Animals, fungi, and plants make use of two major epigenetic repressive modifications on histones that are destined to silence genes and transposable elements (TEs). The Polycomb repressive system applies the repressive trimethylation on lysine 27 of histone H3 (H3K27me3), which mainly serves to silence genes during defined stages of development (Mozgova and Hennig, 2015; Schuettengruber et al., 2017). In contrast, the repressive di- or trimethylation on lysine 9 of histone H3 (H3K9me2/3) is mainly associated with constitutively silenced heterochromatin, present in repeat-rich regions and TEs (Saksouk et al., 2015; Wendte and Schmitz, 2018). Repression mediated by the Polycomb system is transient and dynamically regulated, while repression mediated by H3K9me2/3 is generally stable during development (Mozgova and Hennig, 2015; Saksouk et al., 2015; Schuettengruber et al., 2017; Wendte and Schmitz, 2018). The establishment of H3K27me3 is mediated by the evolutionary conserved Polycomb repressive complex 2 (PRC2). In plants, there are distinct PRC2 complexes that are active during different stages of plant development (Mozgova and Hennig, 2015). In Arabidopsis, the EMBRYONIC FLOWER (EMF) and VERNALIZATION (VRN) PRC2 regulate sporophyte development, while the FERTILIZATION-INDEPENDENT SEED (FIS) PRC2 is active in the central cell of the female gametophyte and the descendent endosperm (Mozgova and Hennig, 2015). The establishment of H3K9me2 in Arabidopsis depends on the SU(VAR)3–9 homologous proteins (SUVHs), KRYPTONITE (or SUVH4), SUVH5 and SUVH6 that act in a feedback loop with CHG methylation (CHGm) established by the CHROMOMETHYLTRANSFERASE 3 (CMT3) (Kenchanmane Raju et al., 2019; Zhang et al., 2018). In animals and plants, H3K27me3 and H3K9me2 are generally exclusive repressive marks (Wiles and Selker, 2017); however, they co-occur in certain tissue types like the plant endosperm (Klosinska et al., 2016; Moreno-Romero et al., 2016; Weinhofer et al., 2010), as well as in specific organisms as filamentous fungi and bryophytes (Carlier et al., 2020; Montgomery et al., 2020). Furthermore, redistribution of H3K27me3 to heterochromatic regions occurs when constitutive heterochromatin is disrupted, indicating that specific features of heterochromatin prevent PRC2 recruitment (Deleris et al., 2012; Jamieson et al., 2016; Peters et al., 2003; Wiles and Selker, 2017).

Erasure of H3K27me3 and H3K9me2 is mediated by different types of JUMONJI lysine demethylases (KDMs) that belong to the KDM4 and KDM3 type, respectively (Cheng et al., 2020). RELATIVE OF EARLY FLOWERING 6 (REF6) and EARLY FLOWERING 6 (ELF6) function redundantly as major erasers of H3K27me3 during Arabidopsis development (Lu et al., 2011; Yan et al., 2018). The zinc-finger (ZnF) domains of REF6 recognize the sequence motif CTCTGYTY (Y = T or C) (Cui et al., 2016; Li et al., 2016). Binding of REF6 to this motif is negatively affected by non-CG methylation (Qiu et al., 2019), revealing cross-talk between different epigenetic modifications.

