Cells react to changes in their environment by altering gene expression, primarily by regulating transcription of inducible genes. The rate of induction of such genes is a product of enhancer and promoter activity (Vo Ngoc et al., 2017) but can also be influenced by the previous experiences of the cells. A number of genes from yeast, flies, worms, mammals, and plants are more strongly induced following a previous exposure to a stimulus, and this primed state can persist for 4–14 mitotic cell divisions (Brickner et al., 2007; D’Urso et al., 2016; Gialitakis et al., 2010; Lämke and Bäurle, 2017; Light et al., 2013; Light et al., 2010; Maxwell et al., 2014; Pascual-Garcia et al., 2017; Siwek et al., 2020; Sood and Brickner, 2017). Because only a subset of genes induced under a particular condition exhibits memory (Light et al., 2013), this can also result in a qualitative change in the global expression pattern.

Although transcriptional memory in different organisms or for different genes has unique features, several common, conserved mechanisms have been identified. For example, in budding yeast, flies, and mammals, transcriptional memory requires the nuclear pore protein Nup98 (homologous to Nup100 in yeast). This protein physically interacts with the promoters of genes that exhibit memory and loss of Nup98/Nup100 disrupts memory (Light et al., 2013; Light et al., 2010; Pascual-Garcia et al., 2017). The interaction with Nup98 with chromatin in flies and mammals can occur away from the nuclear pore complex (NPC; Capelson et al., 2010; Kalverda et al., 2010). However, during memory, the interaction of promoters with Nup98/Nup100 in both yeast and flies occurs at the pore.

Transcriptional memory is also associated with local changes in chromatin modifications and chromosome folding. In Drosophila, memory induced by ecdysone involves a long-distance promoter-enhancer interaction that is strengthened/stabilized by Nup98 (Pascual-Garcia et al., 2017). In yeast, plants, and human cells, histone modifications of the promoter are required for memory: histone H3 lysine 4 dimethylation(H3K4me2) is generally associated with memory in yeast and humans (D’Urso et al., 2016; Gialitakis et al., 2010; Light et al., 2013; Light et al., 2010), while in plants, several forms of epigenetic memory are associated with either H3K4me2 or H3K4me3 (Lämke and Bäurle, 2017). In flies and mammals, Nup98 physically interacts with the H3K4 methyltransferases Trx and Set1A/COMPASS, respectively (Franks et al., 2017; Pascual-Garcia et al., 2014). Nup98/Nup100 is required for memory-associated H3K4me2 in yeast and mammals, and conditional inactivation of either COMPASS (the methyltransferase) or SET3C (a histone deacetylase complex that binds H3K4me2; Kim and Buratowski, 2009) leads to rapid loss of memory in yeast (D’Urso et al., 2016; Light et al., 2013; Light et al., 2010). Likewise, substitution of alanine or arginine for lysine 4 on histone H3 (H3 K4R or K4A) disrupts INO1 transcriptional memory (D’Urso et al., 2016). Importantly, the H3K4me2 during memory in yeast is carried out by a form of COMPASS that lacks the Spp1 subunit (Spp1^- COMPASS), preventing trimethylation (D’Urso et al., 2016).

Finally, transcriptional memory in yeast and mammals leads to binding of a poised RNA polymerase II (RNAPII) pre-initiation complex (PIC; D’Urso et al., 2016; Light et al., 2013; Light et al., 2010). A similar phenomenon, called RNAPII ‘docking,’ has been reported in Caenorhabditis elegans (Maxwell et al., 2014). Work from yeast suggests that this poised RNAPII PIC is distinct from active RNAPII PIC in two ways. First, it fails to recruit Cdk7 (Kin28 in budding yeast), the kinase that phosphorylates serine 5 on the RNAPII carboxy terminal domain upon initiation (D’Urso et al., 2016). Second, it remains associated with Mediator kinase Cdk8 (Ssn3 in budding yeast; D’Urso et al., 2016). Cdk8 is also associated with poised promoters in HeLa cells (D’Urso et al., 2016) and has been found to regulate initiation (Akoulitchev et al., 2000; Pavri et al., 2005), suggesting that it plays a conserved role in transcriptional poising. Conditional depletion of yeast Ssn3 from the nucleus leads to loss RNAPII binding from the INO1 promoter during memory and a defect in the rate of INO1 reactivation (D’Urso et al., 2016). Therefore, transcriptional memory is a conserved phenomenon that may involve a conserved core mechanism.

