The Plant Cell, March 2013, American Society of Plant Biologists. All rights reserved.
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1 Epigenetics (TTPB4) Teaching Guide Overview Epigenetic modifications of DNA and chromatin affect the activity of genes and transposons. Epigenetic controls affect processes as diverse as time-of-flowering, parent-oforigin effects (imprinting), paramutation and transposon silencing. Whole-genome studies of epigenetic marks have revealed that they are unexpectedly pervasive, as well as the critical role of small interfering RNAs in maintaining epigenetic states. This lecture has an accompanying slide set (Methods for epigenetic analyses) describing the methods used for analyses of epigenetic genome modifications. The additional slides describe bisulfite sequencing, chromatin immunoprecipitation, DNA adenine methylation (DamID), and conventional and next-generation methods used in epigenetic studies. Learning Objectives By the end of this lecture the student should be able to: Define the meaning of epigenetics Give an example of an epigenetically controlled process Describe the two common types of epigenetic marks Interpret the histone code Describe the epigenetic control of flowering in Arabidopsis Define imprinting and give an example of it Study / exam questions (understanding and comprehension). What does epigenetics mean, literally and practically? What are the two major types of epigenetic marks? What is the full meaning of the term H3K27me3? Explain how cytosine methylation at a CG position is maintained during DNA replication True or False: Expression of the FLC gene is off in the autumn but switched on during vernalization, to promote flowering in the spring. Why is a zygote produced with two maternal nuclei or two paternal nuclei unviable? Draw the reproductive cycle of an angiosperm, labelling the sporophyte, megegametophyte and microgametophyte. In which parts of the cycle are cells diploid? Haploid? What is a reciprocal cross? Draw the genotypes and phenotypes of a reciprocal cross in which one of the two parents carries a loss-of-function medea allele. What is an epiallele? Two epialleles of the maize b1 locus are B-1 and B. What is the phenotype of plants homozygous for B-1 and B, and a heterozygote with both alleles? What is the genotype of the heterozygote?
2 Discussion Questions (engagement and connections) What experiment can you do that would differentiate between a GA-biosynthesis mutant and GA- response mutant? Look at figure 3b from Sung and Amasino (2004) (Nature 427: ; shown in slide 68). Which probes (P1, V1, and U1) give information that indicates the gene is epigenetically modified? Describe how the banding pattern supports your conclusion. Looking at slides 71 73, how would you expect the lhp1 plant to respond to vernalization? Find the paper that describes this mutant to see if your guess is correct (Sung, S., et al (2006) Nature Genetics 38: ) Parental imprinting is as important for humans as it is for plants. Several genetic disorders associated with imprinting have been identified; the first two identified are Prader-Willi syndrome and Angelman syndrome. Look up these syndromes and determine their genetic basis. How are they related to each other? How are genes silenced in trans? Looking at slides 108 and 109, suggest two reasons why plants and animals reset their epigenome every generation. In what other ways do epigenetic programs participate in plant responses? Find a paper that demonstrates epigenetic controls of a different plant process. Some have argued that epigenetic changes support the ideas of Lamarck. Lamarck suggested that changes to an organism over time could be passed along to its progeny; the familiar story is that a giraffe might extend its neck through its lifetime reaching for high leaves, and then pass the elongated neck trait to its progeny. What is the evidence for transgenerational epigenetic effects in plants and animals? Do you think that a case can be made for Lamarck s ideas? Do you think the different reproductive strategies used by plants and animals makes one more likely than the other to pass along epigenetic information? (Here is an excellent review of this topic: Hauser, M.-T., et al. (2011). Transgenerational epigenetic inheritance in plants. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms. 1809: doi: /j.bbagrm )
