Plant memory: A tentative model

Plant Biology

Volumn 15, Issue 1, 2013, Pages 1-12

  Thellier, M ^a   Luttge U ^b  

^a Technical University of Darmstadt ^*  (France)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Biological clock; Calcium; Epigenetics; Habituation; Priming; Sensitivity; Stimuli; Store recall function; Stress

Indexed keywords

CALCIUM; ECOLOGICAL MODELING; ENVIRONMENTAL STRESS; GENETIC ANALYSIS; GENETICS; HABITUATION; MEMORY; MOLECULAR ANALYSIS; SENSITIVITY ANALYSIS;

EID: 84870418801     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2012.00674.x     Document Type: Review

References (126)

1. Adams K.L. (2010) Dandelions 'remember' stress: heritable stress-induced methylation patterns. New Phytologist, 185, 867-868.
2. Alvarez M.E., Nota F., Cambiagno D.A. (2010) Epigenetic control of plant immunity. Molecular Plant Pathology, 11, 563-576.
3. Baek D., Jiang J., Chung J.S., Wang B., Chen J., Xin Z., Shi H. (2011) Regulated AtHKT1 gene expression by a distal enhancer and DNA methylation in the promoter plays an important role in salt tolerance. Plant Cell Physiology, 52, 149-161.
4. Baluška F., Ninkovic V. (2010) Plant communication from an ecological perspective. Springer, Berlin, Heidelberg, Germany.
5. Baluška F., Mancuso S., Volkmann D., Barlow P. (2004) Root apices as plant command centres: the unique 'brain like' status of the root apex transition zone. Biologia Bratislava, 59, 1-13.
6. Baluška F., Volkmann D., Menzel D. (2005) Plant synapses: actin-based domains for cell-to-cell communication. Trends in Plant Science, 10, 1065-1111.
7. Beck E., Lüttge U. (1990) Streß bei Pflanzen. Biologie in unserer Zeit, 20, 237-244.
8. Bird A. (2002) DNA methylation patterns and epigenetic memory. Genes and Development, 16, 6-21.
9. Bond D.M., Finnegan E.J. (2007) Passing the message on: inheritance of epigenetic traits. Trends in Plant Science, 12, 211-216.
10. Bourgeade P., Boyer N., de Jaegher G., Gaspar T. (1989) Carry-over of thigmomorphogenetic characteristics of calli derived from Bryonia dioica internodes. Plant Cell Tissue and Organ Culture, 19, 199-211.
11. Boyer N., Gaspar T., Lamand M. (1979) Modification des isoperoxydases et de l'allongement des entre-nouds de bryone à la suite d'irritations mécaniques. Zeitschrift für Planzenphysiologie, 93, 459-470.
12. Boyko A., Kovalchuk I. (2008) Epigenetic control of plant stress response. Environmental and Molecular Mutagenesis, 49, 61-72.
13. Bruce T.J.A. (2010) Exploiting plant signals in sustainable agriculture. In: Baluška F., Ninkovic V. (Eds), Plant communication from an ecological perspective. Springer, Berlin, Heidelberg, Germany, pp 215-227.
14. Cervantes-Laurean D., Jacobson E.L., Jacobson M.K. (1996) Glycation and glycoxidation of histones by ADP-ribose. Journal of Biological Chemistry, 271, 10461-10469.
15. Chen M., Lv S., Meng Y. (2010) Epigenetic performers in plants. Developmental Growth and Differentiation, 52, 555-566.
16. Chinnusamy V., Zhu J.-K. (2009) Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology, 12, 133-139.
17. Cubas P., Vincent C., Coen E. (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature, 401, 157-161.
18. Darrah C., Taylor B.L., Edwards K.D., Brown P.E., Hall A., McWatters H.G. (2006) Analysis of phase of LUCIFERASE expression reveals novel circadian quantitative trait loci in Arabidopsis. Plant Physiology, 140, 1464-1474.
19. Daxinger L., Whitelaw E. (2010) Trans-generational epigenetic inheritance: more questions than answers. Genome Research, 20, 1623-1628.
