Time dynamics of stress legacy in clonal transgenerational effects: A case study on Trifolium repens

. 2022 May ; 12 (5) : e8959. [epub] 20220524

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35646308

Stress can be remembered by plants in a form of stress legacy that can alter future phenotypes of previously stressed plants and even phenotypes of their offspring. DNA methylation belongs among the mechanisms mediating the stress legacy. It is however not known for how long the stress legacy is carried by plants. If the legacy is long-lasting, it can become maladaptive in situations when parental-offspring environment do not match. We investigated for how long after the last exposure of a parental plant to drought can the phenotype of its clonal offspring be altered. We grew parental plants of three genotypes of Trifolium repens for five months either in control conditions or in control conditions that were interrupted with intense drought periods applied for two months in four different time slots. We also treated half of the parental plants with a demethylating agent (5-azacytidine, 5-azaC) to test for the potential role of DNA methylation in the stress memory. Then, we transplanted parental cuttings (ramets) individually to control environment and allowed them to produce offspring ramets for two months. The drought stress experienced by parents affected phenotypes of offspring ramets. The stress legacy resulted in enhanced number of offspring ramets originating from plants that experienced drought stress even 56 days before their transplantation to the control environment. 5-azaC altered transgenerational effects on offspring ramets. We confirmed that drought stress can trigger transgenerational effects in T. repens that is very likely mediated by DNA methylation. Most importantly, the stress legacy in parental plants persisted for at least 8 weeks suggesting that the stress legacy can persist in a clonal plant Trifolium repens for relatively long period. We suggest that the stress legacy should be considered in future ecological studies on clonal plants.

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Avramova, Z. (2015). Transcriptional ‘memory’ of a stress; transient chromatin and memory (epigenetic) marks at stress response genes. Plant Journal, 83, 149–159. 10.1111/tpj.12832 PubMed DOI

Bates, D. , Maechler, M. , Bolker, B. , & Walker, S. (2015). Fitting linear mixed effects models using lme4. J. Stat. Soft, 67, 1–48.

Becker, C. , Hagmann, J. , Müller, J. , Koenig, D. , Stegle, O. , Borgwardt, K. , & Weigel, D. (2011). Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature, 480, 245–249. 10.1038/nature10555 PubMed DOI

Bossdorf, O. , Richards, C. L. , & Pigliucci, M. (2008). Epigenetics for ecologists. Ecology Letters, 11(2), 106–115. PubMed

Boyko, A. , Blevins, T. , Yao, Y. L. , Golubov, A. , Bilichak, A. , Ilnytskyy, Y. , Hollander, J. , Meins, F. , & Kovalchuk, I. (2010). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of DICER‐LIKE proteins. PLoS One, 5, e9514. PubMed PMC

Boyko, A. , & Kovalchuk, I. (2011). Genome instability and epigenetic modification‐ heritable responses to environmental stress? Current Opinion Plant Biology, 14, 260–266. 10.1016/j.pbi.2011.03.003 PubMed DOI

Bruce, T. J. , Matthes, M. C. , Napier, J. A. , & Pickett, J. A. (2007). Stressful “memories” of plants: evidence and possible mechanisms. Plant Science, 173, 603–608. 10.1016/j.plantsci.2007.09.002 DOI

Burdon, J. J. (1983). Biological flora of the British Isles: Trifolium repens . Journal of Ecology, 71, 307–330.

Crisp, P. A. , Ganguly, D. , Eichten, S. R. , Borevitz, J. O. , & Pogson, B. J. (2016). Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Science Advances, 2, 1–14. 10.1126/sciadv.1501340 PubMed DOI PMC

Cullins, C. A. (1973). DNA differences between flax genotrophs. Nature, 243, 515–516. 10.1038/243515a0 PubMed DOI

Dai, A. (2012). Increasing drought under global warming in observations and models. Nature Climate Change, 3, 52.

de Mendiburu, F. (2020). agricolae: Statistical procedures for agricultural research. R package version 1.3‐2. https://CRAN.R‐project.org/package=agricolae

Ding, Y. , Fromm, M. , & Avramova, Z. (2012). Multiple exposures to drought “train” transcriptional responses in Arabidopsis. Nature Communications, 3, 740. 10.1038/ncomms1732 PubMed DOI