3 Lecture synopsis Introduction (1 7) Epigenetics literally means above, or on top of genetics. Epigenetics historically has referred to events that affect the expression of the genetic program, such as the interplay between the environment and the genome. Modern usage of epigenetics usually refers to information coded beyond the DNA sequence, particularly covalent modifications to the DNA, or modifications to the chromatin structure, e.g. histone modifications. In practical terms, epigenetic marks change the way an organisms genes are expressed, without affecting the genome sequence. By definition these marks are maintained at least through mitosis, but sometimes through meiosis too. Familiar examples of epigenetics include the inactivation of an X-chromosome in a mammalian female, made visible for example in fur color of cats. Epigenetic programs also silence transposons and maintain centromere function. In plants the most familiar example is in the epigenetic control of flowering time. Epigenetic marks and their maintenance (8 39) Eukaryotic DNA is packaged in nucleosomes. Each nucleosome includes ~147 base pairs of DNA, and a histone octamer, which is made up of two copies each of four histone proteins (H2A, H2B, H3 and H4). The density of nucleosomal packaging is variable. Very densely packaged nucleosomes are found near the centromere of the chromosome and referred to as heterochromatin. Less densely packaged nucleosomes are called euchromatin, and include the actively transcribed genes. Nucleosome packaging and gene expression levels are affected by DNA histone modifications. DNA methylation (13 21) DNA methylation refers to the formation of 5-methycytosine from cytosine, by the action of the enzymes DNA methyltransferase. Arabidopsis has four DNA methylases: MET1, CMT3 and DRM1 and DRM2. MET1 methylates cytosines that are immediately 5 to guanines (gl.g. CG sites), and primarily is involved in silencing of transposons and repetitive elements and some imprinted genes. CMT3 methylates at CHG sites (where H is A, C or T), and this form of methylation feeds into histone modifications. DRM1 and DRM2 methylate so-called asymmetric sites (CHH), primarily at repetitive elements; these enzymes require the participation of small RNAs. CG methylation and CHG methylation can be propagated during DNA replication, by copying the information from the template strand onto the newly synthesized strand. By contrast, during DNA replication the CHH methylation information is not present on one template strand, which is why additional information is needed to maintain them. Mutants are available in each of these methylases, allowing their individual functions to be identified. Histone modification (22 39) The amino terminal tails of the histone proteins hang out from the nucleosome and are accessible to modification by histone modifying enzymes. There are many kinds of histone modifications, including acetylation, phosphorylation and methylation. Histone H3 is frequently modified and the kinds and positions of modifications affect how accessible the DNA is for transcription. Antibodies are available that very specifically recognize specific histone modifications, and can be used to query the positions of them. Some modifications are closely associated with transposons, and others with genes. H3K27me3 is a modification of histone H3, which is a trimethylation (me3) of the lysine (K) at position 27. H3K27me3 is associated with silenced genes. This histone modification is conferred by a protein complex
4 called PRC2 (the name derives from Drosophila genetics and stands for polycomb repressive complex 2; the components of this complex were also identified through genetic studies in Drosophila). Arabidopsis has more than one of each PRC2 subunit, which form different variations of the PRC2 complex that target different subsets of genes. The marks made by PRC2 in animals are maintained by another complex, PRC1. In plants, a similar complex is called PRC1-Like, which includes the protein LHP1. Histone modifications include the insertion of variant histones, including H2A.Z and CENH3. Epigenetic controls in whole-plant processes (40 116) Transposons (41 57) Transposons are mobile genetic elements and can account for more than 50% of genomic DNA content. Epigenetic controls contribute to transposon silencing. Mutation of DNA methylases causes repressive marks to be lost and allows transposons to transpose, leading to an accumulation of mutations. Histone modifications also help to silence transposons, and small interfering RNAs are involved in this process as well. Epigenetic control of flowering time (58 75) The control of flowering time in Arabidopsis has provided an excellent system through which to study epigenetic controls of plant processes. Flowering in promoted by the expression of the FT gene, which is an activator of flowering. FLC is a protein that represses transcription of FT, so when FLC is present plants don t flower. Cold temperatures, such as those experienced by a plant during wintertime, switch off expression of the FLC gene, and the silenced state is stable even after the temperature warm up again. This process, called vernalization, keeps plants in a vegetative state (with FLC expressed) during autumn, but then shuts off FLC in the winter so that they can flower in the spring. Analysis of the epigenetic marks shows that FLC is epigenetically silenced during vernalization. This system lends itself to genetic analysis, for example by screening for mutants that do not require vernalization, or that