Exploiting induced and natural epigenetic variation for crop improvement

Nature

Exploiting induced and natural epigenetic variation for crop improvement"


Play all audios:

Loading...

KEY POINTS * Substantial natural variation in DNA methylation patterns exists within many plant species. This variation can influence gene expression and plant traits. * Variation in DNA


methylation can arise through a range of mechanisms and is often inherited in the progeny of plants. * Clonal propagation can lead to epigenetic alleles, which can be stably inherited by


regenerated plants. This phenomenon has potential applications for agricultural species that are propagated through grafting or tissue culture. * New epigenome editing tools will generate


opportunities for creating novel epiallelic variants by alteration of DNA methylation or other chromatin modifications. These tools can be used for crop improvement through epigenome


engineering. ABSTRACT Plant breeding has traditionally relied on combining the genetic diversity present within a species to develop combinations of alleles that provide desired traits.


Epigenetic diversity may provide additional sources of variation within a species that could be captured or created for crop improvement. It will be important to understand the sources of


epigenetic variation and the stability of newly formed epigenetic variants over generations to fully use the potential of epigenetic variation to improve crops. The development and


application of methods for widespread epigenome profiling and engineering may generate new avenues for using the full potential of epigenetics in crop improvement. Access through your


institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Access Nature and 54 other Nature Portfolio


journals Get Nature+, our best-value online-access subscription $32.99 / 30 days cancel any time Learn more Subscribe to this journal Receive 12 print issues and online access $209.00 per


year only $17.42 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated


during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS DIRECT


INTROGRESSION OF UNTAPPED DIVERSITY INTO ELITE WHEAT LINES Article 07 October 2021 MULTI-PARENT POPULATIONS IN CROPS: A TOOLBOX INTEGRATING GENOMICS AND GENETIC MAPPING WITH BREEDING Article


Open access 03 July 2020 RECENT ADVANCES IN CROP TRANSFORMATION TECHNOLOGIES Article 15 December 2022 REFERENCES * Nelson, G. C. et al. Climate change effects on agriculture: economic


responses to biophysical shocks. _Proc. Natl Acad. Sci. USA_ 111, 3274–3279 (2014). CAS  PubMed  Google Scholar  * Garnett, T. et al. Agriculture. Sustainable intensification in agriculture:


premises and policies. _Science_ 341, 33–34 (2013). CAS  PubMed  Google Scholar  * Wallace, J. G., Larsson, S. J. & Buckler, E. S. Entering the second century of maize quantitative


genetics. _Heredity (Edinb.)_ 112, 30–38 (2014). CAS  Google Scholar  * Ma, X., Zhu, Q., Chen, Y. & Liu, Y. G. CRISPR/Cas9 platforms for genome editing in plants: developments and


applications. _Mol. Plant._ 9, 961–974 (2016). CAS  PubMed  Google Scholar  * Heard, E. & Martienssen, R. A. Transgenerational epigenetic inheritance: myths and mechanisms. _Cell_ 157,


95–109 (2014). CAS  PubMed  PubMed Central  Google Scholar  * Henikoff, S. & Greally, J. M. Epigenetics, cellular memory and gene regulation. _Curr. Biol._ 26, R644–R648 (2016). CAS 


PubMed  Google Scholar  * Cuerda-Gil, D. & Slotkin, R. K. Non-canonical RNA-directed DNA methylation. _Nat. Plants_ 2, 16163 (2016). CAS  PubMed  Google Scholar  * Gutierrez, C.,


Desvoyes, B., Vergara, Z., Otero, S. & Sequeira-Mendes, J. Links of genome replication, transcriptional silencing and chromatin dynamics. _Curr. Opin. Plant Biol._ 34, 92–99 (2016). CAS


  PubMed  Google Scholar  * Jiang, D. & Berger, F. Histone variants in plant transcriptional regulation. _Biochim. Biophys. Acta_ 1860, 123–130 (2017). CAS  Google Scholar  * Wendte, J.


M. & Pikaard, C. S. The RNAs of RNA-directed DNA methylation. _Biochim. Biophys. Acta_ 1860, 140–148 (2017). CAS  Google Scholar  * Xiao, J., Lee, U. S. & Wagner, D. Tug of war:


adding and removing histone lysine methylation in _Arabidopsis_. _Curr. Opin. Plant Biol._ 34, 41–53 (2016). CAS  PubMed  Google Scholar  * Vidalis, A. et al. Methylome evolution in plants.


_Genome Biol._ 17, 264 (2016). PubMed  PubMed Central  Google Scholar  * Chen, X. & Zhou, D. X. Rice epigenomics and epigenetics: challenges and opportunities. _Curr. Opin. Plant Biol._


16, 164–169 (2013). CAS  PubMed  Google Scholar  * Gaydos, L. J., Wang, W. & Strome, S. Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during


development. _Science_ 345, 1515–1518 (2014). CAS  PubMed  PubMed Central  Google Scholar  * Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns


in plants and animals. _Nat. Rev. Genet._ 11, 204–220 (2010). CAS  PubMed  PubMed Central  Google Scholar  * Stroud, H., Greenberg, M. V., Feng, S., Bernatavichute, Y. V. & Jacobsen, S.