20. Desbiez M.O., Champagnat P., Boyer N., Frachisse J.M., Gaspar T., Thellier M. (1983) Inhibition corrélative de la croissance de l'hypocotyle de Bidens pilosus L. par des traumatismes cotylédonaires légers. Bulletin de la Société botanique de France [Actual Botanique], 130, 67-77.
21. Desbiez M.O., Gaspar T., Crouzillat D., Frachisse J.M., Thellier M. (1987) Effect of cotyledonary prickings on growth, ethylene metabolism and peroxidase activity in Bidens pilosus. Plant Physiology and Biochemistry, 25, 137-143.
22. 2+. Plant Physiology and Biochemistry, 29, 457-462.
23. Desbiez M.O., Tort M., Thellier M. (1991b) Control of a symmetry-breaking process in the course of the morphogenesis of plantlets of Bidens pilosa L. Planta, 184, 397-402.
24. Desbiez M.O., Tort M., Monnier C., Thellier M. (1998) Asymmetrical triggering of the cell cycle in opposite buds of a young plant, after a slight cotyledonary wound. Comptes Rendus de l'Académie des Sciences Paris (Sciences de la Vie/Life Sciences), 321, 403-407.
25. Dodd A.N., Salathia N., Hall A., Kevei E., Toth R., Nagy F., Hibberd J.M., Millar A.J., Webb A.A.R. (2005) Plant circadian clocks increase photosynthesis, growth, survival and competitive advantage. Science, 309, 630-633.
26. 2+ response amplitude and duration. Nature, 386, 855-858.
27. Dudai Y. (2004) The neurobiology of consolidations, or, how stable is the engram? Annual Reviews of Psychology, 55, 51-86.
28. Falkner R., Falkner G. (2003) Distinct adaptability during phosphate uptake by the cyanobacterium Anabaena variabilis reflects information processing about preceding phosphate supply. Journal of Trace and Microprobe Techniques, 21, 363-375.
29. Farré E.M. (2012) The regulation of plant growth by the circadian clock. Plant Biology, 14, 401-410.
30. Frankhauser C., Staiger D. (2002) Photoreceptors in Arabidopsis thaliana: light perception, signal transduction and entrainment of the endogenous clock. Planta, 216, 1-16.
31. Franklin-Tong V.E., Drobak B.K., Allan A.C., Watkins P.A.C., Trewavas A.J. (1996) Growth of pollen tubes of Papaver rheoas is regulated by a slow-moving calcium wave propagated by inositol trisphosphate. Plant Cell, 8, 1305-1321.
32. Fujiwara S., Oda A., Yoshida R., Niinuma K., Miyata K., Tomozoe Y., Tajima T., Nakagawa M., Hayashi K., Coupland G., Mizoguchi T. (2008) Circadian clock proteins LHY and CCA1 regulate SVP protein accumulation to control flowering in Arabidopsis. Plant Cell, 20, 2960-2971.
33. Gayler S. (2010) Modélisation de l'effet de facteurs de l'environnement sur la répartition des ressources dans un système végétal mixte. Comptes Rendus de l'Académie des Sciences, Agriculture France, 96, 89-90.
34. Gayler S., Grams T.E.E., Kozovits A., Luedemann G., Winkler J.B., Priesack E. (2006) Analysis of competition effects in mono- and mixed cultures of juvenile beech and spruce by means of the plant growth simulation model PLATHO. Plant Biology, 8, 503-514.
35. Gayler S., Grams T.E.E., Heller W., Treutter D., Priesack E. (2008) A dynamic model of environmental effects on allocation to carbon-based secondary compounds in juvenile trees. Annals of Botany, 101, 1089-1098.
36. Gierer A. (1998) Im Spiegel der Natur erkennen wir uns selbst. Wissenschaft und Menschenbild. Rowohlt, Reinbeck, Germany.
37. Gilroy S., Fricker M., Read N.D., Trewavas A.J. (1991) Role of calcium in signal transduction of Commelina guard cells. Plant Cell, 3, 333-344.