Ding, Y. , Liu, N. , Virlouvet, L. , Riethoven, J. J. , Fromm, M. , & Avramova, Z. (2013). Four distinct types of dehydration stress memory genes in Arabidopsis thaliana . BMC Plant Biology, 13, 229. 10.1186/1471-2229-13-229 PubMed DOI PMC

Ding, Y. , Virlouvet, L. , Liu, N. , Riethoven, J. J. , Fromm, M. , & Avramova, Z. (2014). Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana . BMC Plant Biology, 14, 141. 10.1186/1471-2229-14-141 PubMed DOI PMC

Douhovnikoff, V. , & Dodd, R. S. (2015). Epigenetics: a potential mechanism for clonal plant success. Plant Ecology, 216(2), 227–233. 10.1007/s11258-014-0430-z DOI

Gómez, S. , Latzel, V. , Verhulst, Y. , & Stuefer, J. F. (2007). Costs and benefits of induced resistance in a clonal plant network. Oecologia, 153, 921–930. 10.1007/s00442-007-0792-1 PubMed DOI PMC

González, A. P. , Preite, V. , Verhoeven, K. J. F. , & Latzel, V. (2018). Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens . Frontiers in Plant Science, 9, 1677. 10.3389/fpls.2018.01677 PubMed DOI PMC

González, R. A. P. , Chrtek, J. , Dobrev, P. I. , Dumalasová, V. , Fehrer, J. , Latzel, V. , & Mráz, P. (2016). Stress‐induced memory alters growth of clonal offspring of white clover (Trifolium repens). American Journal of Botany, 103(9), 1567–1574. 10.3732/ajb.1500526 PubMed DOI

González, R. A. P. , Dumalasová, V. , Rosenthal, J. , Skuhrovec, J. , & Latzel, V. (2017). The role of transgenerational effects in adaptation of clonal offspring of white clover (Trifolium repens) to drought and herbivory. Evolutionary Ecology, 31(3), 345–361. 10.1007/s10682-016-9844-5 DOI

Hay, M. J. M. , Newton, P. C. D. , Robin, C. , & Cresswell, A. (2001). Branching responses of a plagiotropic clonal herb to localised incidence of light simulating that reflected from vegetation. Oecologia, 127, 185–190. 10.1007/s004420000582 PubMed DOI

Hilker, M. , & Schmülling, T. (2019). Stress priming, memory, and signalling in plants. Plant and Cell Environment, 42(3), 753–761. 10.1111/pce.13526 PubMed DOI

Iwasaki, M. , & Paszkowski, J. (2014). Epigenetic memory in plants. EMBO Journal, 33(18), 1987–1998. 10.15252/embj.201488883 PubMed DOI PMC

Jiang, J. , Qian, Q. , Ma, B. J. , & Gao, Z. Y. (2014). Epigenetic variation and its application in crop improvement. Hereditas, 36(5), 469–475. (in Chinese with English abstract). PubMed

Klimeš, L. , Klimešová, J. , & Hendriks, R. (1997). Clonal plant architecture: A comparative analysis of form and function. In de Kroon H. & van Groenendael J. M. (Eds.), The ecology and evolution of clonal plants (pp. 1–29). Backhuys.

Latzel, V. , Janeček, Š. , Doležal, J. , Klimešová, J. , & Bossdorf, O. (2014). Adaptive transgenerational plasticity in the perennial Plantago lanceolate . Oikos, 123(1), 41–46.

Latzel, V. , & Klimešová, J. (2010). Year‐to‐year changes in expression of maternal effects in perennial plants. Basic and Applied Ecology, 11(8), 702–708. 10.1016/j.baae.2010.09.004 DOI

Latzel, V. , & Münzbergová, Z. (2018). Anticipatory behavior of the clonal plant Fragaria vesca . Frontiers Plant Science, 9, 1847. 10.3389/fpls.2018.01847 PubMed DOI PMC

Li, P. , Yang, H. , Wang, L. U. , Liu, H. , Huo, H. , Zhang, C. , Liu, A. , Zhu, A. , Hu, J. , Lin, Y. , & Liu, L. I. (2019). Physiological and transcriptome analyses reveal short‐term responses and formation of memory under drought stress in rice. Frontiers in Genetices, 10, 55. 10.3389/fgene.2019.00055 PubMed DOI PMC

Li, X. , Cai, J. , Liu, F. , Dai, T. , Cao, W. , & Jiang, D. (2014). Cold priming drives the sub‐cellular antioxidant systems to protect photosynthetic electron transport against subsequent low temperature stress in winter wheat. Plant Physiology Biochemistry, 82, 34–43. 10.1016/j.plaphy.2014.05.005 PubMed DOI

Li, X. N. , & Liu, F. L. (2016). Drought stress memory and drought stress tolerance in plants: biochemical and molecular basis. Drought Stress Tolerance in Plants, 1, 17–44.