E. Comprehensive analysis of silencing mutants reveals complex regulation of the _Arabidopsis_ methylome. _Cell_ 152, 352–364 (2013). THIS DETAILED ANALYSIS REPORTS THE CONTRIBUTION OF 86


DIFFERENT GENES TO THE DISTRIBUTION OF DNA METHYLATION IN _A. THALIANA_. CAS  PubMed  PubMed Central  Google Scholar  * Bostick, M. et al. UHRF1 plays a role in maintaining DNA methylation


in mammalian cells. _Science_ 317, 1760–1764 (2007). CAS  PubMed  Google Scholar  * Lindroth, A. M. et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. _Science_


292, 2077–2080 (2001). CAS  PubMed  Google Scholar  * Jackson, J. P., Lindroth, A. M., Cao, X. & Jacobsen, S. E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3


methyltransferase. _Nature_ 416, 556–560 (2002). CAS  PubMed  Google Scholar  * Gouil, Q. & Baulcombe, D. C. DNA methylation signatures of the plant chromomethyltransferases. _PLoS


Genet._ 12, e1006526 (2016). PubMed  PubMed Central  Google Scholar  * Cao, X. & Jacobsen, S. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3


methyltransferase genes. _Proc. Natl Acad. Sci. USA_ 99, 16491–16498 (2002). CAS  PubMed  PubMed Central  Google Scholar  * Panda, K. et al. Full-length autonomous transposable elements are


preferentially targeted by expression-dependent forms of RNA-directed DNA methylation. _Genome Biol._ 17, 170 (2016). PubMed  PubMed Central  Google Scholar  * Nuthikattu, S. et al. The


initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. _Plant Physiol._ 162, 116–131 (2013). THIS STUDY


DOCUMENTS THE ROLE OF SPECIFIC COMPONENTS IN TRUE _DE NOVO_ METHYLATION IN PLANTS. CAS  PubMed  PubMed Central  Google Scholar  * Bond, D. M. & Baulcombe, D. C. Epigenetic transitions


leading to heritable, RNA-mediated _de novo_ silencing in _Arabidopsis thaliana_. _Proc. Natl Acad. Sci. USA_ 112, 917–922 (2015). CAS  PubMed  PubMed Central  Google Scholar  * Wu, L., Mao,


L. & Qi, Y. Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. _Plant Physiol._ 160, 990–999 (2012). CAS  PubMed  PubMed Central


  Google Scholar  * Fultz, D. & Slotkin, R. K. Exogenous transposable elements circumvent identity-based silencing, permitting the dissection of expression-dependent silencing. _Plant


Cell_ 29, 360–376 (2017). CAS  PubMed  PubMed Central  Google Scholar  * Zemach, A. et al. The _Arabidopsis_ nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing


heterochromatin. _Cell_ 153, 193–205 (2013). CAS  PubMed  PubMed Central  Google Scholar  * Stroud, H. et al. Non-CG methylation patterns shape the epigenetic landscape in _Arabidopsis_.


_Nat. Struct. Mol. Biol._ 21, 64–72 (2014). CAS  PubMed  Google Scholar  * Bewick, A. J. & Schmitz, R. J. Gene body DNA methylation in plants. _Curr. Opin. Plant Biol._ 36, 103–110


(2017). CAS  PubMed  PubMed Central  Google Scholar  * Tran, R. K. et al. DNA methylation profiling identifies CG methylation clusters in _Arabidopsis_ genes. _Curr. Biol._ 15, 154–159


(2005). CAS  PubMed  Google Scholar  * Niederhuth, C. E. et al. Widespread natural variation of DNA methylation within angiosperms. _Genome Biol._ 17, 194 (2016). THIS STUDY IS A DETAILED


DOCUMENTATION OF SIMILARITIES AND DIFFERENCES IN METHYLOME PATTERNING IN 34 PLANT SPECIES. PubMed  PubMed Central  Google Scholar  * Takuno, S., Ran, J. H. & Gaut, B. S. Evolutionary


patterns of genic DNA methylation vary across land plants. _Nat. Plants_ 2, 15222 (2016). CAS  PubMed  Google Scholar  * Li, Q. et al. RNA-directed DNA methylation enforces boundaries


between heterochromatin and euchromatin in the maize genome. _Proc. Natl Acad. Sci. USA_ 112, 14728–14733 (2015). CAS  PubMed  PubMed Central  Google Scholar  * Zhang, X. et al. Genome-wide


high-resolution mapping and functional analysis of DNA methylation in arabidopsis. _Cell_ 126, 1189–1201 (2006). CAS  PubMed  Google Scholar  * Bewick, A. J. et al. On the origin and


evolutionary consequences of gene body DNA methylation. _Proc. Natl Acad. Sci. USA_ 113, 9111–9116 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Takuno, S. & Gaut, B. S.


Body-methylated genes in _Arabidopsis thaliana_ are functionally important and evolve slowly. _Mol. Biol. Evol._ 29, 219–227 (2012). CAS  PubMed  Google Scholar  * Vaughn, M. W. et al.


Epigenetic natural variation in _Arabidopsis thaliana_. _PLoS Biol._ 5, e174 (2007). PubMed  PubMed Central  Google Scholar  * Eichten, S. R. et al. Heritable epigenetic variation among


maize inbreds. _PLoS Genet._ 7, e1002372 (2011). CAS  PubMed  PubMed Central  Google Scholar  * Chodavarapu, R. K. et al. Transcriptome and methylome interactions in rice hybrids. _Proc.


