Abstract
In forest broadleaves from the temperate zone, a large number of species exhibit seed dormancy phenomena. Tree seeds show some of the most pronounced and complicated forms of dormancy in the plant kingdom. Many seeds are deeply physiologically dormant whatever their moisture level and age. However, dormancy can usually be overcome by a cold or warm stratification for several months. The transition from seed dormancy to germination is a multi-step process. In combination with the availability of genome sequence data, proteomics has opened up enormous possibilities for identifying the total set of expressed proteins as well as expression changes during dormancy breaking. The proteomic approach used for analysis of dormancy breaking of tree seeds offers new data allowing better understanding of the mechanism of deep physiological dormancy. The results of proteomic studies on dormancy breaking and the presence of abscisic and gibberellic acids in tree seeds (beech Fagus sylvatica L., Norway maple Acer platanoides L. and sycamore Acer pseudoplatanus L.), help to explain this process better. Most of the changes in protein expression were observed at the end of stratification and in the germinated seeds. This is the most active period of dormancy breaking when seeds pass from the quiescent state to germination. The analysis of the proteins’ function showed that the mechanism of seed dormancy breaking involves many processes. Energy metabolism, proteasome, transcription, protein synthesis, signal transduction and methionine metabolism proteins have a special importance.
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References
Alkhalfioui F, Renard M, Vensel W, Wong J, Tanaka C, Hurkman W, Buchanan B, Montrichard F (2007) Thioredoxin-linked proteins are reduced during germination of Medicago truncatula seeds. Plant Physiol 144:1559–1579
Auld KL, Silver PA (2006) Transcriptional regulation by the proteasome as a mechanism for cellular protein homeostasis. Cell Cycle 5:1503–1505
Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107
Bais H, Ravishankar G (2002) Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell Tissue Organ Cult 69:1–34
Baskin J, Baskin C (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16
Baumbusch LO, Hughes DW, Galau GA, Jakobsen KS (2004) LEC1, FUS3, ABI3 and Em expression reveals no correlation with dormancy in Arabidopsis. J Exp Bot 55:77–87
Black M, Bewley JD, Halmer P (2008) The encyclopedia of seeds. Science technology and uses. CABI, Wallingford
Cadman C, Toorop P, Hilhorst H, Finch-Savage W (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J 46:805–822
Calvo ES, Rodermel SR, Shoemaker RC (1994) A third highly conserved group 1 Lea gene from Arabidopsis thaliana L. Plant Physiol 106:787–788
Calvo A, Nicolas C, Nicolas G, Rodriguez D (2004) Evidence of a cross-talk regulation of a GA 20-oxidase (FsGA20ox1) by gibberellins and ethylene during the breaking of dormancy in Fagus sylvatica seeds. Physiol Plant 120:623–630
Chibani K, Ali-Rachedi S, Job C, Job D, Jullien M, Grappin P (2006) Proteomic analysis of seed dormancy in Arabidopsis. Plant Physiol 142:1493–1510
Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E (2006) Integration of abscisic acid signalling into plant responses. Plant Biol 8:314–325
Delseny M, Bies-Etheve N, Carles C, Hull G, Vicient C, Raynal M, Grellet F, Aspart L (2001) Late embryogenesis abundant (LEA) protein gene regulation during Arabidopsis seed maturation. J Plant Physiol 158:419–427
Faivre-Nitschke SE, Couée I, Vermel M, Grienenberger JM, Gualberto JM (2001) Purification, characterization and cloning of isovaleryl-CoA dehydrogenase from higher plant mitochondria. Eur J Bioch/FEBS 268:1332–1339
Finch-Savage W, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Finch-Savage W, Cadman C, Toorop P, Lynn J, Hilhorst H (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J 51:60–78
