Maintenance of pre‐existing DNA methylation states through recurring excess‐light stress

Ganguly, Diep R; Crisp, Peter A.; Eichten, Steven R.; Pogson, Barry J.

doi:10.1111/pce.13324

Cited by 34 publications

(31 citation statements)

References 130 publications

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“…A complete understanding of the potential CREs within a particular species would require profiling of chromatin accessibility and/or chromatin interactions in a wide variety of tissues, cell types and conditions. Although chromatin accessibility, histone modifications and chromatin interactions often show substantial variation in different tissues (12,14,21) the majority of DNA methylation patterns are quite stable in plant species especially during vegetative development (22)(23)(24) and in the face of environmental stress (25)(26)(27)(28) . There are well-characterized examples of specific changes in DNA methylation in endosperm tissues (29,30) as well as in specific cell types in plant gametophytes (31)(32)(33)(34)(35) .…”

Section: Introductionmentioning

confidence: 99%

Stable unmethylated DNA demarcates expressed genes and their cis-regulatory space in plant genomes

Crisp

Marand

Noshay

et al. 2020

Preprint

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The genomic sequences of crops continue to be produced at a frenetic pace. However, it remains challenging to develop complete annotations of functional genes and regulatory elements in these genomes. Here, we explore the potential to use DNA methylation profiles to develop more complete annotations. Using leaf tissue in maize, we define ∼100,000 unmethylated regions (UMRs) that account for 5.8% of the genome; 33,375 UMRs are found greater than 2 kilobase pairs from genes. UMRs are highly stable in multiple vegetative tissues and they capture the vast majority of accessible chromatin regions from leaf tissue. However, many UMRs are not accessible in leaf (leaf-iUMRs) and these represent a set of genomic regions with potential to become accessible in specific cell types or developmental stages. Leaf-iUMRs often occur near genes that are expressed in other tissues and are enriched for transcription factor (TF) binding sites of TFs that are also not expressed in leaf tissue. The leaf-iUMRs exhibit unique chromatin modification patterns and are enriched for chromatin interactions with nearby genes. The total UMRs space in four additional monocots ranges from 80-120 megabases, which is remarkably similar considering the range in genome size of 271 megabases to 4.8 gigabases. In summary, based on the profile from a single tissue, DNA methylation signatures pinpoint both accessible regions and regions poised to become accessible or expressed in other tissues. UMRs provide powerful filters to distill large genomes down to the small fraction of putative functional genes and regulatory elements.Significance StatementCrop genomes can be very large with many repetitive elements and pseudogenes. Distilling a genome down to the relatively small fraction of regions that are functionally valuable for trait variation can be like looking for needles in a haystack. The unmethylated regions in a genome are highly stable during vegetative development and can reveal the locations of potentially expressed genes or cis-regulatory elements. This approach provides a framework towards complete annotation of genes and discovery of cis-regulatory elements using methylation profiles from only a single tissue.

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Section: Introductionmentioning

confidence: 99%

Stable unmethylated DNA demarcates expressed genes and their cis-regulatory space in plant genomes

Crisp

Marand

Noshay

et al. 2020

Preprint

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“…GUN4 stimulates chlorophyll biosynthesis 29 , while SIG6 is associated with the plastid-encoded prokaryotic-like RNA polymerase complex and promotes early chloroplast development in cotyledons 30 . Moreover, we included genes for proteins involved in other epigenetic processes like histone (de) methylation, chromatin remodeling, and small RNA biogenesis 31 . In dry seeds, mRNA expression levels were generally low with the exception of a few genes, including DRM1, whose protein product is responsible for the maintenance of CHH methylation (see Supplementary Table S1 online).…”

Section: Resultsmentioning

confidence: 99%

Chloroplast development and genomes uncoupled signaling are independent of the RNA-directed DNA methylation pathway

Wang

Leister

Kleine

2020

Sci Rep

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The Arabidopsis genome is methylated in CG and non-CG (CHG, and CHH in which H stands for A, T, or C) sequence contexts. DNA methylation has been suggested to be critical for seed development, and CHH methylation patterns change during stratification and germination. In plants, CHH methylation occurs mainly through the RNA-directed DNA methylation (RdDM) pathway. To test for an involvement of the RdDM pathway in chloroplast development, we analyzed seedling greening and the maximum quantum yield of photosystem II (Fv/Fm) in Arabidopsis thaliana seedlings perturbed in components of that pathway. Neither seedling greening nor Fv/Fm in seedlings and adult plants were affected in this comprehensive set of mutants, indicating that alterations in the RdDM pathway do not affect chloroplast development. Application of inhibitors like lincomycin or norflurazon inhibits greening of seedlings and represses the expression of photosynthesis-related genes including LIGHT HARVESTING CHLOROPHYLL A/B BINDING PROTEIN1.2 (LHCB1.2) in the nucleus. Our results indicate that the LHCB1.2 promoter is poorly methylated under both control conditions and after inhibitor treatment. Therefore no correlation between LHCB1.2 mRNA transcription and methylation changes of the LHCB1.2 promoter could be established. Moreover, we conclude that perturbations in the RdDM pathway do not interfere with gun signaling.

