Spreading of Heterochromatin Is Limited to Specific Families of Maize Retrotransposons

Eichten, Steven R.; Ellis, Nathanael A.; Makarevitch, Irina; Yeh, Cheng‐Ting; Gent, Jonathan I.; Guo, Lin; McGinnis, Karen M.; Zhang, Xiaoyu; Schnable, Patrick S.; Vaughn, Matthew; Dawe, R. Kelly; Springer, Nathan M.

doi:10.1371/journal.pgen.1003127

Cited by 158 publications

(151 citation statements)

References 63 publications

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“…The nearest elements were classified as terminal inverted repeat (TIR) elements, LTR_spreading, or LTR_nonspreading. The spreading or nonspreading is based upon the assignments from a previous study in which some families of LTR elements were found to result in spread of DNA methylation to low-copy flanking sequences (Eichten et al 2012). The error bars and significance ("*") of the random sets of probes were determined in the same method used in A.…”

Section: Discussionmentioning

confidence: 99%

Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

et al. 2014

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Plants regenerated from tissue culture and their progenies are expected to be identical clones, but often display heritable molecular and phenotypic variation. We characterized DNA methylation patterns in callus, primary regenerants, and regenerantderived progenies of maize using immunoprecipitation of methylated DNA (meDIP) to assess the genome-wide frequency, pattern, and heritability of DNA methylation changes. Although genome-wide DNA methylation levels remained similar following tissue culture, numerous regions exhibited altered DNA methylation levels. Hypomethylation events were observed more frequently than hypermethylation following tissue culture. Many of the hypomethylation events occur at the same genomic sites across independent regenerants and cell lines. The DNA methylation changes were often heritable in progenies produced from self-pollination of primary regenerants. Methylation changes were enriched in regions upstream of genes and loss of DNA methylation at promoters was associated with altered expression at a subset of loci. Differentially methylated regions (DMRs) found in tissue culture regenerants overlap with the position of naturally occurring DMRs more often than expected by chance with 8% of tissue culture hypomethylated DMRs overlapping with DMRs identified by profiling natural variation, consistent with the hypotheses that genomic stresses similar to those causing somaclonal variation may also occur in nature, and that certain loci are particularly susceptible to epigenetic change in response to these stresses. The consistency of methylation changes across regenerants from independent cultures suggests a mechanistic response to the culture environment as opposed to an overall loss of fidelity in the maintenance of epigenetic states. C LONAL propagation of plants and animals is expected to produce individuals identical to the donor. However, this is often not the case. Plant tissue culture involves dedifferentiation, or return to a "stem-cell-like" state, which involves dynamic reprogramming at the chromatin level to induce the formation of callus. Subsequently, proliferating cells start to redifferentiate when specific changes in the balance of growth regulators are introduced in the culture medium, ultimately leading to organogenesis or regeneration into whole plants (Grafi et al. 2011;Miguel and Marum 2011). This process represents a traumatic stress to plant cells and often provokes an array of genetic and epigenetic instabilities that are somatically and meiotically heritable (Phillips et al. 1994;Kaeppler et al. 2000). This suite of molecular and phenotypic phenomena is collectively termed somaclonal variation (Larkin and Scowcroft 1981).At the cellular and molecular levels, somaclonal variation is composed of chromosome rearrangements, polyploidy and aneuploidy, DNA sequence changes, activation of quiescent transposable elements (TEs), and epigenetic variation reflected by altered DNA methylation patterns (Karp and Maddock 1984;Brettell et al. 1986;Dennis et al. 1987;Pe...

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Section: Discussionmentioning

confidence: 99%

Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

et al. 2014

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“…Specifically, all of the six most abundant LTR-retro families that we investigated exhibit high overall levels of internal DNA methylation and H3K9me2 in B73 aerial tissues, as well as spreading of these heterochromatic modifications into adjacent regions of ;1 to 2 kb (Eichten et al, 2012). Nonetheless, members of many of the highly abundant LTR-retro families are closely interspersed with genes in the euchromatic arms of maize chromosomes (SanMiguel et al, 1996;Liu et al, 2007;Baucom et al, 2009).…”

Section: Diversity Of Replication Timing In Te Familiesmentioning

confidence: 93%

“…TEs, which typically contain high levels of DNA methylation and the repressive histone modification H3K9me2 in maize (Eichten et al, 2012;Regulski et al, 2013;West et al, 2014), are traditionally thought of as silenced chromatin. Specifically, all of the six most abundant LTR-retro families that we investigated exhibit high overall levels of internal DNA methylation and H3K9me2 in B73 aerial tissues, as well as spreading of these heterochromatic modifications into adjacent regions of ;1 to 2 kb (Eichten et al, 2012).…”

Section: Diversity Of Replication Timing In Te Familiesmentioning

confidence: 99%

Genomic Analysis of the DNA Replication Timing Program during Mitotic S Phase in Maize (Zea mays) Root Tips

