Epigenetic memory and growth responses of the clonal plant Glechoma longituba to parental recurrent UV-B stress
Xiaoyin Zhang A , Cunxia Li A , Dan Tie A , Jiaxin Quan A , Ming Yue A and Xiao Liu
A B
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, Northwest University, Xi’an 710069, China.
B Corresponding author. Email: liuxiao@nwu.edu.cn
Functional Plant Biology 48(8) 827-838 https://doi.org/10.1071/FP20303
Submitted: 30 September 2020 Accepted: 10 March 2021 Published: 6 April 2021
Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
The responses of plants to recurrent stress may differ from their responses to a single stress event. In this study, we investigated whether clonal plants can remember past environments. Parental ramets of Glechoma longituba (Nakai) Kuprian were exposed to UV-B stress treatments either once or repeatedly (20 and 40 repetitions). Differences in DNA methylation levels and growth parameters among parents, offspring ramets and genets were analysed. Our results showed that UV-B stress reduced the DNA methylation level of parental ramets, and the reduction was enhanced by increasing the number of UV-B treatments. The epigenetic variation exhibited by recurrently stressed parents was maintained for a long time, but that of singly stressed parents was only short-term. Moreover, clonal plants responded to different UV-B stress treatments with different growth strategies. The one-time stress was a eustress that increased genet biomass by increasing offspring leaf allocation and defensive allocation in comparison to the older offspring. In contrast, recurring stress was a distress that reduced genet biomass, increased the biomass of storage stolons, and allocated more defensive substances to the younger ramets. This study demonstrated that the growth of offspring and genets was clearly affected by parental experience, and parental epigenetic memory and the transgenerational effect may play important roles in this effect.
Keywords: environmental stress, phenotypic plasticity, DNA methylation, stress memory, transgenerational effect.
References
Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress‐response genes. The Plant Journal 83, 149–159.| Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress‐response genes.Crossref | GoogleScholarGoogle Scholar | 25788029PubMed |
Bossdorf O, Richards C, Pigliucci M (2008) Epigenetics for ecologists. Ecology Letters 11, 106–115.
Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology 12, 133–139.
| Epigenetic regulation of stress responses in plants.Crossref | GoogleScholarGoogle Scholar | 19179104PubMed |
Choi CS, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Molecular Genetics and Genomics 277, 589–600.
| Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 17273870PubMed |
Cloix C, Jenkins GI (2008) Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin. Molecular Plant 1, 118–128.
| Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin.Crossref | GoogleScholarGoogle Scholar | 20031919PubMed |
Ćuk K, Gogala M, Tkalec M, Vidakovic’Cifrek Z (2010) Transgenerational stress memory in Arabidopsis thaliana (L.) heynh.: antioxidative enzymes and HSP70. Acta Botanica Croatica 69, 183–197.
de Freitas Guedes FA, Nobres P, Ferreira DCR, Menezes-Silva PE, Ribeiro-Alves M, Correa RL, DaMatta FM, Alves-Ferreira M (2018) Transcriptional memory contributes to drought tolerance in coffee (Coffea canephora) plants. Environmental and Experimental Botany 147, 220–233.
| Transcriptional memory contributes to drought tolerance in coffee (Coffea canephora) plants.Crossref | GoogleScholarGoogle Scholar |
Ding Y, Virlouvet L, Liu N, Riethoven JJ, Fromm M, Avramova Z (2014) Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. BMC Plant Biology 14, 141
| Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 24885787PubMed |
Dong BC, Meng J, Yu FH (2019) Effects of parental light environment on growth and morphological responses of clonal offspring. Plant Biology 21, 1083–1089.
| Effects of parental light environment on growth and morphological responses of clonal offspring.Crossref | GoogleScholarGoogle Scholar | 31054216PubMed |
Douhovnikoff V, Dodd RS (2015) Epigenetics: a potential mechanism for clonal plant success. Plant Ecology 216, 227–233.
| Epigenetics: a potential mechanism for clonal plant success.Crossref | GoogleScholarGoogle Scholar |
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data.Crossref | GoogleScholarGoogle Scholar | 1644282PubMed |
Gagliano M, Renton M, Depczynski M, Mancuso S (2014) Experience teaches plants to learn faster and forget slower in environments where it matters. Oecologia 175, 63–72.
