Abstract
Change is a constant in life, and being able to respond to change is essential for every living being. This may be especially true for sessile long-lived perennials with a complex life cycle like trees. In order to synchronize developmental decisions, growth, and performance with prevailing conditions, a precise interpretation of the given, usually static, genome is therefore of particular importance. Here, the epigenome, a fascinating, metastable layer of genome regulation, emerges as a central player. The epigenome integrates internal and external information into existing gene regulatory circuits allowing to shape development and tree responses to the environment. The epigenome comprises a set of modifications to DNA and its associated components that regulate genome function via chromatin modulation without changing the underlying DNA sequence. Epigenetic marks are not necessarily a temporary feature. They can be transmitted faithfully across cell divisions or even generations, thus retaining and passing on information. Here, we compile and integrate the gradually increasing body of knowledge on epigenome plasticity and epigenetic regulation in Populus. We focus on examples for epigenetic contributions to genome-encoded and environmentally modulated processes in development related to organ formation, growth regulation, and sex determination. Recent advances in technologies may spur further interest and hold promise for new insights into the exquisite epigenetic regulation of genome function in complex woody plants.
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References
Akagi T, Henry IM, Tao R, Comai L (2014) Plant genetics. A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science 346:646–650. https://doi.org/10.1126/science.1257225
Akagi T, Henry IM, Kawai T, Comai L, Tao R (2016) Epigenetic regulation of the sex determination gene MeGI in polyploid persimmon. Plant Cell 28:2905–2915. https://doi.org/10.1105/tpc.16.00532
Akagi T, Henry IM, Ohtani H, Morimoto T, Beppu K, Kataoka I, Tao R (2018) A Y-encoded suppressor of feminization arose via lineage-specific duplication of a cytokinin response regulator in kiwifruit. Plant Cell 30:780–795. https://doi.org/10.1105/tpc.17.00787
Azeez A, Zhao YC, Singh RK, Yordanov YS, Dash M, Miskolczi P, Stojkovič K, Strauss SH, Bhalerao RP, Busov VB (2021) EARLY BUD-BREAK 1 and EARLY BUD-BREAK 3 control resumption of poplar growth after winter dormancy. Nat Commun 12:1123. https://doi.org/10.1038/s41467-021-21449-0
Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman T-L, Hahn MW, Kitano J, Mayrose I, Ming R, Perrin N, Ross L, Valenzuela N, Vamosi JC, The Tree of Sex Consortium (2014) Sex determination: why so many ways of doing it? PLoS Biol 12:e1001899. https://doi.org/10.1371/journal.pbio.1001899
Baker M (2011) Making sense of chromatin states. Nat Methods 8:717–722. https://doi.org/10.1038/nmeth.1673
Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395. https://doi.org/10.1038/cr.2011.22
Bewick AJ, Niederhuth CE, Ji L, Rohr NA, Griffin PT, Leebens-Mack J, Schmitz RJ (2017) The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants. Genome Biol 18:65. https://doi.org/10.1186/s13059-017-1195-1
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. https://doi.org/10.1126/science.1126038
Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115. https://doi.org/10.1111/j.1461-0248.2007.01130.x
Bräutigam K, Cronk Q (2018) DNA methylation and the evolution of developmental complexity in plants. Front Plant Sci 9:1447. https://doi.org/10.3389/fpls.2018.01447
