Although epigenetic modifications have been intensely investigated over the last decade due to their role in crop adaptation to rapid climate change, it is unclear which epigenetic changes are heritable and therefore transmitted to their progeny. The identification of epigenetic marks that are transmitted to the next generations is of primary importance for their use in breeding and for the development of new cultivars with a broad-spectrum of tolerance/resistance to abiotic and biotic stresses. In this review, we discuss general aspects of plant responses to environmental stresses and provide an overview of recent findings on the role of transgenerational epigenetic modifications in crops. In addition, we take the opportunity to describe the aims of EPI-CATCH, an international COST action consortium composed by researchers from 28 countries. The aim of this COST action launched in 2020 is: (1) to define standardized pipelines and methods used in the study of epigenetic mechanisms in plants, (2) update, share, and exchange findings in epigenetic responses to environmental stresses in plants, (3) develop new concepts and frontiers in plant epigenetics and epigenomics, (4) enhance dissemination, communication, and transfer of knowledge in plant epigenetics and epigenomics.

Center of Biological Research Margarita Salas CIB CSIC Ramiro de Maeztu 9 28040 Madrid Spain

Centre for Environmental and Marine Studies Biology Department Campus de Santiago University of Aveiro 3810 193 Aveiro Portugal

Chair of Photogrammetry and Remote Sensing Faculty of Geodesy University of Zagreb 10000 Zagreb Croatia

Department of Agricultural Sciences Biotechnology and Food Science Cyprus University of Technology Lemesos 3036 Cyprus

Department of Biology University of Florence 50019 Sesto Fiorentino Italy

Department of Molecular Biology and Genetics Institute of Plant Physiology and Genetics Bulgarian Academy of Sciences Acad Georgi Bonchev Str Bldg 21 1113 Sofia Bulgaria

Department of Vitis Institute of Olive Tree Subtropical Crops and Viticulture Sofokli Venizelou 1 Lykovrysi 14123 Athens Greece

Faculty of Agriculture University of Novi Sad Sq Dositeja Obradovića 8 21000 Novi Sad Serbia

Genebank Department Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben 06466 Seeland Germany

Genomic Research Department Thünen Institute of Forest Genetics 22927 Grosshansdorf Germany

INRAe EA1207 USC1328 Laboratoire de Biologie des Ligneux et des Grandes Cultures Université d'Orléans 45067 Orléans France

Institute of Molecular Cell and Systems Biology College of Medical Veterinary and Life Sciences University of Glasgow Glasgow G12 8QQ UK

Israel Oceanographic and Limnological Research The National Center for Mariculture P O B 1212 Eilat 88112 Israel

Laboratory for Biotechnology Institute of Field and Vegetable Crops Maksima Gorkog 30 21000 Novi Sad Serbia

Laboratory for Plant Physiology Department for Biology Faculty of Science University of Sarajevo 71000 Sarajevo Bosnia and Herzegovina

Laboratory of Plant Breeding and Biometry Department of Crop Science Agricultural University of Athens Iera Odos 75 11855 Athens Greece

Laboratory of Range Science School of Agriculture Forestry and Natural Environment Aristotle University of Thessaloniki 54124 Thessaloniki Greece

Mendeleum Insitute of Genetics Faculty of Horticulture Mendel University in Brno Valtická 334 69144 Lednice Czech Republic

UMR Ecophysiologie et Génomique Fonctionnelle de la Vigne Université de Bordeaux INRAE Bordeaux Science Agro 210 Chemin de Leysotte CS5000833882 Villenave d'Ornon 33076 Bordeaux France

Zobrazit více v PubMed

Crisp P.A., Ganguly D., Eichten S.R., Borevitz J.O., Pogson B.J. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2016;2:e1501340. doi: 10.1126/sciadv.1501340. PubMed DOI PMC

Lamke J., Brzezinka K., Baurle I. HSFA2 orchestrates transcriptional dynamics after heat stress in Arabidopsis thaliana. Transcription. 2016;7:111–114. doi: 10.1080/21541264.2016.1187550. PubMed DOI PMC

Fabrizio P., Garvis S., Palladino F. Histone Methylation and Memory of Environmental Stress. Cells. 2019;8:339. doi: 10.3390/cells8040339. PubMed DOI PMC

Ohama N., Sato H., Shinozaki K., Yamaguchi-Shinozaki K. Transcriptional Regulatory Network of Plant Heat Stress Response. Trends Plant. Sci. 2017;22:53–65. doi: 10.1016/j.tplants.2016.08.015. PubMed DOI

Stief A., Brzezinka K., Lämke J., Bäurle I. Epigenetic responses to heat stress at different time scales and the involvement of small RNAs. Plant. Signal Behav. 2014;9:e970430. doi: 10.4161/15592316.2014.970430. PubMed DOI PMC

Oberkofler V., Pratx L., Bäurle I. Epigenetic regulation of abiotic stress memory: Maintaining the good things while they last. Curr. Opin. Plant. Biol. 2021;61:102007. doi: 10.1016/j.pbi.2021.102007. PubMed DOI PMC

Bouche F., Woods D.P., Amasino R.M. Winter Memory throughout the Plant Kingdom: Different Paths to Flowering. Plant. Physiol. 2017;173:27–35. doi: 10.1104/pp.16.01322. PubMed DOI PMC

Baurle I., Trindade I. Chromatin regulation of somatic abiotic stress memory. J. Exp. Bot. 2020;71:5269–5279. doi: 10.1093/jxb/eraa098. PubMed DOI

Asaari M.S.M., Mertens S., Dhondt S., Inzé D., Wuyts N., Scheunders P. Analysis of hyperspectral images for detection of drought stress and recovery in maize plants in a high-throughput phenotyping platform. Comput. Electron. Agric. 2019;162:749–758. doi: 10.1016/j.compag.2019.05.018. DOI