| Experience teaches plants to learn faster and forget slower in environments where it matters.Crossref | GoogleScholarGoogle Scholar | 24390479PubMed |
González APR, Chrtek J, Dobrev PI, Dumalasová V, Fehrer J, Mráz P, Latzel V (2016) Stress‐induced memory alters growth of clonal offspring of white clover (Trifolium repens). American Journal of Botany 103, 1567–1574.
| Stress‐induced memory alters growth of clonal offspring of white clover (Trifolium repens).Crossref | GoogleScholarGoogle Scholar |
Graindorge S, Cognat V, Berens PJT, Mutterer J, Molinier J (2019) Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure. PLOS Genetics 15, e1008476
| Photodamage repair pathways contribute to the accurate maintenance of the DNA methylome landscape upon UV exposure.Crossref | GoogleScholarGoogle Scholar | 31738755PubMed |
Hauser MT, Aufsatz W, Jonak C, Luschnig C (2011) Transgenerational epigenetic inheritance in plants. Biochimica et Biophysica Acta 1809, 459–468.
| Transgenerational epigenetic inheritance in plants.Crossref | GoogleScholarGoogle Scholar | 21515434PubMed |
Hideg É, Jansen MAK, Strid K (2013) UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates? Trends in Plant Science 18, 107–115.
| UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates?Crossref | GoogleScholarGoogle Scholar | 23084465PubMed |
Huber H, Visser EJW, Clements G, Peters JL (2014) Flooding and fragment size interact to determine survival and regrowth after fragmentation in two stoloniferous Trifolium species. AoB Plants 6, plu024
| Flooding and fragment size interact to determine survival and regrowth after fragmentation in two stoloniferous Trifolium species.Crossref | GoogleScholarGoogle Scholar | 24887003PubMed |
Ikeda Y (2012) Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms. Plant & Cell Physiology 53, 809–816.
| Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms.Crossref | GoogleScholarGoogle Scholar |
Kataria S, Jajoo A, Guruprasad KN (2014) Impact of increasing ultraviolet-B (UV-B) radiation on photosynthetic processes. Journal of Photochemistry and Photobiology. B, Biology 137, 55–66.
| Impact of increasing ultraviolet-B (UV-B) radiation on photosynthetic processes.Crossref | GoogleScholarGoogle Scholar | 24725638PubMed |
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 Physiology 53, 794–800.
| An epigenetic integrator: new insights into genome regulation, environmental stress responses and developmental controls by HISTONE DEACETYLASE 6.Crossref | GoogleScholarGoogle Scholar |
Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant & Cell Physiology 55, 1859–1863.
| Epigenetic memory for stress response and adaptation in plants.Crossref | GoogleScholarGoogle Scholar |
Köhler C, Wolff P, Spillane C (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Annual Review of Plant Biology 63, 331–352.
| Epigenetic mechanisms underlying genomic imprinting in plants.Crossref | GoogleScholarGoogle Scholar | 22404470PubMed |
Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What is stress? Concepts, definitions, and applications in seed science. New Phytologist 188, 655–673.
| What is stress? Concepts, definitions, and applications in seed science.Crossref | GoogleScholarGoogle Scholar |
Latzel V, Jitka K (2010) Transgenerational plasticity in clonal plants. Evolutionary Ecology 24, 1537–1543.
| Transgenerational plasticity in clonal plants.Crossref | GoogleScholarGoogle Scholar |
Latzel V, Rendina González AP, Jonathan R (2016) Epigenetic memory as a basis for intelligent behavior in clonal plants. Frontiers in Plant Science 7, 1354
| Epigenetic memory as a basis for intelligent behavior in clonal plants.Crossref | GoogleScholarGoogle Scholar | 27630664PubMed |
Li X, Liu F (2016) Drought stress memory and drought stress tolerance in plants: biochemical and molecular basis. In ‘Drought Stress Tolerance in Plants, Volume 1.’ (Eds Hossain MA, Wani SH, Bhattacharjee S, Burritt DJ, Tran LSP) pp. 17–44. (Springer International Publishing: Switzerland)
Li Q, Liu X, Yue M, Tang WT, Meng QC (2011a) Response of physiological integration in Trifolium repens to heterogeneity of UV-B radiation. Flora 206, 712–719.
