Vegetal memory through the lens of transcriptomic changes – recent progress and future practical prospects for exploiting plant transcriptional memory

References

• Van Loon LC. The intelligent behavior of plants. Trends Plant Sci. 2016;21(4):286–16. doi:10.1016/j.tplants.2015.11.009.
   PubMed Web of Science ®Google Scholar
• Calvo P, Gagliano M, Souza GM, Trewavas A. Plants are intelligent, here’s how. Ann Bot. 2020;125(1):11–28. doi:10.1093/aob/mcz155.
   PubMed Web of Science ®Google Scholar
• Gagliano M, Abramson CI, Depczynski M. Plants learn and remember: lets get used to it. Oecologia. 2018;186(1):29–31. doi:10.1007/s00442-017-4029-7.
   PubMed Web of Science ®Google Scholar
• Mallatt J, Blatt MR, Draguhn A, Robinson DG, Taiz L. Debunking a myth: plant consciousness. Protoplasma. 2021;258(3):459–476. doi:10.1007/s00709-020-01579-w.
   PubMed Web of Science ®Google Scholar
• Nick P. Intelligence without neurons: a Turing Test for plants? Protoplasma. 2021;258(3):455–458. doi:10.1007/s00709-021-01642-0.
   PubMed Web of Science ®Google Scholar
• Trewavas A, Baluška F, Mancuso S, Calvo P. Consciousness facilitates plant behavior. Trends Plant Sci. 2020;25(3):216–217. doi:10.1016/j.tplants.2019.12.015.
   PubMed Web of Science ®Google Scholar
• Pfeffer W. Physiologische Untersuchungen. Leipzig, Verlag von Wilhelm Engelmann; 1873. p. 217. doi:10.5214/ans.0972-7531.1017309.
   Google Scholar
• Bose JC. Plant response as a Means of physiological investigation. London: Longmans, Green and Co; 1906. p. 781.
   Google Scholar
• Gagliano M, Renton M, Depczynski M, Mancuso S. Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia. 2014;175(1):63–72. doi:10.1007/s00442-013-2873-7.
   PubMed Web of Science ®Google Scholar
• Reed-Guy S, Gehris C, Shi M, Blumstein DT. Sensitive plant (mimosa pudica) hiding time depends on individual and state. PeerJ. 2017;5:e3598. doi:10.7717/peerj.3598.
   PubMed Web of Science ®Google Scholar
• De Houwer J, Barnes-Holmes D, Moors A. What is learning? On the nature and merits of a functional definition of learning. Psychon Bull Rev. 2013;20(4):631–642. doi:10.3758/s13423-013-0386-3.
   PubMed Web of Science ®Google Scholar
• Cooper A, Ton J, Kanyuka K, Hammond-Kosack K. Immune priming in plants: from the onset to transgenerational maintenance. Essays In Biochem. 2022;66(5):635–646. doi:10.1042/EBC20210082.
   PubMed Web of Science ®Google Scholar
• Harris CJ, Amtmann A, Ton J. Epigenetic processes in plant stress priming: open questions and new approaches. Curr Opin Plant Biol. 2023 Oct; 75:102432. doi:10.1016/j.pbi.2023.102432.
   PubMed Web of Science ®Google Scholar
• Hilker M, Schmülling T. Stress priming, memory, and signalling in plants. Plant Cell Environ. 2019;42(3):753–761. doi:10.1111/pce.13526.
   PubMed Web of Science ®Google Scholar
• Galviz Y, Souza GM, Lüttge U. The biological concept of stress revisited: relations of stress and memory of plants as a matter of space–time. Theor Exp Plant Physiol. 2022;34(2):239–264. doi:10.1007/s40626-022-00245-1.
   Web of Science ®Google Scholar
• Lichtenthaler HK. Vegetation stress: an introduction to the stress concept in plants. J Plant Physiol. 1996;148(1–2):4–14. doi:10.1016/S0176-1617(96)80287-2.
   Web of Science ®Google Scholar
• Aleklett K, Boddy L. Fungal behaviour: a new frontier in behavioural ecology. Trends In Ecol & Evol. 2021;36(9):787–796. doi:10.1016/j.tree.2021.05.006.
   PubMed Web of Science ®Google Scholar
• Zhang C, Kong Y, Xiang Q, Ma Y, Guo Q. Bacterial memory in antibiotic resistance evolution and nanotechnology in evolutionary biology. Iscience; 2023. doi:10.1016/j.isci.2023.107433.
   Google Scholar
• Milutinović B, Kurtz J. Immune memory in invertebrates. Semin Immunol. 2016;28(4):328–342). Academic Press. 10.1016/j.smim.2016.05.004.