Natl Acad. Sci. USA_ 109, 12040–12045 (2012). CAS  PubMed  PubMed Central  Google Scholar  * Eichten, S. R. et al. Epigenetic and genetic influences on DNA methylation variation in maize


populations. _Plant Cell_ 25, 2783–2797 (2013). CAS  PubMed  PubMed Central  Google Scholar  * Regulski, M. et al. The maize methylome influences mRNA splice sites and reveals widespread


paramutation-like switches guided by small RNA. _Genome Res._ 23, 1651–1662 (2013). CAS  PubMed  PubMed Central  Google Scholar  * Schmitz, R. J. et al. Epigenome-wide inheritance of


cytosine methylation variants in a recombinant inbred population. _Genome Res._ 23, 1663–1674 (2013). CAS  PubMed  PubMed Central  Google Scholar  * Schmitz, R. J. et al. Patterns of


population epigenomic diversity. _Nature_ 495, 193–198 (2013). CAS  PubMed  PubMed Central  Google Scholar  * Li, Q. et al. Examining the causes and consequences of context-specific


differential DNA methylation in maize. _Plant Physiol._ 168, 1262–1274 (2015). CAS  PubMed  PubMed Central  Google Scholar  * Kawakatsu, T. et al. Epigenomic diversity in a global collection


of _Arabidopsis thaliana_ accessions. _Cell_ 166, 492–505 (2016). THIS STUDY IS AN IN-DEPTH CHARACTERIZATION OF DNA METHYLATION VARIATION IN >1,000 _A. THALIANA_ ACCESSIONS. CAS  PubMed


  PubMed Central  Google Scholar  * Eichten, S. R., Stuart, T., Srivastava, A., Lister, R. & Borevitz, J. O. DNA methylation profiles of diverse _Brachypodium distachyon_ align with


underlying genetic diversity. _Genome Res._ 26, 1520–1531 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Garg, R., Narayana Chevala, V., Shankar, R. & Jain, M. Divergent DNA


methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. _Sci. Rep._ 5, 14922 (2015). CAS  PubMed  PubMed Central  Google


Scholar  * Shen, X. et al. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. _PLoS Genet._ 10, e1004842 (2014). PubMed  PubMed Central 


Google Scholar  * Dubin, M. J. et al. DNA methylation in _Arabidopsis_ has a genetic basis and shows evidence of local adaptation. _eLife_ 4, e05255 (2015). PubMed  PubMed Central  Google


Scholar  * Pignatta, D. et al. Natural epigenetic polymorphisms lead to intraspecific variation in _Arabidopsis_ gene imprinting. _eLife_ 3, e03198 (2014). PubMed  PubMed Central  Google


Scholar  * Zhang, L. et al. A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. _Nat. Commun._ 8, 14789 (2017). CAS  PubMed  PubMed Central 


Google Scholar  * Deng, Y. et al. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. _Science_ 355, 962–965 (2017). CAS  PubMed  Google Scholar


  * Meng, D. et al. Limited contribution of DNA methylation variation to expression regulation in _Arabidopsis thaliana_. _PLoS Genet._ 12, e1006141 (2016). PubMed  PubMed Central  Google


Scholar  * Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. _Nature_ 401, 157–161 (1999). CAS  PubMed  Google Scholar  *


Manning, K. et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. _Nat. Genet._ 38, 948–952 (2006). CAS  PubMed


  Google Scholar  * Chandler, V. L. Paramutation: from maize to mice. _Cell_ 128, 641–645 (2007). CAS  PubMed  Google Scholar  * Reinders, J. et al. Compromised stability of DNA methylation


and transposon immobilization in mosaic _Arabidopsis_ epigenomes. _Genes Dev._ 23, 939–950 (2009). CAS  PubMed  PubMed Central  Google Scholar  * Johannes, F. et al. Assessing the impact of


transgenerational epigenetic variation on complex traits. _PLoS Genet._ 5, e1000530 (2009). REFERENCES 57 AND 58 DESCRIBE THE CREATION AND PHENOTYPIC CHARACTERIZATION OF THE FIRST EPIRIL


POPULATIONS. PubMed  PubMed Central  Google Scholar  * Cortijo, S. et al. Mapping the epigenetic basis of complex traits. _Science_ 343, 1145–1148 (2014). THIS ARTICLE CLEARLY DOCUMENTS THE


POTENTIAL ROLE OF EPIGENETIC VARIATION IN INFLUENCING QUANTITATIVE TRAITS IN PLANTS. CAS  PubMed  Google Scholar  * Kooke, R. et al. Epigenetic basis of morphological variation and


phenotypic plasticity in _Arabidopsis thaliana_. _Plant Cell_ 27, 337–348 (2015). CAS  PubMed  PubMed Central  Google Scholar  * Zhang, Y. Y., Fischer, M., Colot, V. & Bossdorf, O.


Epigenetic variation creates potential for evolution of plant phenotypic plasticity. _New Phytol._ 197, 314–322 (2013). CAS  PubMed  Google Scholar  * Dapp, M. et al. Heterosis and


inbreeding depression of epigenetic _Arabidopsis_ hybrids. _Nat. Plants_ 1, 15092 (2015). CAS  PubMed  Google Scholar  * Hu, L. et al. Mutation of a major CG methylase in rice causes


genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. _Proc. Natl Acad. Sci. USA_ 111, 10642–10647 (2014). CAS  PubMed  PubMed Central  Google Scholar  *


Yamauchi, T., Johzuka-Hisatomi, Y., Terada, R., Nakamura, I. & Iida, S. The MET1b gene encoding a maintenance DNA methyltransferase is indispensable for normal development in rice.


