in

Epigenetic responses of hare barley (Hordeum murinum subsp. leporinum) to climate change: an experimental, trait-based approach

  • Alsdurf J, Anderson C, Siemens DH (2016) Epigenetics of drought-induced trans-generational plasticity: consequences for range limit development. Ann Bot 8:plv146

    Google Scholar 

  • Anderson JT, Willis JH, Mitchell-Olds T (2011) Evolutionary genetics of plant adaptation. Trends Genet 27:258–66

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Aragón-Gastélum JL, Flores J, Yáñez-Espinosa L, Badano E, Ramírez-Tobías HM, Rodas-Ortíz JP et al. (2014) Induced climate change impairs photosynthetic performance in Echinocactus platyacanthus, an especially protected Mexican cactus species. Flora—Morphol Distrib Funct Ecol Plants 209:499–503

    Article  Google Scholar 

  • Banerjee A, Roychoudhury A (2017) Epigenetic regulation during salinity and drought stress in plants: histone modifications and DNA methylation. Plant Gene 11:199–204

    CAS  Article  Google Scholar 

  • Bartels A, Han Q, Nair P, Stacey L, Gaynier H, Mosley M et al. (2018) Dynamic DNA methylation in plant growth and development. Int J Mol Sci 19:2144

    PubMed Central  Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330:612–6

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bongers FJ, Olmo M, Lopez-Iglesias B, Anten NPR, Villar R (2017) Drought responses, phenotypic plasticity and survival of Mediterranean species in two different microclimatic sites. Plant Biol 19:386–395

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115

    PubMed  PubMed Central  Google Scholar 

  • Bossdorf O, Zhang Y (2011) A truly ecological epigenetics study. Mol Ecol 20:1572–1574

    PubMed  Article  PubMed Central  Google Scholar 

  • Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:78–92

    Article  Google Scholar 

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–6

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Dabros A, Fyles JW (2010) Effects of open-top chambers and substrate type on biogeochemical processes at disturbed boreal forest sites in northwestern Quebec. Plant Soil 327:465–479

    CAS  Article  Google Scholar 

  • Delgado-Baquerizo M, Maestre FT, Rodríguez JGP, Gallardo A (2013) Biological soil crusts promote N accumulation in response to dew events in dryland soils. Soil Biol Biochem 62:22–27

    CAS  Article  Google Scholar 

  • Diez CM, Meca E, Tenaillon MI, Gaut BS (2014) Three groups of transposable elements with contrasting copy number dynamics and host responses in the maize (Zea mays ssp. mays) genome. PLoS Genet 10:e1004298

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Ewens WJ (2013) Genetic variation. In: Maloy S, Hughes K (eds) Brenner’s encyclopedia of genetics, pp 290–291

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes. Genetics 131:479–91

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Fernández-Pascual E, Jiménez-Alfaro B, Caujapé-Castells J, Jaén-Molina R, Díaz TE (2013) A local dormancy cline is related to the seed maturation environment, population genetic composition and climate. Ann Bot 112:937–45

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Forestan C, Aiese Cigliano R, Farinati S, Lunardon A, Sanseverino W, Varotto S (2016) Stress-induced and epigenetic-mediated maize transcriptome regulation study by means of transcriptome reannotation and differential expression analysis. Sci Rep 6:30446

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Fotiou C, Damialis A, Krigas N, Vokou D (2007) Hordeum murinum pollen as a contributor to pollinosis: important or trivial aeroallergen? Allergy 62:180

    Google Scholar 

  • Freschet GT, Violle C, Bourget MY, Scherer-Lorenzen M, Fort F (2018) Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress. N Phytol 219:1338–52

    Article  Google Scholar 

  • Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Funct Ecol 15:688–95

    Article  Google Scholar 

  • Gayacharan JA (2013) Epigenetic responses to drought stress in rice (Oryza sativa L.). Physiol Mol Biol Plants 19:379–87

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Gómez JM (2004) Importance of microhabitat and acorn burial on Quercus ilex early recruitment: Non-additive effects on multiple demographic processes. Plant Ecol 172:287–297

