Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements

Secco, David; Wang, Chuang; Shou, Huixia; Schultz, Matthew D.; Chiarenza, Serge; Nussaume, Laurent; Ecker, Joseph R.; Whelan, James; Lister, Ryan

doi:10.7554/elife.09343

Cited by 313 publications

(319 citation statements)

References 81 publications

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“…In rice, it has been reported that the most predominant mechanism of LP-induced differential methylation is the methylation of TEs triggered by changes in the expression of PSR genes (42). Although we also observed this phenomenon in Arabidopsis, we found that the methylation of TEs in close proximity to PSR genes was significantly reduced in comparison with cases in which differential methylation in gene bodies or upstream regions was associated with PSR genes.…”

Section: Discussioncontrasting

confidence: 51%

“…These results suggested the presence of an alternative route of methylation affecting gene expression, such as the positive modulation of transcription via DNA methylation of gene bodies in which methylation acts as a mark for binding specific methylationassociated proteins. Additionally, differential methylation in repetitive elements may result from changes in methylation triggered by the activation or repression of PSR in neighboring genes, as recently reported in rice (42).…”

Section: Discussionmentioning

confidence: 98%

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Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation

Yong-Villalobos

González-Morales

Wróbel

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

178

181

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Phosphate (Pi) availability is a significant limiting factor for plant growth and productivity in both natural and agricultural systems. To cope with such limiting conditions, plants have evolved a myriad of developmental and biochemical strategies to enhance the efficiency of Pi acquisition and assimilation to avoid nutrient starvation. In the past decade, these responses have been studied in detail at the level of gene expression; however, the possible epigenetic components modulating plant Pi starvation responses have not been thoroughly investigated. Here, we report that an extensive remodeling of global DNA methylation occurs in Arabidopsis plants exposed to low Pi availability, and in many instances, this effect is related to changes in gene expression. Modifications in methylation patterns within genic regions were often associated with transcriptional activation or repression, revealing the important role of dynamic methylation changes in modulating the expression of genes in response to Pi starvation. Moreover, Arabidopsis mutants affected in DNA methylation showed that changes in DNA methylation patterns are required for the accurate regulation of a number of Pi-starvation-responsive genes and that DNA methylation is necessary to establish proper morphological and physiological phosphate starvation responses.phosphate | epigenetics | abiotic stress | DNA methylation | methylome D uring evolution, plants have acquired a series of adaptive strategies that allow them to survive and complete their life cycles under adverse environmental conditions. Consequently, plants have evolved a myriad of physiological, cellular, and molecular mechanisms to cope with challenging environments. Plant responses to environmental stress include modifications in postembryonic development and metabolic reprogramming, which are highly dependent on the regulation of gene expression. It is well documented that gene regulation at the transcriptional and posttranscriptional levels plays an important role in plant stress responses; however, more recent evidence suggests that epigenetic mechanisms also play an important role in reprogramming gene expression in response to environmental cues and that epigenetic marks can serve as a priming mechanism to prepare future generations to better withstand biotic and abiotic stresses (1-3). These epigenetic marks include, but are not restricted to, posttranslational histone modifications and DNA methylation, a mechanism by which cytosine DNA methylation regulates the silencing and control of transposable elements (TEs) and repetitive sequences, genomic imprinting, and gene silencing. In plants, this DNA methylation modification is applied in three different sequence contexts (CG, CHG, and CHH, where H = A, C, or T), and the involvement of different pathways is necessary for the establishment, maintenance, and modification of DNA methylation patterns in these contexts (4, 5). These epigenetic processes can interact to orchestrate new heterochromatin states that modify gene expression [for re...

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Section: Discussioncontrasting

confidence: 51%

Section: Discussionmentioning

confidence: 98%

Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation

Yong-Villalobos

González-Morales

Wróbel

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

178

181

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“…For RNA-seq studies, sample preparation and transcript analysis were performed as previously described (Secco et al, 2015), with several exceptions. First, samples were harvested 30 min, 1 h, 3 h, or 24 h after transfer to fresh medium (from low Pi to low Pi, high Pi to high Pi, or low Pi to high Pi).…”