   PubMed Web of Science ®Google Scholar
• Sharrock J, Sun JC. Innate immunological memory: from plants to animals. Curr Opin In Immunol. 2020;62:69–78. doi:10.1016/j.coi.2019.12.001.
   PubMed Web of Science ®Google Scholar
• Martin SJ, Grimwood PD, Morris RG. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci. 2000;23(1):649–711. doi:10.1146/annurev.neuro.23.1.649.
   PubMedGoogle Scholar
• Rosenberg T, Gal-Ben-Ari S, Dieterich DC, Kreutz MR, Ziv NE, Gundelfinger ED, Rosenblum K. The roles of protein expression in synaptic plasticity and memory consolidation. Front Mol Neurosci. 2014;7:86. doi:10.3389/fnmol.2014.00086.
   PubMed Web of Science ®Google Scholar
• Hilker M, Schwachtje J, Baier M, Balazadeh S, Bäurle I, Geiselhardt S, Hincha DK, Kunze R, Mueller-Roeber B, Rillig MC. et al. Priming and memory of stress responses in organisms lacking a nervous system. Biol Rev. 2016;91(4):1118–1133. doi:10.1111/brv.12215.
   PubMed Web of Science ®Google Scholar
• Reid CR, Latty T, Dussutour A, Beekman M. Slime mold uses an externalized spatial “memory” to navigate in complex environments. Proc Natl Acad Sci USA. 2012;109(43):17490–17494. doi:10.1073/pnas.1215037109.
   PubMed Web of Science ®Google Scholar
• Solé R, Moses M, Forrest S. Liquid brains, solid brains. Phil Trans R Soc B. 2019;374(1774):20190040. doi:10.1098/rstb.2019.0040.
   PubMed Web of Science ®Google Scholar
• Wang W, Wang X, Zhang J, Huang M, Cai J, Zhou Q, Dai T, Jiang D. Salicylic acid and cold priming induce late-spring freezing tolerance by maintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat. Plant Growth Regul. 2020;90(1):109–121. doi:10.1007/s10725-019-00553-8.
   Web of Science ®Google Scholar
• Galviz YC, Ribeiro RV, Souza GM. Yes, plants do have memory. Theor Exp Plant Physiol. 2020;32(3):195–202. doi:10.1007/s40626-020-00181-y.
   Web of Science ®Google Scholar
• Thellier M, Lüttge U. Plant memory: a tentative model. Plant Biol. 2013;15(1):1–12. doi:10.1111/j.1438-8677.2012.00674.x.
   PubMed Web of Science ®Google Scholar
• Stiller V, Sperry JS. Cavitation fatigue and its reversal in sunflower (Helianthus annuus L.). J Exp Botany. 2002;53(371):1155–1161. doi:10.1093/jexbot/53.371.1155.
   PubMed Web of Science ®Google Scholar
• Abramson CI, Chicas-Mosier AM. Learning in plants: lessons from Mimosa pudica. Front Psychol. 2016;7:417. doi:10.3389/fpsyg.2016.00417.
   PubMed Web of Science ®Google Scholar
• Vesper MJ, Evans ML. Time-dependent changes in the auxin sensitivity of coleoptile segments: apparent sensory adaptation. Plant Physiol. 1978;61(2):204–208. doi:10.1104/pp.61.2.204.
   PubMed Web of Science ®Google Scholar
• Chester KS. The problem of acquired physiological immunity in plants. The Q Rev Biol. 1933;8(3):275–324. doi:10.1086/394440.
   Google Scholar
• Mauch-Mani B, Baccelli I, Luna E, Flors V. Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol. 2017;68(1):485–512. doi:10.1146/annurev-arplant-042916-041132.
   PubMed Web of Science ®Google Scholar
• Wang X, Li Q, Xie J, Huang M, Cai J, Zhou Q, Dai T, Jiang D. Abscisic acid and jasmonic acid are involved in drought priming-induced tolerance to drought in wheat. Crop J. 2021;9(1):120–132. doi:10.1016/j.cj.2020.06.002.
   Google Scholar
• Yang Z, Zhi P, Chang C. Priming seeds for the future: plant immune memory and application in crop protection. Front Plant Sci. 2022;13:961840. doi:10.3389/fpls.2022.961840.
   PubMed Web of Science ®Google Scholar
• Liu H, Able AJ, Able JA. Priming crops for the future: rewiring stress memory. Trends Plant Sci. 2022;27(7):699–716. doi:10.1016/j.tplants.2021.11.015.
