Epigenetic Responses of Trees to Environmental Stress in the Context of Climate Change
Open accessAbstract
In long‐lived tree populations, when environmental change outpaces rates of evolutionary adaptation, plasticity in traits related to stress tolerance, dormancy, and dispersal may be vital for preventing extinction. While a population's genetic background partly determines its ability to adapt to a changing environment, so too do the many types of epigenetic modifications that occur within and among populations, which vary on timescales orders of magnitude faster than the emergence of new beneficial alleles. Consequently, phenotypic plasticity driven by epigenetic modification may be especially critical for sessile, long‐lived organisms such as trees that must rely on this plasticity to keep pace with rapid anthropogenic environmental change. While studies have reported large effects of DNA methylation, histone modification, and non‐coding RNAs on the expression of stress‐tolerance genes and resulting phenotypic responses, little is known about the role of these effects in non‐model plants and particularly in trees. Here, we review new findings in plant epigenetics with particular relevance to the ability of trees to adapt to or escape stressors associated with rapid climate change. Such findings include specific epigenetic influences over drought, heat, and salinity tolerance, as well as dormancy and dispersal traits. We also highlight promising findings concerning transgenerational inheritance of an epigenetic ‘stress memory’ in plants. As epigenetic information is becoming increasingly easy to obtain, we close by outlining ways in which ecologists can use epigenetic information better to inform population management and forecasting efforts. Understanding the molecular mechanisms behind phenotypic plasticity and stress memory in tree species offers a promising path towards a mechanistic understanding of trees' responses to climate change.
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Hormonal imbalances caused by frequent use of high concentrations of auxins and cytokinins can destabilize the plant's hormonal equilibrium and trigger genetic instability.
“Likewise, hormonal imbalances caused by the frequent use of high concentrations of auxins and cytokinins, though vital for shoot initiation and proliferation, can destabilize the plant's hormonal equilibrium and trigger genetic instability [73,74].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [73]
The Introduction (Background; page unavailable) mentions auxin concentrations as a plant characteristic involved in stress responses, but not the repeated application of high concentrations of auxins or cytokinins. Searches for cytokinins, hormonal imbalance, shoot initiation, and genetic instability found no passage addressing the claimed causal link. (LLM, conf=0.74)
Experimental — accuracy not yet measuredCulture conditions profoundly impact somaclonal variation, as in vitro environments differ from natural conditions, subjecting plant cells to stresses that alter metabolism and trigger somaclonal variation.
“Culture conditions also profoundly impact, as in vitro environments differ significantly from natural conditions, subjecting plant cells to stresses that can alter their metabolism and trigger somaclonal variation [72,73].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [73]
The Introduction discusses environmental stress and epigenetic variation in trees, and the drought-stress section distinguishes controlled experiments from natural populations. Neither addresses whether in vitro culture conditions alter plant-cell metabolism or trigger somaclonal variation (searched: somaclonal variation, in vitro, and culture conditions). (LLM, conf=0.76)
Experimental — accuracy not yet measuredNutrient imbalances in artificial media can cause cellular stress, affect metabolism, and increase mutation rates.
“For example, nutrient imbalances in artificial media can cause cellular stress, affect metabolism, and increase mutation rates [73].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [73]
The Introduction glossary identifies nutrient deficit as a plant stressor, and the biotic-stress section discusses experiments with different nutrient levels. Neither passage addresses nutrient imbalances in artificial media or their claimed effects on cellular metabolism and mutation rates; searches for those terms found no supporting passage. Page numbers were not available in our copy. (LLM, conf=0.73)
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References 170 · Cited by 44
Research works printed but not linked: 161
- Alakärppä, E., Salo, H. M., Valledor, L., Cañal, M. J., Häggman, H. & Vuosku, J. (2018). Natural variation of DNA methylation and gene expression may determine local adaptations of Scots pine populations. Journal of Experimental Botany 69(21), 5293– 5305. 30113688
- Alberto, F. J., Aitken, S. N., Alía, R., González‐Martínez, S. C., Hänninen, H., Kremer, A., Lefèvre, F., Lenormand, T., Yeaman, S., Whetten, R. & Savolainen, O. (2013). Potential for evolutionary responses to climate change – evidence from tree populations. Global Change Biology 19(6), 1645– 1661. 23505261 PMC3664019
- Allen, C. D., Macalady, A. K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D. D. & Hogg, E. H. T. (2010). A global overview of drought and heat‐induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259(4), 660– 684.
- Alonso, C., Pérez, R., Bazaga, P., Medrano, M. & Herrera, C. M. (2018). Within‐plant variation in seed size and inflorescence fecundity is associated with epigenetic mosaicism in the shrub Lavandula latifolia (Lamiaceae). Annals of Botany 121(1), 153– 160. 29186299 PMC5786237
- Amaral, J., Ribeyre, Z., Vigneaud, J., Sow, M. D., Fichot, R., Messier, C., Pinto, G., Nolet, P. & Maury, S. (2020). Advances and promises of epigenetics for forest trees. Forests 11(9), 976.