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“…To investigate whether a perturbed methylome would impair priming to recurring EL we repeated the WLRS time-course experiment (Ganguly et al 2018) on WT, ddc3, rdd, and strs2 ( Figure 3). The week of recurring EL led to the expected morphological differences across all genotypes, namely increased rosette compaction but consistent leaf area (Figure 3 A-B).…”

Section: Excess Light Priming Evident Despite Aberrant Methylome Pattmentioning

confidence: 99%

“…Plants were watered every 2-3 days depending on soil moisture, avoiding pooling of water to prevent algal and fungal growth. Each of three daily EL treatments consisted of 60 minutes of 1000 μ mol photons m -2 s -1 using a mixture of metal halide and high-pressure sodium lamps as previously described (Crisp et al 2017;Ganguly et al 2018).…”

Section: Plant Growth and Germplasmmentioning

confidence: 99%

“…Monitoring PSII performance using chlorophyll fluorescence measurements PSII photochemistry was probed in vivo using measures of chlorophyll fluorescence (Baker 2008) using a PSI FluorCam (Photon System Instruments; Brno, Czech Republic). Measures were taken between 11:00-14:00 across the adaxial side of 30 minute dark adapted rosettes as performed previously (Ganguly et al 2018). In this study, intermittent measures of chlorophyll fluorescence, specifically F t , F m , and F m ′ , were taken after a saturating pulse (3000 µ mol photons m -2 sec -1 ) across 10-minutes in actinic light (700 μ mol photons m -2 sec -1 ) followed by a 4-minute dark period (https://goo.gl/RuYDE2).…”

Section: High-throughput Phenotypingmentioning

confidence: 99%

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Excess light priming in Arabidopsis thaliana genotypes with altered DNA methylomes

Ganguly

Stone

Bowerman

et al. 2018

Preprint

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Author contributions: DRG, BABS, SRE, and BJP conceived and designed the study; DRG, BABS, and AFB designed experiments; BABS performed the experimental work with guidance from DRG and AFB; DRG and BABS performed data analyses with guidance from SRE and AFB; DRG and BABS drafted the manuscript; all authors commented on and edited the manuscript.One sentence summary: Photoprotection and priming against recurring excess light is functional despite impaired maintenance of the DNA methylome. Short title: Excess light priming in Arabidopsis DNA methylation mutantsAbstract Plants must continuously react to the ever-fluctuating nature of their environment. Repeated exposure to stressful conditions can lead to priming, whereby prior encounters heighten a plant's ability to respond to future events. A clear example of priming is provided by the model plant Arabidopsis thaliana (Arabidopsis), in which photosynthetic and photoprotective responses are enhanced following recurring light stress. While there are various post-translational mechanisms underpinning photoprotection, an unresolved question is the relative importance of transcriptional changes towards stress priming and, consequently, the potential contribution from DNA methylation -a heritable chemical modification of DNA capable of influencing gene expression. Here, we systematically investigate the potential molecular underpinnings of physiological priming against recurring excess-light (EL), specifically DNA methylation and transcriptional regulation: the latter having not been examined with respect to EL priming. The capacity for physiological priming of photosynthetic and photoprotective parameters following a recurring EL treatment was not impaired in Arabidopsis mutants with perturbed establishment, maintenance, or removal of DNA methylation. Importantly, no differences in development or basal photoprotective capacity were identified in the mutants that may confound the above result. Little evidence for a causal transcriptional component of physiological priming was identified; in fact, most alterations in primed plants presented as a transcriptional 'dampening' in response to an additional EL exposure, likely a consequence of physiological priming. However, a set of transcripts uniquely regulated in primed plants provide preliminary evidence for a novel transcriptional component of recurring EL priming, independent of physiological changes. Thus, we propose that physiological priming of recurring EL in Arabidopsis occurs independently of DNA methylation; and that the majority of the associated transcriptional alterations are a consequence, not cause, of this physiological priming.

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Maintenance of pre‐existing DNA methylation states through recurring excess‐light stress

Cited by 34 publications

References 130 publications

Stable unmethylated DNA demarcates expressed genes and their cis-regulatory space in plant genomes

Stable unmethylated DNA demarcates expressed genes and their cis-regulatory space in plant genomes

Chloroplast development and genomes uncoupled signaling are independent of the RNA-directed DNA methylation pathway

Excess light priming in Arabidopsis thaliana genotypes with altered DNA methylomes

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