   PubMed Web of Science ®Google Scholar
• Dopp IJ, Yang X, Mackenzie SA. A new take on organelle‐mediated stress sensing in plants. New Phytol. 2021;230(6):2148–2153. doi:10.1111/nph.17333.
   PubMed Web of Science ®Google Scholar
• Fernanda Alves de Freitas Guedes FADFG, Paulo Eduardo Menezes-Silva PEM-S, Fábio Murilo DaMatta FMD, Alves-Ferreira M. Using transcriptomics to assess plant stress memory. Theor Exp Plant Physiol. 2019;31(1):47–58. doi:10.1007/s40626-018-0135-0.
   Web of Science ®Google Scholar
• Saze H. Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol. 2008;19(6):527–536. doi:10.1016/j.semcdb.2008.07.017.
   PubMed Web of Science ®Google Scholar
• Lloyd JPB, Lister R. Epigenome plasticity in plants. Nat Rev Genet. 2022;23(1):55–68. doi:10.1038/s41576-021-00407-y.
   PubMed Web of Science ®Google Scholar
• Guarino F, Cicatelli A, Castiglione S, Agius DR, Orhun GE, Fragkostefanakis S, Leclercq J, Dobránszki J, Kaiserli E, Lieberman-Lazarovich M. et al. An epigenetic alphabet of crop adaptation to climate change. Front Genet. 2022;16(13):818727. doi:10.3389/fgene.2022.818727.
   Google Scholar
• Gallusci P, Agius DR, Moschou PN, Dobránszki J, Kaiserli E, Martinelli F. Deep inside the epigenetic memories of stressed plants. Trends In Plant Sci. 2023;28(2):Sci.142–153. doi:10.1016/j.tplants.2022.09.004.
   PubMed Web of Science ®Google Scholar
• Wibowo A, Becker C, Marconi G, Durr J, Price J, Hagmann J, Papareddy R, Putra H, Kageyama J, Becker J. et al. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. Elife. 2016; doi:10.7554/eLife.13546.
   PubMed Web of Science ®Google Scholar
• Zhang H, Lang Z, Zhu JK. Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018;19(8):489–506. doi:10.1038/s41580-018-0016-z.
   PubMed Web of Science ®Google Scholar
• Agius DR, Kapazoglou A, Avramidou E, Baranek M, Carneros E, Caro E, Castiglione S, Cicatelli A, Radanovic A, Ebejer JP. et al. Exploring the crop epigenome: a comparison of DNA methylation profiling techniques. Front Plant Sci. 2023;30(14):1181039. doi:10.3389/fpls.2023.1181039.
   Google Scholar
• Candela-Ferre J, Diego-Martin B, Pérez-Alemany J, Gallego-Bartolomé J. Mind the gap: epigenetic regulation of chromatin accessibility in plants. Plant Physiol. 2024;194(4):1998–2016. doi:10.1093/plphys/kiae024.
   PubMed Web of Science ®Google Scholar
• Brenya E, Pervin M, Chen ZH, Tissue DT, Johnson S, Braam J, Cazzonelli CI. Mechanical stress acclimation in plants: linking hormones and somatic memory to thigmomorphogenesis. Plant Cell Environ. 2021;45(4):989–1010. doi:10.1111/pce.14252.
   Web of Science ®Google Scholar
• Garai S, Sopory SK. Memory of plants: present understanding. Nucleus. 2023;66(1):47–51. doi:10.1007/s13237-022-00399-y.
   Web of Science ®Google Scholar
• Gutiérrez-Marcos JF, Costa LM, Prà MD, Scholten S, Kranz E, Perez P, Dickinson HG. Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet. 2006;38(8):876–878. doi:10.1038/ng1828.
   PubMed Web of Science ®Google Scholar
• Jahnke S, Scholten S. Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol. 2009;19(19):1677–1681. doi:10.1016/j.cub.2009.08.053.
   PubMed Web of Science ®Google Scholar
• Lucht JM, Mauch-Mani B, Steiner HY, Metraux JP, Ryals J, Hohn B. Pathogen stress increases somatic recombination frequency in arabidopsis. Nat Genet. 2002;30(3):311–314. doi:10.1038/ng846.
   PubMed Web of Science ®Google Scholar
• Ries G, Buchholz G, Frohnmeyer H, Hohn B. UV-damage-mediated induction of homologous recombination in Arabidopsis is dependent on photosynthetically active radiation. Proc Natl Acad Sci USA. 2000;97(24):13425–13429. doi:10.1073/pnas.230251897.