- Avramova, Z. (2019). Defence‐related priming and responses to recurring drought: two manifestations of plant transcriptional memory mediated by the ABA and JA signalling pathways. Plant, Cell & Environment 42(3), 983– 997. 30299553
- Ayanlade, A., Radeny, M., Morton, J. F. & Muchaba, T. (2018). Rainfall variability and drought characteristics in two agro‐climatic zones: an assessment of climate change challenges in Africa. Science of the Total Environment 630, 728– 737. 29499531
- Becker, P. B. & Hörz, W. (2002). ATP‐dependent nucleosome remodeling. Annual Review of Biochemistry 71(1), 247– 273. 12045097
- Bennett, A. C., McDowell, N. G., Allen, C. D. & Anderson‐Teixeira, K. J. (2015). Larger trees suffer most during drought in forests worldwide. Nature Plants 1(10), 15139. 27251391
- Bewick, A. J. & Schmitz, R. J. (2017). Gene body DNA methylation in plants. Current Opinion in Plant Biology 36, 103– 110. 28258985 PMC5413422
- Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C. & Finnegan, S. (2013). Climate change and the past, present, and future of biotic interactions. Science 341(6145), 499– 504. 23908227
- Bose, A. K., Gessler, A., Bolte, A., Bottero, A., Buras, A., Cailleret, M., Camarero, J. J., Haeni, M., Hereş, A. M., Hevia, A., Lévesque, M., Linares, J. C., Martinez‐Vilalta, J., Matías, L., Menzel, A., et al. (2020). Growth and resilience responses of Scots pine to extreme droughts across Europe depend on predrought growth conditions. Global Change Biology 26(8), 4521– 4537. 32388882 PMC7383776
- Bossdorf, O., Richards, C. L. & Pigliucci, M. (2008). Epigenetics for ecologists. Ecology Letters 11(2), 106– 115. 18021243
- Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., Hollunder, J., Meins, F. Jr. & Kovalchuk, I. (2010). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer‐like proteins. PLoS One 5(3), e9514. 20209086 PMC2831073
- Boyko, A. & Kovalchuk, I. (2008). Epigenetic control of plant stress response. Environmental and Molecular Mutagenesis 49(1), 61– 72. 17948278
- Bräutigam, K., Vining, K. J., Lafon‐Placette, C., Fossdal, C. G., Mirouze, M., Marcos, J. G., Fluch, S., Fraga, M. F., Guevara, M. Á. & Abarca, D. (2013). Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecology and Evolution 3(2), 399– 415. 23467802 PMC3586649
- Broennimann, O., Treier, U. A., Müller‐Schärer, H., Thuiller, W., Peterson, A. T. & Guisan, A. (2007). Evidence of climatic niche shift during biological invasion. Ecology Letters 10(8), 701– 709. 17594425
- Bruce, T. J. A., Matthes, M. C., Napier, J. A. & Pickett, J. A. (2007). Stressful ‘memories’ of plants: evidence and possible mechanisms. Plant Science 173(6), 603– 608.
- Cabra‐Rivas, I., Alonso, Á. & Castro‐Díez, P. (2014). Does stream structure affect dispersal by water? A case study of the invasive tree Ailanthus altissima in Spain. Management of Biological Invasions 5(2), 179– 186.
- Cai, Q., He, B., Kogel, K. H. & Jin, H. (2018). Cross‐kingdom RNA trafficking and environmental RNAi–nature's blueprint for modern crop protection strategies. Current Opinion in Microbiology 46, 58– 64. 29549797 PMC6499079
- Camisón, Á., Martín, M. Á., Oliva, J., Elfstrand, M. & Solla, A. (2019). Increased tolerance to Phytophthora cinnamomi in offspring of ink‐diseased chestnut (Castanea sativa Miller) trees. Annals of Forest Science 76(4), 119.
- Cao, D., Ju, Z., Gao, C., Mei, X., Fu, D., Zhu, H., Luo, Y. & Zhu, B. (2014). Genome‐wide identification of cytosine‐5 DNA methyltransferases and demethylases in Solanum lycopersicum. Gene 550(2), 230– 237. 25149677
- Carbó, M., Iturra, C., Correia, B., Colina, F. J., Meijón, M., Álvarez, J. M., Cañal, M. J., Hasbún, R., Pinto, G. & Valledor, L. (2019). Epigenetics in forest trees: keep calm and carry on. In Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications, pp. 381– 403. Springer, Cham, Switzerland.
- Carlson, S. M., Cunningham, C. J. & Westley, P. A. H. (2014). Evolutionary rescue in a changing world. Trends in Ecology & Evolution 29(9), 521– 530. 25038023
- Cavender‐Bares, J., Ackerly, D. D., Baum, D. A. & Bazzaz, F. A. (2004). Phylogenetic overdispersion in Floridian oak communities. The American Naturalist 163(6), 823– 843. 15266381
- Chan, W. Y., Hoffmann, A. A. & van Oppen, M. J. H. (2019). Hybridization as a conservation management tool. Conservation Letters 12(5), e12652.
- Colomé‐Tatché, M., Cortijo, S., Wardenaar, R., Morgado, L., Lahouze, B., Sarazin, A., Etcheverry, M., Martin, A., Feng, S., Duvernois‐Berthet, E., Labadie, K., Wincker, P., Jacobsen, S. E., Jansen, R. C., Colot, V., et al. (2012). Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proceedings of the National Academy of Sciences of the United States of America 109(40), 16240– 16245. 22988127 PMC3479620
- Conde, D., Le Gac, A.‐L., Perales, M., Dervinis, C., Kirst, M., Maury, S., González‐Melendi, P. & Allona, I. (2017 a). Chilling‐responsive DEMETER‐LIKE DNA demethylase mediates in poplar bud break. Plant, Cell & Environment 40(10), 2236– 2249. 28707409
- Conde, D., Moreno‐Cortés, A., Dervinis, C., Ramos‐Sánchez, J. M., Kirst, M., Perales, M., González‐Melendi, P. & Allona, I. (2017 b). Overexpression of DEMETER, a DNA demethylase, promotes early apical bud maturation in poplar. Plant, Cell & Environment 40(11), 2806– 2819. 28810288
- Correia, B., Valledor, L., Hancock, R. D., Jesus, C., Amaral, J., Meijon, M. & Pinto, G. (2016). Depicting how Eucalyptus globulus survives drought: involvement of redox and DNA methylation events. Functional Plant Biology 43(9), 838– 850. 32480508
- Correia, B., Valledor, L., Meijón, M., Rodriguez, J. L., Dias, M. C., Santos, C., Cañal, M. J., Rodriguez, R. & Pinto, G. (2013). Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures? PLoS One 8(1), e53543. 23326451 PMC3543447
- Cubas, P., Vincent, C. & Coen, E. (1999). An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401(6749), 157– 161. 10490023
- De Grandpré, L., Kneeshaw, D. D., Perigon, S., Boucher, D., Marchand, M., Pureswaran, D. & Girardin, M. P. (2019). Adverse climatic periods precede and amplify defoliator‐induced tree mortality in eastern boreal North America. Journal of Ecology 107(1), 452– 467.
