Abstract
Bud dormancy in perennial plants adapts to environmental and seasonal changes. Bud dormancy is of ecological interest because it affects forest population growth characteristics and is of economical interest because it impacts wood production levels. To understand Pinus sylvestris L. var. mongolica litv. bud-dormancy and bud-burst mechanisms, we characterized the proteomes of their apical buds at the four critical stages that occur during the dormancy-to-growth transition. Ninety-six proteins with altered expression patterns were identified using NanoLC–ESI-MS/MS. The majority of these proteins (57%) are involved in metabolic and other cellular processes. For 28% of the proteins, a function could not be assigned. However, because their expression levels changed, they may be potential candidate bud development- or dormancy-related proteins. Of the 75 non-redundant bud proteins identified, ascorbate peroxidase, pathogenesis-related protein PR-10, and heat shock proteins dramatically increased during August and November, suggesting that they may involved in the initiation of bud dormancy. Conversely, S-adenosylmethionine synthetase, abscisic acid/stress-induced proteins, superoxide dismutase (SOD), caffeoyl-CoA O-methyltransferase, actin, and type IIIa membrane protein cp-wap13 had greater expression levels during April, suggesting that they may be involved in the initiation of bud dormancy-release. Cell division cycle protein 48 and eukaryotic initiation factors 4A-15 and 4A had greater expression levels during May, suggesting that they may regulate cell proliferate and differentiation in the shoot apical meristem. These observations provide insights into the molecular mechanisms that induce or break bud dormancy.
Similar content being viewed by others
References
Romberger JA (1963) Meristems, growth and development in woody plants: an analytical review of anatomical, physiological, and morphogenic aspects. US Dept Agric For Serv, Tech Bull 1239:1–214
Viémont J, Crabbé J (2000) Growth cycle and dormancy in plants. CABI, Belgium
Arora R, Rowland LJ, Tanino K (2003) Induction and release of bud dormancy in woody perennials: a science comes of age. HortScience 38:911–921
Frewen BE, Chen THH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845
Eriksson G, Ekberg I, Dormling I, Matérn B, Wettstein D (1978) Inheritance of bud-set and bud-flushing in Picea abies (L.) Karst. Theor Appl Genet 52:3–19
Chen THH, Howe GT, Bradshaw HD Jr (2002) Molecular genetic analysis of dormancy-related traits in poplars. Weed Sci 50:232–240
Howe GT, Saruul P, Davis J, Chen THH (2000) Quantitative genetics of bud phenology, frost damage, and winter survival in an F 2 family of hybrid poplars. Theor Appl Genet 101:632–642
Bradshaw HD Jr, Stettler RF (1995) Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics 139:963–973
Sylven N (1940) Longday and shortday types of Swedish forest trees. Medd Fören Växtförädling Skogsträd (English summary) Sv Papp Tidn 43:351–354
Nitsch JP (1957) Photoperiodism in woody plants. Proc Am Soc Hort Sci 70:526–544
Weiser CJ (1970) Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169:1269–1278
Kermode AR (2005) Role of abscisic acid in seed dormancy. J Plant Growth Regul 24:319–344
Rakwal R, Komatsu S (2005) Abscisic acid promoted changes in the protein profiles of rice seedling by proteome analysis. Mol Biol Rep 31:217–230
Karami O, Saidi A (2009) The molecular basis for stress-induced acquisition of somatic embryogenesis. Molecular Biology Reports doi:10.1007/s11033-11009-19764-11033
Senthil K, Wasnik NG, Kim YJ, Yang DC (2010) Generation and analysis of expressed sequence tags from leaf and root of Withania somnifera (Ashwgandha). Mol Biol Rep 37:893–902
Bohlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH,Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043
Rohde A, Prinsen E, De Rycke R, Engler G, Van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell 14:1885–1901
Ruonala R, Rinne PLH, Baghour M, Moritz T, Tuominen H, Kangasjarvi J (2006) Transitions in the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J 46:628–640
Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294
Simpson GG (2004) The autonomous pathway: epigenetic and post-transcriptional gene regulation in the control of Arabidopsis flowering time. Curr Opin Plant Biol 7:570–574
Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540
Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–210
Katz A, Oliva M, Mosquna A, Hakim O, Ohad N (2004) FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37:707–719
Torres Acosta JA, de Almeida Engler J, Raes J, Magyar Z, De Groodt R, Inze D, De Veylder L (2004) Molecular characterization of Arabidopsis PHO80-like proteins, a novel class of CDKA; 1-interacting cyclins. Cell Mol Life Sci 61:1485–1497
Liu Z, Yang X, Fu Y, Zhang Y, Yan J, Song T, Rocheford T, Li J (2009) Proteomic analysis of early germs with high-oil and normal inbred lines in maize. Mol Biol Rep 36:813–821
Zhu H, Bi YD, Yu LJ, Guo DD, Wang BC (2009) Comparative proteomic analysis of apomictic monosomic addition line of Beta corolliflora and Beta vulgaris L. in sugar beet. Mol Biol Rep 36:2093–2098
Feng JR, Chen XS, Yuan ZH, Zhang LJ, Ci ZJ, Liu XL, Zhang CY (2009) Primary molecular features of self-incompatible and self-compatible F1 seedling from apricot (Prunus armeniaca L.) Katy× Xinshiji. Mol Biol Rep 36:263–272
Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2002) Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 129:823–837
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
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Lee CS, Chien CT, Lin CH, Chiu YY, Yang YS (2006) Protein changes between dormant and dormancy-broken seeds of Prunus campanulata Maxim. Proteomics 6:4147–4154