   PubMed Web of Science ®Google Scholar
• Danchin E, Pocheville A, Rey O, Pujol B, Blanchet S. Epigenetically facilitated mutational assimilation: epigenetics as a hub within the inclusive evolutionary synthesis. Biol Rev. 2019;94(1):259–282. doi:10.1111/brv.12453.
   Web of Science ®Google Scholar
• 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(5):379–390. doi:10.1038/s41422-019-0145-8.
   PubMed Web of Science ®Google Scholar
• Galloway LF. Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytol. 2005;166(1):93–100. doi:10.1111/j.1469-8137.2004.01314.x.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Viejo M, Yakovlev I, Tengs T, Krokene P, Hytönen T, Fossdal CG, Fossdal CG. Major transcriptomic differences are induced by warmer temperature conditions experienced during asexual and sexual reproduction in Fragaria vesca ecotypes. Front Plant Sci. 2023;14:1213311. doi:10.3389/fpls.2023.1213311.
   PubMed Web of Science ®Google Scholar
• Avramova Z. Transcriptional ‘memory’of a stress: transient chromatin and memory (epigenetic) marks at stress‐response genes. Plant J. 2015;83(1):149–159. doi:10.1111/tpj.12832.
   PubMed Web of Science ®Google Scholar
• Ding Y, Fromm M, Avramova Z. Multiple exposures to drought’train’transcriptional responses in Arabidopsis. Nat. Commun. 2012;3(1):1–9. doi:10.1038/ncomms1732.
   Google Scholar
• Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. 2013;13(1):229. doi: 10.1186/1471-2229-13-229.
   PubMedGoogle Scholar
• 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 Web of Science ®Google Scholar
• Berry S, Hartley M, Olsson TS, Dean C, Howard M. Local chromatin environment of a Polycomb target gene instructs its own epigenetic inheritance. eLife. 2015;4:e07205. doi:10.7554/eLife.07205.
   PubMed Web of Science ®Google Scholar
• Angel A, Song J, Dean C, Howard M. A Polycomb-based switch underlying quantitative epigenetic memory. Nature. 2011;476(7358):105–108. doi:10.1038/nature10241.
   PubMed Web of Science ®Google Scholar
• Iwasaki M, Paszkowski J. Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. Proc Natl Acad Sci. 2014;111(23):8547–8552. doi:10.1073/pnas.1402275111.
   PubMed Web of Science ®Google Scholar
• Erdmann RM, Picard CL. RNA-directed DNA methylation. PLOS Genet. 2020;16(10):e1009034. doi:10.1371/journal.pgen.1009034.
   PubMed Web of Science ®Google Scholar
• Wassenegger M, Heimes S, Riedel L, Sänger HL. RNA-directed de novo methylation of genomic sequences in plants. Cell. 1994;76(3):567–576. doi:10.1016/0092-8674(94)90119-8.
   PubMed Web of Science ®Google Scholar
• Gutzat R, Scheid OM. Epigenetic responses to stress: triple defense? Curr Opin Plant Biol. 2012;15(5):568–573. doi:10.1016/j.pbi.2012.08.007.
   PubMed Web of Science ®Google Scholar
• Huang J, Yang M, Zhang X. The function of small RNAs in plant biotic stress response. J Intgr Plant Biol. 2016;58(4):312–327. doi:10.1111/jipb.12463.
   Web of Science ®Google Scholar
• Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. 2012;158(2):854–863. doi:10.1104/pp.111.187831.
   PubMed Web of Science ®Google Scholar
• Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollander J, Meins F, Kovalchuk I. Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLOS ONE. 2010;5(3):e9514. doi:10.1371/journal.pone.0009514.
   PubMed Web of Science ®Google Scholar
• Naumann U, Daxinger L, Kanno T, Eun C, Long Q, Lorkovic ZJ, Matzke M, Matzke AJ. Genetic evidence that DNA methyltransferase DRM2 has a direct catalytic role in RNA-directed DNA methylation in Arabidopsis thaliana. Genetics. 2011;187(3):977–979. doi:10.1534/genetics.110.125401.
   PubMed Web of Science ®Google Scholar
• Cuerda-Gil D, Slotkin RK. Non-canonical RNA-directed DNA methylation. Nat Plants. 2016;2(11):1–8. doi:10.1038/nplants.2016.163.
   Web of Science ®Google Scholar
• Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Ecker JR, Whelan J, Lister R. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. Elife. 2015;4:09343. doi:10.7554/eLife.09343.
   Web of Science ®Google Scholar
• Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8(4):272–285. doi:10.1038/nrg2072.