- de la Peña, E. & Bonte, D. (2014). Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale. Ecology and Evolution 4(16), 3309– 3319. 25473483 PMC4222217
- Deng, X., Song, X., Wei, L., Liu, C. & Cao, X. (2016). Epigenetic regulation and epigenomic landscape in rice. National Science Review 3(3), 309– 327.
- Deng, Y., Zhai, K., Xie, Z., Yang, D., Zhu, X., Liu, J., Wang, X., Qin, P., Yang, Y., Zhang, G., Li, Q., Zhang, J., Wu, S., Milazzo, J., Mao, B., Wang, E., et al. (2017). Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355(6328), 962– 965. 28154240
- * Do Nascimento, A. M. M., Montalbán, I. A., Llamazares De Miguel, D., Goicoa, T., Ugarte, M. D. & Moncaleán, P. (2022). High temperature and water deficit cause epigenetic changes in somatic plants of Pinus radiata D. Don. Plant Cell, Tissue and Organ Culture 151(1), 107– 121.
- Donaldson, J. E., Hui, C., Richardson, D. M., Robertson, M. P., Webber, B. L. & Wilson, J. R. U. (2014). Invasion trajectory of alien trees: the role of introduction pathway and planting history. Global Change Biology 20(5), 1527– 1537. 24343918
- D'Urso, A. & Brickner, J. H. (2017). Epigenetic transcriptional memory. Current Genetics 63(3), 435– 439. 27807647 PMC5413435
- Ellison, A. M. (2019). Foundation species, non‐trophic interactions, and the value of being common. iScience 13, 254– 268. 30870783 PMC6416672
- Estravis‐Barcala, M., Mattera, M. G., Soliani, C., Bellora, N., Opgenoorth, L., Heer, K. & Arana, M. V. (2020). Molecular bases of responses to abiotic stress in trees. Journal of Experimental Botany 71(13), 3765– 3779. 31768543 PMC7316969
- Fan, S. K., Ye, J. Y., Zhang, L. L., Chen, H. S., Zhang, H. H., Zhu, Y. X., Liu, X. X. & Jin, C. W. (2020). Inhibition of DNA demethylation enhances plant tolerance to cadmium toxicity by improving iron nutrition. Plant, Cell & Environment 43(1), 275– 291. 31703150
- Feng, S., Cokus, S. J., Schubert, V., Zhai, J., Pellegrini, M. & Jacobsen, S. E. (2014). Genome‐wide Hi‐C analyses in wild‐type and mutants reveal high‐resolution chromatin interactions in Arabidopsis. Molecular Cell 55(5), 694– 707. 25132175 PMC4347903
- Footitt, S., Müller, K., Kermode, A. R. & Finch‐Savage, W. E. (2015). Seed dormancy cycling in Arabidopsis: chromatin remodelling and regulation of DOG1 in response to seasonal environmental signals. Plant Journal 81(3), 413– 425. PMC4671266 25439058
- Ford, K. R., Harrington, C. A., Bansal, S., Gould, P. J. & St. Clair, J. B. (2016). Will changes in phenology track climate change? A study of growth initiation timing in coast Douglas‐fir. Global Change Biology 22(11), 3712– 3723. 27104650
- Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán‐Espitia, J. D. (2019). Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. The Royal Society 374, 20180174. PMC6365870 30966962
- Fricke, E. C., Ordonez, A., Rogers, H. S. & Svenning, J.‐C. (2022). The effects of defaunation on plants capacity to track climate change. Science 375(6577), 210– 214. 35025640
- Gao, M., Huang, Q., Chu, Y., Ding, C., Zhang, B. & Su, X. (2014). Analysis of the leaf methylomes of parents and their hybrids provides new insight into hybrid vigor in Populus deltoides. BMC Genetics 15(Suppl 1), S8. PMC4118634 25080097
- García‐García, I., Méndez‐Cea, B., Martín‐Gálvez, D., Seco, J. I., Gallego, F. J. & Linares, J. C. (2021). Challenges and perspectives in the epigenetics of climate change‐induced forests decline. Frontiers in Plant Science 12, 797958. 35058957 PMC8764141
- García‐Murillo, L., Valencia‐Lozano, E., Priego‐Ranero, N. A., Cabrera‐Ponce, J. L., Duarte‐Aké, F. P., Vizuet‐de‐Rueda, J. C., Rivera‐Toro, D. M., Herrera‐Ubaldo, H., de Folter, S. & Alvarez‐Venegas, R. (2023). CRISPRa‐mediated transcriptional activation of the SlPR‐1 gene in edited tomato plants. Plant Science 329, 111617. 36731748
- Ghouil, H., Montpied, P., Epron, D., Ksontini, M., Hanchi, B. & Dreyer, E. (2003). Thermal optima of photosynthetic functions and thermostability of photochemistry in cork oak seedlings. Tree Physiology 23(15), 1031– 1039. 12975127
- Gibson, D. J., Connolly, J., Hartnett, D. C. & Weidenhamer, J. D. (1999). Designs for greenhouse studies of interactions between plants. Journal of Ecology 87(1), 1– 16.
- Giovannoni, J., Nguyen, C., Ampofo, B., Zhong, S. & Fei, Z. (2017). The epigenome and transcriptional dynamics of fruit ripening. Annual Review of Plant Biology 68, 61– 84. 28226232
- Gourcilleau, D., Bogeat‐Triboulot, M.‐B., Le Thiec, D., Lafon‐Placette, C., Delaunay, A., El‐Soud, W. A., Brignolas, F. & Maury, S. (2010). DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Annals of Forest Science 67(2), 208.
- Greene, D. F. & Quesada, M. (2011). The differential effect of updrafts, downdrafts and horizontal winds on the seed abscission of Tragopogon dubius. Functional Ecology 25(3), 468– 472.