Seed development in flowering plants is initiated by a double fertilization event, where one of the sperm cells fertilizes the haploid egg, giving rise to the diploid embryo and the other sperm cell fertilizes the diploid central cell, initiating development of the triploid endosperm (Zhou and Dresselhaus, 2019). The endosperm regulates the transfer of nutrients to the developing embryo, similar as the placenta in mammals. (Costa et al., 2012; Lee et al., 2010; Linkies et al., 2009). The endosperm furthermore regulates seed dormancy, a process preventing germination of seeds under favourable conditions (Nonogaki, 2019). Both processes have been linked to genomic imprinting, an epigenetic phenomenon causing parent-of-origin specific gene expression (Batista and Kohler, 2020; Gehring and Satyaki, 2017; Piskurewicz et al., 2016). Imprinted genes are epigenetically modified during gametogenesis, establishing parental-specific expression patterns that are maintained after fertilization. Genomic imprinting leading to maternally biased expression is predominantly connected to DNA demethylation of maternal alleles mediated by the DNA glycosylase DEMETER (Gehring et al., 2009; Hsieh et al., 2011; Park et al., 2016). In contrast, paternally biased expression is predominantly connected to the presence of H3K27me3, H3K9me2, and CHGm on maternal alleles (Klosinska et al., 2016; Moreno-Romero et al., 2019; Moreno-Romero et al., 2016; Moreno-Romero et al., 2017). The FIS-PRC2 establishes H3K27me3 in the central cell, which is maintained on the maternal alleles after fertilization. Loss of FIS-PRC2 function impairs CHGm establishment, indicating that H3K27me3 is the primary imprinting mark and CHGm and H3K9me2 are recruited after H3K27me3 establishment (Moreno-Romero et al., 2019). The biological meaning of the co-occurance of H3K27me3, H3K9me2, and CHGm on the maternal alleles of paternally expressed genes (PEGs) is unclear. In this study, we reveal that genes marked by H3K27me3 on their maternal alleles are targeted by REF6 and become reactivated during germination. In contrast, REF6 fails to activate genes marked by H3K27me3, H3K9me2, and CHGm, consistent with the finding that DNA methylation prevents REF6 binding (Qiu et al., 2019). Among those genes with triple repressive marks was the ABA INSENSITIVE 3 (ABI3) gene, a known positive regulator of seed dormancy (Liu et al., 2013; Shu et al., 2016; Tian et al., 2020). Genes activated by REF6 are enriched for ethylene signaling, a process activated during germination. Consistently, loss of REF6 causes increased dormancy, as recently reported (Chen et al., 2020). Together, our study unveils a mechanism that employs the combination of different repressive epigenetic modifications to time a crucial developmental process.

In this study, we uncovered the molecular function and physiological role of the endosperm-specific triple modification of the maternal genome with H3K27me3/H3K9me2 and CHGm. We found that genes marked by only H3K27me3 became reactivated during seed germination, a process that depends on the H3K27me3 demethylase REF6. In contrast, genes marked by triple repressive modifications remained silenced during germination because REF6 binding is repelled by H3K9me2/CHGm, consistent with previous work (Qiu et al., 2019). Supporting the functional requirement of REF6 to initiate germination, loss of REF6 caused higher seed dormancy (Figure 3, Figure 3—figure supplement 2; Chen et al., 2020), connected with decreased expression of many germination-inducible genes. Loss of SUVH4/5/6 also increased dormancy (Figure 6—figure supplement 1; Zheng et al., 2012), which was associated with increased expression of potential REF6 target genes. Since H3K9me2 acts in a feedback loop with CHGm (Du et al., 2012; Jackson et al., 2002; Lindroth et al., 2001; Malagnac et al., 2002), loss of SUVH4/5/6 is expected to expose unmethylated binding sites for REF6 that can then be activated by REF6. Consistent with this model, loss of CMT3 also caused increased dormancy (Figure 6b, Figure 6—figure supplement 2). Interestingly, among those upregulated SUVH4/5/6 targets was the positive regulator of seed dormancy ABI3 (Liu et al., 2013), providing a possible explanation for the increased dormancy in suvh4/5/6. Consistent with this notion we found that downregulated genes with single H3K27me3 were enriched for ABI3 binding motifs. Nevertheless, the small fraction of germination-inducible genes with triple repressive marks suggests possible additional mechanisms removing triple epigenetic marks.