Martinez-Medina A., Flors V., Heil M., Mauch-Mani B., Pieterse C.M.J., Pozo M.J., Ton J., van Dam N.M., Conrath U. Recognizing Plant Defense Priming. Trends Plant. Sci. 2016;21:818–822. doi: 10.1016/j.tplants.2016.07.009. PubMed DOI

Mauch-Mani B., Baccelli I., Luna E., Flors V. Defense Priming: An Adaptive Part of Induced Resistance. Annu Rev. Plant. Biol. 2017;68:485–512. doi: 10.1146/annurev-arplant-042916-041132. PubMed DOI

Kinoshita T., Seki M. Epigenetic memory for stress response and adaptation in plants. Plant. Cell Physiol. 2014;55:1859–1863. doi: 10.1093/pcp/pcu125. PubMed DOI

Conrath U., Beckers G.J., Langenbach C.J., Jaskiewicz M.R. Priming for enhanced defense. Annu Rev. Phytopathol. 2015;53:97–119. doi: 10.1146/annurev-phyto-080614-120132. PubMed DOI

Balestrini R., Chitarra W., Antoniou C., Ruocco M., Fotopoulos V. Improvement of plant performance under water deficit with the employment of biological and chemical priming agents. J. Agric. Sci. 2018;156:680–688. doi: 10.1017/S0021859618000126. DOI

Ashapkin V.V., Kutueva L.I., Aleksandrushkina N.I., Vanyushin B.F. Epigenetic Mechanisms of Plant Adaptation to Biotic and Abiotic Stresses. Int. J. Mol. Sci. 2020;21:7457. doi: 10.3390/ijms21207457. PubMed DOI PMC

Ioannou A., Gohari G., Papaphilippou P., Panahirad S., Akbari A., Dadpour M.R., Krasia-Christoforou T., Fotopoulos V. Advanced nanomaterials in agriculture under a changing climate: The way to the future? Environ. Exp. Bot. 2020;176:104048. doi: 10.1016/j.envexpbot.2020.104048. DOI

Jaskiewicz M., Conrath U., Peterhänsel C. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 2011;12:50–55. doi: 10.1038/embor.2010.186. PubMed DOI PMC

Savvides A., Ali S., Tester M., Fotopoulos V. Chemical Priming of Plants Against Multiple Abiotic Stresses: Mission Possible? Trends Plant. Sci. 2016;21:329–340. doi: 10.1016/j.tplants.2015.11.003. PubMed DOI

Westman S.M., Kloth K.J., Hanson J., Ohlsson A.B., Albrectsen B.R. Defence priming in Arabidopsis—A Meta-Analysis. Sci. Rep. 2019;9:13309. doi: 10.1038/s41598-019-49811-9. PubMed DOI PMC

Wilkinson S.W., Mageroy M.H., Lopez Sanchez A., Smith L.M., Furci L., Cotton T.E.A., Krokene P., Ton J. Surviving in a Hostile World: Plant Strategies to Resist Pests and Diseases. Annu Rev. Phytopathol. 2019;57:505–529. doi: 10.1146/annurev-phyto-082718-095959. PubMed DOI

De Vega D., Holden N., Hedley P.E., Morris J., Luna E., Newton A. Chitosan primes plant defence mechanisms against Botrytis cinerea, including expression of Avr9/Cf-9 rapidly elicited genes. Plant. Cell Env. 2021;44:290–303. doi: 10.1111/pce.13921. PubMed DOI PMC

Tirnaz S., Batley J. DNA Methylation: Toward Crop Disease Resistance Improvement. Trends Plant. Sci. 2019;24:1137–1150. doi: 10.1016/j.tplants.2019.08.007. PubMed DOI

Kerchev P., van der Meer T., Sujeeth N., Verlee A., Stevens C.V., Van Breusegem F., Gechev T. Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol. Adv. 2020;40:107503. doi: 10.1016/j.biotechadv.2019.107503. PubMed DOI

Turgut-Kara N., Arikan B., Celik H. Epigenetic memory and priming in plants. Genetica. 2020;148:47–54. doi: 10.1007/s10709-020-00093-4. PubMed DOI

Espinas N.A., Saze H., Saijo Y. Epigenetic Control of Defense Signaling and Priming in Plants. Front. Plant. Sci. 2016;7:1201. doi: 10.3389/fpls.2016.01201. PubMed DOI PMC

Lämke J., Bäurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017;18:124. doi: 10.1186/s13059-017-1263-6. PubMed DOI PMC

He Y., Li Z. Epigenetic Environmental Memories in Plants: Establishment, Maintenance, and Reprogramming. Trends Genet. 2018;34:856–866. doi: 10.1016/j.tig.2018.07.006. PubMed DOI

Sani E., Herzyk P., Perrella G., Colot V., Amtmann A. Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol. 2013;14:R59. doi: 10.1186/gb-2013-14-6-r59. PubMed DOI PMC

Johnson R., Puthur J.T. Seed priming as a cost effective technique for developing plants with cross tolerance to salinity stress. Plant. Physiol. Biochem. 2021;162:247–257. doi: 10.1016/j.plaphy.2021.02.034. PubMed DOI

Pastor V., Luna E., Mauch-Mani B., Ton J., Flors V. Primed plants do not forget. Environ. Exp. Bot. 2013;94:46–56. doi: 10.1016/j.envexpbot.2012.02.013. DOI

Singh P., Yekondi S., Chen P.W., Tsai C.H., Yu C.W., Wu K., Zimmerli L. Environmental History Modulates Arabidopsis Pattern-Triggered Immunity in a HISTONE ACETYLTRANSFERASE1-Dependent Manner. Plant. Cell. 2014;26:2676–2688. doi: 10.1105/tpc.114.123356. PubMed DOI PMC

Lopez Sanchez A., Stassen J.H., Furci L., Smith L.M., Ton J. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant. J. 2016;88:361–374. doi: 10.1111/tpj.13252. PubMed DOI PMC