do not respond to vernalization, or that do not maintain FLC in a silenced state after temperatures warm up. Genomic imprinting (78 92) A small number of genes are inherited in a different epigenetic state from their mother or their father. (Several of these genes are known to be active during embryonic development, which has led to a hypothesis that the mediate a parental conflict ). Genomic nonequivalency can be demonstrating by introducing two maternal or two paternal nuclei into an enucleated fertilized cell, but also through a reciprocal cross. The MEDEA gene is imprinted in angiosperms and the parental copy is silent. Therefore, the phenotypes of the progeny are solely determined by the maternal alleles. A maternal plant carrying a single loss-of-function allele gives rise to 50% dead progeny, no matter what the parental genotype. MEDEA encodes a component of PRC2 and regulates its own imprinting. Silencing in trans: silencing of FWA and paramutation (93 107) The FWA gene is also imprinted and silenced in vegetative tissues by DNA methylation. Studies of FWA revealed a surprising result: a non-methylated, expressed FWA allele introduced by Agrobacterium-mediated transformation becomes silenced in the presence of a silent FWA, indicating that the two alleles interact. Genetic studies revealed small interfering RNAs are necessary for trans-silencing. This mechanism also seems to underlie an process known as paramutation. This phenomenon has been recognized for a long time from studies of anthocyanin production in maize. The b1 locus has a wild-type allele, B-1,
5 that is transcribed at high levels conferring a purple color to the plants. The B epiallele is silent, and can silence B-1 in trans, through a mechanism that requires an RNA-dependent RNA polymerase. Resetting the epigenome ( ) We ve seen that vernalization silences FLC to permit flowering, but what happens in the next generation? How is FLC reset to an active allele for the next generation? Similarly, imprinted genes in mammals must be reset every generation. We know in mammals that the process of gametogenesis resets the genome, and it looks like something similar happens in plants. Many silent loci are highly expressed in certain reproductive tissues, including the endosperm and the vegetative cell of the male gametophyte. Perhaps expression of silenced genes in these non-proliferative tissues is a mechanism by which sirnas are produced to reset them in the silenced state. Epigenetic methods We have included an extra set of slides to describe some of the methods used in epigenetic research. Method to investigate DNA methylation - bisulfite sequencing (2 4) DNA methylation directly modifies the DNA, so can be addressed through a modified form of DNA sequencing. Unmethylated cytosine residues are susceptible to conversion to uracil upon treatment with bisulfite, but methylcytosine resists modification. Two DNA samples, one bisulfite treated and one untreated, can be sequenced. All of the cytosines in the untreated sample will be cytosines, but in the modified samples only the methylated cytosines are read as cytosines, the unmethylated ones are read as thymines. Thus, this method allows a very precise determination of DNA methylation within a sample. Methods to investigate histone modification (5-9) Histone modifications do not directly alter the DNA, but it is necessary to somehow link the DNA to the histones being examined to know where the lie within the genome. This is accomplished by a chemical cross-linking that attaches the DNA to the nucleosome. The DNA is sheared to smaller sizes, and then very specific antibodies that recognize modified histones are used to isolate the histone with its associated DNA. After washing, the sequence of the DNA associated with different histone modifications can be asses through standard methods. An alternative method involves fusing a chromatin-binding protein to a methyltransferase, which modifies the DNA in the region close to the protein binding site. DNA modifications can be identified by restriction enzymes sensitive to DNA modifications. Methods to investigate sirnas next-generation sequencing methods (10-26) Advances in DNA sequencing are changing the way we do biology. Healthy competition between platforms has made the pace of innovation rapid and driven the cost of sequencing down, meaning that it is very feasible to sequence genomes, transcriptomes and epigenomes. Combining inexpensive and rapid sequencing methods with bisulfite methods or immunoprectiption methods means that the epigenetic state of every gene in a genome can be assessed between tissues or conditions. These slides demonstrate some of the principles behind next-generation sequencing methods. The major change from old-style sequencing is that the sequencing reactions occur massively in parallel. (You can find a large collection of excellent videos and resources at the YouTube channel of the National Human Genome Research Institute).