    Article  Google Scholar 

  • Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27:857–71

    Article  Google Scholar 

  • Grigorova B, Vaseva I, Demirevska K, Feller U (2011) Combined drought and heat stress in wheat: changes in some heat shock proteins. Biol Plant 55:105–111

    CAS  Article  Google Scholar 

  • Gu Z, Eils R, Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32:2847–9

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Herrera CM, Bazaga P (2010) Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. N Phytol 187:867–76

    CAS  Article  Google Scholar 

  • Herrera CM, Pozo MI, Bazaga P (2012) Jack of all nectars, master of most: DNA methylation and the epigenetic basis of niche width in a flower-living yeast. Mol Ecol 21:2602–16

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Hulting AG, Haavisto JL (2013) Hare barley (Hordeum murinum ssp. leporinum) biology and management in cool season perennial grass pastures of Western Oregon. J Chem Inform Model 33:1689–99

    Google Scholar 

  • Hussain F, Durrani MJ (2009) Seasonal availability, palatability and animal preferences of forage plants in Harboi arid range land, Kalat, Pakistan. Pak J Bot 41:539–554

    Google Scholar 

  • Ibáñez I, Schupp EW (2001) Positive and negative interactions between environmental conditions affecting Cercocarpus ledifolius seedling survival. Oecologia 129:543–550

    PubMed  Article  PubMed Central  Google Scholar 

  • Jakob SS, Meister A, Blattner FR (2004) The considerable genome size variation of Hordeum species (Poaceae) is linked to phylogeny, life form, ecology, and speciation rates. Mol Biol Evol 21:860–9

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Jeremias G, Barbosa J, Marques SM, Asselman J, Gonçalves FJM, Pereira JL (2018) Synthesizing the role of epigenetics in the response and adaptation of species to climate change in freshwater ecosystems. Mol Ecol 27:2790–2806

    PubMed  Article  PubMed Central  Google Scholar 

  • Jiang Y, Huang B (2000) Effects of drought or heat stress alone and in combination on Kentucky bluegrass. Crop Sci 40:1358–62

    Article  Google Scholar 

  • Kaur A, Grewal A, Sharma P (2018) Comparative analysis of DNA methylation changes in two contrasting wheat genotypes under water deficit. Biol Plant 62:471–8

    CAS  Article  Google Scholar 

  • Kronholm I, Bassett A, Baulcombe D, Collins S (2017) Epigenetic and genetic contributions to adaptation in Chlamydomonas. Mol Biol Evol 34:2285–2306

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • de la Riva EG, Tosto A, Pérez-Ramos IM, Navarro-Fernández CM, Olmo M, Anten NPR et al. (2016) A plant economics spectrum in Mediterranean forests along environmental gradients: is there coordination among leaf, stem and root traits? J Veg Sci 27:187–199

    Article  Google Scholar 

  • Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Front Chem 6:26

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Lampei C (2019) Multiple simultaneous treatments change plant response from adaptive parental effects to within-generation plasticity, in Arabidopsis thaliana. Oikos 128:368–379

    Article  Google Scholar 

  • Latzel V, Allan E, Bortolini Silveira A, Colot V, Fischer M, Bossdorf O (2013) Epigenetic diversity increases the productivity and stability of plant populations. Nat Commun 4:2875

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Laughlin DC, Leppert JJ, Moore MM, Sieg CH (2010) A multi-trait test of the leaf-height-seed plant strategy scheme with 133 species from a pine forest flora. Funct Ecol 24:493–501

    Article  Google Scholar 

  • Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H et al. (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genom 2:300

    Article  CAS  Google Scholar 

  • Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J et al. (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Ecol Manag 259:698–709

    Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Liu J, Feng L, Li J, He Z (2015) Genetic and epigenetic control of plant heat responses. Front Plant Sci 6:267

    PubMed  PubMed Central  Google Scholar 

  • Liu G, Xia Y, Liu T, Dai S, Hou X (2018) The DNA methylome and association of differentially methylated regions with differential gene expression during heat stress in Brassica rapa. Int J Mol Sci 19:1414