Gallardo K, Job C, Groot S, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848
Gallardo K, Job C, Groot S, Puype M, Demol H, Vandekerckhove J, Job D (2002a) Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 129:823–837
Gallardo K, Job C, Groot S, Puype M, Demol H, Vandekerckhove J, Job D (2002b) Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiol Plant 116:238–247
Gallardo K, Firnhaber C, Zuber H, Hericher D, Belghazi M, Henry C, Kuster H, Thompson R (2007) A combined proteome and transcriptome analysis of developing Medicago truncatula seeds: evidence for metabolic specialization of maternal and filial tissues. Mol Cell Proteomics 6:2165–2179
Gazzarrini S, McCourt P (2003) Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann Botany 91:605–612
Hallet BP, Bewley JD (2002) Membranes and seed dormancy: beyond the anaesthic hypothesis. Seed Sci Res 8:77–90
Han B, Hughes DW, Galau GA, Bewley JD, Kermode AR (1997) Changes in late-embryogenesis-abundant (LEA) messenger RNAs and dehydrins during maturation and premature drying of Ricinus communis L. seeds. Planta 201:27–35
Haslekås C, Viken MK, Grini PE, Nygaard V, Nordgard SH, Meza TJ, Aalen RB (2003) Seed 1-cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress. Plant Physiol 133:1148–1157
Hong TD, Ellis RH (1990) A comparison of maturation drying, germination, and desiccation tolerance between developing seeds of Acer pseudoplatanus L. and Acer platanoides L. New Phytol 116:589–596
Isola M, Franzoni L (2000) Changes of aspartate aminotransferase activity, its isoform pattern, and free amino acids content in peanut cotyledons during seed germination. Acta Physiologiae Plantarum 22:125–128
Jones HD, Kurup S, Peters NC, Holdsworth MJ (2000) Identification and analysis of proteins that interact with the Avena fatua homologue of the maize transcription factor VIVIPAROUS 1. Plant J 21:133–142
Kim S, Kang S, Wang W, Kim S, Hwang D, Kang K (2008) Analysis of embryonic proteome modulation by GA and ABA from germinating rice seeds. Proteomics 8:3577–3587
Krawiarz K, Szczotka Z (2000) Activity of ATPases during dormancy breaking in Norway maple (Acer platanoides L.) seeds. Acta Soc Bot Pol 69:119–121
Krawiarz K, Szczotka Z (2005) Adenine nucleotides and energy charge during dormancy breaking in embryo axes of Acer platanoides and Fagus sylvatica seeds. Acta Physiol Plant 27:455–461
Kucera B, Cohn M, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sc Res 15:281–307
Kurup S, Jones HD, Holdsworth MJ (2000) Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds. Plant J 21:143–155
Lee C, Chien C, Lin C, Chiu Y, Yang Y (2006) Protein changes between dormant and dormancy-broken seeds of Prunus campanulata Maxim. Proteomics 6:4147–4154
Leon R, Bassham D, Owen M (2007) Thermal and hormonal regulation of the dormancy-germination transition in Amaranthus tuberculatus seeds. Weed Res 47:335–344
Leon-Lobos P, Ellis R (2002) Seed storage behaviour of Fagus sylvatica and Fagus crenata. Seed Sci Res 12:31–37
Li B, Foley ME (1995) Cloning and characterization of differentially expressed genes in imbibed dormant and afterripened Avena fatua embryos. Plant Mol Biol 29:823–831
Lorenzo O, Nicolas C, Nicolas G, Rodriguez D (2002) Molecular cloning of a functional protein phosphatase 2C (FsPP2C2) with unusual features and synergistically up-regulated by ABA and calcium in dormant seeds of Fagus sylvatica. Physiol Plant 114:482–490
Matilla A (2000) Ethylene in seed formation and germination. Seed Sci Res 10:111–126
Morelli JK, Shewmaker CK, Vayda ME (1994) Biphasic stimulation of translational activity correlates with induction of translation Elongation Factor 1 subunit [alpha] upon wounding in potato tubers. Plant Physiol 106:897–903