Li, X. , Zhu, J. D. , Hu, F. Y. , Ge, S. , Ye, M. Z. , Xiang, H. , Zhang, G. J. , Zheng, X. M. , Zhang, H. Y. , Zhang, S. L. , Li, Q. , Luo, R. B. , Yu, C. , Yu, J. , Sun, J. F. , Zou, X. Y. , Cao, X. F. , Xie, X. F. , Wang, J. , & Wang, W. (2012). Single‐base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics, 13, 300. 10.1186/1471-2164-13-300 PubMed DOI PMC

Lukic, N. , Kukavica, B. , Davidovic‐Plavsic, B. , Hasanagic, D. , & Walter, J. (2020). Plant stress memory is linked to high levels of anti‐oxidative enzymes over several weeks. Environmental and Experimental Botany, 178, 104166. 10.1016/j.envexpbot.2020.104166 DOI

Mcintyre, P. J. , & Strauss, S. Y. (2014). Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments. Ecology and Evolution, 28(2), 229–246. 10.1007/s10682-013-9670-y DOI

Mirouze, M. , & Paszkowski, J. (2011). Epigenetic contribution to stress adaptation in plants. Current Opinion Plant Biology, 14, 267–274. 10.1016/j.pbi.2011.03.004 PubMed DOI

Molinier, J. , Ries, G. , Zipfel, C. , & Hohn, B. (2006). Transgeneration memory of stress in plants. Nature, 442, 1046–1049. 10.1038/nature05022 PubMed DOI

Monneveux, P. , Ramírez, D. A. , & Pino, M. T. (2013). Drought tolerance in potato (S. tuberosum L.) Can we learn from drought tolerance research in cereals? Plant Science, 205–206, 76–86. PubMed

Münzbergová, Z. , Latzel, V. , Šurinová, M. , & Hadincová, V. (2019). DNA methylation as a possible mechanism affecting ability of natural populations to adapt to changing climate. Oikos, 128, 124–134.

Pascual, J. , Cañal, M. J. , Correia, B. , Escandon, M. , Hasbún, R. , Meijón, M. , Pinto, G. , & Valledor, L. (2014). Can epigenetics help forest plants to adapt to climate change? In Alvarez‐Venegas R., De la Peña C., & Armando C.‐M. (Eds.), Epigenetics in plants of agronomic importance: Fundamentals and applications (pp. 125–146). Springer International Publishing.

Paszkowski, J. , & Grossniklaus, U. (2011). Selected aspects of transgenerational epigenetic inheritance and resetting in plants. Current Opinion Plant Biology, 14(2), 195–203. 10.1016/j.pbi.2011.01.002 PubMed DOI

Puy, J. , de Bello, F. , Dvorakova, H. , Medina, N. G. , Latzel, V. , & Carmona, C. P. (2020). Competition‐induced transgenerational plasticity influences competitive interactions and leaf decomposition of offspring. New Phytologist, 229(6), 3497–3507. PubMed

Puy, J. , Dvořáková, H. , Carmona, C. P. , de Bello, F. , Hiiesalu, I. , & Latzel, V. (2018). Improved demethylation in ecological epigenetic experiments, Testing a simple and harmless foliar demethylation application. Methods in Ecology and Evolution, 9, 744–753. 10.1111/2041-210X.12903 DOI

R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R‐project.org/

Racette, K. , Rowland, D. , Tillman, B. , Erickson, J. , Munoz, P. , & Vermerris, W. (2019). Transgenerational stress memory in seed and seedling vigor of peanut (Arachis hypogaea L.) varies by genotype. Environmental and Experimental Botany, 162, 541–549. 10.1016/j.envexpbot.2019.03.006 DOI

