Abstract
In nature, plants are regularly exposed to biotic and abiotic stress conditions. These conditions create potential risks for survival. Plants have evolved in order to compete with these stress conditions through physiological adjustments that are based on epigenetic background. Thus, the ecological signals create different levels of stress memory. Recent studies have shown that this stress-induced environmental memory is mediated by epigenetic mechanisms that have fundamental roles in the aspect of controlling gene expression via DNA methylation, histone modifications and, small RNAs and these modifications could be transmitted to the next generations. Thus, they provide alternative mechanisms to constitute stress memories in plants. In this review, we summarized the epigenetic memory mechanisms related with biotic and abiotic stress conditions, and relationship between priming and epigenetic memory in plants by believing that it can be useful for analyzing memory mechanisms and see what is missing out in order to develop plants more resistant and productive under diverse environmental cues.
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References
Al-Lawati A, Al-Bahry S, Victor R et al (2016) Salt stress alters DNA methylation levels in alfalfa (Medicago spp). Genet Mol Res 15(1):15018299. https://doi.org/10.4238/gmr.15018299
Ali A, Yun DJ (2017) Salt stress tolerance; what do we learn from halophytes? J Plant Biol 60:431–439. https://doi.org/10.1007/s12374-017-0133-9
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544. https://doi.org/10.1093/jxb/ers100
Bahuguna RN, Tamilselvan A, Raveendran M et al (2018) Mild preflowering drought priming improves stress defences, assimilation and sink strength in rice under severe terminal drought. Funct Plant Biol 45:827–839. https://doi.org/10.1071/FP17248
Beckers GJM, Jaskiewicz M, Liu Y et al (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell Online 21:944–953. https://doi.org/10.1105/tpc.108.062158
Bernstein BE, Meissner A, Lander ES (2007) The mammalian epigenome. Cell 128:669–681. https://doi.org/10.1016/j.cell.2007.01.033
Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72. https://doi.org/10.1002/em.20347
Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608. https://doi.org/10.1016/j.plantsci.2007.09.002
Caparrotta S, Boni S, Taiti C et al (2018) Induction of priming by salt stress in neighboring plants. Environ Exp Bot 147:261–270. https://doi.org/10.1016/j.envexpbot.2017.12.017
Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896. https://doi.org/10.1038/nrg2179
Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139. https://doi.org/10.1016/j.pbi.2008.12.006
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot. https://doi.org/10.1093/jxb/erh005
Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451. https://doi.org/10.1016/j.tplants.2007.07.002
Conley AB, Jordan IK (2012) Endogenous retroviruses and the epigenome. In: Witzany G (ed) Viruses: essential agents of life. Springer, Dordrecht, pp 309–323. https://doi.org/10.1007/978-94-007-4899-6_16
Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR (2015) Priming for enhanced defense. Annu Rev Phytopathol 53:97–119. https://doi.org/10.1146/annurev-phyto-080614-120132
Conrath U, Beckers GJM, Flors V et al (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071. https://doi.org/10.1094/MPMI-19-1062
Correia B, Valledor L, Meijón M et al (2013) Is the interplay between epigenetic markers related to the acclimation of cork oak plants to high temperatures? PLoS ONE 8:e53543. https://doi.org/10.1371/journal.pone.0053543
Csiszár J, Brunner S, Horváth E et al (2018) Exogenously applied salicylic acid maintains redox homeostasis in salt-stressed Arabidopsis gr1 mutants expressing cytosolic roGFP1. Plant Growth Regul 86:181–194. https://doi.org/10.1007/s10725-018-0420-6
Dai LF, Chen YL, Luo XD et al (2015) Level and pattern of DNA methylation changes in rice cold tolerance introgression lines derived from Oryza rufipogon Griff. Euphytica 205:73–83. https://doi.org/10.1007/s10681-015-1389-0
Ding Y, Avramova Z, Fromm M (2011) The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J 66:735–744. https://doi.org/10.1111/j.1365-313X.2011.04534.x
Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nat Commun 3:740. https://doi.org/10.1038/ncomms1732
Dowen RH, Pelizzola M, Schmitz RJ et al (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci 109:E2183–E2191. https://doi.org/10.1073/pnas.1209329109
Dubin MJ, Zhang P, Meng D et al (2015) DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife 4:e05255. https://doi.org/10.7554/eLife.05255
Eckardt NA (2009) Deep sequencing maps the maize epigenomic landscape. Plant Cell Online 21:1024–1026. https://doi.org/10.1105/tpc.109.068064
Efimova MV, Khripach VA, Boyko EV et al (2018) The priming of potato plants induced by brassinosteroids reduces oxidative stress and increases salt tolerance. Dokl Biol Sci 478:33–36. https://doi.org/10.1134/S0012496618010106
Erpen L, Devi HS, Grosser JW, Dutt M (2018) Potential use of the DREB/ERF, MYB, NAC and WRKY transcription factors to improve abiotic and biotic stress in transgenic plants. Plant Cell Tissue Organ Cult 132(1):1–25. https://doi.org/10.1007/s11240-017-1320-6
Fan Y, Ma C, Huang Z et al (2018) Heat priming during early reproductive stages enhances thermo-tolerance to post-anthesis heat stress via improving photosynthesis and plant productivity in winter wheat (Triticum aestivum L.). Front Plant Sci 9:805. https://doi.org/10.3389/fpls.2018.00805
Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45. https://doi.org/10.1105/tpc.010441
Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431. https://doi.org/10.1093/aob/mcu217
Friedrich T, Faivre L, Bäurle I, Schubert D (2019) Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ 42:762–770. https://doi.org/10.1111/pce.13373
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863. https://doi.org/10.1146/annurev-arplant-042811-105606
Fujita M, Fujita Y, Maruyama K et al (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876. https://doi.org/10.1111/j.1365-313X.2004.02171.x
Fujita M, Fujita Y, Noutoshi Y et al (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442. https://doi.org/10.1016/j.pbi.2006.05.014
Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136. https://doi.org/10.1126/science.1148766
Gamir J, Cerezo M, Flors V (2014) The plasticity of priming phenomenon activates not only common metabolomic fingerprint but also specific responses against p. Cucumerina. Plant Signal Behav 9:e28916. https://doi.org/10.4161/psb.28916
Gharbi E, Lutts S, Dailly H, Quinet M (2018) Comparison between the impacts of two different modes of salicylic acid application on tomato (Solanum lycopersicum) responses to salinity. Plant Signal Behav 13(5):e1469361. https://doi.org/10.1080/15592324.2018.1469361
Gimenez E, Salinas M, Manzano-Agugliaro F (2018) Worldwide research on plant defense against biotic stresses as improvement for sustainable agriculture. Sustainability 10:391. https://doi.org/10.3390/su10020391
González RM, Ricardi MM, Iusem ND (2013) Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics 8:864–872. https://doi.org/10.4161/epi.25524
Gully K, Celton J-M, Degrave A et al (2019) Biotic stress-induced priming and de-priming of transcriptional memory in Arabidopsis and apple. Epigenomes 3:3. https://doi.org/10.3390/epigenomes3010003
He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435. https://doi.org/10.1146/annurev-arplant-042110-103806
Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci 104:5467–5472. https://doi.org/10.1073/pnas.0610266104
Herrera CM, Bazaga P (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol 20:1675–1688. https://doi.org/10.1111/j.1365-294X.2011.05026.x
Hilker M, Schwachtje J, Baier M et al (2016) Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev 91:1118–1133. https://doi.org/10.1111/brv.12215
Jakab G (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274. https://doi.org/10.1104/pp.105.065698
Jakab G, Cottier V, Toquin V et al (2001) β-Aminobutyric acid-induced resistance in plants. Eur J Plant Pathol 107:29–37. https://doi.org/10.1023/A:1008730721037
Jaskiewicz M, Conrath U, Peterhälnsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55. https://doi.org/10.1038/embor.2010.186
Jayakannan M, Bose J, Babourina O et al (2015) Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regul 76:25–40. https://doi.org/10.1007/s10725-015-0028-z
Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576. https://doi.org/10.1034/j.1399-3054.2002.1150411.x
Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292. https://doi.org/10.1007/s00442-006-0365-8
Kim JM, To TK, Seki M (2012) An epigenetic integrator: new insights into genome regulation, environmental stress responses and developmental controls by histone deacetylase 6. Plant Cell Physiol 53:794–800. https://doi.org/10.1093/pcp/pcs004
King GJ, Amoah S, Kurup S (2010) Exploring and exploiting epigenetic variation in crops. Genome 53:856–868. https://doi.org/10.1139/G10-059
Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55:1859–1863. https://doi.org/10.1093/pcp/pcu125
Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751. https://doi.org/10.1111/j.1469-8137.2012.04239.x
Köhler C, Wolff P, Spillane C (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Annu Rev Plant Biol 63:331–352. https://doi.org/10.1146/annurev-arplant-042811-105514
Lafos M, Kroll P, Hohenstatt ML, Thorpe FL, Clarenz O, Schubert D (2011) Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet 7:e1002040
Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18:124. https://doi.org/10.1186/s13059-017-1263-6
Lee K, Seo PJ (2014) Airborne signals from salt-stressed Arabidopsis plants trigger salinity tolerance in neighboring plants. Plant Signal Behav 9:e28392. https://doi.org/10.4161/psb.28392
Li H, Yan S, Zhao L et al (2014) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 14:105. https://doi.org/10.1186/1471-2229-14-105
Ling Y, Serrano N, Gao G et al (2018) Thermopriming triggers splicing memory in Arabidopsis. J Exp Bot 69:2659–2675. https://doi.org/10.1093/jxb/ery062
Liu W, Zhang Y, Yuan X et al (2015) Exogenous salicylic acid improves salinity tolerance of Nitraria tangutorum. Russ J Plant Physiol 63:132–142. https://doi.org/10.1134/S1021443716010118
Mahalingam R (2015) Consideration of combined stress: a crucial paradigm for improving multiple stress tolerance in plants. In: Combined stresses in plants: physiological, molecular, and biochemical aspects. Springer, Cham, pp 1–26. https://doi.org/10.1007/978-3-319-07899-1
Mimouni H, Wasti S, Manaa A et al (2016) Does salicylic acid (sa) improve tolerance to salt stress in plants? A study of sa effects on tomato plant growth, water dynamics, photosynthesis, and biochemical parameters. Omics 20:180–190. https://doi.org/10.1089/omi.2015.0161
Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274. https://doi.org/10.1016/j.pbi.2011.03.004
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19. https://doi.org/10.1016/j.tplants.2005.11.002
Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15:349–357. https://doi.org/10.1016/j.pbi.2012.05.006
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:e0537. https://doi.org/10.3389/fpls.2017.00537
Pastor V, Balmer A, Gamir J et al (2014) Preparing to fight back: generation and storage of priming compounds. Front Plant Sci 5:e0295. https://doi.org/10.3389/fpls.2014.00295
Pastor V, Luna E, Mauch-Mani B et al (2013) Primed plants do not forget. Environ Exp Bot 94:46–56. https://doi.org/10.1016/j.envexpbot.2012.02.013
Pikaard CS, Scheid OM (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a019315
Ramegowda V, Senthil-Kumar M (2015) The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J Plant Physiol 176:47–54. https://doi.org/10.1016/j.jplph.2014.11.008
Ramirez-Prado JS, Abulfaraj AA, Rayapuram N et al (2018) Plant immunity: from signaling to epigenetic control of defense. Trends Plant Sci 23:833–844. https://doi.org/10.1016/j.tplants.2018.06.004
Riechmann JL, Heard J, Martin G et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110. https://doi.org/10.1126/science.290.5499.2105
Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25:511–517. https://doi.org/10.1016/j.tig.2009.09.013
Rozema J, Flowers T (2008) Ecology: crops for a salinized world. Science 322:1478–1480. https://doi.org/10.1126/science.1168572
Sahu PP, Pandey G, Sharma N et al (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151–1159. https://doi.org/10.1007/s00299-013-1462-x
Saze H, Tsugane K, Kanno T, Nishimura T (2012) DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol 53:766–784. https://doi.org/10.1093/pcp/pcs008
Sheth BP, Thaker VS (2014) Plant systems biology: insights, advances and challenges. Planta 240:33–54. https://doi.org/10.1007/s00425-014-2059-5