_Plant Mol. Biol._ 85, 219–232 (2014). CAS  PubMed  Google Scholar  * Li, Q. et al. Genetic perturbation of the maize methylome. _Plant Cell_ 26, 4602–4616 (2014). PubMed  PubMed Central 


Google Scholar  * Richards, E. J. Inherited epigenetic variation — revisiting soft inheritance. _Nat. Rev. Genet._ 7, 395–401 (2006). CAS  PubMed  Google Scholar  * Taudt, A., Colome-Tatche,


M. & Johannes, F. Genetic sources of population epigenomic variation. _Nat. Rev. Genet._ 17, 319–332 (2016). CAS  PubMed  Google Scholar  * Hollister, J. D. & Gaut, B. S. Epigenetic


silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. _Genome Res._ 19, 1419–1428 (2009). CAS  PubMed  PubMed


Central  Google Scholar  * Bender, J. & Fink, G. R. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of _Arabidopsis_. _Cell_ 83, 725–734


(1995). CAS  PubMed  Google Scholar  * Gehring, M., Bubb, K. L. & Henikoff, S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. _Science_


324, 1447–1451 (2009). CAS  PubMed  PubMed Central  Google Scholar  * Hsieh, T. F. et al. Genome-wide demethylation of _Arabidopsis_ endosperm. _Science_ 324, 1451–1454 (2009). CAS  PubMed


  PubMed Central  Google Scholar  * Zemach, A. et al. Local DNA hypomethylation activates genes in rice endosperm. _Proc. Natl Acad. Sci. USA_ 107, 18729–18734 (2010). CAS  PubMed  PubMed


Central  Google Scholar  * Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. _Cell_ 136, 461–472 (2009). CAS  PubMed  PubMed Central


  Google Scholar  * Ibarra, C. A. et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. _Science_ 337, 1360–1364 (2012). CAS  PubMed  PubMed


Central  Google Scholar  * Park, K. et al. DNA demethylation is initiated in the central cells of _Arabidopsis_ and rice. _Proc. Natl Acad. Sci. USA_ 113, 15138–15143 (2016). CAS  PubMed 


PubMed Central  Google Scholar  * Rodrigues, J. A. & Zilberman, D. Evolution and function of genomic imprinting in plants. _Genes Dev._ 29, 2517–2531 (2015). CAS  PubMed  PubMed Central


  Google Scholar  * Yuan, J. et al. Both maternally and paternally imprinted genes regulate seed development in rice. _New Phytol._ http://dx.doi.org/10.1111/nph.14510 (2017). * Costa, L. M.


et al. Maternal control of nutrient allocation in plant seeds by genomic imprinting. _Curr. Biol._ 22, 160–165 (2012). CAS  PubMed  Google Scholar  * Calarco, J. P. et al. Reprogramming of


DNA methylation in pollen guides epigenetic inheritance via small RNA. _Cell_ 151, 194–205 (2012). CAS  PubMed  PubMed Central  Google Scholar  * Hsieh, P. H. et al. _Arabidopsis_ male


sexual lineage exhibits more robust maintenance of CG methylation than somatic tissues. _Proc. Natl Acad. Sci. USA_ 113, 15132–15137 (2016). CAS  PubMed  PubMed Central  Google Scholar  *


Liu, R. et al. A DEMETER-like DNA demethylase governs tomato fruit ripening. _Proc. Natl Acad. Sci. USA_ 112, 10804–10809 (2015). CAS  PubMed  PubMed Central  Google Scholar  * Satge, C. et


al. Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula. _Nat. Plants_ 2, 16166 (2016). CAS  PubMed  Google Scholar  * Kawakatsu, T. et al. Unique


cell-type-specific patterns of DNA methylation in the root meristem. _Nat. Plants_ 2, 16058 (2016). THIS DISSECTION OF CELL TYPE-SPECIFIC METHYLATION PATTERNS IN PLANTS REVEALS MOSTLY


SIMILAR PATTERNS, WITH THE EXCEPTION OF COLUMELLA CELLS. CAS  PubMed  PubMed Central  Google Scholar  * Pecinka, A. & Mittelsten Scheid, O. Stress-induced chromatin changes: a critical


view on their heritability. _Plant Cell Physiol._ 53, 801–808 (2012). CAS  PubMed  PubMed Central  Google Scholar  * Secco, D. et al. Stress induced gene expression drives transient DNA


methylation changes at adjacent repetitive elements. _eLife_ 4, e09343 (2015). THIS DETAILED ANALYSIS OF METHYLOME AND TRANSCRIPTOME RESPONSE TO PHOSPHATE STRESS FINDS EVIDENCE FOR


EXPRESSION-INDUCED CHANGES IN METHYLATION IN RESPONSE TO ABIOTIC STRESS IN RICE. PubMed Central  Google Scholar  * Jiang, C. et al. Environmentally responsive genome-wide accumulation of _de


novo Arabidopsis thaliana_ mutations and epimutations. _Genome Res._ 24, 1821–1829 (2014). CAS  PubMed  PubMed Central  Google Scholar  * Wibowo, A. 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_ 5, e13546 (2016). PubMed  PubMed


Central  Google Scholar  * Kaeppler, S. M., Kaeppler, H. F. & Rhee, Y. Epigenetic aspects of somaclonal variation in plants. _Plant Mol. Biol._ 43, 179–188 (2000). CAS  PubMed  Google


Scholar  * Peschke, V. M., Phillips, R. L. & Gengenbach, B. G. Discovery of transposable element activity among progeny of tissue culture — derived maize plants. _Science_ 238, 804–807


(1987). CAS  PubMed  Google Scholar  * Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H. & Kanda, M. Retrotransposons of rice involved in mutations induced by tissue culture. _Proc.