Bertini L., Proietti S., Focaracci F., Sabatini B., Caruso C. Epigenetic control of defense genes following MeJA-induced priming in rice (O. sativa) J. Plant. Physiol. 2018;228:166–177. PubMed

Kim J.M., To T.K., Matsui A., Tanoi K., Kobayashi N.I., Matsuda F., Habu Y., Ogawa D., Sakamoto T., Matsunaga S., et al. Acetate-mediated novel survival strategy against drought in plants. Nat. Plants. 2017;3:17097. doi: 10.1038/nplants.2017.97. PubMed DOI

Li J.W., Zhang X.C., Wang M.R., Bi W.L., Faisal M., da Silva J.A.T., Volk G.M., Wang Q.C. Development, progress and future prospects in cryobiotechnology of Lilium spp. Plant. Methods. 2019;15:125. doi: 10.1186/s13007-019-0506-9. PubMed DOI PMC

Luna E., Bruce T.J., Roberts M.R., Flors V., Ton J. Next-generation systemic acquired resistance. Plant. Physiol. 2012;158:844–853. doi: 10.1104/pp.111.187468. PubMed DOI PMC

De Palma M., Salzano M., Villano C., Aversano R., Lorito M., Ruocco M., Docimo T., Piccinelli A.L., D’Agostino N., Tucci M. Transcriptome reprogramming, epigenetic modifications and alternative splicing orchestrate the tomato root response to the beneficial fungus Trichoderma harzianum. Hortic Res. 2019;6:5. doi: 10.1038/s41438-018-0079-1. PubMed DOI PMC

Zhang T., Cooper S., Brockdorff N. The interplay of histone modifications—Writers that read. EMBO Rep. 2015;16:1467–1481. doi: 10.15252/embr.201540945. PubMed DOI PMC

Sako K., Nguyen H.M., Seki M. Advances in Chemical Priming to Enhance Abiotic Stress Tolerance in Plants. Plant. Cell Physiol. 2021;61:1995–2003. doi: 10.1093/pcp/pcaa119. PubMed DOI

Sako K., Kim J.-M., Matsui A., Nakamura K., Tanaka M., Kobayashi M., Saito K., Nishino N., Kusano M., Taji T., et al. Ky-2, a Histone Deacetylase Inhibitor, Enhances High-Salinity Stress Tolerance in Arabidopsis thaliana. Plant. Cell Physiol. 2015;57:776–783. doi: 10.1093/pcp/pcv199. PubMed DOI

Nguyen H.M., Sako K., Matsui A., Ueda M., Tanaka M., Ito A., Nishino N., Yoshida M., Seki M. Transcriptomic analysis of Arabidopsis thaliana plants treated with the Ky-9 and Ky-72 histone deacetylase inhibitors. Plant. Signal Behav. 2018;13:e1448333. doi: 10.1080/15592324.2018.1448333. PubMed DOI PMC

Goldschmidt E.E. Plant grafting: New mechanisms, evolutionary implications. Front. Plant. Sci. 2014;5:727. doi: 10.3389/fpls.2014.00727. PubMed DOI PMC

Mudge K., Janick J., Scofield S., Goldschmidt E.E. A History of Grafting. John Wiley & Sons; Hoboken, NJ, USA: 2009.

Wu R., Wang X., Lin Y., Ma Y., Liu G., Yu X., Zhong S., Liu B. Inter-species grafting caused extensive and heritable alterations of DNA methylation in Solanaceae plants. PLoS ONE. 2013;8:e61995. doi: 10.1371/journal.pone.0061995. PubMed DOI PMC

Kapazoglou A., Tani E., Avramidou E.V., Abraham E.M., Gerakari M., Megariti S., Doupis G., Doulis A.G. Epigenetic Changes and Transcriptional Reprogramming Upon Woody Plant Grafting for Crop Sustainability in a Changing Environment. Front. Plant. Sci. 2021;11:2160. doi: 10.3389/fpls.2020.613004. PubMed DOI PMC

Tsaballa A., Xanthopoulou A., Madesis P., Tsaftaris A., Nianiou-Obeidat I. Vegetable Grafting From a Molecular Point of View: The Involvement of Epigenetics in Rootstock-Scion Interactions. Front. Plant. Sci. 2020;11:621999. doi: 10.3389/fpls.2020.621999. PubMed DOI PMC

Molnar A., Melnyk C.W., Bassett A., Hardcastle T.J., Dunn R., Baulcombe D.C. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science. 2010;328:872–875. doi: 10.1126/science.1187959. PubMed DOI

Haroldsen V., Szczerba M.W., Aktas H., Lopez J., Odias M.J., Chi-Ham C.L., Labavitch J., Bennett A.B., Powell A.L. Mobility of transgenic nucleic acids and proteins within grafted rootstocks for agricultural improvement. Front. Plant. Sci. 2012;3:39. doi: 10.3389/fpls.2012.00039. PubMed DOI PMC

Tamiru M., Hardcastle T.J., Lewsey M.G. Regulation of genome-wide DNA methylation by mobile small RNAs. New Phytol. 2018;217:540–546. doi: 10.1111/nph.14874. PubMed DOI

Lewsey M.G., Hardcastle T.J., Melnyk C.W., Molnar A., Valli A., Urich M.A., Nery J.R., Baulcombe D.C., Ecker J.R. Mobile small RNAs regulate genome-wide DNA methylation. Proc. Natl. Acad. Sci. USA. 2016;113:E801–E810. doi: 10.1073/pnas.1515072113. PubMed DOI PMC

Xanthopoulou A., Tsaballa A., Ganopoulos I., Kapazoglou A., Avramidou E., Aravanopoulos F.A., Moysiadis T., Osathanunkul M., Tsaftaris A., Doulis A.G., et al. Intra-species grafting induces epigenetic and metabolic changes accompanied by alterations in fruit size and shape of Cucurbita pepo L. Plant. Growth Regul. 2019;87:93–108. doi: 10.1007/s10725-018-0456-7. DOI