- Greer, B. T., Still, C., Cullinan, G. L., Brooks, J. R. & Meinzer, F. C. (2018). Polyploidy influences plant‐environment interactions in quaking aspen (Populus tremuloides Michx.). Tree Physiology 38(4), 630– 640. 29036397 PMC6527095
- Gugger, P. F., Fitz‐Gibbon, S., PellEgrini, M. & Sork, V. L. (2016). Species‐wide patterns of DNA methylation variation in Quercus lobata and their association with climate gradients. Molecular Ecology 25(8), 1665– 1680. 26833902
- Hahn, E. E., Grealy, A., Alexander, M. & Holleley, C. E. (2020). Museum epigenomics: charting the future by unlocking the past. Trends in Ecology Evolution 35(4), 295– 300. 31955919
- He, Y. & Li, Z. (2018). Epigenetic environmental memories in plants: establishment, maintenance, and reprogramming. Trends in Genetics 34(11), 856– 866. 30144941
- Hernández, C. A., Kafuri, L. A., Isaza, R. A. & Arias, M. L. (2006). Analysis of genetic variation in clones of rubber (Hevea brasiliensis) from Asian, South and Central American origin using RAPDs markers. Revista Colombiana de Biotecnología 8(2), 29– 34.
- Hilker, M. & Schmülling, T. (2019). Stress priming, memory, and signalling in plants. Plant, Cell & Environment 42, 753– 761. 30779228
- Holeski, L. M., Jander, G. & Agrawal, A. A. (2012). Transgenerational defense induction and epigenetic inheritance in plants. Trends in Ecology & Evolution 27(11), 618– 626. 22940222
- Iwasaki, M. & Paszkowski, J. (2014). Epigenetic memory in plants. The EMBO Journal 33(18), 1987– 1998. 25104823 PMC4195768
- Jia, J., Zhou, J., Shi, W., Cao, X., Luo, J., Polle, A. & Luo, Z. B. (2017). Comparative transcriptomic analysis reveals the roles of overlapping heat‐/drought‐responsive genes in poplars exposed to high temperature and drought. Scientific Reports 7, 43215. 28233854 PMC5324098
- Jin, H., Hu, W., Wei, Z., Wan, L., Li, G., Tan, G., Zhu, L. & He, G. (2008). Alterations in cytosine methylation and species‐specific transcription induced by interspecific hybridization between Oryza sativa and O. officinalis. Theoretical and Applied Genetics 117(8), 1271– 1279. 18719877
- Johnson, J. S., Cantrell, R. S., Cosner, C., Hartig, F., Hastings, A., Rogers, H. S., Schupp, E. W., Shea, K., Teller, B. J., Yu, X., Zurell, D. & Pufal, G. (2019). Rapid changes in seed dispersal traits may modify plant responses to global change. AoB Plants 11(3), plz020. 31198528 PMC6548345
- Jump, A. S. & Peñuelas, J. (2005). Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8(9), 1010– 1020. 34517682
- Karban, R. & Orrock, J. L. (2018). A judgment and decision‐making model for plant behavior. Ecology 99(9), 1909– 1919. 29893002
- Kawakatsu, T., Huang, S. C., Jupe, F., Sasaki, E., Schmitz, R. J., Urich, M. A., Castanon, R., Nery, J. R., Barragan, C., He, Y., Chen, H., Dubin, M., Lee, C.‐R., Wang, C., Bemm, F., et al. (2016). Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166(2), 492– 505. 27419873 PMC5172462
- Keller, T. E., Lasky, J. R. & Yi, S. V. (2016). The multivariate association between genomewide DNA methylation and climate across the range of Arabidopsis thaliana. Molecular Ecology 25(8), 1823– 1837. 26850505
- Kinoshita, T. & Seki, M. (2014). Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiology 55(11), 1859– 1863. 25298421
- Klupczyńska, E. A. & Ratajczak, E. (2021). Can forest trees cope with climate change?‐effects of DNA methylation on gene expression and adaptation to environmental change. International Journal of Molecular Science 22(24), 13524. PMC8703565 34948318
- Kumar, G., Rattan, U. K. & Singh, A. K. (2016). Chilling‐mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple (Malus x domestica Borkh.). PLoS One 11(2), e0149934. 26901339 PMC4763039
- Lafon‐Placette, C., Le Gac, A.‐L., Chauveau, D., Segura, V., Delaunay, A., Lesage‐Descauses, M.‐C., Hummel, I., Cohen, D., Jesson, B., Le Thiec, D., Bogeat‐Triboulot, M.‐B., Brignolas, F. & Maury, S. (2018). Changes in the epigenome and transcriptome of the poplar shoot apical meristem in response to water availability affect preferentially hormone pathways. Journal of Experimental Botany 69(3), 537– 551. 29211860
- Lamelas, L., Valledor, L., Escandón, M., Pinto, G., Cañal, M. J. & Meijón, M. (2020). Integrative analysis of the nuclear proteome in Pinus radiata reveals thermopriming coupled to epigenetic regulation. Journal of Experimental Botany 71(6), 2040– 2057. 31781741 PMC7094079
- Lang‐Mladek, C., Popova, O., Kiok, K., Berlinger, M., Rakic, B., Aufsatz, W., Jonak, C., Hauser, M. T. & Luschnig, C. (2010). Transgenerational inheritance and resetting of stress‐induced loss of epigenetic gene silencing in Arabidopsis. Molecular Plant 3(3), 594– 602. 20410255 PMC2877484
- * Le Gac, A.‐L., Lafon‐Placette, C., Chauveau, D., Segura, V., Delaunay, A., Fichot, R., Marron, N., Le Jan, I., Berthelot, A., Bodineau, G., Bastien, J.‐C., Brignolas, F. & Maury, S. (2018). Winter‐dormant shoot apical meristem in poplar trees shows environmental epigenetic memory. Journal of Experimental Botany 69(20), 4821– 4837. 30107545 PMC6137975
- Le Gac, A.‐L., Lafon‐Placette, C., Delaunay, A. & Maury, S. (2019). Developmental, genetic and environmental variations of global DNA methylation in the first leaves emerging from the shoot apical meristem in poplar trees. Plant Signaling & Behavior 14(6), 1596717. 30915897 PMC6546136
- Ledón‐Rettig, C. C. (2013). Ecological epigenetics: an introduction to the symposium. Integrative and Comparative Biology 53(2), 307– 318. 23696554
- Leida, C., Conesa, A., Llácer, G., Badenes, M. L. & Ríos, G. (2012). Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar‐dependent manner. New Phytologist 193(1), 67– 80. 21899556
- Li, R., Hu, F., Li, B., Zhang, Y., Chen, M., Fan, T. & Wang, T. (2020). Whole genome bisulfite sequencing methylome analysis of mulberry (Morus alba) reveals epigenome modifications in response to drought stress. Scientific Reports 10(1), 8013. 32415195 PMC7228953
- Li, S., Lin, Y. J., Wang, P., Zhang, B., Li, M., Chen, S., Shi, R., Tunlaya‐Anukit, S., Liu, X., Wang, Z., Dai, X., Yu, J., Zhou, C., Liu, B., Wang, J. P., et al. (2019). The AREB1 transcription factor influences histone acetylation to regulate drought responses and tolerance in Populus trichocarpa. Plant Cell 31(3), 663– 686. 30538157 PMC6482633
- Liang, D., Zhang, Z., Wu, H., Huang, C., Shuai, P., Ye, C. Y., Tang, S., Wang, Y., Yang, L., Wang, J., Yin, W. & Xia, X. (2014). Single‐base‐resolution methylomes of Populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genetics 15 Suppl 1(Suppl 1), S9. PMC4118614 25080211
- Lind, B. M., Menon, M., Bolte, C. E., Faske, T. M. & Eckert, A. J. (2018). The genomics of local adaptation in trees: are we out of the woods yet? Tree Genetics & Genomes 14(2), 29.