| Response of physiological integration in Trifolium repens to heterogeneity of UV-B radiation.Crossref | GoogleScholarGoogle Scholar |
Li Q, Liu X, Yue M, Zhang XF, Zhang RC (2011b) Effects of physiological integration on photosynthetic efficiency of Trifolium repens in response to heterogeneous UV-B radiation. Photosynthetica 49, 539–545.
| Effects of physiological integration on photosynthetic efficiency of Trifolium repens in response to heterogeneous UV-B radiation.Crossref | GoogleScholarGoogle Scholar |
Li P, Yang H, Wang L, Liu HJ, Huo HQ, Zhang CJ, Liu AZ, Zhu AD, Hu JY, Liu YJ, Liu L (2019) Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice. Frontiers in Genetics 10, 55
| Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice.Crossref | GoogleScholarGoogle Scholar | 30800142PubMed |
Liang X, Hou X, Li J, Han Y, Zhang YX, Feng NJ, Du J, Zhang WH, Zheng DF, Fang SM (2019) High-resolution DNA methylome reveals that demethylation enhances adaptability to continuous cropping comprehensive stress in soybean. BMC Plant Biology 19, 79
| High-resolution DNA methylome reveals that demethylation enhances adaptability to continuous cropping comprehensive stress in soybean.Crossref | GoogleScholarGoogle Scholar | 30777019PubMed |
Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PCG (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5, e10326
| Epigenetic variation in mangrove plants occurring in contrasting natural environment.Crossref | GoogleScholarGoogle Scholar | 20436669PubMed |
Liu S, Sun K, Jiang T, Ho JP, Liu B, Feng J (2012) Natural epigenetic variation in the female great roundleaf bat (Hipposideros armiger) populations. Molecular Genetics and Genomics 287, 643–650.
| Natural epigenetic variation in the female great roundleaf bat (Hipposideros armiger) populations.Crossref | GoogleScholarGoogle Scholar | 22773086PubMed |
Liu X, Li Q, Yue M, Zhang X, Zhang R, Zhang B, Wang M (2015) Nitric oxide is involved in integration of UV-B absorbing compounds among parts of clonal plants under a heterogeneous UV-B environment. Physiologia Plantarum 155, 180–191.
| Nitric oxide is involved in integration of UV-B absorbing compounds among parts of clonal plants under a heterogeneous UV-B environment.Crossref | GoogleScholarGoogle Scholar | 25424287PubMed |
McIntyre PJ, Strauss SY (2014) Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments. Evolutionary Ecology 28, 229–246.
| Phenotypic and transgenerational plasticity promote local adaptation to sun and shade environments.Crossref | GoogleScholarGoogle Scholar |
McKenzie RL, Aucamp PJ, Bais AF, Bjorn LO, Ilyas M, Madronich S (2011) Ozone depletion and climate change: impacts on UV radiation. Photochemical & Photobiological Sciences 10, 182–198.
| Ozone depletion and climate change: impacts on UV radiation.Crossref | GoogleScholarGoogle Scholar |
Molinier J (2017) Genome and epigenome surveillance processes underlying UV exposure in plants. Genes 8, 316
| Genome and epigenome surveillance processes underlying UV exposure in plants.Crossref | GoogleScholarGoogle Scholar |
Müller-Xing R, Xing Q, Goodrich J (2014) Footprints of the sun: memory of UV and light stress in plants. Frontiers in Plant Science 5, 474
Münzbergová Z, Hadincová V (2017) Transgenerational plasticity as an important mechanism affecting response of clonal species to changing climate. Ecology and Evolution 7, 5236–5247.
| Transgenerational plasticity as an important mechanism affecting response of clonal species to changing climate.Crossref | GoogleScholarGoogle Scholar | 28770062PubMed |
Ohlsson AB, Segerfeldt P, Lindstrom A, Borg-Karlson AK, Berglund T (2013) UV-B exposure of indoor-grown Picea abies seedlings causes an epigenetic effect and selective emission of terpenes. Zeitschrift fur Naturforschung. C, Journal of Biosciences 68, 139–147.