Cao L., Yu N., Li J., Qi Z., Wang D., Chen L. Heritability and Reversibility of DNA Methylation Induced by in vitro Grafting between Brassica juncea and B. oleracea. Sci. Rep. 2016;6:27233. doi: 10.1038/srep27233. PubMed DOI PMC

Ojolo S.P., Cao S., Priyadarshani S.V.G.N., Li W., Yan M., Aslam M., Zhao H., Qin Y. Regulation of Plant Growth and Development: A Review from a Chromatin Remodeling Perspective. Front. Plant. Sci. 2018;9:1232. doi: 10.3389/fpls.2018.01232. PubMed DOI PMC

Maury S., Sow M.D., Le Gac A.L., Genitoni J., Lafon-Placette C., Mozgova I. Phytohormone and Chromatin Crosstalk: The Missing Link for Developmental Plasticity? Front. Plant. Sci. 2019;10:395. doi: 10.3389/fpls.2019.00395. PubMed DOI PMC

Yona A.H., Frumkin I., Pilpel Y. A relay race on the evolutionary adaptation spectrum. Cell. 2015;163:549–559. doi: 10.1016/j.cell.2015.10.005. PubMed DOI

Saravana Kumar R.M., Wang Y., Zhang X., Cheng H., Sun L., He S., Hao F. Redox Components: Key Regulators of Epigenetic Modifications in Plants. Int. J. Mol. Sci. 2020;21:1419. PubMed PMC

Robert-Seilaniantz A., Navarro L., Bari R., Jones J.D. Pathological hormone imbalances. Curr. Opin. Plant. Biol. 2007;10:372–379. doi: 10.1016/j.pbi.2007.06.003. PubMed DOI

Baulcombe D.C., Dean C. Epigenetic regulation in plant responses to the environment. Cold Spring Harb. Perspect. Biol. 2014;6:a019471. doi: 10.1101/cshperspect.a019471. PubMed DOI PMC

Heard E., Martienssen R.A. Transgenerational epigenetic inheritance: Myths and mechanisms. Cell. 2014;157:95–109. doi: 10.1016/j.cell.2014.02.045. PubMed DOI PMC

Mozgova I., Munoz-Viana R., Hennig L. PRC2 Represses Hormone-Induced Somatic Embryogenesis in Vegetative Tissue of Arabidopsis thaliana. PLoS Genet. 2017;13:e1006562. doi: 10.1371/journal.pgen.1006562. PubMed DOI PMC

Gaillochet C., Lohmann J.U. The never-ending story: From pluripotency to plant developmental plasticity. Development. 2015;142:2237–2249. doi: 10.1242/dev.117614. PubMed DOI PMC

Lafos M., Kroll P., Hohenstatt M.L., Thorpe F.L., Clarenz O., Schubert D. Dynamic Regulation of H3K27 Trimethylation during Arabidopsis Differentiation. PLoS Genet. 2011;7:e1002040. doi: 10.1371/journal.pgen.1002040. PubMed DOI PMC

Hébrard C., Peterson D.G., Willems G., Delaunay A., Jesson B., Lefèbvre M., Barnes S., Maury S. Epigenomics and bolting tolerance in sugar beet genotypes. J. Exp. Bot. 2016;67:207–225. doi: 10.1093/jxb/erv449. PubMed DOI PMC

Sow M.D., Allona I., Ambroise C., Conde D., Fichot R., Gribkova S., Jorge V., Le-Provost G., Pâques L., Plomion C., et al. Chapter Twelve—Epigenetics in Forest Trees: State of the Art and Potential Implications for Breeding and Management in a Context of Climate Change. In: Mirouze M., Bucher E., Gallusci P., editors. Advances in Botanical Research. Volume 88. Academic Press; Cambridge, MA, USA: 2018. pp. 387–453.

Ueda M., Seki M. Histone Modifications Form Epigenetic Regulatory Networks to Regulate Abiotic Stress Response. Plant. Physiol. 2020;182:15–26. doi: 10.1104/pp.19.00988. PubMed DOI PMC

Leung J., Gaudin V. Who Rules the Cell? An Epi-Tale of Histone, DNA, RNA, and the Metabolic Deep State. Front. Plant. Sci. 2020;11:181. doi: 10.3389/fpls.2020.00181. PubMed DOI PMC

Chen X., Ding A.B., Zhong X. Functions and mechanisms of plant histone deacetylases. Sci. China Life Sci. 2020;63:206–216. doi: 10.1007/s11427-019-1587-x. PubMed DOI

Chen H., Feng H., Zhang X., Zhang C., Wang T., Dong J. An Arabidopsis E3 ligase HUB2 increases histone H2B monoubiquitination and enhances drought tolerance in transgenic cotton. Plant. Biotechnol. J. 2019;17:556–568. doi: 10.1111/pbi.12998. PubMed DOI PMC

Wang L., Wang C., Liu X., Cheng J., Li S., Zhu J.-K., Gong Z. Peroxisomal β-oxidation regulates histone acetylation and DNA methylation in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2019;116:10576–10585. doi: 10.1073/pnas.1904143116. PubMed DOI PMC

Rasheed S., Bashir K., Kim J.-M., Ando M., Tanaka M., Seki M. The modulation of acetic acid pathway genes in Arabidopsis improves survival under drought stress. Sci. Rep. 2018;8:7831. doi: 10.1038/s41598-018-26103-2. PubMed DOI PMC

Imran M., Hussain S., Rana M.S., Saleem M.H., Rasul F., Ali K.H., Potcho M.P., Pan S., Duan M., Tang X. Molybdenum improves 2-acetyl-1-pyrroline, grain quality traits and yield attributes in fragrant rice through efficient nitrogen assimilation under cadmium toxicity. Ecotoxicol. Environ. Saf. 2021;211:111911. doi: 10.1016/j.ecoenv.2021.111911. PubMed DOI