- Lira‐Medeiros, C. F., Parisod, C., Fernandes, R. A., Mata, C. S., Cardoso, M. A. & Ferreira, P. C. (2010). Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5(4), e10326. 20436669 PMC2859934
- Liu, C., Li, H., Lin, J., Wang, Y., Xu, X., Cheng, Z.‐M. & Chang, Y. (2018). Genome‐wide characterization of DNA demethylase genes and their association with salt response in Pyrus. Genes 9(8), 398. 30082643 PMC6116010
- Lloret, A., Badenes, M. L. & Ríos, G. (2018). Modulation of dormancy and growth responses in reproductive buds of temperate trees. Frontiers in Plant Science 9, 1368. 30271422 PMC6146825
- Lloret, A., Martínez‐Fuentes, A., Agustí, M., Badenes, M. L. & Ríos, G. (2017). Chromatin‐associated regulation of sorbitol synthesis in flower buds of peach. Plant Molecular Biology 95, 507– 517. 29038917
- Loarie, S. R., Duffy, P. B., Hamilton, H., Asner, G. P., Field, C. B. & Ackerly, D. D. (2009). The velocity of climate change. Nature 462(7276), 1052– 1055. 20033047
- Manning, K., Tör, M., Poole, M., Hong, Y., Thompson, A. J., King, G. J., Giovannoni, J. J. & Seymour, G. B. (2006). A naturally occurring epigenetic mutation in a gene encoding an SBP‐box transcription factor inhibits tomato fruit ripening. Nature Genetics 38(8), 948– 952. 16832354
- Marin, P., Genitoni, J., Barloy, D., Maury, S., Gibert, P., Ghalambor, C. K. & Vieira, C. (2020). Biological invasion: the influence of the hidden side of the (epi)genome. Functional Ecology 34(2), 385– 400.
- Martin, A., Troadec, C., Boualem, A., Rajab, M., Fernandez, R., Morin, H., Pitrat, M., Dogimont, C. & Bendahmane, A. (2009). A transposon‐induced epigenetic change leads to sex determination in melon. Nature 461(7267), 1135– 1138. 19847267
- Meyer, P. (2015). Epigenetic variation and environmental change. Journal of Experimental Botany 66(12), 3541– 3548. 25694547
- Mirouze, M., Reinders, J., Bucher, E., Nishimura, T., Schneeberger, K., Ossowski, S., Cao, J., Weigel, D., Paszkowski, J. & Mathieu, O. (2009). Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461(7262), 427– 430. 19734882
- Miryeganeh, M. (2021). Plants' epigenetic mechanisms and abiotic stress. Genes 12(8), 1106. 34440280 PMC8394019
- Miryeganeh, M. (2022). Mangrove forests: natural laboratories for studying epigenetic and climate changes. Frontiers in Plant Science 13, 85151518. PMC8915441 35283879
- Miryeganeh, M., Marlétaz, F., Gavriouchkina, D. & Saze, H. (2022). De novo genome assembly and in natura epigenomics reveal salinity‐induced DNA methylation in the mangrove tree Bruguiera gymnorhiza. New Phytologist 233(5), 2094– 2110. 34532854 PMC9293310
- Molnar, A., Melnyk, C. W., Bassett, A., Hardcastle, T. J., Dunn, R. & Baulcombe, D. C. (2010). Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328(5980), 872– 875. 20413459
- Mostafa, S., Wang, Y., Zeng, W. & Jin, B. (2022). Plant responses to herbivory, wounding, and infection. International Journal of Molecular Science 23(13), 7031. PMC9266417 35806046
- Mounger, J., Ainouche, M. L., Bossdorf, O., Cavé‐Radet, A., Li, B., Parepa, M., Salmon, A., Yang, J. & Richards, C. L. (2021). Epigenetics and the success of invasive plants. Philosophical Transactions of the Royal Society B: Biological Sciences 376(1826), 20200117. PMC8059582 33866809
- Muhammad, T., Zhang, F., Zhang, Y. & Liang, Y. (2019). RNA interference: a natural immune system of plants to counteract biotic stressors. Cells 8(1), 38. 30634662 PMC6356646
- Müller, K., Bouyer, D., Schnittger, A. & Kermode, A. R. (2012). Evolutionarily conserved histone methylation dynamics during seed life‐cycle transitions. PLoS One 7(12), e51532. 23240039 PMC3519861
- Neves, D. M., Almeida, L. A. H., Santana‐Vieira, D. D. S., Freschi, L., Ferreira, C. F., Soares Filho, W. S., Costa, M. G. C., Micheli, F., Coelho Filho, M. A. & Gesteira, A. S. (2017). Recurrent water deficit causes epigenetic and hormonal changes in citrus plants. Scientific Reports 7(1), 13684. 29057930 PMC5651809
- Niederhuth, C. E. & Schmitz, R. J. (2017). Putting DNA methylation in context: from genomes to gene expression in plants. Biochimica et Biophysica Acta (BBA)‐Gene Regulatory Mechanisms 1860(1), 149– 156. 27590871 PMC5203807
- Notarnicola, R. F., Nicotra, A. B., Kruuk, L. E. B. & Arnold, P. A. (2023). Effects of warming temperatures on germination responses and trade‐offs between seed traits in an alpine plant. Journal of Ecology 111(1), 62– 76.