38. Goh C.-H., Nam H.G., Park Y.S. (2003) Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. The Plant Journal, 36, 240-255.
39. Gong Z., Morales-Ruiz T., Ariza R.R., Roldán-Arjona T., David L., Zhu J.-K. (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell, 111, 803-814.
40. Grabov A., Blatt M.R. (1998) Membrane voltage initiates calcium waves and potentiates calcium increase with abscisic acid in guard cells. Proceedings of the National Academy of Sciences USA, 95, 4778-4783.
41. Green R.M., Tingay S., Wang Z.-Y., Tobin E.M. (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiology, 129, 576-584.
42. Grunstein M. (1997) Histone acetylation in chromatin structure and transcription. Nature, 389, 349-352.
43. Guitiérrez-Marcos J.F., Costa L.M., Prà M.D., Scholten S., Kranz E., Perez P., Dickinson H.G. (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nature Genetics, 38, 876-878.
44. Harmer S.L., Kay S.A. (2005) Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis. Plant Cell, 17, 1926-1940.
45. Heil M. (2010) Within-plant signaling by volatiles triggers systemic defences. In: Baluška F., Ninkovic V. (Eds), Plant communication from an ecological perspective. Springer, Berlin Heidelberg, Germany, pp 99-112.
46. Henderson I.R., Jacobsen S.E. (2007) Epigenetic inheritance in plants. Nature, 447, 418-424.
47. Henry-Vian C., Vian A., Dietrich A., Ledoigt G., Desbiez M.O. (1995) Change in the polysomal mRNA population upon wound signal expression or storage in Bidens pilosa. Plant Physiology and Biochemistry, 33, 337-344.
48. Herms D.A., Mattson W.J. (1992) The dilemma of plants: to grow or defend. Quarterly Reviews in Biology, 67, 283-335.
49. Holliday R., Pugh J.E. (1975) DNA modification mechanisms and gene activity during development. Science, 186, 226-232.
50. Hotta C.T., Gardner M.J., Hubbard K.E., Baek S.J., Dalchau N., Suhita D., Dodd A.N., Webb A.A.R. (2007) Modulation of environmental responses of plants by circadian clocks. Plant, Cell and Environment, 30, 333-349.
51. van Hulten M., Ton J., Pieterse C.M.J., van Wees S.C.M. (2010) Plant defense signaling from the underground primes aboveground defenses to confer enhanced resistance in a cost-efficient manner. In: Baluška F., Ninkovic V. (Eds), Plant communication from an ecological perspective. Springer, Berlin Heidelberg, Germany, pp 43-60.
52. Ibáñez C., Kozarewa I., Johansson M., Ögren E., Rohde A., Eriksson M.E. (2010) Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiology, 153, 1823-1833.
53. Jablonka E., Lamb M.J. (1989) The inheritance of acquired epigenetic variation. Journal of Theoretical Biology, 139, 69-83.
54. Johnson C.H., Golden S.S. (1999) Circadian programs in cyanobacteria: adaptiveness and mechanism. Annual Reviews of Microbiology, 53, 389-409.
55. Kikis E.A., Khanna R., Quail P.H. (2005) ELF4 is a phytochrome-regulated component of a negative-feedback loop involving the central oscillator components CCA1 and LHY. The Plant Journal, 44, 300-313.
56. Knight M.R., Campbell A.K., Smith S.M., Trewavas A.J. (1991) Transgenic plan aequorin reports the effect of touch and cold-shock and elicitors on cytoplasmic calcium. Nature, 352, 524-526.
57. Knight M.R., Smith S.M., Trewavas A.J. (1992) Wind-induced plant motion immediately increases cytosolic calcium. Proceedings of the National Academy of Sciences USA, 89, 4967-4971.
58. Knight H., Brandt S., Knight M.R. (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. The Plant Journal, 16, 681-687.
59. Kou H.P., Li Y., Song X.X., Ou X.F., Xing S.C., Ma J., von Wettstein D., Liu B. (2011) Heritable alteration in DNA methylation induced by nigtrogen-deficiency stress accompanies enhanced tolerancee by progenies to stress in rice (Oryza sativa L.). Journal of Plant Physiology, 168, 1685-1693.