Pandey N, Pandey-Rai S (2015) Deciphering UV-B-induced variation in DNA methylation pattern and its influence on regulation of DBR2 expression in Artemisia annua L. Planta 242, 869–879.
| Deciphering UV-B-induced variation in DNA methylation pattern and its influence on regulation of DBR2 expression in Artemisia annua L.Crossref | GoogleScholarGoogle Scholar | 25998525PubMed |
Pandey N, Goswami N, Tripathi D, Rai KK, Rai SK, Singh S, Pandey-Rai S (2019) Epigenetic control of UV-B-induced flavonoid accumulation in Artemisia annua L. Planta 249, 497–514.
| Epigenetic control of UV-B-induced flavonoid accumulation in Artemisia annua L.Crossref | GoogleScholarGoogle Scholar | 30267151PubMed |
Pascual J, Caňal MJ, Correia B, Escandon M, Hasbún R, Meijón M, Pinto G, Valledor L (2014) Can epigenetics help forest plants to adapt to climate change? In ‘Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications.’ (Eds Alvarez-Venegas R, De la Peña C, Casas-Mollano JA) pp. 125–146. (Springer International Publishing: Switzerland)
Paszkowski J, Grossniklaus U (2011) Selected aspects of transgenerational epigenetic inheritance and resetting in plants. Current Opinion in Plant Biology 14, 195–203.
| Selected aspects of transgenerational epigenetic inheritance and resetting in plants.Crossref | GoogleScholarGoogle Scholar | 21333585PubMed |
Pérez-Figueroa A (2013) Msap: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data. Molecular Ecology Resources 13, 522–527.
| Msap: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data.Crossref | GoogleScholarGoogle Scholar | 23311622PubMed |
Preite V, Oplaat C, Biere A, Kirschner J, van der Putten WH, Verhoeven KJF (2018) Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages. Ecology and Evolution 8, 3047–3059.
| Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages.Crossref | GoogleScholarGoogle Scholar | 29531716PubMed |
Qüesta JI, Walbot V, Casati P (2010) Mutator transposon activation after UV-B involves chromatin remodeling. Epigenetics 5, 352–363.
| Mutator transposon activation after UV-B involves chromatin remodeling.Crossref | GoogleScholarGoogle Scholar | 20421734PubMed |
Qüesta JI, Fina JP, Paula C (2013) DDM1 and ROS1 have a role in UV-B induced- and oxidative DNA damage in A. thaliana. Frontiers in Plant Science 4, 420
| DDM1 and ROS1 have a role in UV-B induced- and oxidative DNA damage in A. thaliana.Crossref | GoogleScholarGoogle Scholar | 24155752PubMed |
Ramírez DA, Rolando JL, 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.
| Improving potato drought tolerance through the induction of long-term water stress memory.Crossref | GoogleScholarGoogle Scholar | 26259171PubMed |
Rendina González AP, Chrtek J, Dobrev PI, Dumalasová V, Fehrer J, Mráz P, Latzel V (2016) Stress‐induced memory alters growth of clonal offspring of white clover (Trifolium repens). American Journal of Botany 103, 1567–1574.
| Stress‐induced memory alters growth of clonal offspring of white clover (Trifolium repens).Crossref | GoogleScholarGoogle Scholar |
Rendina González AP, Preite V, Verhoeven KJF, Latzel V (2018) Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens. Frontiers in Plant Science 9, 1677
| Transgenerational effects and epigenetic memory in the clonal plant Trifolium repens.Crossref | GoogleScholarGoogle Scholar | 30524458PubMed |
Rius SP, Emiliani J, Casati P (2016) P1 epigenetic regulation in leaves of high altitude maize landraces: effect of UV-B radiation. Frontiers in Plant Science 7, 523
| P1 epigenetic regulation in leaves of high altitude maize landraces: effect of UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 27148340PubMed |
Robson TM, Klem K, Urban O, Jansen MAK (2015) Re-interpreting plant morphological responses to UV-B radiation. Plant, Cell & Environment 38, 856–866.
| Re-interpreting plant morphological responses to UV-B radiation.Crossref | GoogleScholarGoogle Scholar |
Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Science 174, 61–70.
| Brassica oleracea displays a high level of DNA methylation polymorphism.Crossref | GoogleScholarGoogle Scholar |
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 Physiology 53, 766–784.
| DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation.Crossref | GoogleScholarGoogle Scholar |
Schulz B, Eckstein LR, Durka W (2013) Scoring and analysis of methylation-sensitive amplification polymorphisms for epigenetic population studies. Molecular Ecology Resources 13, 642–653.
| Scoring and analysis of methylation-sensitive amplification polymorphisms for epigenetic population studies.Crossref | GoogleScholarGoogle Scholar | 23617735PubMed |
Sokolova D, Vengzhen G, Kravets A (2014) The effect of DNA methylation modification polymorphism of corn seeds on their germination rate, seedling resistance and adaptive capacity under UV-C exposure. American Journal of Plant Biology 1, 1–14.