- Ogneva, V. Z., Suprun, R. A., Dubrovina, S. A. & Kiselev, V. K. (2019). Effect of 5‐azacytidine induced DNA demethylation on abiotic stress tolerance in Arabidopsis thaliana. Plant Protection Science 55(2), 73– 80.
- Orr, A. J., Padovan, A., Kainer, D., Külheim, C., Bromham, L., Bustos‐Segura, C., Foley, W., Haff, T., Hsieh, J. F., Morales‐Suarez, A., Cartwright, R. A. & Lanfear, R. (2020). A phylogenomic approach reveals a low somatic mutation rate in a long‐lived plant. Proceedings: Biological Sciences 287(1922), 20192364. 32156194 PMC7126060
- Orsenigo, S., Abeli, T., Rossi, G., Bonasoni, P., Pasquaretta, C., Gandini, M. & Mondoni, A. (2015). Effects of autumn and spring heat waves on seed germination of high mountain plants. PLoS One 10(7), e0133626. 26197387 PMC4509759
- Osland, M. J., Stevens, P. W., Lamont, M. M., Brusca, R. C., Hart, K. M., Waddle, J. H., Langtimm, C. A., Williams, C. M., Keim, B. D., Terando, A. J., Reyier, E. A., Marshall, K. E., Loik, M. E., Boucek, R. E. & Lewis, A. B. (2021). Tropicalization of temperate ecosystems in North America: the northward range expansion of tropical organisms in response to warming winter temperatures. Global Change Biology 27(13), 3009– 3034. 33605004
- Pan, Y., Birdsey, R. A., Fang, J., Houghton, R., Kauppi, P. E., Kurz, W. A., Phillips, O. L., Shvidenko, A., Lewis, S. L., Canadell, J. G., Ciais, P., Jackson, R. B., Pacala, S. W., Mcguire, D. A. & Piao, S. (2011). A large and persistent carbon sink in the world's forests. Science 333(6045), 988– 993. 21764754
- Peng, H. & Zhang, J. (2009). Plant genomic DNA methylation in response to stresses: potential applications and challenges in plant breeding. Progress in Natural Science 19(9), 1037– 1045.
- Perrella, G., Bäurle, I. & van Zanten, M. (2022). Epigenetic regulation of thermomorphogenesis and heat stress tolerance. New Phytologist 234(4), 1144– 1160. 35037247
- Petit, R. J. & Hampe, A. (2006). Some evolutionary consequences of being a tree. Annual Review of Ecology, Evolution, and Systematics 37, 187– 214.
- Platt, A., Gugger, P. F., Pellegrini, M. & Sork, V. L. (2015). Genome‐wide signature of local adaptation linked to variable CpG methylation in oak populations. Molecular Ecology 24(15), 3823– 3830. 25951436
- Plitta‐Michalak, B. P., Naskret‐Barciszewska, M. Z., Kotlarski, S., Tomaszewski, D., Tylkowski, T., Barciszewski, J., Chmielarz, P. & Michalak, M. (2018). Changes in genomic 5‐methylcytosine level mirror the response of orthodox (Acer platanoides L.) and recalcitrant (Acer pseudoplatanus L.) seeds to severe desiccation. Tree Physiology 38(4), 617– 629. 29121348
- * Prudencio, Á. S., Werner, O., Martínez‐García, P. J., Dicenta, F., Ros, R. M. & Martínez‐Gómez, P. (2018). DNA methylation analysis of dormancy release in almond (Prunus dulcis) flower buds using epi‐genotyping by sequencing. International Journal of Molecular Science 19(11), 3542. PMC6274898 30423798
- Raj, S., Bräutigam, K., Hamanishi, E. T., Wilkins, O., Thomas, B. R., Schroeder, W., Mansfield, S. D., Plant, A. L. & Campbell, M. M. (2011). Clone history shapes Populus drought responses. Procedings of the National Academy of Science USA 108(30), 12521– 12526. PMC3145742 21746919
- Raju, S. K. K., Shao, M. R., Sanchez, R., Xu, Y. Z., Sandhu, A., Graef, G. & Mackenzie, S. (2018). An epigenetic breeding system in soybean for increased yield and stability. Plant Biotechnology Journal 16(11), 1836– 1847. 29570925 PMC6181216
- Ramirez‐Prado, J. S., Abulfaraj, A. A., Rayapuram, N., Benhamed, M. & Hirt, H. (2018). Plant immunity: from signaling to epigenetic control of defense. Trends in Plant Science 23(9), 833– 844. 29970339
- Reinders, J., Wulff, B. B. H., Mirouze, M., Marí‐Ordóñez, A., Dapp, M., Rozhon, W., Bucher, E., Theiler, G. & Paszkowski, J. (2009). Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes & Development 23(8), 939– 950. 19390088 PMC2675864
- Rey, O., Eizaguirre, C., Angers, B., Baltazar‐Soares, M., Sagonas, K., Prunier, J. G. & Blanchet, S. (2020). Linking epigenetics and biological conservation: towards a conservation epigenetics perspective. Functional Ecology 34(2), 414– 427.