Natl Acad. Sci. USA_ 93, 7783–7788 (1996). CAS  PubMed  PubMed Central  Google Scholar  * Rhee, Y., Sekhon, R. S., Chopra, S. & Kaeppler, S. Tissue culture-induced novel epialleles of a


Myb transcription factor encoded by pericarp color1 in maize. _Genetics_ 186, 843–855 (2010). CAS  PubMed  PubMed Central  Google Scholar  * Ong-Abdullah, M. et al. Loss of Karma transposon


methylation underlies the mantled somaclonal variant of oil palm. _Nature_ 525, 533–537 (2015). THIS STUDY REPORTS THE IDENTIFICATION OF EPIALLELES INDUCED IN TISSUE CULTURE IN CLONALLY


PROPAGATED OIL PALMS. CAS  PubMed  PubMed Central  Google Scholar  * Tanurdzic, M. et al. Epigenomic consequences of immortalized plant cell suspension culture. _PLoS Biol._ 6, 2880–2895


(2008). CAS  PubMed  Google Scholar  * Stroud, H. et al. Plants regenerated from tissue culture contain stable epigenome changes in rice. _eLife_ 2, e00354 (2013). PubMed  PubMed Central 


Google Scholar  * Stelpflug, S. C., Eichten, S. R., Hermanson, P. J., Springer, N. M. & Kaeppler, S. M. Consistent and heritable alterations of DNA methylation are induced by tissue


culture in maize. _Genetics_ 198, 209–218 (2014). CAS  PubMed  PubMed Central  Google Scholar  * Eichten, S. R. & Springer, N. M. Minimal evidence for consistent changes in maize DNA


methylation patterns following environmental stress. _Front. Plant. Sci._ 6, 308 (2015). PubMed  PubMed Central  Google Scholar  * Song, Q. X. et al. Genome-wide analysis of DNA methylation


in soybean. _Mol. Plant_ 6, 1961–1974 (2013). CAS  PubMed  Google Scholar  * Hagmann, J. et al. Century-scale methylome stability in a recently diverged _Arabidopsis thaliana_ lineage. _PLoS


Genet._ 11, e1004920 (2015). PubMed  PubMed Central  Google Scholar  * Le, T. N. et al. DNA demethylases target promoter transposable elements to positively regulate stress responsive genes


in _Arabidopsis_. _Genome Biol._ 15, 458 (2014). PubMed  PubMed Central  Google Scholar  * Hollick, J. B. Paramutation and related phenomena in diverse species. _Nat. Rev. Genet._ 18, 5–23


(2017). CAS  PubMed  Google Scholar  * Greaves, I. K. et al. Twenty-four-nucleotide siRNAs produce heritable _trans_-chromosomal methylation in F1 _Arabidopsis_ hybrids. _Proc. Natl Acad.


Sci. USA_ 113, E6895–E6902 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Greaves, I. K. et al. Trans chromosomal methylation in _Arabidopsis_ hybrids. _Proc. Natl Acad. Sci. USA_


109, 3570–3575 (2012). CAS  PubMed  PubMed Central  Google Scholar  * Zhang, Q. et al. Methylation interactions in _Arabidopsis_ hybrids require RNA-directed DNA methylation and are


influenced by genetic variation. _Proc. Natl Acad. Sci. USA_ 113, E4248–E4256 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Jordan, W. T. & Schmitz, R. J. The shocking


consequences of hybrid epigenomes. _Genome Biol._ 17, 85 (2016). PubMed  PubMed Central  Google Scholar  * Rigal, M. et al. Epigenome confrontation triggers immediate reprogramming of DNA


methylation and transposon silencing in _Arabidopsis thaliana_ F1 epihybrids. _Proc. Natl Acad. Sci. USA_ 113, E2083–E2092 (2016). IN THIS REPORT, EPIHYBRIDS BETWEEN A WILD-TYPE PARENT AND A


HYPOMETHYLATED PARENT REVEAL WIDESPREAD REDISTRIBUTION OF HETEROCHROMATIN MARKS. CAS  PubMed  PubMed Central  Google Scholar  * Lei, M. et al. Regulatory link between DNA methylation and


active demethylation in _Arabidopsis_. _Proc. Natl Acad. Sci. USA_ 112, 3553–3557 (2015). CAS  PubMed  PubMed Central  Google Scholar  * Williams, B. P., Pignatta, D., Henikoff, S. &


Gehring, M. Methylation-sensitive expression of a DNA demethylase gene serves as an epigenetic rheostat. _PLoS Genet._ 11, e1005142 (2015). PubMed  PubMed Central  Google Scholar  * Wendel,


J. F., Jackson, S. A., Meyers, B. C. & Wing, R. A. Evolution of plant genome architecture. _Genome Biol._ 17, 37 (2016). PubMed  PubMed Central  Google Scholar  * Zhang, J. et al.


Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression. _Proc. Natl Acad. Sci. USA_ 112, E7022–E7029 (2015). THIS


STUDY PROVIDES EVIDENCE FOR PLOIDY-INDUCED CHANGES IN DNA METHYLATION AND GENE EXPRESSION IN RICE. CAS  PubMed  PubMed Central  Google Scholar  * Edgar, P. P. et al. Subgenome dominance in


an interspecific hybrid, synthetic allopolyploid, and a 140 year old naturally established neo-allopolyploid monkeyflower. Preprint at _bioRxiv_ https://doi.org/10.1101/094797 (2016). *


Becker, C. et al. Spontaneous epigenetic variation in the _Arabidopsis thaliana_ methylome. _Nature_ 480, 245–249 (2011). CAS  PubMed  Google Scholar  * Schmitz, R. J. et al.


Transgenerational epigenetic instability is a source of novel methylation variants. _Science_ 334, 369–373 (2011). CAS  PubMed  PubMed Central  Google Scholar  * van der Graaf, A. et al.


Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. _Proc. Natl Acad. Sci. USA_ 112, 6676–6681 (2015). THIS STUDY IS A CAREFUL DISSECTION OF THE RATES OF SPONTANEOUS


CHANGE IN DNA METHYLATION IN PLANTS. CAS  PubMed  PubMed Central  Google Scholar  * Shaw, R. G., Byers, D. L. & Darmo, E. Spontaneous mutational effects on reproductive traits of


_Arabidopsis thaliana_. _Genetics_ 155, 369–378 (2000). CAS  PubMed  PubMed Central  Google Scholar  * Ossowski, S. et al. The rate and molecular spectrum of spontaneous mutations in


_Arabidopsis thaliana_. _Science_ 327, 92–94 (2010). CAS  PubMed  Google Scholar  * Zheng, X. et al. Transgenerational epimutations induced by multi-generation drought imposition mediate


rice plant's adaptation to drought condition. _Sci. Rep._ 7, 39843 (2017). CAS  PubMed  PubMed Central  Google Scholar  * Li, Q., Eichten, S. R., Hermanson, P. J. & Springer, N. M.


Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines. _Genetics_ 196, 667–676 (2014). CAS  PubMed  Google Scholar  * Eichten, S. R. et al. Spreading


of heterochromatin is limited to specific families of maize retrotransposons. _PLoS Genet._ 8, e1003127 (2012). CAS  PubMed  PubMed Central  Google Scholar  * Catoni, M. et al. DNA sequence


properties that predict susceptibility to epiallelic switching. _EMBO J._ 36, 617–628 (2017). CAS  PubMed  PubMed Central  Google Scholar  * Lewsey, M. G. et al. Mobile small RNAs regulate


genome-wide DNA methylation. _Proc. Natl Acad. Sci. USA_ 113, E801–E810 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Melnyk, C. W., Molnar, A. & Baulcombe, D. C. Intercellular


and systemic movement of RNA silencing signals. _EMBO J._ 30, 3553–3563 (2011). CAS  PubMed  PubMed Central  Google Scholar  * Kasai, A., Bai, S., Hojo, H. & Harada, T. Epigenome editing


of potato by grafting using transgenic tobacco as siRNA donor. _PLoS ONE_ 11, e0161729 (2016). PubMed  PubMed Central  Google Scholar  * Jaligot, E. et al. Epigenetic imbalance and the


floral developmental abnormality of the _in vitro_-regenerated oil palm _Elaeis guineensis_. _Ann. Bot._ 108, 1453–1462 (2011). CAS  PubMed  PubMed Central  Google Scholar  * Telias, A. et


al. Apple skin patterning is associated with differential expression of MYB10. _BMC Plant Biol._ 11, 93 (2011). CAS  PubMed  PubMed Central  Google Scholar  * Xu, J., Tanino, K. K. &


Robinson, S. J. Stable epigenetic variants selected from an induced hypomethylated _Fragaria vesca_ population. _Front. Plant Sci._ 7, 1768 (2016). PubMed  PubMed Central  Google Scholar  *


Amabile, A. et al. Inheritable silencing of endogenous genes by hit-and-run targeted epigenetic editing. _Cell_ 167, 219–232.e14 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Liu,


X. S. et al. Editing DNA methylation in the mammalian genome. _Cell_ 167, 233–247.e17 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Park, M., Keung, A. J. & Khalil, A. S. The


epigenome: the next substrate for engineering. _Genome Biol._ 17, 183 (2016). PubMed  PubMed Central  Google Scholar  * Bikard, D. et al. Programmable repression and activation of bacterial


gene expression using an engineered CRISPR–Cas system. _Nucleic Acids Res._ 41, 7429–7437 (2013). CAS  PubMed  PubMed Central  Google Scholar  * Johnson, L. M. et al. SRA- and


SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. _Nature_ 507, 124–128 (2014). IN THIS STUDY, THE AUTHORS USE ZINC FINGER ENDONUCLEASES TO DIRECT _DE NOVO_


DNA METHYLATION IN _A. THALIANA_. CAS  PubMed  PubMed Central  Google Scholar  * Griffin, P. T., Niederhuth, C. E. & Schmitz, R. J. A. Comparative analysis of 5-azacytidine- and


zebularine-induced DNA demethylation. _G3 (Bethesda)_ 6, 2773–2780 (2016). CAS  Google Scholar  * Waddington, C. H. Canalization of development and genetic assimilation of acquired


characters. _Nature_ 183, 1654–1655 (1959). CAS  PubMed  Google Scholar  * Wolff, P. et al. High-resolution analysis of parent-of-origin allelic expression in the _Arabidopsis_ endosperm.