   PubMed Web of Science ®Google Scholar
• Chan SWL, Henderson IR, Zhang X, Shah G, Chien JSC, Jacobsen SE, Doebley J. RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in arabidopsis. PLOS Genet. 2006;2(6):e83. doi:10.1371/journal.pgen.0020083.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Jampala P, Garhewal A, Lodha M. Functions of long non-coding RNA in Arabidopsis thaliana. Plant Signaling & Behav. 2021;16(9):1925440. doi:10.1080/15592324.2021.1925440.
   PubMed Web of Science ®Google Scholar
• Song X, Li Y, Cao X, Qi Y. MicroRNAs and their regulatory roles in plant–environment interactions. Annu Rev Plant Biol. 2019;70(1):489–525. doi:10.1146/annurev-arplant-050718-100334.
   PubMed Web of Science ®Google Scholar
• Yu Y, Zhang Y, Chen X, Chen Y. Plant noncoding RNAs: hidden players in development and stress responses. Annu Rev Cell And Dev Biol. 2019;35(1):407–431. doi:10.1146/annurev-cellbio-100818-125218.
   PubMedGoogle Scholar
• Zhang Y, Zhou Y, Zhu W, Liu J, Cheng F. Non-coding RNAs fine-tune the balance between plant growth and abiotic stress tolerance. Front Plant Sci. 2022;13:965745. doi:10.3389/fpls.2022.965745.
   PubMed Web of Science ®Google Scholar
• Lucero L, Ferrero L, Fonouni‐Farde C, Ariel F. Functional classification of plant long noncoding RNAs: a transcript is known by the company it keeps. New Phytol. 2021;229(3):1251–1260. doi:10.1111/nph.16903.
   PubMed Web of Science ®Google Scholar
• Wu H, Yang L, Chen LL. The diversity of long noncoding RNAs and their generation. Trends Genet. 2017;33(8):540–552. doi:10.1016/j.tig.2017.05.004.
   PubMed Web of Science ®Google Scholar
• Fan C, Zhiqiang H, Jiahong Y, Guanglin L. Genome-wide identification and functional analysis of lincRNAs acting as miRNA targets or decoys in maize. BMC Genom. 2015;16(1):1–19. doi:10.1186/s12864-015-2024-0.
   PubMedGoogle Scholar
• Jha UC, Nayyar H, Jha R, Khurshid M, Zhou M, Mantri N, Siddique KH. Long non-coding RNAs: emerging players regulating plant abiotic stress response and adaptation. BMC Plant Biol. 2020;20(1):1–20. doi:10.1186/s12870-020-02595-x.
   PubMed Web of Science ®Google Scholar
• Laurent GS, Wahlestedt C, Kapranov P. The landscape of long noncoding RNA classification. Trends Genet. 2015;31(5):239–251. doi:10.1016/j.tig.2015.03.007.
   PubMed Web of Science ®Google Scholar
• Bourgeois Y, Boissinot S. On the population dynamics of junk: a review on the population genomics of transposable elements. Genes. 2019;10(6):419. doi:10.3390/genes10060419.
   PubMed Web of Science ®Google Scholar
• Wang D, Qu Z, Yang L, Zhang Q, Liu ZH, Do T, Adelson DL, Wang ZY, Searle I, Zhu JK. Transposable elements (TE s) contribute to stress‐related long intergenic noncoding RNA s in plants. Plant J. 2017;90(1):133–146. doi:10.1111/tpj.13481.
   PubMed Web of Science ®Google Scholar
• Ma L, Bajic VB, Zhang Z. On the classification of long non-coding RNAs. RNA Biol. 2013;10(6):924–933. doi:10.4161/rna.24604.
   PubMed Web of Science ®Google Scholar
• Yu X, Yang J, Li X, Liu X, Sun C, Wu F, He Y. Global analysis of cis-natural antisense transcripts and their heat-responsive nat-siRNAs in Brassica rapa. BMC Plant Biol. 2013;13(1):1–13. doi:10.1186/1471-2229-13-208.
   PubMedGoogle Scholar
• Chu Q, Bai P, Zhu X, Zhang X, Mao L, Zhu Q-H, Fan L, Ye C-Y. Characteristics of plant circular RNAs. Brief Bioinf. 2020;21(1):135–143. doi:10.1093/bib/bby111.
   PubMed Web of Science ®Google Scholar
• Wang HLV, Chekanova JA. Long noncoding RNAs in plants. Adv Exp Med Biol. 2017;1008:133–154. doi:10.1007/978-981-10-5203-3_5.
   PubMed Web of Science ®Google Scholar
• Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv. 2016;2(2):e1501340. doi:10.1126/sciadv.1501340.