    PubMed Central  Article  CAS  Google Scholar 

  • Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y et al. (2015) Temporal transcriptome profiling reveals expression partitioning of homoeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15:1

    Article  CAS  Google Scholar 

  • Maestre FT, Escolar C, de Guevara ML, Quero JL, Lázaro R, Delgado-Baquerizo M et al. (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Glob Chang Biol 19:3835–3847

    PubMed  PubMed Central  Article  Google Scholar 

  • Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH et al. (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3:20–32

    Article  Google Scholar 

  • Mariotte P, Vandenberghe C, Kardol P, Hagedorn F, Buttler A (2013) Subordinate plant species enhance community resistance against drought in semi‐natural grasslands (S Schwinning, Ed.). J Ecol 101:763–773

    Article  Google Scholar 

  • Mastan SG, Rathore MS, Bhatt VD, Yadav P, Chikara J (2012) Assessment of changes in DNA methylation by methylation-sensitive amplification polymorphism in Jatropha curcas L. subjected to salinity stress. Gene 508:125–9

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Matías L, Godoy O, Gómez-Aparicio L, Pérez-Ramos IM (2018) An experimental extreme drought reduces the likelihood of species to coexist despite increasing intransitivity in competitive networks. J Ecol 106:826–837

    Article  Google Scholar 

  • Metzger DCH, Schulte PM (2017) Persistent and plastic effects of temperature on DNA methylation across the genome of threespine stickleback (Gasterosteus aculeatus). Proc R Soc B Biol Sci 284:20171667

    Article  CAS  Google Scholar 

  • Mitchell P, Wardlaw T, Pinkard L (2015) Combined stresses in forests (R Mahalingam, Ed.). Springer International Publishing, Switzerland

    Google Scholar 

  • Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92:372–383

    Article  Google Scholar 

  • Moore LM, Lauenroth WK (2017) Differential effects of temperature and precipitation on early- vs. late-flowering species. Ecosphere 8:e01819

    Article  Google Scholar 

  • Muller-Landau HC (2010) The tolerance-fecundity trade-off and the maintenance of diversity in seed size. Proc Natl Acad Sci USA 107:4242–4247

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 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 128:124–34

    Article  CAS  Google Scholar 

  • Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U et al. (2010) Plant phenotypic plasticity in a changing climate. Trends Plant Sci 15:684–92

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Ogaya R, Peñuelas J, Martínez-Vilalta J, Mangirón M (2003) Effect of drought on diameter increment of Quercus ilex, Phillyrea latifolia, and Arbutus unedo in a holm oak forest of NE Spain. Ecol Manag 180:175–184

    Article  Google Scholar 

  • Olea L, San Miguel A (2006) The Spanish dehesa. A traditional Mediterranean silvopastoral system linking production and nature conservation. In: Sustainable grassland productivity: Proceedings of the 21st General Meeting of the European Grassland Federation

  • Paun O, Bateman RM, Fay MF, Hedrén M, Civeyrel L, Chase MW (2010) Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Mol Biol Evol 27:2465–73

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Pérez-Figueroa A (2013) msap: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data. Mol Ecol Resour 13:522–527

    PubMed  Article  PubMed Central  Google Scholar 

  • Pérez-Ramos IM, Cambrollé J, Hidalgo-Galvez MD, Matías L, Montero-Ramírez A, Santolaya S et al. (2020) Phenological responses to climate change in communities of plants species with contrasting functional strategies. Environ Exp Bot 170:103852

    Article  CAS  Google Scholar 

  • Pérez-Ramos IM, Díaz-Delgado R, de la Riva EG, Villar R, Lloret F, Marañon T (2017) Climate variability and community stability in Mediterranean shrublands: the role of functional diversity and soil environment. J Ecol 105:1335–1346

    Article  Google Scholar 

  • Pérez-Ramos IM, Matías L, Gómez-Aparicio L, Godoy Ó (2019) Functional traits and phenotypic plasticity modulate species coexistence across contrasting climatic conditions. Nat Commun 10:2555

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Piikkia K, De Temmerman L, Högy P, Pleijel H (2008) The open-top chamber impact on vapour pressure deficit and its consequences for stomatal ozone uptake. Atmos Environ 42:6513–22

    Article  CAS  Google Scholar 

  • Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): A meta-analysis. N Phytol 182:565–588

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. 55: 275–286.