Jun Z, Zhang KH, Hui TAN, Ling XUM, Jun W (2005) Natural regeneration characteristics of Pinus sylvestris var. mongolica forests on sandy land in Honghuaerji, China. J For Res 16:253–259
Wang BC, Pan YH, Meng DZ, Zhu YX (2006) Identification and quantitative analysis of significantly accumulated proteins during the Arabidopsis seedling de-etiolation process. J Integr Plant Biol 48:104–113
Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68:850–858
Samish RM (1954) Dormancy in woody plants. Annu Rev Plant Physiol 5:183–204
Kainer KA, Duryea ML, White TL, Johnson JD (1991) Slash pine bud dormancy as affected by lifting date and root wrenching in the nursery. Tree Physiol 9:479–489
Rison SCG, Hodgman TC, Thornton JM (2000) Comparison of functional annotation schemes for genomes. Funct Integr Genomics 1:56–69
Lange BM, Ghassemian M (2005) Comprehensive post-genomic data analysis approaches integrating biochemical pathway maps. Phytochemistry 66:413–451
Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390
Peyret P, Perez P, Alric M (1995) Structure, genomic organization, and expression of the Arabidopsis thaliana aconitase gene. J Biol Chem 270:8131–8137
Comai L, Dietrich RA, Maslyar DJ, Baden CS, Harada JJ (1989) Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L. Plant Cell Online 1:293–300
Turley RB, Trelease RN (1990) Development and regulation of three glyoxysomal enzymes during cotton seed maturation and growth. Plant Mol Biol 14:137–146
Gallardo K, Job C, Groot SPC, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848
Cheng L, Fuchigami LH (2002) Growth of young apple trees in relation to reserve nitrogen and carbohydrates. Tree Physiol 22:1297–1303
Bryan JK, Miflin BJ, Lea PJ (1991) The biochemistry of plants. A comprehensive treatise. Amino acids and derivatives. Academic Press, New York
Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004) Current understanding of the regulation of methionine biosynthesis in plants. J Exp Bot 55:1799–1808
Szegő D, Kósa E, Horváth E (2007) Role of S-methylmethionine in the plant metabolism. Acta Agron Hung 55:491–508
Mijnsbrugge KV, Meyermans H, Van Montagu M, Bauw G, Boerjan W (2000) Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210:589–598
Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M (2005) Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation 1 [w]. Plant Physiol 137:949–960
Suarez MF, Avila C, Gallardo F, Canton FR, Garcia-Gutierrez A, Claros MG,Canovas FM (2002) Molecular and enzymatic analysis of ammonium assimilation in woody plants. Soc Experiment Biol 53:891–904
Cánovas FM, Avila C, Cantón FR, Cañas RA, Fdl Torre (2007) Ammonium assimilation and amino acid metabolism in conifers. J Exp Bot 58:2307–2318
Canton FR, Suarez MF, Canovas FM (2005) Molecular aspects of nitrogen mobilization and recycling in trees. Photosynth Res 83:265–278
Wareing PF, Saunders PF (1971) Hormones and dormancy. Annu Rev Plant Physiol 22:261–288
De Smet I, Zhang H, Inz D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439
Tanino KK (2004) Hormones and endodormancy induction in woody plants. J Crop Improv 10:157–199
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223
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
Oracz K, Bouteau HEM, Farrant JM, 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
Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Am Soc Plant Biol 129:460–468
Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364
Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plant 113:158–164
Wang SY, Jiao HJ, Faust M (1991) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiol Plant 82:231–236
Wang SY, Faust M (1994) Changes in the antioxidant system associated with budbreak in ‘Anna’ apple (Malus domestica Borkh.) buds. J Am Soc Hortic Sci 119:735–741
Pérez FJ, Lira W (2005) Possible role of catalase in post-dormancy bud break in grapevines. J Plant Physiol 162:301–308
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Hon WC, Griffith M, Mlynarz A, Kwok YC, Yang DSC (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Am Soc Plant Biol 109:879–889
Gaudet DA, Laroche A, Frick M, Davoren J, Puchalski B, Ergon (2000) Expression of plant defence-related (PR-protein) transcripts during hardening and dehardening of winter wheat. Physiol Mol Plant Pathol 57:15–24
Yu X, Ekramoddoullah AKM, Misra S (2000) Characterization of Pin m III cDNA in western white pine. Tree Physiol 20:663–671
Liu JJ, Ekramoddoullah AKM, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119:544–553
Feiler HS, Desprez T, Santoni V, Kronenberger J, Caboche M, Traas J (1995) The higher plant Arabidopsis thaliana encodes a functional CDC48 homologue which is highly expressed in dividing and expanding cells. EMBO J 14:5626
Rancour DM, Dickey CE, Park S, Bednarek SY (2002) Characterization of AtCDC48. Evidence for multiple membrane fusion mechanisms at the plane of cell division in plants. Plant Physiol 130:1241–1253
Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163
Chen T, Wu X, Chen Y, Li X, Huang M, Zheng M, Baluska F, Samaj J, Lin J (2009) Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth. Plant Physiol 149:1111–1126
Acknowledgements
We are grateful for financial support from the National Natural Sciences Foundation of China (Grant 30972330); Key project of Science and technology of Ministry of Education of the people’s republic of China (Grant 108048) and Natural sciences Foundation of Heilongjiang province (Grant C200930).
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bi, YD., Wei, ZG., Shen, Z. et al. Comparative temporal analyses of the Pinus sylvestris L. var. mongolica litv. apical bud proteome from dormancy to growth. Mol Biol Rep 38, 721–729 (2011). https://doi.org/10.1007/s11033-010-0159-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-010-0159-2