Our work furthermore revealed the connection between maternal-specific repressive marks, gene imprinting, and seed dormancy. Imprinted genes were previously shown to play a role in regulating seed germination and were connected to the maternal inheritance of seed dormancy levels (Iwasaki et al., 2019; Piskurewicz et al., 2016). The non-canonical RdDM pathway was found to target and silence the paternal alleles of the dormancy-related gene ALN1 (Iwasaki et al., 2019). Our data suggests that in addition to RdDM, maternally biased expression of dormancy-related genes also requires REF6, which activates maternal H3K27me3 marked genes. We propose that both mechanisms together ensure the maternal control of seed dormancy; while REF6 regulates the time of activation of certain genes, RdDM-mediated CHHm on the paternal alleles prevents their activation. Interestingly, the timing of REF6 action probably differs for distinct genes. While some genes, like ALN1, CYP707A1, and CYP707A3 (Chen et al., 2020) are likely activated in the central cell of the female gametophyte and therefore lack detactable H3K27me3 in the endosperm, other genes are activated during endoperm development. To the latter category belongs the previously reported gene CP1, which is maternally biased in dormant seeds and biallelically expressed in non-dormant seeds (Piskurewicz et al., 2016) and marked with single H3K27me3 on the maternal alleles (Moreno-Romero et al., 2016). In contrast to genes with single H3K27me3, genes with triple repressive marks on maternal alleles are not targeted by REF6, causing the maternal alleles to be silenced and the paternal alleles to be active. Genes with triple repressive marks on REF6-binding sites were upregulated in suvh4/5/6 and were paternally biased during germination. Although more detailed parental-specific DNA methylome analyses in germinating endosperm are required to precisely determine the molecular mechanism repressing the paternal alleles of genes with maternal H3K27me3 during germination, this data supports the model that the presence of single H3K27me3 and triple repressive marks determines whether genes are maternally or paternally biased during germination, respectively (Figure 8—figure supplement 5).

The SUVH4/5/6 genes are not imprinted (Hsieh et al., 2011; Moreno-Romero et al., 2019; Pignatta et al., 2014); however, the delay of germination in suvh4/5/6 was under maternal control (Figure 6a). This indicates that maternal-specific triple repressive marks are established before fertilization in the central cell and maintained after fertilization, consistent with previous data (Moreno-Romero et al., 2019). This suggests that maternal-specific triple epigenetic marks of H3K27me3/H3K9me2 and CHGm contribute to maternally controlled seed dormancy (Iwasaki et al., 2019; Piskurewicz et al., 2016). Likewise, also REF6 is not imprinted (Hsieh et al., 2011; Pignatta et al., 2014), but ref6 had a maternal effect (Figure 3b), supporting the notion that derepression of some dormancy-controlling genes starts in the central cell of the female gametophyte. Nevertheless, the fact that some REF6 targets have detectable levels of H3K27me3 in the endosperm and since we could partially complement the ref6 mutant by expressing REF6 in the micropylar domain of the endosperm (Figure 5a), strongly suggests that REF6 also acts after fertilization. In support of this view, homozygous ref6 mutants had a stronger delay in germination than maternal ref6 mutants (Figure 3b).

Our data furthermore uncovered a relationship among REF6, ethylene, and ABA. Consistent with previous work showing that loss of ABA2 does not completely suppress the delayed germination of ref6 after stratification (Chen et al., 2020), we found that the ABA biosynthesis inhibitor fluridone was not sufficient to suppress delayed germination phenotypes of ref6 (Figure 5—figure supplement 4). Similarly, the ethylene precursor ACC caused only a partial suppression of the germination delay. However, the combined treatment with fluridone and ACC completely suppressed the ref6 germination phenotype (Figure 5—figure supplement 4), supporting our and previous data revealing that REF6 is required to activate ABA catabolism and ethylene signaling through removal of H3K27me3. Since the activation of the ABA catabolism genes CYP707A1 and CYC707A3 likely occurs in the central cell while activation of ethylene signaling genes occurs during endosperm development, we propose that there is a two-step maternal control of germination by REF6. The first step occurs in the central cell and leads to the suppression of ABA signaling, while the second step occurs in the endosperm and leads to the activation of ethylene signaling. This two-step control of germination may ensure the best timing of germination. Understanding by which mechanism the timing of REF6 action is regulated will be subject of future investigations.

Previous data showed that loss of FIS-PRC2 function causes upregulation of genes with both H3K27me3 and H3K9me2 (Hsieh et al., 2011; Moreno-Romero et al., 2016), suggesting that establishment of H3K9me2 depends on H3K27me3. This idea was substantiated by data showing that deficiency of FIS-PRC2 in the central cell causes depletion of CHGm (Moreno-Romero et al., 2019), pointing that H3K9me2/CHGm depend on FIS-PRC2. Also data shown in this study are consistent with this scenario; we demonstrate that loss of H3K9me2/CHGm only caused an effect if H3K27me3 was removed by REF6, revealing that H3K27me3 is the primary repressive mark. Additionally, we found that maternal loss of SUVH4/5/6 was sufficient to cause delayed gemination (Figure 6a), while that of CMT3 was not (Figure 6c). One possible explanation is that the effects caused by loss of SUVH4/5/6 and CMT3 function differ. While H3K9me2 and CHGm are severely depleted in suvh4/5/6; loss of CMT3 mainly affects CHGm with only intermediate effects on H3K9me2 (Stroud et al., 2014; Underwood et al., 2018). Thus, genes with H3K27me3/H3K9me2 can likely be suppressed by CMT3 after fertilization.