60. Langebartels C., Heller W., Führer G., Lippert M., Simons S., Sandermann H. (1998) Memory effects in the action of ozone on conifers. Ecotoxicology and Environmental Safety, 41, 62-72.
61. Larcher W. (1987) Stress bei Pflanzen. Naturwissenschaften, 74, 158-167.
62. Lesburguères E., Gobbo O.L., Alaux-Cantin S., Hambucken A., Trifilieff P., Bontempi B. (2011) Early tagging of cortical networks is required for the formation of enduring associative memory. Science, 331, 924-928.
63. Levitt J. (1980) Responses of plants to environmental stresses, Vol 1. Academic Press, New York, NY, USA.
64. Lo W.S., Duggan L., Emre N.C.T., Belotserkovskya R., Lane W.S., Shiekhattar R., Berger S.L. (2001) Snf1 - a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science, 293, 1142-1146.
65. Lodish H., Berk A., Zipursky S.L., Matsudaira P., Baltimore D., Darnell J. (2000) Molecular cell biology, 4th edition. WH Freeman, New York, NY, USA. Section 21-7: Learning and Memory.
66. Love J., Dodd A.N., Webb A.A.R. (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. The Plant Cell, 16, 956-966.
67. Lüttge U. (2002) Circadian rhythmicity: is the "biological clock" hardware or software. Progress in Botany, 64, 277-319.
68. Lüttge U. (2012) The system vascular plant: whole plant physiology's outlooks for systems biology with emergence by contrast to modularity. Progress in Botany, 74, 165-190.
69. Manning G.S. (1969) Limiting laws and counter-ion condensation in polyelectrolyte solutions. I Colligative properties. Journal of Chemical Physics, 51, 924-933.
70. Matzke M., Matzke A.J., Pruss G.J., Vance V.B. (2001) RNA-based silencing strategies in plants. Current Opinion in Genetics and Development, 11, 221-227.
71. Matzke M., Kanno T., Huettel B., Daxinger L., Matzke A.J. (2007) Targets of RNA directed DNA methylation. Current Opinion in Plant Biology, 10, 512-519.
72. 2+ signalling systems. Trends in Plant Science, 3, 32-36.
73. McClung C.R. (2006) Plant circadian rhythms. Plant Cell, 18, 792-803.
74. Michael T.P., McClung C.R. (2002) Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiology, 130, 627-638.
75. Molinier J., Ries G., Zipfel C., Hohn B. (2006) Transgeneration memory of stress in plants. Nature, 442, 1046-1049.
76. Nakamichi N. (2011) Molecular mechanisms underlying the Arabidopsis circadian clock. Plant and Cell Physiology, 52, 1709-1718.
77. Nick P., Schäfer E. (1988) Spatial memory during the tropism of maize (Zea mays L.) coleoptiles. Planta, 175, 380-388.
78. Niwa Y., Yamashino T., Mizuno T. (2009) The circadian clock regulates the photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant and Cell Physiology, 50, 838-854.
79. Ogudi T., Sage-Ono K., Kamada H., Ono M. (2004) Characterization of transcriptional oscillation of an Arabidopsis homolog of PnC401 related to photoperiodic induction of flowering in Pharbitis nil. Plant and Cell Physiology, 45, 232-235.
80. Onai K., Okamoto K., Nishimoto H., Morioka C., Hirano M., Kami-Ike N., Ishiura M. (2004) Large-scale screening of Arabidopsis circadian clock mutants by a high-throughput real-time bioluminescence monitoring system. The Plant Journal, 40, 1-11.
81. Osmond C.B., Grace S.C. (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? Journal of Experimental Botany, 46, 1351-1362.
82. Ouyang Y., Andersson C.R., Kondo T., Golden S.S., Johnson C.H. (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proceedings of the National Academy of Sciences USA, 95, 8660-8664.
