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\begin{document}

\title{H3K4 trimethylation dynamics impact diverse developmental and
environmental responses in plants}



\author[1]{Maryam Foroozani}%
\author[1]{Matthew Vandal}%
\author[1]{Aaron Smith}%
\affil[1]{Louisiana State University}%


\vspace{-1em}



  
  \date{May 14, 2024}


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\selectlanguage{english}
\begin{abstract}
Plants execute developmental programs and respond to changing
environmental conditions via adjustments in gene expression, which are
modulated in part by chromatin structure dynamics. Histone modifications
alter chromatin in precise ways on a global scale, having the potential
to influence the expression of numerous genes. Trimethylation of lysine
4 on histone H3 (H3K4me3) is a prominent histone modification that is
dogmatically associated with gene activity, but more recently has also
been linked to gene repression. As in other eukaryotes, the distribution
of H3K4me3 in plant genomes suggests it plays a central role in gene
expression regulation, however the underlying mechanisms are not fully
understood. Transcript levels of many genes related to flowering, root,
and shoot development are affected by dynamic H3K4me3 levels, as are
those for a number of stress-responsive and stress memory-related genes.
This review examines the current understanding of how H3K4me3 functions
in modulating plant responses to developmental and environmental cues.%
\end{abstract}%



\sloppy


\textbf{1. Introduction}

Eukaryotic DNA is complexed with histones into nucleosomes, which form
the basic repeating unit of chromatin (Luger, M\selectlanguage{ngerman}äder, Richmond, Sargent,
\& Richmond, 1997). Histone tails that protrude from nucleosome cores
are subject to post-translational modifications, such as methylation,
acetylation, ubiquitination, and phosphorylation, which alter chromatin
structure in distinct ways. For example, histone methylation is an
important modification involved in diverse processes including
transcriptional regulation, heterochromatin formation, and DNA repair
(Greer \& Shi, 2012; C. Liu, Lu, Cui, \& Cao, 2010). Methylation can
occur on lysine or arginine residues with varying numbers of methyl
groups, including mono-, di-, and trimethylation.

Trimethylated lysine 4 on histone H3 (H3K4me3) is a prominent histone
mark whose biological importance is clear in light of phenotypic
consequences of perturbing its deposition, such as poor chronological
aging in yeast (Cruz et al., 2018), defective murine stem cell
differentiation (Carlone \& Skalnik, 2001), and pleiotropic
developmental defects in plants (Alvarez-Venegas \& Avramova, 2005; Guo,
Yu, Law, \& Zhang, 2010b). Genome-level studies have revealed that
H3K4me3 distribution is largely conserved among species and is enriched
in genic regions, particularly around transcription start sites (TSSs;
Barski et al., 2007; Bradley E Bernstein et al., 2002; X. Li et al.,
2008; C. L. Liu et al., 2005; Ram et al., 2011; van Dijk et al., 2010;
X. Zhang, Bernatavichute, Cokus, Pellegrini, \& Jacobsen, 2009). Also,
H3K4me3 abundance is strongly correlated with transcript levels; hence,
H3K4me3 has long been associated with gene activation (Françoise S Howe,
Fischl, Murray, \& Mellor, 2017; Santos-Rosa et al., 2002). Despite
these observations, the identification of clear causal relationships
between H3K4me3 and gene expression are lacking. A recent study in yeast
showed that H3K4me3 does not function in transcription initiation but
modulates gene expression in other ways (Murray et al., 2019). On the
other hand, Arabidopsis ATX1, a histone lysine methyltransferase (HKMT)
that catalyzes H3K4 trimethylation, plays a dual role in gene
expression, functioning in both transcription initiation and elongation
(Ding, Avramova, \& Fromm, 2011b).

Studies in diverse plant species and tissues have investigated genic
levels of H3K4me3 in response to a variety of stresses (Foroozani et
al., 2019; Jaskiewicz, Conrath, \& Peterhänsel, 2011; Kim et al., 2008;
Pan et al., 2017; Sokol, Kwiatkowska, Jerzmanowski, \&
Prymakowska-Bosak, 2007; Tsuji, Saika, Tsutsumi, Hirai, \& Nakazono,
2006; van Dijk et al., 2010; Zeng et al., 2019; Zheng et al., 2019).
Generally these studies reported positive correlations between H3K4me3
abundance and stress-induced gene expression, further supporting an
active role for H3K4me3. However, the genome-level studies showed large
decreases in 5' localization of H3K4me3 in averaged genic profiles of
stressed samples relative to controls (Foroozani et al., 2019; Zeng et
al., 2019; Zong, Zhong, You, \& Xiong, 2013). Also, in two recent
studies in rice, examination of specific subsets of stress-responsive
genes revealed negative correlations between H3K4me3 abundance and gene
up-regulation in response to salt stress (Zheng et al., 2019) or
phosphate (Pi) deficiency (Foroozani et al., 2019). These observations
support a role for H3K4me3 in not only activation but also repression,
consistent with findings in other systems (Clouaire et al., 2012;
Françoise S Howe et al., 2017; Lenstra et al., 2011). Here we review the
current understanding of H3K4me3 in plants, including the enzymes that
alter its deposition in chromatin, how the mark influences gene
expression and transcriptional memory, interactions between H3K4me3 and
other modifications, and the specific developmental processes and stress
responses that are modulated by H3K4me3 dynamics.

