Poplar stems show opposite epigenetic patterns during winter dormancy and vegetative growth
Tóm tắt
In this study the identification of epigenetic marks of closed and open chromatin states has been performed by immunofluorescence in vibratome-thick sections from poplar stems, followed by quantification of the signal in a representative population of individual nuclei on a confocal microscope. Unlike other methods often used for detection of global DNA methylation levels, the procedure hereby proposed can be applied to a wide range of specimens regardless of the purity and yield of genomic DNA extraction and in a tissue-dependent manner. Using antibodies to 5-methylcytidine and acetylated lysine 8 of histone H4, as reliable indicators of transcription incompatible and compatible chromatin states, respectively, the influence of epigenetic regulation on differential gene expression during the growth and arrest periods in xylem and phloem tissues was assessed. The fluorescence signal of 5-methylcytosine was significantly higher in winter as compared with summer. Conversely, the fluorescence signal for acetylated Lys 8 of histone H4 was significantly higher in summer than in winter in both tissues examined. Collectively, these results put forward an epigenetic control of winter dormancy in poplar stems.
Tài liệu tham khảo
Allona I, Ramos A, Ibañez C, Contreras A, Casado R, Aragoncillo C (2008) Review: molecular control of winter dormancy establishment in trees. Span J Agric Res 6(special issue):201–210
Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559
Barány I, Fadón B, Risueño MC, Testillano PS (2010) Cell wall components and pectin esterification levels as markers of proliferation and differentiation events during pollen development and pollen embryogenesis in Capsicum annuum L. J Exp Bot 61(4):1159–1175
Battey NH (2000) Aspects of seasonality. J Exp Bot 51:1769–1780
Berdasco M, Alcázar R, García-Ortiz MV, Ballestar E, Fernández AF, Roldán-Arjona T, Tiburcio AF, Altabella T, Buisine N, Quesneville H, Baudry A, Lepiniec L, Alaminos M, Rodríguez R, Lloyd A, Colot V, Bender J, Canal MJ, Esteller M, Fraga MF (2008) Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells. PLoS One 3:e3306
Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol 147:263–279
Böhlenius 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
Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510
Feil R, Fraga MF (2012) Epigenetics and the environment: emerging patterns and implications. Nat Rev 13:97–109
Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA Methylation in Plants. Ann Rev Plant Physiol Plant Mol Biol 49:223–247
Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Genet Dev 10:217–223
Fraga MF, Uriol E, Borja Diego L, Berdasco M, Esteller M, Canal MJ, Rodriguez R (2002) High-performance capillary electrophoretic method for the quantification of 5-methyl 2′-deoxycytidine in genomic DNA: application to plant, animal and human cancer tissues. Electrophoresis 23:1677–1681
Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102:10604–10609
Gónzalez-Melendi P, Ramírez C, Testillano PS, Kumlehn J, Risueño MC (2005) Three dimensional confocal and electron microscopy imaging define the dynamics and mechanisms of diploidisation at early stages of barley microspore-derived embryogenesis. Planta 222:47–57
Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19
Heide OM, Prestrud AK (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114
Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540
Horvath DP, Sung S, Kim D, Chao W, Anderson J (2010) Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Mol Biol 73:169–179
Ibáñez C, Ramos A, Acebo P, Contreras A, Casado R, Allona I, Aragoncillo C (2008) Overall alteration of circadian clock gene expression in the chestnut cold response. PLoS One 3:e3567
Ibáñez C, Kozarewa I, Johansson M, Ogren E, Rodhe A, Eriksson ME (2010) Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiol 153(4):1823–1833
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080
Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181:512–521
Lang GA, Early JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. Hort Sci 22:371–377
Law RD, Suttle JC (2003) Transient decreases in methylation at 5′-CCGG-3′ sequences in potato (Solanum tuberosum L.) meristem DNA during progression of tubers through dormancy precede the resumption of sprout growth. Plant Mol Biol 51:437–447
Meijón M, Valledor L, Santamaría E, Testillano PS, Risueño MC, Rodríguez R, Feito I, Canal MJ (2009) Epigenetic characterization of the vegetative and floral stages of azalea buds: dynamics of DNA methylation and histone H4 acetylation. J Plant Physiol 166:1624–1636
Moreno-Cortés A, Hernández-Verdeja T, Sánchez-Jiménez P, González-Melendi P, Aragoncillo C, Allona I (2012) CsRAV1 induces sylleptic branching in hybrid poplar. New Phytol 194:83–90
Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628
Ramchandani S, Bhattacharya SK, Cervoni N, Szyf M (1999) DNA methylation is a reversible biological signal. Proc Natl Acad Sci USA 96:6107–6112
Ramos A, Pérez-Solís E, Ibáñez C, Casado R, Collada C, Gómez L, Aragoncillo C, Allona I (2005) Winter disruption of the circadian clock in chestnut. Proc Natl Acad Sci USA 102:7037–7042
Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:489–500
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223
Rohde A, Bastien C, Boerjan W (2011) Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiol 31:472–482
Ryden P, Sugimoto-Shirasu K, Smith AC, Findlay K, Reiter WD, McCann MC (2003) Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 132:1033–1040
Santamaría ME, Hasbún R, Valera MJ, Meijón M, Valledor L, Rodríguez JL, Toorop PE, Canal MJ, Rodríguez R (2009) Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa. J Plant Physiol 166:1360–1369
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265
Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120
Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20:244–251
Valledor L, Hasbún R, Meijón M, Rodríguez JL, Santamaría ME, Viejo M, Berdasco M, Feito I, Fraga MF, Cañal MJ, Rodríguez R (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Organ Cult 91:75–86
Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH (2012) Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13:27
Wagner D (2003) Chromatin regulation of plant development. Curr Opin Plant Biol 6:20–28
Wareing PF (1956) Photoperiodism in woody plants. Annu Rev Plant Physiol 7:191–214
Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–312