  • Reyna-López GE, Simpson J, Ruiz-Herrera J (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet 253:703–710

    PubMed  Article  PubMed Central  Google Scholar 

  • Richards CL, Verhoeven KJF, Bossdorf O (2012) Evolutionary significance of epigenetic variation. In: Plant Genome Diversity Volume 1: Plant Genomes, their Residents, and their Evolutionary Dynamics, pp 257–274

  • Rizhsky L (2004) When defense pathways collide. the response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–96

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Rodríguez-Calcerrada J, Letts MG, Rolo V, Roset S, Rambal S (2013) Multiyear impacts of partial throughfall exclusion on Buxus sempervirens in a Mediterranean forest. Syst 22:202–213

    Google Scholar 

  • Seifan M, Tielbörger K, Kadmon R (2010) Direct and indirect interactions among plants explain counterintuitive positive drought effects on an eastern Mediterranean shrub species. Oikos 119:1601–9

    Article  Google Scholar 

  • Sharifi-Rigi P, Saeidi H, Rahiminejad MR (2014) Genetic diversity and geographic distribution of variation of Hordeum murinum as revealed by retroelement insertional polymorphisms in Iran. Biology 69:469–77

    Google Scholar 

  • Shen X, De Jonge J, Forsberg SKG, Pettersson ME, Sheng Z, Hennig L et al. (2014) Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genet 10:e1004842

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Suzuki MM, Bird A (2008) DNA methylation landscapes: Provocative insights from epigenomics. Nat Rev Genet 9:465–76

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Tan MP (2010) Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism. Plant Physiol Biochem 48:21–6

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Tani E, Polidoros AN, Nianiou-Obeidat I, Tsaftaris AS (2005) DNA methylation patterns are differently affected by planting density in maize inbreeds and their hybrids. Maydica 50:19–23

    Google Scholar 

  • Valencia E, Méndez M, Saavedra N, Maestre FT (2016) Plant size and leaf area influence phenological and reproductive responses to warming in semiarid Mediterranean species. Perspect Plant Ecol Evol Syst 21:31–40

    PubMed  PubMed Central  Article  Google Scholar 

  • Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. N Phytol 185:1108–18

    CAS  Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Van De Lee T, Hornes M et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–14

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wang WS, Pan YJ, Zhao XQ, Dwivedi D, Zhu LH, Ali J et al. (2011) rought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa) L.). J Exp Bot 62:1951–60

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Watson RGA, Baldanzi S, Pérez-Figueroa A, Gouws G, Porri F (2018) Morphological and epigenetic variation in mussels from contrasting environments. Mar Biol 165:50

    Article  CAS  Google Scholar 

  • Westoby M (1998) A Leaf-Height-Seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227

    CAS  Article  Google Scholar 

  • Whittington HR, Tilman D, Wragg PD, Powers JS, Browning DM (2015) Phenological responses of prairie plants vary among species and year in a three-year experimental warming study. Ecosphere 6:1–15

    Article  Google Scholar 

  • Wolkovich EM, Cleland EE (2014) Phenological niches and the future of invaded ecosystems with climate change. AoB Plants 6:plu013

    PubMed  PubMed Central  Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F et al. (2004) The worldwide leaf economics spectrum. Nature 428:821–7

    CAS  Article  Google Scholar 

  • Zhang Y-Y, Parepa M, Fischer M, Bossdorf O (2016) Epigenetics of colonizing species? A study of japanese knotweed in central Europe. In: Barrett SC., Colautti RI, Dlugosch KM, Rieseberg LH (eds) Invasion genetics: the baker and Stebbins legacy, John Wiley & Sons, Ltd, pp 328–340

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126:1189–201

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–24

    CAS  PubMed  PubMed Central  Article  Google Scholar 


  • Source: Ecology - nature.com

    The catalyzing potential of J-WAFS seed grants

    Viromes outperform total metagenomes in revealing the spatiotemporal patterns of agricultural soil viral communities