Rahavi, S. M. , & Kovalchuk, I. (2013a). Changes in homologous recombination frequency in Arabidopsis thaliana plants exposed to stress depend on time of exposure during development and on duration of stress exposure. Physiology and Molecular Biology of Plants, 19, 479–488. 10.1007/s12298-013-0197-z PubMed DOI PMC

Rahavi, S. M. , & Kovalchuk, I. (2013b). Transgenerational changes in Arabidopsis thaliana in response to UV‐C, heat and cold. Biocatalysis Agricutural Biotechnology, 2, 226–233. 10.1016/j.bcab.2013.05.001 DOI

Ramírez, D. A. , Rolando, J. L. , Yactayo, W. , Monneveux, P. , Mares, V. , & Quiroz, R. (2015). Improving potato drought tolerance through the induction of long‐term water stress memory. Plant Science, 238, 26–32. 10.1016/j.plantsci.2015.05.016 PubMed DOI

Richards, C. L. , Alonso, C. , Becker, C. , Bossdorf, O. , Bucher, E. , Colomé‐Tatché, M. , Durka, W. , Engelhardt, J. , Gaspar, B. , Gogol‐Döring, A. , Grosse, I. , van Gurp, T. P. , Heer, K. , Kronholm, I. , Lampei, C. , Latzel, V. , Mirouze, M. , Opgenoorth, L. , Paun, O. , … Verhoeven, K. J. F. (2017). Ecological plant epigenetics: evidence from model and non‐model species, and the way forward. Ecology Letters, 20, 1576–1590. 10.1111/ele.12858 PubMed DOI

Richards, E. J. (2006). Inherited epigenetic variation–revisiting soft inheritance. Nature Reviews Genetics, 7(5), 395–401. PubMed

Sherwood, S. , & Fu, Q. (2014). Climate change. A drier future? Science, 343, 737–739. PubMed

Shi, W. , Chen, X. , Gao, L. , Xu, C. Y. , Ou, X. , Bossdorf, O. , Yang, J. , & Geng, Y. (2019). Transient stability of epigenetic population differentiation in a clonal invader. Frontiers in Plant Science, 9, 1851. 10.3389/fpls.2018.01851 PubMed DOI PMC

Shock, C. C. , Feibert, E. B. G. , & Saunders, L. D. (1998). Potato yield and quality response to deficit irrigation. HortScience, 33(4), 655–659. 10.21273/HORTSCI.33.4.655 DOI

Tombesi, S. , Frioni, T. , Poni, S. , & Palliotti, A. (2018). Effect of water stress “memory” on plant behavior during subsequent drought stress. Environmental and Experimental Botany, 150, 106–114. 10.1016/j.envexpbot.2018.03.009 DOI

Trewavas, A. (2014). Plant behaviour and intelligence. Oxford University Press.

van Groenendael, J. M. , Klimeš, L. , Klimešová, J. , & Hendriks, R. J. J. (1996). Comparative ecology of clonal plants. Philosophical Transactions of the Royal Society B‐Biological Sciences, 351, 1331–1339.

Verhoeven, K. J. F. , Jansen, J. J. , van Dijk, P. J. , & Biere, A. (2010). Stress‐induced DNA methylation changes and their heritability in asexual dandelions . New Phytologist, 185, 1108–1118. 10.1111/j.1469-8137.2009.03121.x PubMed DOI

Verhoeven, K. J. F. , & Preite, V. (2014). Epigenetic variation in asexually reproducing organisms. Evolution, 68(3), 644–655. 10.1111/evo.12320 PubMed DOI

Verhoeven, K. J. F. , & van Gurp, T. P. (2012). Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS One, 6, e38605. 10.1371/journal.pone.0038605 PubMed DOI PMC

Virlouvet, L. , Avenson, T. J. , Du, Q. , Zhang, C. , Liu, N. , Fromm, M. , Avramova, Z. , & Russo, S. E. (2018). Dehydration stress memory: Gene networks linked to physiological responses during repeated stresses of Zea mays. Frontiers . Plant Science, 9, 1058. 10.3389/fpls.2018.01058 PubMed DOI PMC

Xu, J. H. , Tanino, K. K. , & Robinson, S. J. (2016). Stable epigenetic variants selected from an induced hypomethylated fragaria vesca population. Frontiers in Plant Science, 7, 1768. 10.3389/fpls.2016.01768 PubMed DOI PMC

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