Abstract
Abscisic acid (ABA) and sugars have been well established to be crucial factors controlling seed germination of Arabidopsis. Here we demonstrate that AtMKK1 and AtMPK6 are both critical signals involved in ABA and sugar-regulated seed germination. Wild type plants depended on stratification and after-ripening for seed germination, whereas this dependence on either stratification or after-ripening was not required for mutants of mkk1 and mpk6 as well as their double mutant mkk1 mpk6. While seed germination of wild type plants was sensitively inhibited by ABA and glucose, mkk1, mpk6 and mkk1 mpk6 were all strongly resistant to ABA or glucose treatments, and in contrast, plants overexpressing MKK1 or MPK6 were super-sensitive to ABA and glucose. Glucose treatment significantly induced increases in MKK1 and MPK6 activities. These results clearly indicate that MKK1 and MPK6 are involved in the ABA and sugar signaling in the process of seed germination. Further experiments showed that glucose was capable of inducing ABA biosynthesis by up-regulating NCED3 and ABA2, and furthermore, this up-regulation of NCED3 and ABA2 was arrested in the mkk1 mpk6 double mutant, indicating that the inhibition of seed germination by glucose is potentially resulted from sugar-induced up-regulation of the ABA level.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H et al (2003) Genome-wide insertional mutagensis of Arabidopsis thaliana. Science 301:653–657. doi:10.1126/science.1086391
Apel K, Hirt H (2004) Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genet Dev 14:2085–2096
Assmann SM (2003) OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells. Trends Plant Sci 8:151–153. doi:10.1016/S1360-1385(03)00052-9
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066. doi:10.1105/tpc.9.7.1055
Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the ear of the Arabidopsis genome. Plant Cell Environ 25:153–161. doi:10.1046/j.1365-3040.2002.00746.x
Chen JG, Jones AM (2004) AtRGS1 function in Arabidopsis thaliana. Methods Enzymol 389:338–350. doi:10.1016/S0076-6879(04)89020-7
Chen JG, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, Jones AM (2004) GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 135:907–915. doi:10.1104/pp.104.038992
Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743. doi:10.1105/tpc.006494
Chow B, McCourt P (2004) Hormone signaling from a developmental context. J Exp Bot 55:247–251. doi:10.1093/jxb/erh032
Coruzzi GM, Zhou L (2001) Carbon and nitrogen sensing and signaling in plants: emerging ‘matrix effects’. Curr Opin Plant Biol 4:247–253. doi:10.1016/S1369-5266(00)00168-0
Dekkers BJ, Schuurmans JA, Smeekens SC (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218:579–588. doi:10.1007/s00425-003-1154-9
Ephritikhine G, Fellner M, Vannini C, Lapous D, Barbier-Brygoo H (1999) The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid. Plant J 18:303–314. doi:10.1046/j.1365-313X.1999.00454.x
Finkelestein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45
Finkelstein RR, Gibson SI (2002) ABA and sugar interaction regulating development. Cross-talk or voices in a crowd? Curr Opin Plant Biol 5:26–32. doi:10.1016/S1369-5266(01)00225-4
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609
Finkelstein RR, Somerville CR (1990) Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol 94:1172–1179. doi:10.1104/pp.94.3.1172
Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054
Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494. doi:10.1105/tpc.106.048538
Gazzarrini S, McCourt P (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr Opin Plant Biol 4:387–391. doi:10.1016/S1369-5266(00)00190-4
Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102. doi:10.1016/j.pbi.2004.11.003
Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261
Hendricks SB, Taylorson RB (1975) Breaking of seed dormancy by catalase inhibition. Proc Natl Acad Sci USA 72:306–309. doi:10.1073/pnas.72.1.306
Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479. doi:10.1016/S1369-5266(03)00090-6
Hirt H (1997) Multiple roles of MAP kinase in plant signal transduction. Trends Plant Sci 2:11–15. doi:10.1016/S1360-1385(96)10048-0
Hirt H, Asard H (2000) An international conference with a high ambition: meeting report. Trends Plant Sci 5:3–4. doi:10.1016/S1360-1385(99)01508-3
Huang YD, Li CY, Biddle KD, Gibson SI (2008) Identification, cloning and characterization of sis7 and sis10 sugar-insensitive mutants of Arabidopsis. BMC Plant Biol 8:1–24. doi:10.1186/1471-2229-8-104
Huijser C, Kortstee A, Pego J, Weisbeek P, Wisman E, Smeekens S (2000) The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses. Plant J 23:577–585. doi:10.1046/j.1365-313x.2000.00822.x
Koornneef M, Reuling G, Karssen CM (1984) The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61:377–383. doi:10.1111/j.1399-3054.1984.tb06343.x
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36. doi:10.1016/S1369-5266(01)00219-9
Kuhn JM, Schroeder JI (2003) Impacts of altered RNA metabolism on abscisic acid signaling. Curr Opin Plant Biol 6:463–469. doi:10.1016/S1369-5266(03)00084-0
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633. doi:10.1093/emboj/cdg277
Laby RJ, Kincaid MS, Kim D, Gibson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis 5 are defective in abscisic acid synthesis and response. Plant J 23:587–596. doi:10.1046/j.1365-313x.2000.00833.x