   PubMed Web of Science ®Google Scholar
• Cools T, De Veylder L. DNA stress checkpoint control and plant development. Curr Opin Plant Biol. 2009;12(1):23–28. doi:10.1016/j.pbi.2008.09.012.
   PubMed Web of Science ®Google Scholar
• Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR. Protein degradation–an alternative respiratory substrate for stressed plants. Trends Plant Sci. 2011;16(9):489–498. doi:10.1016/j.tplants.2011.05.008.
   PubMed Web of Science ®Google Scholar
• Christie M, Brosnan CA, Rothnagel JA, Carroll BJ. RNA decay and RNA silencing in plants: competition or collaboration? Front Plant Sci. 2011;2:99. doi:10.3389/fpls.2011.00099.
   PubMed Web of Science ®Google Scholar
• Jiang D, Berger F. DNA replication–coupled histone modification maintains polycomb gene silencing in plants. Science. 2017;357(6356):1146–1149. doi:10.1126/science.aan4965.
   PubMed Web of Science ®Google Scholar
• Crevillén P, Yang H, Cui X, Greeff C, Trick M, Qiu Q, Cao X, Dean C. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature. 2014;515(7528):587–590. doi:10.1038/nature13722.
   PubMed Web of Science ®Google Scholar
• Borg M, Jacob Y, Susaki D, LeBlanc C, Buendía D, Axelsson E, Kawashima T, Voigt P, Boavida L, Becker J. et al. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat Cell Biol. 2020;22(6):621–629. doi:10.1038/s41556-020-0515-y.
   PubMed Web of Science ®Google Scholar
• Antoniou C, Savvides A, Christou A, Fotopoulos V. Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr Opin Plant Biol. 2016;33:101–107. doi:10.1016/j.pbi.2016.06.020.
   PubMed Web of Science ®Google Scholar
• Bond DM, Baulcombe DC. Small RNAs and heritable epigenetic variation in plants. Trends Cell Biol. 2014;24(2):100–107. doi:10.1016/j.tcb.2013.08.001.
   PubMed Web of Science ®Google Scholar
• Byun YJ, Koo MY, Joo HJ, Ha‐Lee YM, Lee DH. Comparative analysis of gene expression under cold acclimation, deacclimation and reacclimation in arabidopsis. Physiol Plant. 2014;152(2):256–274. doi:10.1111/ppl.12163.
   PubMed Web of Science ®Google Scholar
• Iba K. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol. 2002;53(1):225–245. doi:10.1146/annurev.arplant.53.100201.160729.
   PubMed Web of Science ®Google Scholar
• Thomashow MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol. 1999;50(1):571–599. doi:10.1146/annurev.arplant.50.1.571.
   PubMed Web of Science ®Google Scholar
• Kosová K, Vítámvás P, Planchon S, Renaut J, Vanková R, Prášil IT. Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. J Proteome Res. 2013;12(11):4830–4845. doi:10.1021/pr400600g.
   PubMed Web of Science ®Google Scholar
• Ding Y, Shi Y, Yang S. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol. 2019;222(4):1690–1704. doi:10.1111/nph.15696.
   PubMed Web of Science ®Google Scholar
• Xue GP, Sadat S, Drenth J, McIntyre CL. The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes. J Exp Bot. 2014;65(2):539–557. doi:10.1093/jxb/ert399.
   PubMed Web of Science ®Google Scholar
• Singh AK, Dhanapal S, Finkelshtein A, Chamovitz DA. CSN5A subunit of COP9 signalosome is required for resetting transcriptional stress memory after recurrent heat stress in arabidopsis. Biomolecules. 2021;11(5):668. doi:10.3390/biom11050668.
   PubMed Web of Science ®Google Scholar
• Kim TH, Hofmann K, Von Arnim AG, Chamovitz DA. PCI complexes: pretty complex interactions in diverse signaling pathways. Trends Plant Sci. 2001;6(8):379–386. doi:10.1016/s1360-1385(01)02015-5.
   PubMed Web of Science ®Google Scholar
• Hidvégi N, Gulyás A, Dobránszki J. Ultrasound, as a hypomethylating agent, remodels DNA methylation and alters mRNA transcription in winter wheat (Triticum aestivum L.) seedlings. Physiol Plant. 2022;174(5):e13777. doi:10.1111/ppl.13777.
   PubMed Web of Science ®Google Scholar
• Ben Abdallah M, Methenni K, Taamalli W, Hessini K, Ben Youssef N. Cross-priming approach induced beneficial metabolic adjustments and repair processes during subsequent drought in olive. Water. 2022;14(24):4050. doi:10.3390/w14244050.