A possible mechanism is that the FIS2-PRC2 complex or H3K27me3 recruits SUVH4/5/6 and that H3K9me2 recruits CMT3, suggesting the presence of a molecular mechanism that distinguishes target genes to be marked by single H3K27me3 or triple marks of H3K27me3/H3K9me2 and CHGm. To identify this distinguishing mechanism remains an important future endeavor.

Our data bear striking similarities to maternal H3K27me3-dependent non-canonical imprinting reported in mammals (Chen et al., 2019; Hanna et al., 2019; Inoue et al., 2017a; Inoue et al., 2017b). In non-canonical imprinting, maternal-specific H3K27me3 inherited from oocytes serves as the primary epigenetic mark for imprinted paternal-specific expression. Most of this non-canonical imprinting is transient and restricted to preimplantation embryos, with only some genes important for placental development remain imprinted in extraembryonic cells (Inoue et al., 2017a). Maintenance of non-canonical imprinting is mediated by DNA methylation, which is specifically applied on the maternal alleles of previously H3K27me3 marked regions (Chen et al., 2019; Hanna et al., 2019). Thus, similar to the findings reported in this study, genes regulated by non-canonical imprinting in mammals are transiently imprinted by inheriting maternal-specific H3K27me3 and only few genes remain imprinting by establishing DNA methylation as secondary imprint. Genomic imprinting has independently evolved in flowering plants and mammals; however, rather remarkably, similar molecular mechanisms have been coopted to regulate imprinted genes in the accessory, nutrient-transferring tissues.

The combined presence of H3K27me3 with the heterochromatic modification H3K9me3 was also reported to occur on TEs and repeat-rich regions in the protozoa Tetrahymena and Paramecium (Frapporti et al., 2019; Liu et al., 2007; Zhao et al., 2019) and the fungus Podospora anserine (Carlier et al., 2020). In P. anserine, the presence of double repressive modifications is restricted to TEs and repeat-rich regions, while H3K27me3 alone is located in genic regions, indicating a similar molecular distinction of constitutively silenced regions marked by double modifications from regions that require activation during specific developmental stages marked by H3K27me3 alone. It is tempting to speculate that the co-occurrence of H3K9me3 and H3K27me3 may prevent H3K27me3 demethylases to target and activate those regions, similar to the findings reported in this study.

In summary, in this study, we uncovered a new molecular mechanism leading to maternal-specific dormancy control that distinguishes genes marked by either H3K27me3 alone from genes marked by the generally antagonistic repressive epigenetic modifications, H3K27me3, H3K9me2, and CHGm. We uncovered how the H3K27me3 demethylase REF6 controls release of dormancy and revealed the underlying mechanism for the H3K9me2 methylases SUVH4/5/6 in controlling dormancy and propose that these regulators form a regulatory network through ABA and ethylene pathways. Our data provide new insights into how maternal-specific epigenetic modifications control dormancy and thus ensure timely germination.

All data generated in this study were deposited to the Gene Expression Omnibus and are available under the accession number GSE158907.

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Author details

1. Hikaru Sato

   Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Centre for Plant Biology, Uppsala, Sweden

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Validation, Visualization, Writing - original draft, Writing - review and editing

   Competing interests

   none

   "This ORCID iD identifies the author of this article:" 0000-0001-7628-0414

2. Juan Santos-González

   Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Centre for Plant Biology, Uppsala, Sweden

   Contribution

   Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization

   Competing interests

   none

   "This ORCID iD identifies the author of this article:" 0000-0002-8712-9776

3. Claudia Köhler

   1. Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Centre for Plant Biology, Uppsala, Sweden
   2. Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany

   Contribution

   Conceptualization, Data curation, Funding acquisition, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing - review and editing

   For correspondence

   claudia.kohler@slu.se

   Competing interests

   none

   "This ORCID iD identifies the author of this article:" 0000-0002-2619-4857

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