Laloi C, Apel K, Danon A (2004) Reactive oxygen signaling: the latest news. Curr Opin Plant Biol 7:323–328. doi:10.1016/j.pbi.2004.03.005
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. doi:10.1111/j.1365-313X.2005.02622.x
Leon P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116. doi:10.1016/S1360-1385(03)00011-6
Ligterink W, Kroj T, zur Nieden U, Hirt H, Scheel D (1997) Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276:2054–2057. doi:10.1126/science.276.5321.2054
Lopez-Molina L, Mongrand S, Chua NH (2001) A post germination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98:4782–4787. doi:10.1073/pnas.081594298
Lu C, Han MH, Guevara-Garcia A, Fedoroff NV (2002) Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci USA 99:15812–15817. doi:10.1073/pnas.242607499
Mizoguchi T, Ichimura K, Shinozaki K (1997) Environmental stress response in plants: the role of mitogen-activated protein kinases. Trends Biotechnol 15:15–19. doi:10.1016/S0167-7799(96)10074-3
Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10:339–346. doi:10.1016/j.tplants.2005.05.009
Nambara E, Marion-Poll A (2003) ABA action and interactions in seeds. Trends Plant Sci 8:213–217. doi:10.1016/S1360-1385(03)00060-8
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. doi:10.1111/j.1365-313X.2007.03107.x
Ooms J, Leon-Kloosterziel KM, Bartels D, Koornneef M, Karssen CM (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana. A comparative study using abscisic acid-insensitive abi3 mutants. Plant Physiol 102:1185–1191
Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programes during Arabidopsis seed development. Roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582
Price J, Li TC, Kang SG, Na JK, Jang JC (2003) Mechanisms of glucose signaling during germination of Arabidopsis. Plant Physiol 132:1424–1438. doi:10.1104/pp.103.020347
Qin X, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana lumbaginifolia increases absisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551. doi:10.1104/pp.010663
Quarrie SA, Whitford PN, Appleford NEJ, Wang TL, Cook SK, Henson IE, Loveys BR (1988) A monoclonal antibody to (S)-abscisic acid: its characterization and use in a radioimmunoassay for measuring abscisic acid in crude extracts of cereal and lupin leaves. Planta 173:330–339. doi:10.1007/BF00401020
Rolland F, Winderickx J, Thevelein JM (2001) Glucose-sensing mechanisms in eukaryotic cells. Trends Biochem Sci 26:310–317. doi:10.1016/S0968-0004(01)01805-9
Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709. doi:10.1146/annurev.arplant.57.032905.105441
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330. doi:10.1038/35066500
Seo M, Hanada A, Kuwahara A, Endo A, Okamoto M, Yamauchi Y, North H, Marion-Poll A, Sun TP, Koshiba T et al (2006) Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J 48:354–366. doi:10.1111/j.1365-313X.2006.02881.x
Sheen J, Zhou L, Jan JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418. doi:10.1016/S1369-5266(99)00014-X
Smeekens S (2000) Sugar-induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol 51:49–81. doi:10.1146/annurev.arplant.51.1.49
Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB (2000) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23:363–374. doi:10.1046/j.1365-313x.2000.00789.x
Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Hanada A, Aso Y, Ishiyama K, Tamura N et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385. doi:10.1104/pp.107.113738
Ullah H, Chen JG, Wang S, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129:897–907. doi:10.1104/pp.005017
Xing Y, Jia WS, Zhang JH (2007) AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J Exp Bot 58:2969–2981. doi:10.1093/jxb/erm144
Xing Y, Jia WS, Zhang JH (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451. doi:10.1111/j.1365-313X.2008.03433.x
Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36. doi:10.1104/pp.103.025395
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. doi:10.1146/annurev.arplant.57.032905.105444
Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T (2006) ABA-Hypersensitive Germination3 Encodes a Protein Phosphatase 2C (AtPP2CA) That Strongly Regulates Abscisic Acid Signaling during Germination among Arabidopsis Protein Phosphatase 2Cs. Plant Physiol 140:115–126. doi:10.1104/pp.105.070128
Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci USA 95:10294–10299. doi:10.1073/pnas.95.17.10294
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. doi:10.1146/annurev.arplant.53.091401.143329
Acknowledgments
We are grateful to grants support from Hong Kong University Grants Committee (AoE/B-07/99), Hong Kong Research Grants Council (HKBU262708) and Hong Kong Baptist University Matching Research Fund. Wensuo Jia is grateful to grants support from the Ph.D. Programs Foundation of Ministry of Education of China (200800190019) and the High-Tech Research and Development (863) Program of China (2006AA100202).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xing, Y., Jia, W. & Zhang, J. AtMKK1 and AtMPK6 are involved in abscisic acid and sugar signaling in Arabidopsis seed germination. Plant Mol Biol 70, 725–736 (2009). https://doi.org/10.1007/s11103-009-9503-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-009-9503-0