The highly inducible budding yeast gene INO1 has served as a model for epigenetic transcriptional memory. INO1 is an essential enzyme that catalyzes the conversion of glucose to myo-inositol for the biosynthesis of phosphatidylinositol. Our current understanding of INO1 memory is summarized in Figure 1A. Repressed INO1 localizes in the nucleoplasm. Upon activation, the gene repositions to the nuclear periphery through interaction with the NPC (Ahmed et al., 2010; Brickner and Walter, 2004; Sumner et al., 2021). Interaction of active INO1 with the NPC requires two transcription factors, Put3 and Cbf1, that bind to the upstream DNA zip codes GRSI and GRSII (Figure 1A; Ahmed et al., 2010; Brickner and Walter, 2004; Randise-Hinchliff et al., 2016). Upon repression, recently repressed INO1 acquires memory-specific chromatin marks, poised RNAPII PIC, and associates with the NPC by another mechanism (Brickner et al., 2007; Light et al., 2013; Light et al., 2010). Whereas nucleosomes in the promoter and 5’ end of active INO1 are hyper-acetylated and show both H3K4me2 and H3K4me3; the nucleosomes at the 5’ end of recently repressed INO1 are hypo-acetylated and show only H3K4me2 (D’Urso et al., 2016; Light et al., 2013). Also, the histone variant H2A.Z is incorporated into an upstream nucleosome during INO1 memory (Brickner et al., 2007; Light et al., 2010). The interaction with the NPC requires the Sfl1 transcription factor, the memory recruitment sequence (MRS) DNA zip code to which Sfl1 binds, and the nuclear pore protein Nup100 (D’Urso et al., 2016; Light et al., 2013; Light et al., 2010). Loss of Nup100 or Sfl1, or mutations in the MRS, disrupt INO1 localization to the nuclear periphery, cause loss of H3K4me2, H2A.Z and RNAPII binding, and slow the rate of reactivation of INO1 without affecting repression or activation. INO1 memory, as monitored by gene positioning, histone modification or RNAPII binding, is both maintained in mother cells and inherited to daughter cells through up to four mitotic divisions before being lost (Brickner et al., 2007; D’Urso et al., 2016; Light et al., 2010).

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Here we exploited our knowledge of INO1 transcriptional memory to address four critical questions. First, although transcription rates are impacted by memory, how it impacts fitness has not been generally assessed. We find that inositol memory provides a competitive fitness advantage during inositol starvation that is Nup100-, Cdk8-, and H3K4me2-dependent. Second, we assessed the function of H3K4me2 during memory. Sfl1 is required for H3K4 dimethylation, and H3K4me2 is essential for both Sfl1 binding and for RNAPII recruitment during INO1 memory, suggesting that memory involves a chromatin-dependent positive feedback loop. Third, we define ways in which the dimethylation of H3K4 during transcription is different from dimethylation of H3K4 during memory. While transcription-associated H3K4 methylation is RNAPII-dependent, memory-associated H3K4me2 is RNAPII-independent and requires both overlapping and distinct factors. Finally, we explore the molecular mechanism of epigenetic inheritance of INO1 memory. We rule out that protein production during inositol starvation promotes memory and instead highlight the critical role of heritable H3K4me2. Although establishing H3K4me2 during memory requires Sfl1, once established, H3K4me2 is maintained and inherited through ~4 cell divisions in the absence of Sfl1. A putative reader of H3K4me2 (SET3C) that is essential for this inheritance physically interacts with the writer of H3K4me2 (COMPASS), suggesting a molecular mechanism by which H3K4me2 is inherited during DNA replication. This work provides a compelling example of a heritable histone modification that stimulates future transcription and is inherited over a shorter timescale than other heritable histone modifications like H3K9 or H3K27 methylation.