Bräutigam K, Soolanayakanahally R, Champigny M, Mansfield S, Douglas C, Campbell MM, Cronk Q (2017) Sexual epigenetics: gender-specific methylation of a gene in the sex determining region of Populus balsamifera. Sci Rep 7:45388. https://doi.org/10.1038/srep45388
Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Gutierrez Marcos J, Fluch S, Fernandez Fraga M, Angeles Guevara M, Abarca D, Johnsen O, Maury S, Strauss SH, Campbell MM, Rohde A, Diaz-Sala C, Cervena M-T (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3:399–415. https://doi.org/10.1002/ece3.461
Chen Y, Tong S, Jiang Y, Ai F, Feng Y, Zhang J, Gong J, Qin J, Zhang Y, Zhu Y, Liu J, Ma T (2021) Transcriptional landscape of highly lignified poplar stems at single-cell resolution. Genome Biol 22:319. https://doi.org/10.1186/s13059-021-02537-2
Conde D, le Gac AL, Perales M, Dervinis C, Kirst M, Maury S, Gonzalez-Melendi P, Allona I (2017a) Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud break. Plant Cell Environ 40:2236–2249. https://doi.org/10.1111/pce.13019
Conde D, Moreno-Cortés A, Dervinis C, Ramos-Sanchez JM, Kirst M, Perales M, Gonzalez-Melendi P, Allona I (2017b) Overexpression of DEMETER, a DNA demethylase, promotes early apical bud maturation in poplar. Plant Cell Environ 40:2806–2819. https://doi.org/10.1111/pce.13056
Cronk Q, Soolanayakanahally R, Bräutigam K (2020) Gene expression trajectories during male and female reproductive development in balsam poplar (Populus balsamifera L.). Sci Rep 10:8413. https://doi.org/10.1038/s41598-020-64938-w
Erdmann RM, Picard CL (2020) RNA-directed DNA Methylation. PLoS Genet 16:e1009034. https://doi.org/10.1371/journal.pgen.1009034
Feng S, Cokus SJ, Zhang X, Chen P-Y, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Haplern ME, Ukomadu C, Sadler KC, Pradhan S, Pellegrini M, Jacobsen SE (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107:8689–8694. https://doi.org/10.1073/pnas.1002720107
Gao J, Ni X, Li H, Hayat F, Shi T, Gao Z (2021) MiR169 and PmRGL2 synergistically regulate the NF-Y complex to activate dormancy release in Japanese apricot (Prunus mume Sieb. et Zucc.). Plant Mol Biol 105:83–97. https://doi.org/10.1007/s11103-020-01070-3
Geraldes A, Hefer CA, Capron A, Kolosova N, Martinez-Nunez F, Soolanayakanahally RY, Stanton B, Guy RD, Mansfield SD, Douglas CJ, Cronk QCB (2015) Recent y chromosome divergence despite ancient origin of dioecy in poplars (Populus). Mol Ecol 24:3243–3256. https://doi.org/10.1111/mec.13126
Gómez-Soto D, Ramos-Sánchez JM, Alique D, Conde D, Triozzi PM, Perales M, Allona I (2021) Overexpression of a SOC1-related gene promotes bud break in ecodormant poplars. Front Plant Sci 12:670497. https://doi.org/10.3389/fpls.2021.670497
Han SK, Wu MF, Cui S, Wagner D (2015) Roles and activities of chromatin remodeling ATPases in plants. Plant J 83:62–77. https://doi.org/10.1111/tpj.12877
Hofmeister BT, Denkena J, Colomé-Tatché M, Shahryary Y, Hazarika R, Grimwood J, Mamidi S, Jenkins J, Grabowski PP, Sreedasyam A, Shu S, Barry K, Lail K, Adam C, Lipzen A, Sorek R, Kudrna D, Talag J, Wing R, Hall DW, Jacobsen D, Tuskan GA, Schmutz J, Johannes F, Schmitz RJ (2020) A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa. Genome Biol 21:259. https://doi.org/10.1186/s13059-020-02162-5
Hou X, Zhou J, Liu C, Liu L, Shen L, Yu H (2014) Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis. Nat Commun 5:4601. https://doi.org/10.1038/ncomms5601
Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH (2015) Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Front Plant Sci 6:989. https://doi.org/10.3389/fpls.2015.00989