_PLoS Genet._ 7, e1002126 (2011). CAS  PubMed  PubMed Central  Google Scholar  * Zhang, M. et al. Genome-wide high resolution parental-specific DNA and histone methylation maps uncover


patterns of imprinting regulation in maize. _Genome Res._ 24, 167–176 (2014). CAS  PubMed  PubMed Central  Google Scholar  * Moreno-Romero, J., Jiang, H., Santos-Gonzalez, J. & Kohler,


C. Parental epigenetic asymmetry of PRC2-mediated histone modifications in the _Arabidopsis_ endosperm. _EMBO J._ 35, 1298–1311 (2016). CAS  PubMed  PubMed Central  Google Scholar  * Probst,


A. V. & Mittelsten Scheid, O. Stress-induced structural changes in plant chromatin. _Curr. Opin. Plant Biol._ 27, 8–16 (2015). CAS  PubMed  Google Scholar  * Chen, X., Liu, X., Zhao, Y.


& Zhou, D. X. Histone H3K4me3 and H3K27me3 regulatory genes control stable transmission of an epimutation in rice. _Sci. Rep._ 5, 13251 (2015). CAS  PubMed  PubMed Central  Google


Scholar  * Guo, Z. et al. Global epigenomic analysis indicates that epialleles contribute to allele-specific expression via allele-specific histone modifications in hybrid rice. _BMC


Genomics_ 16, 232 (2015). PubMed  PubMed Central  Google Scholar  * Song, X. J. et al. Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and


plant biomass in rice. _Proc. Natl Acad. Sci. USA_ 112, 76–81 (2015). CAS  PubMed  Google Scholar  * Jaskiewicz, M., Conrath, U. & Peterhansel, C. Chromatin modification acts as a


memory for systemic acquired resistance in the plant stress response. _EMBO Rep._ 12, 50–55 (2011). CAS  PubMed  Google Scholar  * Ding, Y., Fromm, M. & Avramova, Z. Multiple exposures


to drought 'train' transcriptional responses in _Arabidopsis_. _Nat. Commun._ 3, 740 (2012). PubMed  Google Scholar  * Sani, E., Herzyk, P., Perrella, G., Colot, V. & Amtmann,


A. Hyperosmotic priming of _Arabidopsis_ seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. _Genome Biol._ 14, R59 (2013). PubMed  PubMed


Central  Google Scholar  * Du, J. et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. _Cell_ 151, 167–180 (2012). CAS  PubMed


  PubMed Central  Google Scholar  * Deleris, A. et al. Loss of the DNA methyltransferase MET1 Induces H3K9 hypermethylation at PcG target genes and redistribution of H3K27 trimethylation to


transposons in _Arabidopsis thaliana_. _PLoS Genet._ 8, e1003062 (2012). THIS STUDY SHOWS HOW LOSS OF DNA METHYLATION AT SOME LOCI LEADS TO TRANSCRIPTIONAL REPRESSION BY THE POLYCOMB


COMPLEX. CAS  PubMed  PubMed Central  Google Scholar  * Greenberg, M. V. et al. Interplay between active chromatin marks and RNA-directed DNA methylation in _Arabidopsis thaliana_. _PLoS


Genet._ 9, e1003946 (2013). PubMed  PubMed Central  Google Scholar  * Laprell, F., Finkl, K. & Muller, J. Propagation of Polycomb-repressed chromatin requires sequence-specific


recruitment to DNA. _Science_ 356, 85–88 (2017). CAS  PubMed  Google Scholar  * Wang, X. & Moazed, D. DNA sequence-dependent epigenetic inheritance of gene silencing and histone H3K9


methylation. _Science_ 356, 88–91 (2017). CAS  PubMed  PubMed Central  Google Scholar  * Zhang, L. et al. Identification and characterization of an epi-allele of FIE1 reveals a regulatory


linkage between two epigenetic marks in rice. _Plant Cell_ 24, 4407–4421 (2012). CAS  PubMed  PubMed Central  Google Scholar  * Zabet, N. R., Catoni, M., Prischi, F. & Paszkowski, J.


Cytosine methylation at CpCpG sites triggers accumulation of non-CpG methylation in gene bodies. _Nucleic Acids Res._ 45, 3777–3784 (2017). CAS  PubMed  PubMed Central  Google Scholar  * Du,


J., Johnson, L. M., Jacobsen, S. E. & Patel, D. J. DNA methylation pathways and their crosstalk with histone methylation. _Nat. Rev. Mol. Cell Biol._ 16, 519–532 (2015). CAS  PubMed 


PubMed Central  Google Scholar  * Bewick, A. J. et al. The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants. _Genome Biol._ 18, 65 (2017). PubMed  PubMed Central  Google


Scholar  * West, P. T. et al. Genomic distribution of H3K9me2 and DNA methylation in a maize genome. _PLoS ONE_ 9, e105267 (2014). PubMed  PubMed Central  Google Scholar  Download


references ACKNOWLEDGEMENTS The authors are grateful to the vibrant community of epigenetic researchers and acknowledge that only a subset of critical works is cited in this article owing to


space limitations. The authors are grateful to J. Noshay for assistance with figure preparation. C. Hirsch, S. Anderson and S. Eichten provided valuable feedback on the manuscript. The


authors also appreciate the constructive feedback from several anonymous reviewers that helped to improve the article. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Plant and


Microbial Biology, University of Minnesota, Saint Paul, 55108, Minnesota, USA Nathan M. Springer * Department of Genetics, The University of Georgia, Athens, 30602, Georgia, USA Robert J.