83. Paulsen M. (2007) Genomic imprinting in Säugetieren: das epigenetische Gedächtnis. Biologie in unserer Zeit, 37, 86-91.
84. Pikaard C.S. (2006) Cell biology of the Arabidopsis nuclear siRNA pathway for RNA-directed chromatin modification. Cold Spring Harbor Symposia on Quantitative Biology, 71, 473-480.
85. Plieth C., Hansen U.P., Knight H., Knight M.R. (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. The Plant Journal, 18, 491-497.
86. Richards E.J. (2006) Inherited epigenetic variation - revisiting soft inheritance. Nature Reviews Genetics, 76, 395-401.
87. Ripoll C., Norris V., Thellier M. (2004) Ion condensation and signal transduction. BioEssays, 26, 549-557.
88. Ripoll C., Le Sceller L., Verdus M.C., Norris V., Tafforeau M., Thellier M. (2009) Memorization of abiotic stimuli in plants: a complex role for calcium. In: Baluška F. (Ed.), Plant-environment interactions. Springer, Berlin, Germany, pp 267-283.
89. Roden L.C., Song H.-R., Jackson S., Morris K., Carré I.A. (2002) Floral responses to photoperiod are correlated with the timing of rhythmic expression relative to dawn and dusk in Arabidopsis. Proceedings of the National Academy of Sciences USA, 99, 13313-13318.
90. Roux D., Vian A., Girard S., Bonnet P., Paladian F., Davies E., Ledoigt G. (2006) Electromagnetic fields (900 MHz) evoke consistent molecular responses in tomato plants. Physiologia Plantarum, 128, 283-288.
91. Salomé P.A., Michael T.P., Kearns E.V., Fett-Neto A.G., Sharrock R.A., McClung C.R. (2002) The out of phase 1 mutant defines a role for PHYB in circadian phase control in Arabidopsis. Plant Physiology, 129, 1674-1685.
92. Sasek T.W., Richardson C.J., Fendick E.A., Bevington S.R., Kress L.W. (1991) Carryover effects of acid rain and ozone on the physiology of multiple flushes of loblolly pine seedlings. Forest Science, 37, 1078-1098.
93. Saze H. (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Seminars in Cell and Developmental Biology, 19, 527-536.
94. Selye H. (1973) The evolution of the stress concept. American Scientist, 61, 693-699.
95. Shen J., Xie K., Xiong L. (2010) Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Molecular and General Genetics, 284, 477-488.
96. Sridhar V.V., Kapoor A., Zhang K., Zhu J., Zhou T., Hasegawa P.M., Bressan R.A., Zhu J.K. (2007) Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature, 447, 735-738.
97. Sunkar R., Zhu J.K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001-2019.
98. Tafforeau M., Verdus M.C., Charlionet R., Cabin-Flaman A., Ripoll C. (2002a) Two-dimensional electrophoresis investigation of short term response of flax seedlings to cold shock. Electrophoresis, 23, 2534-2540.
99. Tafforeau M., Verdus M.C., Norris V., White G., Demarty M., Thellier M., Ripoll C. (2002b) SIMS study of the calcium-deprivation step related to epidermal meristem production induced in flax by cold shock or radiation from a GSM telephone. Journal of Trace and Microprobe Techniques, 20, 611-623.
100. Tafforeau M., Verdus M.C., Norris V., White G.J., Cole M., Demarty M., Thellier M., Ripoll C. (2004) Plant sensitivity to low intensity 105 GHz electromagnetic radiation. Bioelectromagnetics, 25, 403-407.
101. Tafforeau M., Verdus M.C., Norris V., Ripoll C., Thellier M. (2006) Memory processes in the response of plants to environmental signals. Plant Signaling and Behavior, 1, 9-14.
102. Tanigawa Y., Tsuchiya M., Imai Y., Shimoyama M. (1984) ADP-ribosyltransferase from hen liver nuclei. Purification and characterization. Journal of Biological Chemistry, 259, 2022-2029.