Storozhenko S., De Brouwer V., Volckaert M., Navarrete O., Blancquaert D., Zhang G.F., Lambert W., Van Der Straeten D. Folate fortification of rice by metabolic engineering. Nat. Biotechnol. 2007;25:1277–1279. doi: 10.1038/nbt1351. PubMed DOI

Fesenko I., Spechenkova N., Mamaeva A., Makhotenko A.V., Love A.J., Kalinina N.O., Taliansky M. Role of the methionine cycle in the temperature-sensitive responses of potato plants to potato virus Y. Mol. Plant. Pathol. 2021;22:77–91. doi: 10.1111/mpp.13009. PubMed DOI PMC

González B., Vera P. Folate Metabolism Interferes with Plant Immunity through 1C Methionine Synthase-Directed Genome-wide DNA Methylation Enhancement. Mol. Plant. 2019;12:1227–1242. doi: 10.1016/j.molp.2019.04.013. PubMed DOI

Martinelli F., Dandekar A.M. Genetic Mechanisms of the Devious Intruder Candidatus Liberibacter in Citrus. Front. Plant. Sci. 2017;8:904. doi: 10.3389/fpls.2017.00904. PubMed DOI PMC

Tosetti R., Martinelli F., Tonutti P., Barupal D.K. Metabolomics Approach to Studying Minimally Processed Peach (Prunus Persica) Fruit. International Society for Horticultural Science (ISHS); Leuven, Belgium: 2012. pp. 1017–1021.

Natali L., Giordani T., Lercari B., Maestrini P., Cozza R., Pangaro T., Vernieri P., Martinelli F., Cavallini A. Light induces expression of a dehydrin-encoding gene during seedling de-etiolation in sunflower (Helianthus annuus L.) J. Plant. Physiol. 2007;164:263–273. doi: 10.1016/j.jplph.2006.01.015. PubMed DOI

Balan B., Caruso T., Martinelli F. Gaining Insight into Exclusive and Common Transcriptomic Features Linked with Biotic Stress Responses in Malus. Front. Plant. Sci. 2017;8:1569. doi: 10.3389/fpls.2017.01569. PubMed DOI PMC

Liu J., He Z. Small DNA Methylation, Big Player in Plant Abiotic Stress Responses and Memory. Front. Plant. Sci. 2020;11:595603. doi: 10.3389/fpls.2020.595603. PubMed DOI PMC

Shanker A.K., Bhanu D., Maheswari M. Epigenetics and transgenerational memory in plants under heat stress. Plant. Physiol. Rep. 2020;25:583–593. doi: 10.1007/s40502-020-00557-x. DOI

Huang S., Zhang A., Jin J.B., Zhao B., Wang T.J., Wu Y., Wang S., Liu Y., Wang J., Guo P., et al. Arabidopsis histone H3K4 demethylase JMJ17 functions in dehydration stress response. New Phytol. 2019;223:1372–1387. doi: 10.1111/nph.15874. PubMed DOI

Vriet C., Hennig L., Laloi C. Stress-induced chromatin changes in plants: Of memories, metabolites and crop improvement. Cell Mol. Life Sci. 2015;72:1261–1273. doi: 10.1007/s00018-014-1792-z. PubMed DOI PMC

Gao G., Li J., Li H., Li F., Xu K., Yan G., Chen B., Qiao J., Wu X. Comparison of the heat stress induced variations in DNA methylation between heat-tolerant and heat-sensitive rapeseed seedlings. Breed. Sci. 2014;64:125–133. doi: 10.1270/jsbbs.64.125. PubMed DOI PMC

Baránek M., Čechová J., Raddová J., Holleinová V., Ondrušíková E., Pidra M. Dynamics and Reversibility of the DNA Methylation Landscape of Grapevine Plants (Vitis vinifera) Stressed by In Vitro Cultivation and Thermotherapy. PLoS ONE. 2015;10:e0126638. doi: 10.1371/journal.pone.0126638. PubMed DOI PMC

Wang W.S., Pan Y.J., Zhao X.Q., Dwivedi D., Zhu L.H., Ali J., Fu B.Y., Li Z.K. Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.) J. Exp. Bot. 2011;62:1951–1960. doi: 10.1093/jxb/erq391. PubMed DOI PMC

Secco D., Wang C., Shou H., Schultz M.D., Chiarenza S., Nussaume L., Ecker J.R., Whelan J., Lister R. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife. 2015;4:e09343. doi: 10.7554/eLife.09343. PubMed DOI PMC

Kangaspeska S., Stride B., Metivier R., Polycarpou-Schwarz M., Ibberson D., Carmouche R.P., Benes V., Gannon F., Reid G. Transient cyclical methylation of promoter DNA. Nature. 2008;452:112–115. doi: 10.1038/nature06640. PubMed DOI

Centomani I., Sgobba A., D’Addabbo P., Dipierro N., Paradiso A., De Gara L., Dipierro S., Viggiano L., de Pinto M.C. Involvement of DNA methylation in the control of cell growth during heat stress in tobacco BY-2 cells. Protoplasma. 2015;252:1451–1459. doi: 10.1007/s00709-015-0772-y. PubMed DOI

Ding Y., Shi Y., Yang S. Molecular Regulation of Plant Responses to Environmental Temperatures. Mol. Plant. 2020;13:544–564. doi: 10.1016/j.molp.2020.02.004. PubMed DOI

Ito H., Gaubert H., Bucher E., Mirouze M., Vaillant I., Paszkowski J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature. 2011;472:115–119. doi: 10.1038/nature09861. PubMed DOI

Iwasaki M., Paszkowski J. Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proc. Natl. Acad. Sci. USA. 2014;111:8547–8552. doi: 10.1073/pnas.1402275111. PubMed DOI PMC