   Web of Science ®Google Scholar
• Friedrich T, Faivre L, Bäurle I, Schubert D. Chromatin‐based mechanisms of temperature memory in plants. Plant Cell Environ. 2019;42(3):762–770. doi:10.1111/pce.13373.
   PubMed Web of Science ®Google Scholar
• Johnson R, Puthur JT. 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 Web of Science ®Google Scholar
• Wang X, Vignjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B. Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regul. 2015;75(3):677–687. doi:10.1007/s10725-014-9969-x.
   Web of Science ®Google Scholar
• Brenya E, Chen ZH, Tissue D, Papanicolaou A, Cazzonelli CI. Prior exposure of Arabidopsis seedlings to mechanical stress heightens jasmonic acid-mediated defense against necrotrophic pathogens. BMC Plant Biol. 2020;20(1):548. doi:10.1186/s12870-020-02759-9.
   PubMed Web of Science ®Google Scholar
• Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol. 2005;139(1):267–274. doi:10.1104/pp.105.065698.
   PubMed Web of Science ®Google Scholar
• Capiati DA, País SM, Téllez-Iñón MT. Wounding increases salt tolerance in tomato plants: evidence on the participation of calmodulin-like activities in cross-tolerance signalling. J Exp Bot. 2006;57(10):2391–2400. doi:10.1093/jxb/erj212.
   PubMed Web of Science ®Google Scholar
• Hsu YT, Kao CH. Heat shock-mediated H2O2 accumulation and protection against Cd toxicity in rice seedlings. Plant Soil. 2007;300(1–2):137–147. doi:10.1007/s11104-007-9396-0.
   Web of Science ®Google Scholar
• Streb P, Aubert S, Gout E, Feierabend J, Bligny R. Cross tolerance to heavy-metal and cold-induced photoinhibiton in leaves of Pisum sativum acclimated to low temperature. Physiol Mol Biol Plants. 2008;14(3):185–193. doi:10.1007/s12298-008-0018-y.
   PubMedGoogle Scholar
• Salama KH, Mansour MM, Hassan NS. Choline priming improves salt tolerance in wheat (Triticum aestivum L.). Aust J Basic Appl Sci. 2011;5(11):126–132.
   Google Scholar
• Kreyling J, Wiesenberg GL, Thiel D, Wohlfart C, Huber G, Walter J, Jentschd A, Konnert M, Beierkuhnlein C. Cold hardiness of Pinus nigra Arnold as influenced by geographic origin, warming, and extreme summer drought. Environ Exp Bot. 2012;78:99–108. doi:10.1016/j.envexpbot.2011.12.026.
   Web of Science ®Google Scholar
• Hossain MA, Mostofa MG, Fujita M. Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings. J Plant Sci Mol Breed. 2013;2(1):2. doi:10.7243/2050-2389-2-2.
   Google Scholar
• Hossain MA, Mostofa MG, Fujita M. Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (Brassica campestris L.) seedlings. Mol Plant Breed. 2013;4(7):50–70. doi:10.5376/mpb.2013.04.0007.
   Google Scholar
• Faralli M, Lektemur C, Rosellini D, Gürel F. Effects of heat shock on salinity tolerance in barley (hordeum vulgare L.): plant growth and stress-related gene transcription. Biol Plant. 2015;59(3):537–546g. doi:10.1007/s10535-015-0518-x.
   Web of Science ®Google Scholar
• Kataria S, Baghel L, Jain M, Guruprasad KN. Magnetopriming regulates antioxidant defense system in soybean against salt stress. Biocatal Agric Biotechnol. 2019;18:101090. doi:10.1016/j.bcab.2019.101090.
   Web of Science ®Google Scholar
• Shumaila S, Ullah S. Mitigation of salinity-induced damages in capsicum annum l. (sweet pepper) seedlings using priming techniques: a future perspective of climate change in the region. Commun Soil Sci Plant Anal. 2020;51(12):1602–1625. doi:10.1080/00103624.2020.1791154.
   Web of Science ®Google Scholar
• Yadav R, Juneja S, Kumar S. Cross priming with drought improves heat-tolerance in chickpea (Cicer arietinum L.) by stimulating small heat shock proteins and antioxidative defense. Environ Sustain. 2021;4(1):171–182. doi:10.1007/s42398-020-00156-4.
   Google Scholar
• Sáenz-de LOD, Morales LO, Strid Å, Torres-Pacheco I, Guevara-González RG. Ultraviolet-B exposure and exogenous hydrogen peroxide application lead to cross-tolerance toward drought in Nicotiana tabacum L. Physiol Plant. 2021;173(3):666–679. doi:10.1111/ppl.13448.