- Reyna‐López, G. E., Simpson, J. & Ruiz‐Herrera, J. (1997). Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Molecular and General Genetics 253(6), 703– 710. 9079881
- Richards, C. L., Alonso, C., Becker, C., Bossdorf, O., Bucher, E., Colomé‐Tatché, M., Durka, W., Engelhardt, J., Gaspar, B. & Gogol‐Döring, A. (2017). Ecological plant epigenetics: evidence from model and non‐model species, and the way forward. Ecology Letters 20(12), 1576– 1590. 29027325
- Richards, E. J. (2011). Natural epigenetic variation in plant species: a view from the field. Current Opinion in Plant Biolgy 14(2), 204– 209. 21478048
- Rico, L., Ogaya, R., Barbeta, A. & Peñuelas, J. (2014). Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Plant Biology 16(2), 419– 427. 23889779
- * Rothkegel, K., Sandoval, P., Soto, E., Ulloa, L., Riveros, A., Lillo‐Carmona, V., Cáceres‐Molina, J., Almeida, A. M. & Meneses, C. (2020). Dormant but active: chilling accumulation modulates the epigenome and transcriptome of Prunus avium during bud dormancy. Frontiers in Plant Science. 17, 1115. PMC7380246 32765576
- Rubi, T. L., Knowles, L. L. & Dantzer, B. (2020). Museum epigenomics: characterizing cytosine methylation in historic museum specimens. Molecular Ecology Resources 20(5), 1161– 1170. 31682062
- Santamaría, M., Hasbún, R., Valera, M., Meijón, M., Valledor, L., Rodríguez, J. L., Toorop, P. E., Cañal, M. & Rodríguez, R. (2009). Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa. Journal of Plant Physiology 166(13), 1360– 1369. 19376609
- Schmitz, R. J. & Ecker, J. R. (2012). Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends in Plant Science 17(3), 149– 154. 22342533 PMC3645451
- Singh, D., Chaudhary, P., Taunk, J., Kumar, S. C., Sharma, S., Singh, V. J., Singh, D., Chinnusamy, V., Yadav, R. & Pal, M. (2021). Plant epigenomics for extenuation of abiotic stresses: challenges and future perspectives. Journal of Experimental Botany 72(20), 6836– 6855. 34302734
- Sollars, E. S. A. & Buggs, R. J. A. (2018). Genome‐wide epigenetic variation among ash trees differing in susceptibility to a fungal disease. BMC Genomics 19(1), 502. 29954338 PMC6022711
- Sow, M. D., Segura, V., Chamaillard, S., Jorge, V., Delaunay, A., Lafon‐Placette, C., Fichot, R., Faivre‐Rampant, P., Villar, M., Brignolas, F. & Maury, S. (2018 b). Narrow‐sense heritability and PST estimates of DNA methylation in three Populus nigra L. populations under contrasting water availability. Tree Genetics & Genomes 14(5), 78.
- Takamiya, T., Hosobuchi, S., Noguchi, T., Asai, K., Nakamura, E., Habu, Y., Paterson, A. H., Iijima, H., Murakami, Y. & Okuizumi, H. (2008). Inheritance and alteration of genome methylation in F1 hybrid rice. Electrophoresis 29(19), 4088– 4095. 18958879
- * Tang, X., Wang, Q., Yuan, H. & Huang, X. (2018). Chilling‐induced DNA demethylation is associated with the cold tolerance of Hevea brasiliensis. BMC Plant Biology 18, 70. 29685105 PMC5913804
- Teskey, R., Wertin, T., Bauweraerts, I., Ameye, M., McGuire, M. A. & Steppe, K. (2015). Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment 38(9), 1699– 1712. 25065257
- Usui, T., Lerner, D., Eckert, I., Angert, A. L., Garroway, C. J., Hargreaves, A., Lancaster, L. T., Lessard, J. P., Riva, F., Schmidt, C., van der Burg, K. & Marshall, K. E. (2023). The evolution of plasticity at geographic range edges. Trends in Ecology and Evolution 38(9), 831– 842. 37183152
- Uthup, T. K., Ravindran, M., Bini, K. & Thakurdas, S. (2011). Divergent DNA methylation patterns associated with abiotic stress in Hevea brasiliensis. Molecular Plant 4(6), 996– 1013. 21705581
- van Gurp, T. P., Wagemaker, N. C., Wouters, B., Vergeer, P., Ouborg, J. N. & Verhoeven, K. J. (2016). epiGBS: reference‐free reduced representation bisulfite sequencing. Nature Methods 13(4), 322– 324. 26855363
- * Viejo, M., Tengs, T., Yakovlev, I., Cross, H., Krokene, P., Olsen, J. E. & Fossdal, C. G. (2023). Epitype‐inducing temperatures drive DNA methylation changes during somatic embryogenesis in the long‐lived gymnosperm Norway spruce. Frontiers in Plant Science 14, 1196806. 37546277 PMC10399239
- Walck, J. L., Hidayati, S. N., Dixon, K. W., Thompson, K. E. N. & Poschlod, P. (2011). Climate change and plant regeneration from seed. Global Change Biology 17(6), 2145– 2161.
- Wilkinson, S. W., Magerøy, M. H., López Sánchez, A., Smith, L. M., Furci, L., Cotton, T. E. A., Krokene, P. & Ton, J. (2019). Surviving in a hostile world: plant strategies to resist pests and diseases. Annual Review of Phytopathology 57(1), 505– 529. 31470772
- Xiao, D., Zhou, K., Yang, X., Yang, Y., Ma, Y. & Wang, Y. (2021). Crosstalk of DNA methylation triggered by pathogen in poplars with different resistances. Frontiers in Microbioogyl 12, 750089. PMC8748266 35027912
- * Xu, J., Zhou, S., Gong, X., Song, Y., van Nocker, S., Ma, F. & Guan, Q. (2018). Single‐base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnology Journal 16(2), 672– 687. 28796917 PMC5787839
- Yakovlev, I. A., Carneros, E., Lee, Y., Olsen, J. E. & Fossdal, C. G. (2016). Transcriptional profiling of epigenetic regulators in somatic embryos during temperature induced formation of an epigenetic memory in Norway spruce. Planta 243(5), 1237– 1249. 26895338
- Yakovlev, I. A., Lee, Y., Rotter, B., Olsen, J. E., Skrøppa, T., Johnsen, Ø. & Fossdal, C. G. (2014). Temperature‐dependent differential transcriptomes during formation of an epigenetic memory in Norway spruce embryogenesis. Tree Genetics & Genomes 10(2), 355– 366.