Mortensen L, Eriksen E (2004) The effect of gibberellic acid, paclobutrazol and ethephon on the germination of Fagus sylvatica and Picea sitchensis seeds exposed to varying durations of moist chilling. Seed Sci Tech 32:21–33
Mortensen LC, Rodríguez D, Nicolás G, Eriksen EN, Nicolás C (2004) Decline in a seed-specific abscisic acid-responsive glycine-rich protein (GRPF1) mRNA may reflect the release of seed dormancy in Fagus sylvatica during moist prechilling. Seed Sci Res 14:27–34
Nagao M, Parimoo B, Tanaka K (1993) Developmental, nutritional, and hormonal regulation of tissue-specific expression of the genes encoding various acyl-CoA dehydrogenases and alpha-subunit of electron transfer flavoprotein in rat. J Biol Chem 268:24114–24124
Nicolás C, Rodríguez D, Poulsen F, Eriksen EN, Nicolás G (1997) The expression of an abscisic acid-responsive glycine-rich protein coincides with the level of seed dormancy in Fagus sylvatica. Plant Cell Physiol 38:1303–1310
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Olszewski N, Sun T, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80
Oracz K, Bouteau H, Farrant J, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50:452–465
Østergaard H, Rasmussen S, Roberts T, Hejgaard J (2000) Inhibitory serpins from wheat grain with reactive centers resembling glutamine-rich repeats of prolamin storage proteins—cloning and characterization of five major molecular forms. J Biol Chem 275:33272–33279
Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582
Park S, Rancour D, Bednarek S (2008) In planta analysis of the cell cycle-dependent localization of AtCDC48A and its critical roles in cell division, expansion, and differentiation. Plant Physiol 148:246–258
Pawłowski TA (2007) Proteomics of European beech (Fagus sylvatica L.) seed dormancy breaking: Influence of abscisic and gibberellic acids. Proteomics 7:2246–2257
Pawłowski TA (2009) Proteome analysis of Norway maple (Acer platanoides L.) seeds dormancy breaking and germination: influence of abscisic and gibberellic acids. BMC Plant Biol 9:48
Pawłowski T, Szczotka Z (1997) Qualitative changes in protein content during cold and warm stratification of Norway maple (Acer platanoides L.) seeds. Seed Sci Res 7:385–390
Pawłowski TA, Bergervoet J, Bino R, Groot S (2004) Cell cycle activity and β-tubulin accumulation during dormancy breaking of Acer platanoides L. seeds. Biologia Plant 48:211–218
Penfield S, Hall A (2009) A role for multiple circadian clock genes in the response to signals that break seed dormancy in Arabidopsis. Plant Cell. doi: 10.1105/tpc.108.064022
Penfield S, Josse E, Kannangara R, Gilday A, Halliday K, Graham I (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol 15:1998–2006
Penfield S, Gilday A, Halliday K, Graham I (2006) DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy. Curr Biol 16:2366–2370
Pinfield NJ, Stutchbury PA, Bazaid SA, Gwarazimba VE (1990) Abscisic acid and the regulation of embryo dormancy in the genus Acer. Tree Physiol 6:79–85
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
Piskurewicz U, Turečková V, Lacombe E, Lopez-Molina L (2009) Far-red light inhibits germination through DELLA-dependent stimulation of ABA synthesis and ABI3 activity. The EMBO J. doi: 10.1038/emboj.2009.170
Pukacka S (1983) Phospholipid changes and loss of viability in Norway maple (Acer platanoides L.) seeds. Zeitschrift fiir Pflanzenphysiologie 112:199–205
Pukacka S, Czubak A (1998) The effect of desiccation on viability and membrane lipid composition of Acer pseudoplatanus seeds. Acta Soc Bot Pol 67:249–252
Pukacka S, Ratajczak E (2005) Production and scavenging of reactive oxygen species in Fagus sylvatica seeds during storage at varied temperature and humidity. J Plant Physiol 162:873–885
Pukacka S, Ratajczak E (2007) Ascorbate and glutathione metabolism during development and desiccation of orthodox and recalcitrant seeds of the genus Acer. Funct Plant Biol 34:601–613