6 Slide Concepts: 1 Title 2-3 What does epigenetics mean? On top of genetics; refers to the effects of DNA and chromatin modifications that affect gene expression levels 4 X chromosome inactivation in mammals is an example of epigenetic silencing 5 Epigenetic programs silence transposons and help maintain centromere function 6 Epigenetic programming in plants helps control developmental transitions 8-29 Epigenetic marks and their maintenance 9 Eukaryotic DNA is packaged in nucleosomes Chromatin consists of heterochromatin and euchromatin 12 Epigenetic modifications affect chromatin structure DNA methylation 14 Arabidopsis has three DNA methyltransferases 15 CG methylation can be propagated during DNA replication Asymmetric sites (e.g., CHH) require additional information, sometimes in the form of small interfering RNAs Different DNA methylases act on different sites and different regions of the genome Heterochromatin DNA is highly methylated Histone Modifications 22 The amino terminal regions of histone proteins are accessible for modification The histone code is a shorthand way to indicate which position of which histone is modified in which way Different histone modifications affect chromatin structure and gene expression levels differently; some are associated with actively expressed genes, and others with silent regions of DNA H3K27me3 is found in euchromatin associated with silenced genes. It is produced by polychrome repressor protein 2 (PRC2). Arabidopsis has different forms of PRC2 subunits that are involved in regulating genes and processes LHP1 is a component of a PRC1 complex that maintains H3K27me3-modified genes in a silenced state Another modification is the substitution of histone variants into the nucleosome. Examples are H2A.Z, H3.1, H3.3 and CENH3. 39 Epigenetic marks summary DNA methylation and histone modifications and variants are ways that genes are regulated epigenetically Epigenetic controls in whole-plant processes Epigenetic silencing of transposons Transposons are mobile genetic elements that can be very abundant in genomes, can induce mutations by moving into genes, and can be active or inactive Epigenetic controls maintain transposons in silent states. Disrupting the epigenetic machinery (e.g., by mutating DNA methylases) can release the transposons and lead to mutations Small interfering RNAs recruit DNA methylases and histonemodifying enzymes to targets to maintain epigenetic silencing
7 58 - Epigenetic regulation of endogenous genes and developmental 116 processes Epigenetic control of flowering time Arabidopsis can be made competent to flower by winter cold temperatures (vernalization), a process that involves epigenetic change FLC represses FT, an activator of flowering. As FLC is an inhibitor of flowering, loss-of-function flc mutants flower prematurely FLC is silenced by vernalization, and the silenced state is conferred by epigenetic changes. Probes from different regions of the FLC gene show a decrease in activating marks and an increase in silencing marks during the vernalization period VIN3 is induced during vernalization and necessary to silence FLC Long noncoding RNAs also contribute to FLC regulation LHP1 is necessary to maintain the silenced state after the vernalization period is over (also see slides 34 37) 75 Summary epigenetic control of flowering Many developmental genes and stress responsive genes are epigenetically regulated Genomic imprinting some genes are inherited in different epigenetic states from the maternal and paternal parents Genomic non-equivalency can be demonstrated by nuclear transplant experiments a zygote needs a maternal and paternal genome for viability Review of angiosperm reproduction, including multicellular gametophytes and double fertilization The parental allele of the Arabidopsis MEDEA gene is silent; results from reciprocal crosses show the parent-of-origin effect MEDEA encodes a component of PRC2 and regulates its own imprinting 93 - Silencing in trans: FWA FWA is an imprinted gene that is normally silent in vegetative tissues. Introducing an active allele of FWA gives the surprising result that it becomes silenced, but only in plants carrying a wildtype, silenced FWA allele A tandem repeat upstream of FWA promotes sirna production, and is necessary for silencing in cis and in trans, through sirna Silencing in trans: paramutation. Paramutation is another example of silencing in trans. The silenced, B allele of the b1 locus is paramutagenic and can silence the active, wild-type B-1 allele in trans. Resetting the epigenome In animals and plants, reproduction provides opportunities to reset the epigenome. The endosperm and the pollen vegetative cell are both hypomethylated as compared to other tissues. Transposons are activated in pollen. The activation of silenced genes can activate RNA-mediated DNA methylation pathways Summary
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