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417. https://doi.org/10.1016/S1369-5266(03)00092-X
Silveira JAG, Carvalho FEL (2016) Proteomics, photosynthesis and salt resistance in crops: an integrative view. J Proteomics 143:24–35. https://doi.org/10.1016/j.jprot.2016.03.013
Singh PK, Gautam S (2013) Role of salicylic acid on physiological and biochemical mechanism of salinity stress tolerance in plants. Acta Physiol Plant 35:2345–2353. https://doi.org/10.1007/s11738-013-1279-9
Slama I, Abdelly C, Bouchereau A et al (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447. https://doi.org/10.1093/aob/mcu239
Slaughter A, Daniel X, Flors V et al (2012) Descendants of primed arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843. https://doi.org/10.1104/pp.111.191593
Song J, Irwin J, Dean C (2013) Remembering the prolonged cold of winter. Curr Biol 23:R807–R811. https://doi.org/10.1016/j.cub.2013.07.027
Song Y, Liu L, Feng Y et al (2015) Chilling and freezing induced alterations in cytosine methylation and its association with the cold tolerance of an alpine subnival plant Chorispora bungeana. PLoS ONE 10:e135485. https://doi.org/10.1371/journal.pone.0135485
Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilisation. Plant Growth Regul 49:77–83. https://doi.org/10.1007/s10725-006-0019-1
Tarhan Ç, Turgut-Kara N (2016) Epigenetics and applications in plants. In: Plant omics: trends and applications. Springer, Cham, pp 255–270. https://doi.org/10.1007/978-3-319-31703-8
Ton J, Jakab G (2007) Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Journal 17:987–999. https://doi.org/10.1105/tpc.104.029728
Ton J, D’Alessandro M, Jourdie V et al (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26. https://doi.org/10.1111/j.1365-313X.2006.02935.x
Van Oosten MJ, Di Stasio E, Cirillo V et al (2018) Root inoculation with Azotobacter chroococcum 76A enhances tomato plants adaptation to salt stress under low N conditions. BMC Plant Biol 18:205. https://doi.org/10.1186/s12870-018-1411-5
Wang X, Lai LF, Jiang D (2017) Priming: a promising strategy for crop production in response to future climate. J Integr Agric 16:2709–2716. https://doi.org/10.1016/S2095-3119(17)61786-6
Wasilewska A, Vlad F, Sirichandra C et al (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217. https://doi.org/10.1093/mp/ssm022
Whittle C, Otto S, Johnston M, Krochko J (2009) Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany-Botanique 87:650–657. https://doi.org/10.1139/B09-030
Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667–685
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94. https://doi.org/10.1016/j.tplants.2004.12.012
Yamamuro C, Zhu JK, Yang Z (2016) Epigenetic modifications and plant hormone action. Mol Plant 9(1):57–70
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539. https://doi.org/10.1111/nph.14920
Yong-Villalobos L, González-Morales SI, Wrobel K et al (2015) Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc Natl Acad Sci 112:E7293–E7302. https://doi.org/10.1073/pnas.1522301112
Zandalinas SI, Mittler R, Balfagón D et al (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12. https://doi.org/10.1111/ppl.12540
Zhang X (2008) The epigenetic landscape of plants. Science 320:489–492. https://doi.org/10.1126/science.1153996
Zheng Y, Ding Y, Sun X et al (2016) Histone deacetylase HDA9 negatively regulates salt and drought stress responsiveness in Arabidopsis. J Exp Bot 67:1703–1713. https://doi.org/10.1093/jxb/erv562
Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Zhu JK (2008) Epigenome sequencing comes of age. Cell 133:395–397. https://doi.org/10.1016/j.cell.2008.04.016
Zhu Q, Zhang J, Gao X et al (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12. https://doi.org/10.1016/j.gene.2010.02.011
Zong W, Zhong X, You J, Xiong L (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81:175–188. https://doi.org/10.1007/s11103-012-9990-2
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Turgut-Kara, N., Arikan, B. & Celik, H. Epigenetic memory and priming in plants. Genetica 148, 47–54 (2020). https://doi.org/10.1007/s10709-020-00093-4
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DOI: https://doi.org/10.1007/s10709-020-00093-4