Ravanel S, Gakiere B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Nat Acad Sci USA 95:7805–7812
Rocha PSCF, Sheikh M, Melchiorre R, Fagard M, Boutet S, Loach R, Moffatt B, Wagner C, Vaucheret H, Furner I (2005) The Arabidopsis HOMOLOGY-DEPENDENT GENE SILENCING1 gene codes for an S-adenosyl-L-homocysteine hydrolase required for DNA methylation-dependent gene silencing. Plant Cell 17:404–417
Satoh S, Esashi Y (1979) Protein synthesis in dormant and non-dormant cocklebur seed segments. Physiol Plant 47:229–234
Schaller A (2004) A cut above the rest: the regulatory function of plant proteases. Planta 220:183–197
Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69:463–472
Shen S, Sharma A, Komatsu S (2003) Characterization of proteins responsive to gibberellin in the leaf-sheath of rice (Oryza sativa L.) seedling using proteome analysis. Biol Pharm Bull 26:129–136
Smalle J, Kurepa J, Yang P, Emborg TJ, Babiychuk E, Kushnir S, Vierstra RD (2003) The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15:965–980
Steffens B, Wang J, Sauter M (2006) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604–612
Stephen J, Dent K, Finch-Savage W (2003) A cDNA encoding a cold-induced glycine-rich RNA binding protein from Prunus avium expressed in embryonic axes. Gene 320:177–183
Stephen J, Dent K, Finch-Savage W (2004) Molecular responses of Prunus avium (wild cherry) embryonic axes to temperatures affecting dormancy. New Phytol 161:401–413
Suszka B, Muller C, Bonnet-Masimbert M (1996) Seeds of forest broadleaves. From harvest to sowing. INRA, Paris
Szczotka Z, Lewandowska U, Jakubowski H (1988) Endogenous and exogenous polyamines in dormancy breaking of Acer platanoides seeds under condition of cold stratification. Acta Physiol Plant 10:181–189
Szczotka Z, Pawłowski T, Krawiarz K (2003) Proteins and polyamines during dormancy breaking of European beech (Fagus sylvatica L.) seeds. Acta Physiol Plant 25:423–435
Thompson J, Hopkins M, Taylor C, Wang T (2004) Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci 9:174–179
Twardowski T, Szczotka Z (1989) The influence of selected polyamines on elongation binding factor 1 activity during the stratification of Norway maple seeds. J Plant Physiol 134:32–36
Vashisht AA, Pradhan A, Tuteja R, Tuteja N (2005) Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J 44:76–87
Wehmeyer N, Vierling E (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol 122:1099–1108
Wong P, Abubakar S (2005) Post-germination changes in Hevea brasiliensis seeds proteome. Plant Sci 169:303–311
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
Yang P, Li X, Wang X, Chen H, Chen F, Shen S (2007) Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 7:3358–3368
Zegzouti H, Jones B, Marty C, Lelievre J, Latche A, Pech J, Bouzayen M (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA-like protein: characterization and expression in response to drought, ABA and wounding. Plant Mol Biol 35:847–854
Zhang H, Sreenivasulu N, Weschke W, Stein N, Rudd S, Radchuk V, Potokina E, Scholz U, Schweizer P, Zierold U, Langridge P, Varshney RK, Wobus U, Graner A (2004) Large-scale analysis of the barley transcriptome based on expressed sequence tags. Plant J 40:276–290
Acknowledgments
The author wishes to thank Zofia Szczotka, Marzenna Guzicka and Kazimierz Krawiarz for their advice and helpful discussions. The work was supported by the Ministry of Science and Higher Education, Poland, grant number: N N309 2491 33.
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Pawłowski, T.A. Proteomic approach to analyze dormancy breaking of tree seeds. Plant Mol Biol 73, 15–25 (2010). https://doi.org/10.1007/s11103-010-9623-6
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DOI: https://doi.org/10.1007/s11103-010-9623-6