Song J, Irwin J, Dean C (2013) Remembering the prolonged cold of winter. Current Biology 23, R807–R811.
| Remembering the prolonged cold of winter.Crossref | GoogleScholarGoogle Scholar | 24028964PubMed |
Steward N (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. The Journal of Biological Chemistry 277, 37741–37746.
| Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress.Crossref | GoogleScholarGoogle Scholar | 12124387PubMed |
Thellier M, Lüttge U (2013) Plant memory: a tentative model. Plant Biology 15, 1–12.
| Plant memory: a tentative model.Crossref | GoogleScholarGoogle Scholar | 23121044PubMed |
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.
| Effect of water stress “memory” on plant behavior during subsequent drought stress.Crossref | GoogleScholarGoogle Scholar |
Verhoeven KJF, van Gurp TP (2012) Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS One 7, e38605
| Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion.Crossref | GoogleScholarGoogle Scholar |
Verhoeven KJF, Jansen JJ, Biere DA (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist 185, 1108–1118.
| Stress-induced DNA methylation changes and their heritability in asexual dandelions.Crossref | GoogleScholarGoogle Scholar |
Virlouvet L, Avenson TJ, Qian D, Chi Z, Ning L, Michael F, Avramova Z, Russo SE (2018) Dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays. Frontiers in Plant Science 9, 1058
| Dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays.Crossref | GoogleScholarGoogle Scholar | 30087686PubMed |
Wada Y, Miyamoto K, Kusano T, Sano H (2004) Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Molecular Genetics and Genomics 271, 658–666.
| Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 15148604PubMed |
Walter J, Nagy L, Hein R, Rascher U, Beierkuhnlein C, Willner E, Jentsch A (2011) Do plants remember drought? hints towards a drought-memory in grasses. Environmental and Experimental Botany 71, 34–40.
| Do plants remember drought? hints towards a drought-memory in grasses.Crossref | GoogleScholarGoogle Scholar |
Wang W, Zhao X, Pan Y, Zhu L, Fu B, Li Z (2011) DNA methylation changes detected by methylation-sensitive amplified polymorphism in two contrasting rice genotypes under salt stress. Journal of Genetics and Genomics 38, 419–424.
| DNA methylation changes detected by methylation-sensitive amplified polymorphism in two contrasting rice genotypes under salt stress.Crossref | GoogleScholarGoogle Scholar | 21930101PubMed |
Wang X, Vignjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B (2015) Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regulation 75, 677–687.
| Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat.Crossref | GoogleScholarGoogle Scholar |
Wargent JJ, Gegas VC, Jenkins GI, Doonan JH, Paul ND (2009) UVR8 in Arabidopsis thaliana regulates multiple aspects of cellular differentiation during leaf development in response to ultraviolet B radiation. New Phytologist 183, 315–326.
| UVR8 in Arabidopsis thaliana regulates multiple aspects of cellular differentiation during leaf development in response to ultraviolet B radiation.Crossref | GoogleScholarGoogle Scholar |
Willing EM, Piofczyk T, Albert A, Winkler JB, Schneeberger K, Pecinka A (2016) UVR2 ensures transgenerational genome stability under simulated natural UV-B in Arabidopsis thaliana. Nature Communications 7, 13522
| UVR2 ensures transgenerational genome stability under simulated natural UV-B in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 27905394PubMed |
Yaish MW, Abbas AL, Ibtisam AH, Vishwas PH (2018) Genome-wide DNA methylation analysis in response to salinity in the model plant caliph medic (Medicago truncatula). BMC Genomics 19, 78
| Genome-wide DNA methylation analysis in response to salinity in the model plant caliph medic (Medicago truncatula).Crossref | GoogleScholarGoogle Scholar | 29361906PubMed |