- Yamane, H., Singh, A. K. & Cooke, J. E. K. (2021). Plant Dormancy Research: From Environmental Control to Molecular Regulatory Networks, Tree Physiology 41(4), 523– 528. 33834235
- Yan, L., Fan, G. & Li, X. (2019). Genome‐wide analysis of three histone marks and gene expression in Paulownia fortunei with phytoplasma infection. BMC Genomics 20(1), 234. 30898112 PMC6429711
- Yong‐Villalobos, L., González‐Morales, S. I., Wrobel, K., Gutiérrez‐Alanis, D., Cervantes‐Peréz, S. A., Hayano‐Kanashiro, C., Oropeza‐Aburto, A., Cruz‐Ramírez, A., Martínez, O. & Herrera‐Estrella, L. (2015). Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proceedings of the National Academy of Sciences 112(52), E7293– E7302. PMC4702951 26668375
- Yu, Q., Liu, S., Yu, L., Xiao, Y., Zhang, S., Wang, X., Xu, Y., Yu, H., Li, Y. & Yang, J. (2021). RNA demethylation increases the yield and biomass of rice and potato plants in field trials. Nature Biotechnology 39(12), 1581– 1588. 34294912
- Yu, W. H., Zhang, L. M., Luo, F. L., Yu, F. H. & Li, M. H. (2022). Roles of clonal parental effects in regulating interspecific competition between two floating plants. Frontiers in Plant Science 13, 924001. 35937331 PMC9355590
- Zemach, A., McDaniel, I. E., Silva, P. & Zilberman, D. (2010). Genome‐wide evolutionary analysis of eukaryotic DNA methylation. Science 328(5980), 916– 919. 20395474
- Zeng, F. S., Zhou, S., Zhan, Y. G. & Dong, J. (2014). Drought resistance and DNA methylation of interspecific hybrids between Fraxinus mandshurica and Fraxinus americana. Trees 28(6), 1679– 1692.
- Zeng, Y. & Kermode, A. R. (2004). A gymnosperm ABI3 gene functions in a severe abscisic acid‐insensitive mutant of Arabidopsis (abi3‐6) to restore the wild‐type phenotype and demonstrates a strong synergistic effect with sugar in the inhibition of post‐germinative growth. Plant Molecular Biology 56, 731– 746. 15803411
- Zeng, Y., Raimondi, N. & Kermode, A. R. (2003). Role of an ABI3 homologue in dormancy maintenance of yellow‐cedar seeds and in the activation of storage protein and Em gene promoters. Plant Molecular Biology 51(1), 39– 49. 12602889
- Zhang, H., Lang, Z. & Zhu, J. K. (2018). Dynamics and function of DNA methylation in plants. Nature Reviews Molecular Cell Biology 19(8), 489– 506. 29784956
- Zhang, M. S., Yan, H. Y., Zhao, N., Lin, X. Y., Pang, J. S., Xu, K. Z., Liu, L. X. & Liu, B. (2007). Endosperm‐specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) inter‐strain hybrids. Theoretical and Applied Genetics 115(2), 195– 207. 17486309
- Zhang, R., Jongejans, E. & Shea, K. (2011). Warming increases the spread of an invasive thistle. PLoS One 6(6), e21725. 21738779 PMC3126854
- Zhao, J., Lu, Z., Wang, L. & Jin, B. (2020). Plant responses to heat stress: physiology, transcription, noncoding RNAs, and epigenetics. International Journal of Molecular Science 22(1), 117. PMC7795586 33374376
- *Zhou, J., Xiao, L., Huang, R., Song, F., Li, L., Li, P., Fang, Y., Lu, W., Lv, C., Quan, M., Zhang, D. & Du, Q. (2023). Local diversity of drought resistance and resilience in Populus tomentosa correlates with the variation of DNA methylation. Plant Cell Environment 46(2), 479– 497. 36385613
- * Zhu, H., Chen, P. Y., Zhong, S., Dardick, C., Callahan, A., An, Y.‐Q., van Knocker, S., Yang, Y., Zhong, G.‐Y., Abbott, A. & Liu, Z. (2020). Thermal‐responsive genetic and epigenetic regulation of DAM cluster controlling dormancy and chilling requirement in peach floral buds. Horticulture Research 7, 114. 32821397 PMC7395172
- Zhu, K., Woodall, C. W. & Clark, J. S. (2012). Failure to migrate: lack of tree range expansion in response to climate change. Global Change Biology 18(3), 1042– 1052.
- Authors
- Miryeganeh, M., & Armitage, D. W.
- Affiliations
- Okinawa Institute of Science and Technology Graduate University (JP)
- Corresponding author
- Miryeganeh, Matin
- ORCID
- Miryeganeh, Matin
- Venue
- Biological Reviews
- Publisher
- Wiley
- Published
- 2024-08-27
- Volume
- 100
- Issue
- 1
- Pages
- 131-148
- ISSN
- 0006-3231 (ISSN-L)
- 1464-7931
- 1469-185X
- PMC
- PMC11718629
- OpenAlex
- W4401967606
- Cited by
- 44
- References
- 170
- Citations by year
- 2026: 24 · 2025: 20
- FWCI
- 1.80
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Biological reviews/Biological reviews of the Cambridge Philosophical Society (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Okinawa Institute of Science and Technology Graduate University (Okinawa Institute of Science and Technology Graduate University) (submittedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc-nd)
- Funders
- Fusion Oriented REsearch for disruptive Science and Technology (JPMJFR224G)
- Okinawa Institute of Science and Technology Graduate University
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Keywords
- plant epigenetics, phenotypic plasticity, trees, climate change adaptation, drought tolerance, heat tolerance, salt tolerance, dormancy, seed dispersal, transgenerational epigenetic inheritance, stress memory, DNA methylation, histone modifications, non-coding RNA, long-lived species, extinction risk, population management
- MeSH terms
- Adaptation, Physiological, Stress, Physiological, Trees, Epigenesis, Genetic, Climate Change
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