Huang Y, Chen DH, Liu B-Y, Shen W-H, Ruan Y (2017) Conservation and diversification of polycomb repressive complex 2 (PRC2) proteins in the green lineage. Brief Funct Genomics 16:106–119. https://doi.org/10.1093/bfgp/elw007
Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129. https://doi.org/10.1242/dev.063511
IPCC (2021) Summary for policymakers. In: Masson-Delmotte V et al. (eds) Climate change 2021: The physical science basis. contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press
Janoušek B, Siroký J, Vyskot B (1996) Epigenetic control of sexual phenotype in a dioecious plant, Melandrium album. Mol Gen Genet 250:483–490. https://doi.org/10.1007/BF02174037
Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski J, Albuisson A, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530. https://doi.org/10.1371/journal.pgen.1000530
Karlberg A, Englund M, Petterle A, Molnar G, Sjödin A, Bako L, Bhalerao RP (2010) Analysis of global changes in gene expression during activity-dormancy cycle in hybrid aspen apex. Plant Biotechnol 27:1–16. https://doi.org/10.5511/plantbiotechnology.27.1
Kersten B, Pakull B, Groppe K, Lueneburg J, Fladung M (2014) The sex-linked region in Populus tremuloides Turesson 141 corresponds to a pericentromeric region of about two million base pairs on P. trichocarpa chromosome 19. Plant Biol 16:411–418. https://doi.org/10.1111/plb.12048
Khadka J, Yadav NS, Guy M, Grafi G, Golan-Goldhirsh A (2019) Epigenetic aspects of floral homeotic genes in relation to sexual dimorphism in the dioecious plant Mercurialis annua. J Exp Bot 70:6245–6259. https://doi.org/10.1093/jxb/erz379
Kornberg RD (1974) Chromatin structure: A repeating unit of histones and DNA. Science 184:868–871. https://doi.org/10.1126/science.184.4139.868
Ku WL, Nakamura K, Gao W, Cui K, Hu G, Tang Q, Ni B, Zhao K (2019) Single-cell chromatin immunocleavage sequencing (scChIC-seq) to profile histone modification. Nat Methods 16:323–325. https://doi.org/10.1038/s41592-019-0361-7
Le Gac AL, 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. J Exp Bot 69:4821–4837. https://doi.org/10.1093/jxb/ery271
Lei L, Zhou SL, Ma H, Zhang LS (2012) Expansion and diversification of the SET domain gene family following whole-genome duplications in Populus trichocarpa. BMC Evol Biol 12:51. https://doi.org/10.1186/1471-2148-12-51
Lester DT (1963) Variation in sex expression in Populus tremuloides Michx. Silvae Genetica 12:141–152
Liang Z, Shen L, Cui X, Bao S, Geng Y, Yu G, Liang F, Xie S, Lu T, Gu X, Yu H (2018) DNA N6-adenine methylation in Arabidopsis thaliana. Dev Cell 45:406-416.e3. https://doi.org/10.1016/j.devcel.2018.03.012
Liao X, Li Y, Hu Z, Lin Y, Zheng B, Ding J (2021) Poplar acetylome profiling reveals lysine acetylation dynamics in seasonal bud dormancy release. Plant Cell Environ 44:1830–1845. https://doi.org/10.1111/pce.14040
Lloyd JPB, Lister R (2022) Epigenome plasticity in plants. Nat Rev Genet 23(1):55–68. https://doi.org/10.1038/s41576-021-00407-y
Luger K, Der Mä AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260. https://doi.org/10.1038/38444
Ma XJ, Yang CP, Xia DA (2016) Characterization and expression analysis of histone deacetylases family RPD3/HDA1 in Populus trichocarpa. Biol Plant 60:235–243. https://doi.org/10.1007/s10535-015-0579-x
Mattiroli F, Penengo L (2021) Histone ubiquitination: an integrative signaling platform in genome stability. Trends Genet 37:566–581. https://doi.org/10.1016/j.tig.2020.12.005
Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408. https://doi.org/10.1038/nrg3683
Maurya JP, Bhalerao RP (2017) Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: A molecular perspective. Ann Bot 120:351–360. https://doi.org/10.1093/aob/mcx061
McKown AD, Klápště J, Guy RD, Soolanayakanahally RY, La Mantia J, Porth I, Skyba O, Unda F, Douglas CJ, El-Kassaby YA, Hamelin RC, Mansfield SD, Cronk QCB (2017) Sexual homomorphism in dioecious trees: extensive tests fail to detect sexual dimorphism in Populus. Sci Rep 7:1831. https://doi.org/10.1038/s41598-017-01893-z
Melnikova NV, Pushkova EN, Dvorianinova EM, Beniaminov AD, Novakovskiy RO, Povkhova LV, Bolsheva NL, Snezhkina AV, Kudryavtseva A, Krasnov GS, Dimitriev AA (2021) Genome assembly and sex-determining region of male and female Populus × sibirica. Front Plant Sci 12:625416. https://doi.org/10.3389/fpls.2021.625416
Mohamed R, Wang CT, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng X, Meilan R, Strauss SH, Brunner AM (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688. https://doi.org/10.1111/j.1365-313X.2010.04185.x
Müller NA, Kersten B, Leite Montalvão AP, Mähler N, Bernhardsson C, Bräutigam K, Carracedo Lorenzo Z, Hoenicka H, Kumar V, Mader M, Pakull B, Robinson KM, Sabatti M, Vettori C, Ingvarsson PK, Cronk Q, Street NR, Fladung M (2020) A single gene underlies the dynamic evolution of poplar sex determination. Nat Plants 6:630–637. https://doi.org/10.1038/s41477-020-0672-9
Ni J, Shah FA, Liu W, Wang Q, Wang D, Zhao W, Lu W, Huang S, Fu S, Wu L (2018) Comparative transcriptome analysis reveals the regulatory networks of cytokinin in promoting the floral feminization in the oil plant Sapium sebiferum. BMC Plant Biol 18:96. https://doi.org/10.1186/s12870-018-1314-5
Novotná K, Štochlová P (2013) Aspects of sexual reproduction in rare monoecious Populus nigra var. nigra trees. Silvae Genetica 62:117–124. https://doi.org/10.1515/sg-2013-0015
Ntorla A, Burgoyne JR (2021) The regulation and function of histone crotonylation. Front Cell Develop Biol 9:624914. https://doi.org/10.3389/fcell.2021.624914
Pakull B, Groppe K, Meyer M, Markussen T, Fladung M (2009) Genetic linkage mapping in aspen (Populus tremula L. and Populus tremuloides Michx.). Tree Genet Genomes 5:505–515. https://doi.org/10.1007/s11295-009-0204-2
Petterle A (2011) ABA and chromatin remodelling regulate the activity-dormancy cycle in hybrid aspen. Doctoral Thesis, Swedish University of Agricultural Sciences
Potkar R, Recla J, Busov V (2013) Ptr-MIR169 is a posttranscriptional repressor of PtrHAP2 during vegetative bud dormancy period of aspen (Populus tremuloides) trees. Biochem Biophys Res Commun 431:512–518. https://doi.org/10.1016/j.bbrc.2013.01.027
Puzey JR, Karger A, Axtell M, Kramer EM (2012) Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS ONE 7:e33034. https://doi.org/10.1371/journal.pone.0033034
Qi YL, Xue LJ, El-Kassaby YA, Guo Y (2022) Identification and comparative analysis of conserved and species-specific microRNAs in four Populus sections. Forests 13:873. https://doi.org/10.3390/f13060873
Reinders J, Wulff BBH, Mirouze M, Moari-Ordonez 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 Dev 23:939–950. https://doi.org/10.1101/gad.524609
Ríos G, Leida C, Conejero A, Badenes ML (2014) Epigenetic regulation of bud dormancy events in perennial plants. Front Plant Sci 5:247. https://doi.org/10.3389/fpls.2014.00247
Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L, Giraut L, Despres B, Drevensek S, Barneche F, Derozier S, Brunaud V, Aubourg S, Schnittger A, Bowler C, Martin-Magniette M-L, Robin S, Caboche M, Colot V (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938. https://doi.org/10.1038/emboj.2011.103
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. https://doi.org/10.1105/tpc.107.052811
Santamaría ME, Hasbún R, Valera MJ, Meijon M, Valledor L, Rodriguez JL, Toorop PE, Canal MJ, Rodriguez 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. https://doi.org/10.1016/j.jplph.2009.02.014
Scheid R, Chen J, Zhong X (2021) Biological role and mechanism of chromatin readers in plants. Curr Opin Plant Biol 61:102008. https://doi.org/10.1016/j.pbi.2021.102008
Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693
Shim D, Ko JH, Kim WC, Wang Q, Keathley DE, Han K-H (2014) A molecular framework for seasonal growth-dormancy regulation in perennial plants. Hortic Res 1:14059. https://doi.org/10.1038/hortres.2014.59
Song Y, Tian M, Ci D, Zhang D (2015) Methylation of microRNA genes regulates gene expression in bisexual flower development in andromonoecious poplar. J Exp Bot 66(7):1891–1905. https://doi.org/10.1093/jxb/eru531
Sow MD, le Gac AL, Fichot R, Lanciano S, Delaunay A, Le Jan I, Lasage-Descauses M-C, Cisterne S, Caius J, Brunaud V, Soubigou-Taconnat L, Cochard H, Segure V, Chaparro C, Grunau C, Daviaud C, Tost J, Brignolas F, Strauss SH, Mirouze M, Maury S (2021) RNAi suppression of DNA methylation affects the drought stress response and genome integrity in transgenic poplar. New Phytol 232:80–97. https://doi.org/10.1111/nph.17555
Stettler R (1971) Variation in sex expression of black cottonwood and related hybrids. Silvae Genetica 20:42–46
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. https://doi.org/10.1186/1471-2164-13-27
Waititu JK, Zhang C, Liu J, Wang H (2020) Plant non-coding RNAs: origin, biogenesis, mode of action and their roles in abiotic stress. Int J Mol Sci 21:8401. https://doi.org/10.3390/ijms21218401
Xue L, Wu H, Chen Y, Li X, Hou J, Lu J, Wei S, Dai X, Olson MS, Liu J, Wang M, Charlesworth D, Yin T (2020) Evidences for a role of two Y-specific genes in sex determination in Populus deltoides. Nat Commun 11:5893. https://doi.org/10.1038/s41467-020-19559-2
Zhang TQ, Xu ZG, Shang GD, Wang JW (2019) A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol Plant 12:648–660. https://doi.org/10.1016/j.molp.2019.04.004
Zhao S, Allis CD, Wang GG (2021) The language of chromatin modification in human cancers. Nat Rev Cancer 21:413–430. https://doi.org/10.1038/s41568-021-00357-x
Zhao Y, Garcia BA (2015) Comprehensive catalog of currently documented histone modifications. Cold Spring Harb Perspect Biol 7:a025064. https://doi.org/10.1101/cshperspect.a025064
Zhou R, Macaya-Sanz D, Carlson CH, Schmutz J, Jenkins JW, Kudrna D, Sharma A, Sandor L, Shu S, Barry K, Tuskan GA, Ma T, Liu J, Olson M, Smart LB, DiFazio SP (2020a) A willow sex chromosome reveals convergent evolution of complex palindromic repeats. Genome Biol 21:38. https://doi.org/10.1186/s13059-020-1952-4
Zhou R, Macaya-Sanz D, Schmutz J, Jenkins JW, Tuskan GA, DiFazio SP (2020b) Sequencing and analysis of the sex determination region of Populus trichocarpa. Genes (basel) 11:843. https://doi.org/10.3390/genes11080843
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Nunez-Martinez, O.F., Jones, L.M., Bräutigam, K. (2024). Epigenetic Regulation of Genome Function in Populus. In: Porth, I., Klápště, J., McKown, A. (eds) The Poplar Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-031-50787-8_3
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