Section: Transcript Analysismentioning

confidence: 99%

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

et al. 2018

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Phosphate starvation-mediated induction of the HAD-type phosphatases PPsPase1 (AT1G73010) and PECP1 (AT1G17710) has been reported in Arabidopsis (Arabidopsis thaliana). However, little is known about their in vivo function or impact on plant responses to nutrient deficiency. The preferences of PPsPase1 and PECP1 for different substrates have been studied in vitro but require confirmation in planta. Here, we examined the in vivo function of both enzymes using a reverse genetics approach. We demonstrated that PPsPase1 and PECP1 affect plant phosphocholine and phosphoethanolamine content, but not the pyrophosphate-related phenotypes. These observations suggest that the enzymes play a similar role in planta related to the recycling of polar heads from membrane lipids that is triggered during phosphate starvation. Altering the expression of the genes encoding these enzymes had no effect on lipid composition, possibly due to compensation by other lipid recycling pathways triggered during phosphate starvation. Furthermore, our results indicated that PPsPase1 and PECP1 do not influence phosphate homeostasis, since the inactivation of these genes had no effect on phosphate content or on the induction of molecular markers related to phosphate starvation. A combination of transcriptomics and imaging analyses revealed that PPsPase1 and PECP1 display a highly dynamic expression pattern that closely mirrors the phosphate status. This temporal dynamism, combined with the wide range of induction levels, broad expression, and lack of a direct effect on Pi content and regulation, makes PPsPase1 and PECP1 useful molecular markers of the phosphate starvation response.Plant growth is highly sensitive to a lack of phosphate (Pi); hence, the application of Pi fertilizers has become standard practice for high-throughput crop production (Cordell et al., 2009). Most phosphorus in the soil is not available to plants, as it is combined with other minerals or parts of organic compounds (Bieleski, 1973;Raghothama and Karthikeyan, 2005). Only a small fraction of soluble Pi (usually present at a concentration of ,10 mM in the soil) can be taken up by plants.Although growth is not optimal under limiting conditions, plants can withstand changing Pi concentrations within heterogeneous soils or in the external nutrient supply that can lead to reprogramming of their metabolism and architecture (Hammond et al., 2003;Péret et al., 2011;Plaxton and Tran, 2011). Root architecture can be modified to facilitate Pi uptake by favoring the development of lateral roots (at the expense of primary root elongation in many plants including Arabidopsis), increasing the density and length of root hairs, and limiting the development of aerial parts (López-Bucio et al., 2002;Svistoonoff et al., 2007;Gruber et al., 2013). Pi uptake mechanisms are enhanced at the root/soil interface, particularly through the stimulation of Pi transport activity (Mudge et al., 2002;Shin et al., 2004;Nussaume et al., 2011; Ayadi et al., 2015). In parallel, mobilization of Pi sources fr...

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“…This elevation of mCHH in regions surrounding genes is much less prevalent in Arabidopsis (10). A recent study showed that high mCHH can also be induced near genes that are up-regulated in plants subjected to phosphate starvation (15).…”

mentioning

confidence: 99%

RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome

Gent

Zynda

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

191

249

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The maize genome is relatively large (∼2.3 Gb) and has a complex organization of interspersed genes and transposable elements, which necessitates frequent boundaries between different types of chromatin. The examination of maize genes and conserved noncoding sequences revealed that many of these are flanked by regions of elevated asymmetric CHH (where H is A, C, or T) methylation (termed mCHH islands). These mCHH islands are quite short (∼100 bp), are enriched near active genes, and often occur at the edge of the transposon that is located nearest to genes. The analysis of DNA methylation in other sequence contexts and several chromatin modifications revealed that mCHH islands mark the transition from heterochromatin-associated modifications to euchromatin-associated modifications. The presence of an mCHH island is fairly consistent in several distinct tissues that were surveyed but shows some variation among different haplotypes. The presence of insertion/ deletions in promoters often influences the presence and position of an mCHH island. The mCHH islands are dependent upon RNA-directed DNA methylation activities and are lost in mop1 and mop3 mutants, but the nearby genes rarely exhibit altered expression levels. Instead, loss of an mCHH island is often accompanied by additional loss of DNA methylation in CG and CHG contexts associated with heterochromatin in nearby transposons. This suggests that mCHH islands and RNA-directed DNA methylation near maize genes may act to preserve the silencing of transposons from activity of nearby genes.T he cytosine bases in a genome can be modified to 5-methylcytosine by adding a methyl group at the 5′ position. This process, called DNA methylation, is conserved from algae to animals and plants (1, 2). DNA methylation can be separated into different types based on the local sequence context. In plants DNA methylation is found at the symmetric CG or CHG (where H = A, C, or T) sites or at nonsymmetric CHH sites. CG and CHG methylation are maintained at high fidelity following DNA replication due to activity of maintenance methyltransferases such as MET1 or chromomethylase (CMT) 3 (3, 4), whereas CHH methylation (mCHH) requires targeting by either domains rearranged methylase 2 (DRM2) or CMT2 (3-6). The DRM2 targeting occurs via RNAdirected DNA methylation (RdDM) and requires the activity of polymerase IV (PolIV) and polymerase V (PolV) complexes (3, 4). There is evidence that recruitment of PolIV and PolV may require the presence of dimethylation of lysine 9 of histone H3 (H3K9me2) or DNA methylation at the targeted genomic regions (7,8). The specific mechanisms that recruit CMT2 are not well characterized but may require specific histone modifications (5, 6).Much of our knowledge of DNA methylation in plants is derived from studies of the model plant Arabidopsis thaliana, which has a relatively small genome and relatively few examples of genes with nearby transposons (36.3%; ref. 9). The maize genome is much more complex, with the majority (85.5%) of genes positioned within 1...

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Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements

Cited by 313 publications

References 81 publications

Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation

Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome

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