\textbf{2. H3K4 Methyltransferases}

Histone lysine methyltransferases (HKMTs) that methylate H3K4 contain an
evolutionarily conserved SET (Su(var)3-9, Enhancer-of-zeste, and
Trithorax) domain, which is required for catalytic activity
(Shilatifard, 2012). In yeast (\emph{Saccharomyces cerevisiae} ), the
Set1 HKMT is solely responsible for H3K4 methylation,
whereas\emph{Drosophila melanogaster} contains three Set1 orthologs:
dSet1, Trithorax\emph{,} and Trithorax-related (Roguev et al., 2001;
Shilatifard, 2012). In plants, all HKMTs belong to the SET Domain Group
(SDG). In Arabidopsis, the HKMTs are further categorized into seven
classes based on function and domain structure (Ng et al., 2007; H. Zhou
et al., 2020). The methyltransferases specific to H3K4 are members of
class III, which is comprised of five Arabidopsis Trithorax-like (ATX)
proteins, ATX1 through ATX5, and two ATX-related (ATXR) proteins, ATXR3
and ATXR7 (Avramova, 2009; Guo et al., 2010b; Tamada, Yun, chul Woo, \&
Amasino, 2009). All class III proteins bear the SET and post-SET
domains, but they contain varying combinations of other domains that
allow for distinct functionality.

Perhaps the most studied of the ATX proteins is ATX1, which was found to
methylate H3K4 at distinct genes in Arabidopsis (Alvarez-Venegas \&
Avramova, 2005). The yeast Set1 methyltransferase must interact with
structural proteins in a complex known as COMPASS (Complex Proteins
Associated with Set1) to achieve H3K4 methylation (Schneider et al.,
2005). The identification of an Arabidopsis COMPASS-like complex and its
interaction with ATX1 confirms a similar scenario in plants (Ding,
Ndamukong, et al., 2012a; D. Jiang, Kong, Gu, Li, \& He, 2011). ATX2
shows structural parallels with ATX1, but has divergent regulatory
sequences that allow for differences in function. Whereas ATX1 catalyzes
trimethylation at H3K4, ATX2 catalyzes dimethylation (Saleh et al.,
2008). Also, ATX1 and ATX2 appear to regulate different subsets of genes
(Saleh et al., 2008). ATXR3 (also named SDG2) is the predominant enzyme
responsible for genome-wide trimethylation at H3K4 (Guo et al., 2010b).
The \emph{sdg2} mutant shows a pleiotropic phenotype, with stunted
growth, impaired fertility, and differential expression of numerous
genes (Guo, Yu, Law, \& Zhang, 2010a). In addition to trimethylation
activity, SDG2 is capable of catalyzing dimethylation on H3K4, however,
the significance of this function appears limited, as the
\emph{sdg2}mutant exhibited a minimal reduction in genome-wide H3K4me2
(Guo et al., 2010b). ATX3, ATX4, and ATX5 are redundantly necessary for
genome-wide di- and trimethylation of H3K4 at sites distinct from those
targeted by ATXR3/SDG2 (L. Chen et al., 2017). Lastly, ATXR7 is able to
methylate H3K4, but may also be involved in the dimethylation of H3K36
(Berr et al., 2009). In rice, five class III HKMTs have been described.
Two of these, OsSDG723 (also named OsTrx1) and OsSDG701, are orthologs
of ATX1 and ATXR3/SDG2, respectively, and contribute to H3K4 methylation
levels (Choi et al., 2014; K. Liu, Yu, Dong, \& Shen, 2017).