Wear

Song²,

Zynda³

et al. 2017

Plant Cell

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All plants and animals must replicate their DNA, using a regulated process to ensure that their genomes are completely and accurately replicated. DNA replication timing programs have been extensively studied in yeast and animal systems, but much less is known about the replication programs of plants. We report a novel adaptation of the "Repli-seq" assay for use in intact root tips of maize (Zea mays) that includes several different cell lineages and present whole-genome replication timing profiles from cells in early, mid, and late S phase of the mitotic cell cycle. Maize root tips have a complex replication timing program, including regions of distinct early, mid, and late S replication that each constitute between 20 and 24% of the genome, as well as other loci corresponding to ;32% of the genome that exhibit replication activity in two different time windows. Analyses of genomic, transcriptional, and chromatin features of the euchromatic portion of the maize genome provide evidence for a gradient of early replicating, open chromatin that transitions gradually to less open and less transcriptionally active chromatin replicating in mid S phase. Our genomic level analysis also demonstrated that the centromere core replicates in mid S, before heavily compacted classical heterochromatin, including pericentromeres and knobs, which replicate during late S phase.

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“…It is unclear how pure epigenetic variation could occur, but failure to faithfully maintain methylation patterns by methyltransferase has been proposed as one possible mechanism (Schmitz et al 2011). Alternatively, DNA methylation variation could be dependent on genetic polymorphisms such as structural rearrangements (Melquist et al 1999) or polymorphic transposon insertions (Martin et al 2009;Eichten et al 2012;Yang et al 2013) that occur near the affected region. DNA methylation variation could also be triggered by signals from trans-acting loci (Cao and Jacobsen 2002;Riddle and Richards 2002;Bender 2004).…”

mentioning

confidence: 99%

Inheritance Patterns and Stability of DNA Methylation Variation in Maize Near-Isogenic Lines

Eichten

Hermanson

et al. 2014

Genetics

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DNA methylation is a chromatin modification that contributes to epigenetic regulation of gene expression. The inheritance patterns and trans-generational stability of 962 differentially methylated regions (DMRs) were assessed in a panel of 71 near-isogenic lines (NILs) derived from maize (Zea mays) inbred lines B73 and Mo17. The majority of DMRs exhibit inheritance patterns that would be expected for local (cis) inheritance of DNA methylation variation such that DNA methylation level was coupled to local genotype. There are few examples of DNA methylation that exhibit trans-acting control or paramutation-like patterns. The cis-inherited DMRs provide an opportunity to study the stability of inheritance for DNA methylation variation. There was very little evidence for alterations of DNA methylation levels at these DMRs during the generations of the NIL population development. DNA methylation level was associated with local genotypes in nearly all of the .30,000 potential cases of inheritance. The majority of the DMRs were not associated with small RNAs. Together, our results suggest that a significant portion of DNA methylation variation in maize exhibits locally (cis) inherited patterns, is highly stable, and does not require active programming by small RNAs for maintenance. DNA methylation may contribute to heritable epigenetic information in many eukaryotic genomes. In this study, we have documented the inheritance patterns and trans-generational stability for nearly 1000 DNA methylation variants in a segregating maize population. At most loci studied, the DNA methylation differences are locally inherited and are not influenced by the other allele or other genomic regions. The inheritance of DNA methylation levels across generations is quite robust with almost no examples of unstable inheritance, suggesting that DNA methylation differences can be quite stably inherited, even in segregating populations. MANY organisms exhibit abundant phenotypic diversity within a species. This observed diversity is often attributed to genetic variation, but there is a large part of this diversity that cannot be explained by genetic polymorphisms alone (Manolio et al. 2009). It has been proposed that epigenetic variation could be one component of this missing heritability (Petronis 2010). DNA methylation is a well-studied contributor to epigenetic information in many eukaryotes. In plants, DNA methylation occurs in three sequence contexts, CG, CHG, and CHH (where H = A, T, or C). It is widely accepted that de novo establishment of DNA methylation is often guided by small RNA (RNA-directed DNA methylation, RdDM), while maintenance of DNA methylation is performed by different methyltransferases, namely MET1 (METHYL-TRANSFERASE 1) for CG methylation, CMT3 (CHROMOME-THYLASE 3), and DRM1/2 (DOMAINS REARRANGED METHYLTRANSFERASE 1 and 2) for non-CG methylation (CHG and CHH) (Chan et al. 2005). Variation in DNA methylation profiles has been observed in many species (Vaughn et al. 2007;Eichten et al. 2011bEichten et al. , 2013Re...

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Spreading of Heterochromatin Is Limited to Specific Families of Maize Retrotransposons

Cited by 158 publications

References 63 publications

Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

Consistent and Heritable Alterations of DNA Methylation Are Induced by Tissue Culture in Maize

Genomic Analysis of the DNA Replication Timing Program during Mitotic S Phase in Maize (Zea mays) Root Tips

Inheritance Patterns and Stability of DNA Methylation Variation in Maize Near-Isogenic Lines

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