Schmitz Authors * Nathan M. Springer View author publications You can also search for this author inPubMed Google Scholar * Robert J. Schmitz View author publications You can also search for


this author inPubMed Google Scholar CORRESPONDING AUTHORS Correspondence to Nathan M. Springer or Robert J. Schmitz. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing


financial interests. POWERPOINT SLIDES POWERPOINT SLIDE FOR FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3 POWERPOINT SLIDE FOR FIG. 4 GLOSSARY * Traits Any measurable


aspect of an organism, including morphological, biochemical and molecular properties. * Transgressive segregation The situation in which offspring (F1, F2 or later generations) exhibit


phenotypes that transgress (are outside of) the parental phenotypic range. * Heritable variation Information in the genome that is transmitted to offspring or daughter cells. * Genomic


selection The use of genetic markers that are spread throughout the genome to select individuals with desired predicted breeding values. * Paramutation An interaction between alleles in


which one alleles triggers a heritable change at the other allele, resulting in altered expression or chromatin state. * Imprinting Differential expression of alleles depending on


parent-of-origin of the allele. * Wide crosses Crosses between very distantly related members of the same species or between individuals of related species. * RNA-directed DNA methylation


(RdDM). The mechanism by which 24-nt small interfering RNAs can direct DNA methylation to specific genomic loci. * Accessions Individuals isolated from a single geographical area. An ecotype


comprises many accessions from a similar ecological range. * Differentially methylated regions (DMRs). Genomic regions that have different levels of methylation between sample groups. Can


be context specific (CG, CHG or CHH) or can refer to overall methylcytosine content. * Epialleles Chromatin differences at a locus between different individuals or cells. Note that an


epiallele may be due to genetic differences (at _cis_-genomic or _trans_-genomic locations). Thus, some epialleles may reflect epigenetic variation but others may reflect genetic variation.


* Epigenetic recombinant inbred line (epiRIL). A quasi-homozygous line that is almost identical at the genetic level but that segregates at the DNA methylation level. Produced from an


initial cross between two individuals with few DNA sequence differences but with contrasting DNA methylation profiles, followed by 6–8 generations of self-pollination. * Polyploidization


Whole-genome duplication events that can occur through the doubling of the chromosomes in a single species (autopolyploidization) or through a cross between related species followed by


chromosome doubling (allopolyploidization). * Linkage disequilibrium A measure of whether alleles at two loci coexist in a population in a nonrandom manner. Alleles that are in linkage


disequilibrium are found together on the same haplotype more often than would be expected under a random combination of alleles. * Scions Shoot or branch of a plant that is grafted to a


rootstock. * Grafting The joining of living material from two individuals to generate a chimaera. In plants this generally is performed through grafting of a scion (a branch or bud) from one


plant to a rootstock from another plant. * Rootstock The root system of a plant with the shoot removed onto which another variety is grafted. * Epigenetic quantitative trait loci (epiQTL).


Epigenetic variants that are associated with a trait and that do not have any changes in the DNA sequence. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS


ARTICLE Springer, N., Schmitz, R. Exploiting induced and natural epigenetic variation for crop improvement. _Nat Rev Genet_ 18, 563–575 (2017). https://doi.org/10.1038/nrg.2017.45 Download


citation * Published: 03 July 2017 * Issue Date: September 2017 * DOI: https://doi.org/10.1038/nrg.2017.45 SHARE THIS ARTICLE Anyone you share the following link with will be able to read


this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative


Trending News

Sean ‘diddy’ combs’ first christmas in jail will include card games, soccer competition and special meal

From lavish to lockdown. Sean “Diddy” Combs’ first Christmas behind bars will reportedly include an array of games, spor...

How subi suresh, a dancer, became one of the few women in comedy in kerala

The very mention of Subi Suresh may bring, to those familiar with her onstage work in Kerala, a lot of mirth and laughte...

Oops! That page can't be found

Oops! That page can't be found It seems we can't find what you're looking for.Latest from HITC More latest from HITC...

Erode bye-polls: aiadmk cadre attack journalists for reporting on bribe distribution to voters

According to reports, journalists Rajesh and Karupaiya of News Tamil 24/7 channel were attacked at the Veerappanchatram ...

Gawande says leaving Haven CEO job will allow him to focus on Covid-19

Atul Gawande on Wednesday confirmed that he will step down as chief executive of the health care company formed by Amazo...

Latests News

Exploiting induced and natural epigenetic variation for crop improvement

KEY POINTS * Substantial natural variation in DNA methylation patterns exists within many plant species. This variation ...

Court action launched to stop logging near iconic mountain bike track in Northern Tasmania

AdNewsLocal NewsNewsLocal NewsNews HomeGood evening, Your ContentNewslettersMy saved ListAccountMy AccountLogoutNewsSpor...

Attention Required! | Cloudflare

Please enable cookies. Sorry, you have been blocked You are unable to access alarabiya.net Why have I been blocked? This...

Virtual davos summit 2021 to begin from today, pm modi, xi jinping among listed speakers

Prime Minister Narendra Modi will deliver his address on Thursday. The six-day online Davos Agenda Summit of the World E...

Women in states that ban abortion will still be able to get abortion pills online from overseas

In this photo illustration, a person looks at an Abortion Pill (RU-486) for unintended pregnancy from Mifepristone displ...

Top