Bilichak A., Kovalchuk I. Transgenerational response to stress in plants and its application for breeding. J. Exp. Bot. 2016;67:2081–2092. doi: 10.1093/jxb/erw066. PubMed DOI

Bose A.K., Moser B., Rigling A., Lehmann M.M., Milcu A., Peter M., Rellstab C., Wohlgemuth T., Gessler A. Memory of environmental conditions across generations affects the acclimation potential of scots pine. Plant. Cell Environ. 2020;43:1288–1299. doi: 10.1111/pce.13729. PubMed DOI PMC

Hauben M., Haesendonckx B., Standaert E., Van Der Kelen K., Azmi A., Akpo H., Van Breusegem F., Guisez Y., Bots M., Lambert B., et al. Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc. Natl. Acad. Sci. USA. 2009;106:20109–20114. doi: 10.1073/pnas.0908755106. PubMed DOI PMC

Verhoeven K.J., Jansen J.J., van Dijk P.J., Biere A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010;185:1108–1118. doi: 10.1111/j.1469-8137.2009.03121.x. PubMed DOI

Kathiria P., Sidler C., Golubov A., Kalischuk M., Kawchuk L.M., Kovalchuk I. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant. Physiol. 2010;153:1859–1870. doi: 10.1104/pp.110.157263. PubMed DOI PMC

Bhadouriya S.L., Mehrotra S., Basantani M.K., Loake G.J., Mehrotra R. Role of Chromatin Architecture in Plant Stress Responses: An Update. Front. Plant. Sci. 2020;11:603380. doi: 10.3389/fpls.2020.603380. PubMed DOI PMC

Ding Y., Fromm M., Avramova Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat. Commun. 2012;3:740. doi: 10.1038/ncomms1732. PubMed DOI

Muller-Xing R., Xing Q., Goodrich J. Footprints of the sun: Memory of UV and light stress in plants. Front. Plant. Sci. 2014;5:474. PubMed PMC

Pecinka A., Rosa M., Schikora A., Berlinger M., Hirt H., Luschnig C., Scheid O.M. Transgenerational Stress Memory Is Not a General Response in Arabidopsis. PLoS ONE. 2009;4:e5202. doi: 10.1371/journal.pone.0005202. PubMed DOI PMC

Paszkowski J., Grossniklaus U. Selected aspects of transgenerational epigenetic inheritance and resetting in plants. Curr. Opin. Plant. Biol. 2011;14:195–203. doi: 10.1016/j.pbi.2011.01.002. PubMed DOI

Latzel V., Rendina González A.P., Rosenthal J. Epigenetic Memory as a Basis for Intelligent Behavior in Clonal Plants. Front. Plant. Sci. 2016;7:1354. doi: 10.3389/fpls.2016.01354. PubMed DOI PMC

Springer N.M., Schmitz R.J. Exploiting induced and natural epigenetic variation for crop improvement. Nat. Rev. Genet. 2017;18:563–575. doi: 10.1038/nrg.2017.45. PubMed DOI

Tirnaz S., Batley J. Epigenetics: Potentials and Challenges in Crop Breeding. Mol. Plant. 2019;12:1309–1311. doi: 10.1016/j.molp.2019.09.006. PubMed DOI

Kawakatsu T., Ecker J.R. Diversity and dynamics of DNA methylation: Epigenomic resources and tools for crop breeding. Breed. Sci. 2019;69:191–204. doi: 10.1270/jsbbs.19005. PubMed DOI PMC

Perrone A., Martinelli F. Plant stress biology in epigenomic era. Plant. Sci. 2020;294:110376. doi: 10.1016/j.plantsci.2019.110376. PubMed DOI

Varotto S., Tani E., Abraham E., Krugman T., Kapazoglou A., Melzer R., Radanovic A., Miladinovic D. Epigenetics: Possible applications in climate-smart crop breeding. J. Exp. Bot. 2020;71:5223–5236. doi: 10.1093/jxb/eraa188. PubMed DOI PMC

Gallusci P., Dai Z., Genard M., Gauffretau A., Leblanc-Fournier N., Richard-Molard C., Vile D., Brunel-Muguet S. Epigenetics for Plant Improvement: Current Knowledge and Modeling Avenues. Trends Plant. Sci. 2017;22:610–623. doi: 10.1016/j.tplants.2017.04.009. PubMed DOI

Ingouff M., Rademacher S., Holec S., Soljic L., Xin N., Readshaw A., Foo S.H., Lahouze B., Sprunck S., Berger F. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 2010;20:2137–2143. doi: 10.1016/j.cub.2010.11.012. PubMed DOI

Xiao J., Wagner D. Polycomb repression in the regulation of growth and development in Arabidopsis. Curr. Opin. Plant. Biol. 2015;23:15–24. doi: 10.1016/j.pbi.2014.10.003. PubMed DOI

Zhou T., Yang X., Guo K., Deng J., Xu J., Gao W., Lindsey K., Zhang X. ROS Homeostasis Regulates Somatic Embryogenesis via the Regulation of Auxin Signaling in Cotton. Mol. Cell Proteom. 2016;15:2108–2124. doi: 10.1074/mcp.M115.049338. PubMed DOI PMC

Zhong S.H., Liu J.Z., Jin H., Lin L., Li Q., Chen Y., Yuan Y.X., Wang Z.Y., Huang H., Qi Y.J., et al. Warm temperatures induce transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2013;110:9171–9176. doi: 10.1073/pnas.1219655110. PubMed DOI PMC

Liu J., Feng L., Gu X., Deng X., Qiu Q., Li Q., Zhang Y., Wang M., Deng Y., Wang E., et al. An H3K27me3 demethylase-HSFA2 regulatory loop orchestrates transgenerational thermomemory in Arabidopsis. Cell Res. 2019;29:379–390. doi: 10.1038/s41422-019-0145-8. PubMed DOI PMC