Epigenetic phenomena result in heritable changes in phenotype without changes in DNA sequence (Nanney, 1958; Waddington, 2012). The classic examples are stable states, metastable states, or regulated switches in state. Stable states include transcriptionally silent subtelomeric, pericentromeric regions, or mating type loci (Gartenberg and Smith, 2016; Holoch and Moazed, 2015; Zofall and Grewal, 2006). Metastable states include colony morphology switching in microbes (Klar et al., 2001; Slutsky et al., 1987) and position effect variegation in animals (Elgin and Reuter, 2013). Stable switching of transcriptional states occurs during development, such as silencing of the mammalian X chromosome or establishment of the gene expression programs required for differentiation (Campos et al., 2014; Galupa and Heard, 2018; Gibney and Nolan, 2010; Tee and Reinberg, 2014). Such phenomena often require histone modifications, sometimes called epigenetic marks. However, histone modifications are generally regulated by sequence-specific DNA binding proteins that interact with cis-acting, genetically encoded DNA elements (Holoch et al., 2021; Holoch and Moazed, 2015; Laprell et al., 2017). Thus, signal transduction that alters the activity of a TF can produce a heritable change in phenotype that requires histone modifications without the histone modification itself being heritable. Unlike DNA methylation, in which the methyl marks retained on one strand after replication serve to stimulate methylation of the other (Edwards et al., 2017; Hermann et al., 2004), histone/nucleosome modifications are not necessarily re-incorporated at the same location after DNA replication (Escobar et al., 2021; Wang et al., 2009). However, both H3K9 methylation (constitutive heterochromatin; Ragunathan et al., 2015; Zhang et al., 2008) and H3K27 methylation (facultative heterochromatin; Coleman and Struhl, 2017; Hansen and Helin, 2009; Hansen et al., 2008; Margueron et al., 2009) can be inherited through mitosis following removal of the initiating factors (albeit not as stably as with those factors). Furthermore, elegant proximity labeling studies show that nucleosomes at certain silent loci are re-incorporated locally after DNA replication (Escobar et al., 2019). Thus, mitotic inheritance requires both the local reincorporation of marked nucleosomes and reinforcement of these modifications through covalent modification of unmarked nucleosomes following DNA replication. The histone marks for which there is the clearest data for heritability share several features: (1) they tend to occur over large regions, encompassing many nucleosomes, (2) they are associated with transcriptional repression, and (3) inheritance requires an interaction between a writer and a reader that recruits or stimulates the writer.

Here we find that H3K4 dimethylation of nucleosomes over the same location in the genome can either be stable and heritable or unstable and rapidly removed, depending on the mechanism by which it is deposited. During active transcription, nucleosomes in the INO1 promoter are marked with histone acetylation (D’Urso et al., 2016; Rundlett et al., 1998), H3K4me3, and H3K4me2 (Santos-Rosa et al., 2002). This H3K4 methylation is catalyzed by COMPASS and requires RNAPII and the preinitiation complex (Figure 4C; D’Urso et al., 2016). In mutants that lack memory, these marks are rapidly removed upon transcriptional repression (Figure 6—figure supplement 1; D’Urso et al., 2016). In contrast, during memory, histone acetylation and H3K4me3 are lost and H3K4me2 is deposited (Figure 6C; D’Urso et al., 2016). This mechanism of H3K4 dimethylation during memory is mechanistically distinct from that observed during transcription: it is catalyzed by Spp1^- COMPASS, does not require RNAPII and requires SET3C, Leo1, Sfl1, and Nup100 (D’Urso et al., 2016; Light et al., 2013). Critically, once established, H3K4me2 is both stable and inherited for ~4 cell divisions following degradation of Sfl1 (Figure 6). This is distinct from the effects of inactivating COMPASS or SET3C (Figures 4 and 6; D’Urso et al., 2016). Therefore, H3K4me2 can be maintained and inherited in the absence of an essential initiating factor but continuously requires the writer and reader. We conclude that, as with histone marks associated with heterochromatin (Reinberg and Vales, 2018), a histone mark associated with transcriptional poising is epigenetically inherited.

