • Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20:2729–2745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preston J, Tatematsu K, Kanno Y, Hobo T, Kimura M, Jikumaru Y, Yano R, Kamiya Y, Nambara E (2009) Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant Cell Physiol 50:1786–1800

    Article  CAS  PubMed  Google Scholar 

  • Raz V, Bergervoet J, Koornneef M (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128:243–252

    CAS  PubMed  Google Scholar 

  • Robichaud CS, Wong J, Sussex IM (1979) Control of in vitro growth of viviparous embryo mutants of maize by abscisic acid. Dev Genet 1:325–330

    Article  Google Scholar 

  • Roscoe TT, Guilleminot J, Bessoule J-J, Berger F, Devic M (2015) Complementation of seed maturation phenotypes by ectopic expression of ABSCISIC ACID INSENSITIVE3, FUSCA3 and LEAFY COTYLEDON2 in Arabidopsis. Plant Cell Physiol 56:1215–1228

    Article  CAS  PubMed  Google Scholar 

  • Rueda-Romero P, Barrero-Sicilia C, Gómez-Cadenas A, Carbonero P, Oñate-Sánchez L (2012) Arabidopsis thaliana DOF6 negatively affects germination in non-after-ripened seeds and interacts with TCP14. J Exp Bot 63:1937–1949

    Article  CAS  PubMed  Google Scholar 

  • Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620

    Article  CAS  PubMed  Google Scholar 

  • Sasaki K, Kim M-H, Kanno Y, Seo M, Kamiya Y, Imai R (2015) Arabidopsis COLD SHOCK DOMAIN PROTEIN 2 influences ABA accumulation in seed and negatively regulates germination. Biochem Biophys Res Commun 456:380–384

    Article  CAS  PubMed  Google Scholar 

  • Schramm EC, Nelson SK, Kidwell KK, Steber CM (2012a) Increased ABA sensitivity results in higher seed dormancy in soft white spring wheat cultivar ‘Zak’. Theor Appl Genet 126:791–803

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schramm EC, Nelson SK, Steber CM (2012b) Wheat ABA-insensitive mutants result in reduced grain dormancy. Euphytica 188:35–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz SH, Qin X, Zeevaart JA (2003) Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol 131:1591–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69:463–472

    Article  CAS  PubMed  Google Scholar 

  • Shang Y, Yan L, Liu Z-Q, Cao Z, Mei C, Xin Q, Wu F-Q, Wang X-F, Du S-Y, Jiang T, Zhang X-F, Zhao R, Sun H-L, Liu R, Yu Y-T, Zhang D-P (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Y, Devic M, Lepiniec L, Zhou D-X (2015) Chromodomain, Helicase and DNA-binding CHD1 protein, CHR5, are involved in establishing active chromatin state of seed maturation genes. Plant Biotechnol J 13:811–820

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 9:1

    Article  CAS  Google Scholar 

  • Shu K, Chen Q, Wu Y, Liu R, Zhang H, Wang P, Li Y, Wang S, Tang S, Liu C, Yang W, Cao X, Serino G, Xie Q (2016) ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels. Plant J 85:348–361

    Article  CAS  PubMed  Google Scholar 

  • S-j Lee, Lee MH, Kim J-I, Kim SY (2015) Arabidopsis putative MAP kinase kinase kinases Raf10 and Raf11 are positive regulators of seed dormancy and ABA response. Plant Cell Physiol 56:84–97

    Article  CAS  Google Scholar 

  • Söderman EM, Brocard IM, Lynch TJ, Finkelstein RR (2000) Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiol 124:1752–1765

    Article  PubMed  PubMed Central  Google Scholar 

  • Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Shantharaj D, Kang X, Ni M (2010) Transcriptional and hormonal signaling control of Arabidopsis seed development. Curr Opin Plant Biol 13:611–620

    Article  CAS  PubMed  Google Scholar 

  • Tan B-C, Joseph LM, Deng W-T, Liu L, Li Q-B, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35:44–56

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Ji Q, Huang Y, Jiang Z, Bao M, Wang H, Lin R (2013) FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol 163:857–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18:1642–1651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant Cell Environ 32:1211–1229

    Article  PubMed  Google Scholar 

  • Vaistij FE, Gan Y, Penfield S, Gilday AD, Dave A, He Z, Josse E-M, Choi G, Halliday KJ, Graham IA (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proc Natl Acad Sci 110:10866–10871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Qi Q, Schorr P, Cutler Adrian J, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 15:501–510

    Article  PubMed  Google Scholar 

  • Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309

    Article  CAS  PubMed  Google Scholar 

  • Weng J-K, Ye M, Li B, Noel JP (2016) Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166:881–893

    Article  CAS  PubMed  Google Scholar 

  • West M, Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell 5:1361–1369

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu J, Seng S, Sui J, Vonapartis E, Luo X, Gong B, Liu C, Wu C, Liu C, Zhang F, He J, Yi M (2015) Gladiolus hybridus ABSCISIC ACID INSENSITIVE 5 (GhABI5) is an important transcription factor in ABA signaling that can enhance Gladiolus corm dormancy and Arabidopsis seed dormancy. Front Plant Sci 6:960

    PubMed  PubMed Central  Google Scholar 

  • Wu T, Yang C, Ding B, Feng Z, Wang Q, He J, Tong J, Xiao L, Jiang L, Wan J (2016) Microarray-based gene expression analysis of strong seed dormancy in rice cv. N22 and less dormant mutant derivatives. Plant Physiol Biochem 99:27–38

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu J-K (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress—and osmotic stress-responsive gene expression. Plant Cell 13:2063–2084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Z-Y, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun D-J, Hwang I (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, Li J, Gangappa SN, Hettiarachchi C, Lin F, Andersson MX, Jiang Y, Deng XW, Holm M (2014) Convergence of light and ABA signaling on the ABI5 promoter. PLoS Genet 10:e1004197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:367–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Yu X, Song L, An C (2011) ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol 156:873–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Zhang H, Cui P, Ding F, Wang G, Li R, Jenks MA, Lü S, Xiong L (2014) The putative E3 ubiquitin ligase ECERIFERUM9 regulates abscisic acid biosynthesis and response during seed germination and postgermination growth in Arabidopsis. Plant Physiol 165:1255–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng J, Chen F, Wang Z, Cao H, Li X, Deng X, Soppe WJJ, Li Y, Liu Y (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytol 193:605–616

    Article  CAS  PubMed  Google Scholar 

  • Zhou S-F, Sun L, Valdés AE, Engström P, Song Z-T, Lu S-J, Liu J-X (2015) Membrane-associated transcription factor peptidase, site-2 protease, antagonizes ABA signaling in Arabidopsis. New Phytol 208:188–197

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhong Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by N. Sreenivasulu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, A., Chen, Z. The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Rep 36, 689–703 (2017). https://doi.org/10.1007/s00299-016-2082-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-2082-z

Keywords

Navigation