103. Taylor A.R., Manison N.F.H., Fernandez C., Wood J., Brownlee C. (1996) Spatial organisation of calcium signalling involved in volume control of the Fucus rhizoids. Plant Cell, 8, 2015-2031.
104. Thellier M. (2011) A half-century adventure in the dynamics of living systems. Progress in Botany, 73, 3-53.
105. Thellier M., Desbiez M.O., Champagnat P., Kergosien Y. (1982) Do memory processes also exist in plants? Physiologia Plantarum, 56, 281-284.
106. Thellier M., Le Sceller L., Norris V., Verdus M.C., Ripoll C. (2000) Long-distance transport, storage and recall of morphogenetic information in plants: the existence of a primitive plant "memory". Comptes Rendus de l'Académie des Sciences, Paris (Sciences de la Vie/Life Sciences), 323, 81-91.
107. Thellier M., Ripoll C., Norris V. (2012) Memory processes in the control of plant growth and morphogenesis. Nova Acta Leopoldina NF, in press.
108. Trewavas A. (1999) Le calcium, c'est la vie: calcium makes waves. Plant Physiology, 120, 1-6.
109. Trewavas A. (2003) Aspects of plant intelligence. Annals of Botany, 92, 1-20.
110. Ueda M., Nakamura Y. (2006) Metabolites involved in plant movement and "memory": nyctinasty of legumes and trap movement in the Venus flytrap. Natural Products Reports, 23, 548-557.
111. Verdus M.C., Thellier M., Ripoll C. (1997) Storage of environmental signals in flax: their morphogenetic effect as enabled by a transient depletion of calcium. The Plant Journal, 12, 1399-1410.
112. Verdus M.C., Le Sceller L., Norris V., Thellier M., Ripoll C. (2007) Pharmacological evidence for calcium involvement in the long-term processing of abiotic stimuli in plants. Plant Signaling and Behavior, 2, 212-220.
113. Verdus M.C., Ripoll C., Norris V., Thellier M. (2012) The role of calcium in the recall of stored morphogenetic information by plants. Acta Biotheoretica, 60, 83-97.
114. Verhoeven K.J.F., Jansen J.J., van Dijk P.J., Biere A. (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist, 185, 1108-1118.
115. Vian A., Roux D., Girard S., Bonnet P., Paladian F., Davies E., Ledoigt G. (2006) Microwave irradiation affects gene expression in plants. Plant Signaling and Behavior, 1, 67-70.
116. Volkov A.G., Carrell H., Adesina T., Markin V.S., Jovanov V.S. (2008) Plant electrical memory. Plant Signaling and Behavior, 3, 490-492.
117. Wang W.S., Pan Y.J., Zhao X.Q., Dwivedi D., Zhu L.H., Ali J., Fu B.Y., Li Z.K. (2010) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). Journal of Experimental Botany, 62, 1951-1960.
118. Woelfle M.A., Ouyang Y., Phanvijhitsiri K., Johnson C.H. (2004) The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Current Biology, 14, 1481-1486.
119. Yaish M.W., Colasanti J., Rothstein S.J. (2011) The role of epigenetic processes in controlling flowering time in plants exposed to stress. Journal of Experimental Botany, 62, 3727-3735.
120. Yerushalmi S., Green R.M. (2009) Evidence for the adaptive significance of circadian rhythms. Ecology Letters, 12, 970-981.
121. Yerushalmi S., Yakir E., Green R.M. (2011) Circadian clocks and adaptation in Arabidopsis. Molecular Ecology, 20, 1155-1165.
122. Zhang X. (2008) The epigenetic landscape of plants. Science, 320, 489-492.
123. Zhang X., Yazaki J., Sundaresan A., Cokus S., Chan S.W.-L., Chen H., Henderson I.R., Shinn P., Pellegrini M., Jacobsen S.E., Ecker J.R. (2006) Genome-wide high resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell, 126, 1189-1201.
124. Zhang Y., Reinberg D. (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes and Development, 15, 2343-2360.
125. 3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature, 455, 1259-1262.
126. Zhu J.-K. (2008) Epigenome sequencing comes of age. Cell, 133, 395-397.