How is heritable H3K4me2 distinguished from unstable H3K4me2? It is possible that the heritable signal comprises H3K4me2 and additional histone marks. Although the incorporation of H2A.Z during memory is an intriguing possibility for a second signal, it is not essential for H3K4 dimethylation (Light et al., 2013). Alternatively, unacetylated histones may stimulate heritable H3K4 dimethylation, perhaps by regulating the activity of Spp1^- COMPASS or the Paf complex via Leo1. This may explain why the SET3C histone deacetylase is the reader for this mark.

Whereas H3K9 methylation or H3K27 methylation is generally very stable and state switching promotes long-term or permanent switches, transcriptional memory persists for shorter timescales, generally between 4 and 14 mitotic divisions. This limited inheritance may reflect a balance between the fitness benefits of memory and its costs in a fluctuating environment. Regardless, our current understanding suggests that the duration of memory relates to limits on inheritance following each round of DNA replication. Whereas H3K9 methylation or H3K27 methylation generally covers tens to hundreds of thousands of base pairs (Barski et al., 2007; Cutter DiPiazza et al., 2021; Pauler et al., 2009; Yu et al., 2014), the chromatin changes associated with epigenetic transcriptional memory are more local, covering hundreds of base pairs (D’Urso et al., 2016). Following DNA replication, nucleosomes are randomly segregated into the two daughter molecules (Petryk et al., 2018; Yu et al., 2018). Approximately half of the nucleosomes should retain regulatory marks and the inheritance of those marks requires recognizing these nucleosomes and modifying adjacent, unmarked nucleosomes (Escobar et al., 2021; Loyola et al., 2006). If recognition and/or modification is imperfect, the efficiency of such an inheritance mechanism should increase with the number of nucleosomes (Cutter DiPiazza et al., 2021). If so, then the duration of memory could be limited by a combination of the number of modified nucleosomes, the fidelity, and efficiency of the reader-writer system and the regulation of the initiating transcription factors.

Our current model for INO1 transcriptional memory is shown in Figure 7. When active, INO1 interacts with the NPC through upstream DNA zip codes and the TFs Put3 and Cbf1. Two TFs essential for transcription, Ino2 and Ino4, bind to two UAS_INO elements that flank the MRS. These TFs recruit co-activators, including histone acetyltransferases like SAGA. Hms2 binds the MRS but has no known role in localization or transcription of active INO1. RNAPII recruits the Paf1C and COMPASS, leading to H3K4me3 (Figure 7A).

Figure 7

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Upon repression, the Opi1 repressor binds to Ino2 (Brickner and Walter, 2004; Heyken et al., 2005), repressing transcription by recruiting the Rpd3L histone deacetylase (Kadosh and Struhl, 1997; Randise-Hinchliff et al., 2016). To establish memory, Hms2 facilitates recruitment of Sfl1 to the MRS and Nup100-dependent interaction with the NPC (Figure 7). Because Nup98 physically interacts with the H3K4 methyltransferases Trithorax in flies (Pascual-Garcia et al., 2014) and MLL in mammals (Franks et al., 2017), we envision that Nup100 helps recruit Spp1^- COMPASS to dimethylate H3K4 and establish memory (Figure 7). To-date, we have not observed co-immunoprecipitation of Nup100 with COMPASS (not shown). However, it is possible that Sfl1, Hms2, or Nup100 compete with Spp1 for binding to COMPASS to ensure this switch. Alternatively, these proteins may recruit Paf1C and COMPASS through interaction with Leo1.