Stassen J.H.M., López A., Jain R., Pascual-Pardo D., Luna E., Smith L.M., Ton J. The relationship between transgenerational acquired resistance and global DNA methylation in Arabidopsis. Sci. Rep. 2018;8:14761. doi: 10.1038/s41598-018-32448-5. PubMed DOI PMC

Furci L., Jain R., Stassen J., Berkowitz O., Whelan J., Roquis D., Baillet V., Colot V., Johannes F., Ton J. Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. Elife. 2019;8 doi: 10.7554/eLife.40655. PubMed DOI PMC

Johannes F., Porcher E., Teixeira F.K., Saliba-Colombani V., Simon M., Agier N., Bulski A., Albuisson J., Heredia F., Audigier P., et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009;5:e1000530. doi: 10.1371/journal.pgen.1000530. PubMed DOI PMC

Reinders J., Wulff B.B., Mirouze M., Mari-Ordonez A., Dapp M., Rozhon W., Bucher E., Theiler G., Paszkowski J. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 2009;23:939–950. doi: 10.1101/gad.524609. PubMed DOI PMC

Alvarez-Venegas R., De la Peña C., Casas-Mollano J.A. Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications. Springer International Publishing; Cham, Switzerland: 2014.

Raju S.K.K., Shao M.R., Sanchez R., Xu Y.Z., Sandhu A., Graef G., Mackenzie S. An epigenetic breeding system in soybean for increased yield and stability. Plant. Biotechnol. J. 2018;16:1836–1847. doi: 10.1111/pbi.12919. PubMed DOI PMC

Kundariya H., Yang X., Morton K., Sanchez R., Axtell M.J., Hutton S.F., Fromm M., Mackenzie S.A. MSH1-induced heritable enhanced growth vigor through grafting is associated with the RdDM pathway in plants. Nat. Commun. 2020;11:5343. doi: 10.1038/s41467-020-19140-x. PubMed DOI PMC

Yang X., Sanchez R., Kundariya H., Maher T., Dopp I., Schwegel R., Virdi K., Axtell M.J., Mackenzie S.A. Segregation of an MSH1 RNAi transgene produces heritable non-genetic memory in association with methylome reprogramming. Nat. Commun. 2020;11:2214. doi: 10.1038/s41467-020-16036-8. PubMed DOI PMC

Rendina Gonzalez A.P., Preite V., Verhoeven K.J.F., Latzel V. Transgenerational Effects and Epigenetic Memory in the Clonal Plant Trifolium repens. Front. Plant. Sci. 2018;9:1677. doi: 10.3389/fpls.2018.01677. PubMed DOI PMC

Zheng X., Chen L., Xia H., Wei H., Lou Q., Li M., Li T., Luo L. Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition. Sci. Rep. 2017;7:39843. doi: 10.1038/srep39843. PubMed DOI PMC

Cong W., Miao Y., Xu L., Zhang Y., Yuan C., Wang J., Zhuang T., Lin X., Jiang L., Wang N., et al. Transgenerational memory of gene expression changes induced by heavy metal stress in rice (Oryza sativa L.) BMC Plant. Biol. 2019;19:282. doi: 10.1186/s12870-019-1887-7. PubMed DOI PMC

Byeon B., Bilichak A., Kovalchuk I. Transgenerational Response to Heat Stress in the Form of Differential Expression of Noncoding RNA Fragments in Brassica rapa Plants. Plant. Genome. 2019;12 doi: 10.3835/plantgenome2018.04.0022. PubMed DOI

Dalakouras A., Dadami E., Zwiebel M., Krczal G., Wassenegger M. Transgenerational maintenance of transgene body CG but not CHG and CHH methylation. Epigenetics. 2012;7:1071–1078. doi: 10.4161/epi.21644. PubMed DOI PMC

Zhang J., Zhang H., Srivastava A.K., Pan Y., Bai J., Fang J., Shi H., Zhu J.-K. Knockdown of Rice MicroRNA166 Confers Drought Resistance by Causing Leaf Rolling and Altering Stem Xylem Development. Plant. Physiol. 2018;176:2082–2094. doi: 10.1104/pp.17.01432. PubMed DOI PMC

Ferreira L.J., Donoghue M.T.A., Barros P., Saibo N.J., Santos A.P., Oliveira M.M. Uncovering Differentially Methylated Regions (DMRs) in a Salt-Tolerant Rice Variety under Stress: One Step towards New Regulatory Regions for Enhanced Salt Tolerance. Epigenomes. 2019;3:4. doi: 10.3390/epigenomes3010004. PubMed DOI PMC

Wu K., Wang S., Song W., Zhang J., Wang Y., Liu Q., Yu J., Ye Y., Li S., Chen J., et al. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science. 2020;367:6478. doi: 10.1126/science.aaz2046. PubMed DOI

Cui X., Zhao P., Liang W., Cheng Q., Mu B., Niu F., Yan J., Liu C., Xie H., Kav N.N.V., et al. A Rapeseed WRKY Transcription Factor Phosphorylated by CPK Modulates Cell Death and Leaf Senescence by Regulating the Expression of ROS and SA-Synthesis-Related Genes. J. Agric. Food Chem. 2020;68:7348–7359. doi: 10.1021/acs.jafc.0c02500. PubMed DOI

Song X., Cao X. Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptation in rice. Curr. Opin. Plant. Biol. 2017;36:111–118. doi: 10.1016/j.pbi.2017.02.004. PubMed DOI

Quadrana L., Etcheverry M., Gilly A., Caillieux E., Madoui M.-A., Guy J., Bortolini Silveira A., Engelen S., Baillet V., Wincker P., et al. Transposition favors the generation of large effect mutations that may facilitate rapid adaption. Nat. Commun. 2019;10:3421. doi: 10.1038/s41467-019-11385-5. PubMed DOI PMC