   PubMed Web of Science ®Google Scholar
• Hossain MA, Li ZG, Hoque TSBD, Fujita M, Munné-Bosch S, Munné-Bosch S. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma. 2018;255(1):399–412. doi:10.1007/s00709-017-1150-8.
   PubMed Web of Science ®Google Scholar
• Cai Q, He B, Kogel KH, Jin H. Cross-kingdom RNA trafficking and environmental RNAi—nature’s blueprint for modern crop protection strategies. Curr Opin Microbiol. 2018;46:58–64. doi:10.1016/j.mib.2018.02.003.
   PubMed Web of Science ®Google Scholar
• Loreti E, Perata P. Mobile plant microRNAs allow communication within and between organisms. New Phytol. 2022;235(6):2176–2182. doi:10.1111/nph.18360.
   PubMed Web of Science ®Google Scholar
• Zhang T, Zhao YL, Zhao JH, Wang S, Jin Y, Chen ZQ, Guo HS, Hua C-L, Ding S-W, Guo H-S. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat Plants. 2016;2(10):1–6. doi:10.1038/nplants.2016.153.
   Web of Science ®Google Scholar
• Pavlov IP G. V. Anrep. Translated and Edited by. Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. London: Oxford University Press; 1927.
   Google Scholar
• Gagliano M. Inside the vegetal mind: on the cognitive abilities of plants. In: Baluska F, editors. Memory and learning in plants. Signaling and communication in plants. Springer International publishing AG; 2018. p. 215–220. doi:10.1007/978-3-31975596-0_11.
   Google Scholar
• Gagliano M, Vyazovskiy B VV., Grimonprez AA, M, Depczynski M, Grimonprez M. Learning by association in plants. Sci Rep. 2016;6(1):38427. doi:10.1038/srep38427.
   PubMedGoogle Scholar
• Markel K. Pavlov’s pea plants? Not so fast. An attempted replication of Gagliano et al. eLife. 2016;9:e57614. doi:10.1101/2020.04.05.026823.
   Google Scholar
• Gagliano M, Vyazovskiy VV, Borbély AA, Depczynski M, Radford B. Comment on ‘lack of evidence for associative learning in pea plants’ eLife. eLife. 2020;9:e61141. doi:10.7554/eLife.61141.
   PubMed Web of Science ®Google Scholar
• Markel K. Response to comment on ‘lack of evidence for associative learning in pea plants’. eLife. 2020;9:e61689. doi:10.7554/eLife.61689.
   PubMed Web of Science ®Google Scholar
• Plesser HE. Reproducibility vs. replicability: a brief history of a confused terminology. Front Neuroinform. 2018;11:1309. doi:10.3389/fninf.2017.00076.
   Web of Science ®Google Scholar
• Cvrčková F, Konrádová H. Associative learning in plants: light quality history may matter. Biocell. 2022;46(3):645–649. doi:10.32604/biocell.2022.018114.
   Web of Science ®Google Scholar
• Bhandawat A, Jayaswall K, Sharma H, Roy J. Sound as a stimulus in associative learning for heat stress in arabidopsis. Commun Integr Biol. 2020;13(1):1–5. doi:10.1080/19420889.2020.1713426.
   PubMedGoogle Scholar
• Burgos JE. Is a nervous system necessary for learning? Perspect Behav Sci. 2018;41(2):343–368. doi:10.1007/s40614-018-00179-7.
   PubMed Web of Science ®Google Scholar
• Lyon P. The cognitive cell: bacterial behavior reconsidered. Front Microbiol. 2015;6:1292. doi:10.3389/fmicb.2015.00264.
   PubMedGoogle Scholar
• Molvray M. Biological factors in the evolution of intelligence. 2007 [accessed 2022 Feb 14]. http://www.molvray.com/sf/exobio/recog.htm.
   Google Scholar
• Campbell BM, Thornton P, Zougmoré R, Van Asten P, Lipper L. Sustainable intensification: what is its role in climate smart agriculture? Curr Opin Environ. 2014;8:39–43. doi:10.1016/j.cosust.2014.07.002.
   Web of Science ®Google Scholar
• Varotto S, Tani E, Abraham E, Krugman T, Kapazoglou A, Melzer R, Radanović A, Miladinović D. Epigenetics: possible applications in climate-smart crop breeding. J Exp Bot. 2020;71(17):5223–5236. doi:10.1093/jxb/eraa188.
   PubMed Web of Science ®Google Scholar