Importantly, the H3K4me2 mark is required for both Sfl1 binding and H2A.Z incorporation during memory, forming a positive feedback loop between interaction with the NPC and chromatin changes. Because the MRS at an ectopic site is sufficient to induce chromatin changes without recruiting RNAPII (Light et al., 2013) or Mediator (our unpublished results), cis-acting promoter elements presumably facilitate RNAPII recruitment. We hypothesize that Ino2/Ino4 collaborate with Sfl1/Hms2 to recruit Cdk8⁺ Mediator, which is essential for RNAPII poising (Figure 7). This would explain why loss of H3K4 methylation leads to loss of Sfl1 binding, peripheral localization, and RNAPII.

Following DNA replication, we proposed that inheritance requires methylation of unmodified H3K4 on nucleosomes near those that were previously modified (Figure 7; Moazed, 2011). This pathway would involve recognition of the H3K4me2 mark on reincorporated nucleosomes by SET3C, recruitment of Spp1^- COMPASS, and dimethylation of H3K4 on adjacent nucleosomes. Once the INO1 promoter nucleosomes are methylated, Sfl1/Hms2 can bind, mediating interaction with the NPC and re-establishing memory. Loss of Leo1 seems to both weaken the interaction between COMPASS and SET3C and to disrupt persistence/inheritance of INO1 memory, suggesting that it facilitates Spp1^- COMPASS recruitment after DNA replication.

Do all genes that exhibit transcriptional memory utilize the same molecular mechanism? No. Several of the molecules required for INO1 memory are not generally involved in memory, such as Sfl1 and Hms2 (our unpublished data). However, INO1 epigenetic memory has also identified factors and mechanisms that are implicated in memory more generally and suggest a core, conserved, epigenetic poising mechanism. For example, Nup100-dependent interaction with the NPC is associated with transcriptional memory of several yeast genes and Nup98 plays an essential role in both interferon gamma memory in HeLa cells (Light et al., 2010) and in ecdysone memory in flies (Gozalo et al., 2020; Pascual-Garcia et al., 2017). In yeast and mammals, memory leads to H3K4me2, RNAPII binding, and Cdk8 association (D’Urso et al., 2016; Light et al., 2013). Therefore, many genes from yeast to mammals employ a common transcriptional poising mechanism. What selects which genes exhibit memory? Many yeast TFs can mediate Nup100-dependent interaction with the NPC (Brickner et al., 2019). Therefore, different stimuli may induce memory through regulating the activity of these TFs to induce memory in different subsets of genes. Diverse, transient signals could be interpreted through TFs to alter future fitness in distinct ways for several generations.

The scripts used to analyze the competition experiments are available at https://github.com/jasonbrickner/SeqComp, (copy archived at swh:1:rev:3eb152971adc09d0b4559bb86e4ad036eebd4dc7).

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Author details

1. Bethany Sump

   Department of Molecular Biosciences, Northwestern University, Evanston, United States

   Contribution

   Conceptualization, Data curation, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

2. Donna G Brickner

   Department of Molecular Biosciences, Northwestern University, Evanston, United States

   Contribution

   Data curation, Formal analysis, Investigation

   Competing interests

   No competing interests declared

3. Agustina D'Urso

   Department of Molecular Biosciences, Northwestern University, Evanston, United States

   Present address

   Arcturus Therapeutics, San Diego, California, United States

   Contribution

   Conceptualization, Investigation

   Competing interests

   is affiliated with Arcturus Therapeutics. The author has no financial interests to declare

4. Seo Hyun Kim

   Department of Molecular Biosciences, Northwestern University, Evanston, United States

   Present address

   Virginia Tech Carilion School of Medicine, Roanoke, Virginia, United States

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

5. Jason H Brickner

   Department of Molecular Biosciences, Northwestern University, Evanston, United States

   Contribution

   Conceptualization, Formal analysis, Funding acquisition, Project administration, Supervision, Visualization, Writing - review and editing

   For correspondence

   j-brickner@northwestern.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8019-3743

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