Thieme M., Lanciano S., Balzergue S., Daccord N., Mirouze M., Bucher E. Inhibition of RNA polymerase II allows controlled mobilisation of retrotransposons for plant breeding. Genome Biol. 2017;18:134. doi: 10.1186/s13059-017-1265-4. PubMed DOI PMC

Yang Q., Li Z., Li W., Ku L., Wang C., Ye J., Li K., Yang N., Li Y., Zhong T., et al. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc. Natl. Acad. Sci. USA. 2013;110:16969–16974. doi: 10.1073/pnas.1310949110. PubMed DOI PMC

Mao X., Chen S., Li A., Zhai C., Jing R. Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS ONE. 2014;9:e84359. doi: 10.1371/journal.pone.0084359. PubMed DOI PMC

Zhang H., Tao Z., Hong H., Chen Z., Wu C., Li X., Xiao J., Wang S. Transposon-derived small RNA is responsible for modified function of WRKY45 locus. Nat. Plants. 2016;2:16016. doi: 10.1038/nplants.2016.16. PubMed DOI

Ha J., Kwon H., Cho K.-H., Yoon M.Y., Kim M.Y., Lee S.-H. Identification of epigenetic variation associated with synchronous pod maturity in mungbean (Vigna radiata L.) Sci. Rep. 2020;10:17414. doi: 10.1038/s41598-020-74520-z. PubMed DOI PMC

Testillano P.S. Microspore embryogenesis: Targeting the determinant factors of stress-induced cell reprogramming for crop improvement. J. Exp. Bot. 2019;70:2965–2978. doi: 10.1093/jxb/ery464. PubMed DOI

De-la-Pena C., Nic-Can G.I., Galaz-Avalos R.M., Avilez-Montalvo R., Loyola-Vargas V.M. The role of chromatin modifications in somatic embryogenesis in plants. Front. Plant. Sci. 2015;6:635. doi: 10.3389/fpls.2015.00635. PubMed DOI PMC

Solis M.T., Rodriguez-Serrano M., Meijon M., Canal M.J., Cifuentes A., Risueno M.C., Testillano P.S. DNA methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis. J. Exp. Bot. 2012;63:6431–6444. doi: 10.1093/jxb/ers298. PubMed DOI PMC

Berenguer E., Barany I., Solis M.T., Perez-Perez Y., Risueno M.C., Testillano P.S. Inhibition of Histone H3K9 Methylation by BIX-01294 Promotes Stress-Induced Microspore Totipotency and Enhances Embryogenesis Initiation. Front. Plant. Sci. 2017;8:1161. doi: 10.3389/fpls.2017.01161. PubMed DOI PMC

Li Q., Eichten S.R., Hermanson P.J., Zaunbrecher V.M., Song J., Wendt J., Rosenbaum H., Madzima T.F., Sloan A.E., Huang J., et al. Genetic perturbation of the maize methylome. Plant. Cell. 2014;26:4602–4616. doi: 10.1105/tpc.114.133140. PubMed DOI PMC

Solís M.-T., El-Tantawy A.-A., Cano V., Risueño M.C., Testillano P.S. 5-azacytidine promotes microspore embryogenesis initiation by decreasing global DNA methylation, but prevents subsequent embryo development in rapeseed and barley. Front. Plant. Sci. 2015;6:472. doi: 10.3389/fpls.2015.00472. PubMed DOI PMC

Osorio-Montalvo P., Saenz-Carbonell L., De-la-Pena C. 5-Azacytidine: A Promoter of Epigenetic Changes in the Quest to Improve Plant Somatic Embryogenesis. Int. J. Mol. Sci. 2018;19:3182. doi: 10.3390/ijms19103182. PubMed DOI PMC

Surdonja K., Eggert K., Hajirezaei M.-R., Harshavardhan V.T., Seiler C., Von Wirén N., Sreenivasulu N., Kuhlmann M. Increase of DNA Methylation at the HvCKX2.1 Promoter by Terminal Drought Stress in Barley. Epigenomes. 2017;1:9. doi: 10.3390/epigenomes1020009. DOI

Hu J., Yang H., Mu J., Lu T., Peng J., Deng X., Kong Z., Bao S., Cao X., Zuo J. Nitric Oxide Regulates Protein Methylation during Stress Responses in Plants. Mol. Cell. 2017;67:702–710. doi: 10.1016/j.molcel.2017.06.031. PubMed DOI

Johnson L.M., Du J., Hale C.J., Bischof S., Feng S., Chodavarapu R.K., Zhong X., Marson G., Pellegrini M., Segal D.J., et al. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature. 2014;507:124–128. doi: 10.1038/nature12931. PubMed DOI PMC

Eichten S.R., Schmitz R.J., Springer N.M. Epigenetics: Beyond Chromatin Modifications and Complex Genetic Regulation. Plant. Physiol. 2014;165:933–947. doi: 10.1104/pp.113.234211. PubMed DOI PMC

Tal O., Kisdi E., Jablonka E. Epigenetic Contribution to Covariance Between Relatives. Genetics. 2010;184:1037–1050. doi: 10.1534/genetics.109.112466. PubMed DOI PMC

Hofmeister B.T., Lee K., Rohr N.A., Hall D.W., Schmitz R.J. Stable inheritance of DNA methylation allows creation of epigenotype maps and the study of epiallele inheritance patterns in the absence of genetic variation. Genome Biol. 2017;18:155. doi: 10.1186/s13059-017-1288-x. PubMed DOI PMC

Lane A.K., Niederhuth C.E., Ji L., Schmitz R.J. pENCODE: A plant encyclopedia of DNA elements. Annu Rev. Genet. 2014;48:49–70. doi: 10.1146/annurev-genet-120213-092443. PubMed DOI PMC

Plant Responses to Biotic Stress: Old Memories Matter