\textbf{3. H3K4 Demethylases}

The dynamic nature of histone methylation became apparent after the
identification of Lysine Specific Demethylase 1 (LSD1) in humans, which
demethylates mono- and dimethyl H3K4 (Shi et al., 2004). Subsequently,
proteins containing jumonji C (JmjC) domains (JMJ) were identified as
another family of histone demethylases. JMJ proteins can demethylate not
only mono- and dimethylated, but also trimethylated substrates (Tsukada
et al., 2006). Arabidopsis demethylases that target H3K4 include three
homologs of LSD, FLOWERING LOCUS D (FLD), LSD1-LIKE1 (LDL1), and
LSD1-LIKE2 (LDL2), and five JMJ proteins, JMJ14 through JMJ18 (P. Liu et
al., 2019; Ueda \& Seki, 2020). An important aspect of H3K4 demethylase
function appears to be its relationship with RNA-mediated DNA
methylation (RdDM). H3K4me2 and H3K4me3 marks antagonize RdDM at many
sites throughout the genome; therefore, demethylases (e.g. JMJ14, LDL1
and LDL2), act to maintain RdDM genomic patterns (Greenberg et al.,
2013).

Arabidopsis H3K4 demethylases from both the LSD and JMJ families play
important roles in regulating flowering. The three LSD demethylases have
distinct and partially redundant roles in suppressing floral repressor
genes (D. Jiang, Yang, He, \& Amasino, 2007). Similarly, JMJ14, JMJ15,
and JMJ18 reduce H3K4me3 abundance at various flowering regulatory
genes, thereby reducing their expression (Ning et al., 2015; H. Yang,
Han, et al., 2012; H. Yang, Mo, et al., 2012). In addition to regulating
the transition to flowering, Arabidopsis demethylases also play roles in
RNA silencing (JMJ14; Searle, Pontes, Melnyk, Smith, \& Baulcombe,
2010), defense (JMJ14; D. Li et al., 2019), salinity stress (JMJ15; Shen
et al., 2014), senescence (JMJ16; P. Liu et al., 2019), and dehydration
stress (JMJ17; Huang et al., 2019). Rice demethylases that target H3K4
include OsJMJ701, OsJMJ703, and OsJMJ704 (X. Chen, Hu, \& Zhou, 2011; T.
Song et al., 2018). OsJMJ701 and OsJMJ703 are involved in regulating
flowering (Q. Chen et al., 2013; T. Song et al., 2018; Yokoo et al.,
2014), whereas OsJMJ704 plays a role in modulating responses to a
bacterial pathogen (Hou et al., 2015). Taken together, these studies
indicate that demethylation of H3K4 at distinct loci is an important
regulatory component of developmental and stress responses in plants.

\textbf{4. Functions of H3K4me3}

H3K4me3 is a prevalent mark conserved among species. Because it is
enriched in genic regions and correlates with transcript levels, it is
considered an active histone mark (Françoise S Howe et al., 2017;
Santos-Rosa et al., 2002). However, H3K4me3 dynamics have been
associated with not only activation, but also repression of subsets of
genes (Clouaire et al., 2012; Foroozani et al., 2019; Françoise S Howe
et al., 2017; Lenstra et al., 2011). Unlike its counterpart in yeast,
Arabidopsis ATX1 has been shown to play a dual role in transcription
(Ding et al., 2011b). Mutation of \emph{ATX1} led to substantial
decreases in TATA Binding Protein (TBP) and RNA Polymerase II (Pol II)
accumulation at the promoters of ATX1-target genes. This disruption of
the transcription preinitiation complex (PIC) was associated with
reduced target gene expression (Ding et al., 2011b). When \emph{ATX1}was
mutated in only the SET catalytic domain, there was no observable
decrease in the formation of the PIC (Ding, Ndamukong, et al., 2012b).
This indicates that the deposition of H3K4me3 by ATX1 is not required
for establishment of the PIC, but rather the formation of the
ATX1/COMPASS-like complex is responsible for regulating transcription
initiation. In addition to its recruitment to promoters, ATX1 is
recruited to a promoter-proximal region where it catalyzes H3K4
trimethylation, which peaks at approximately 300-bp downstream of the
TSS (Ding et al., 2011b). This recruitment is facilitated by the Ser5P
(phosphorylated at serine 5 of the carboxyl terminal domain) form of Pol
II, which is prevalent during early elongation. Continued elongation
alters the phosphorylation state of Pol II to the Ser2P form, releasing
ATX1 due to a lack of binding to this form. SET-domain mutants of ATX1
exhibit wild-type levels of Ser5P Pol II but have a considerable
reduction in the level of Ser2P Pol II. This indicates that the rate of
Pol II exit from initiation to elongation is reduced in the mutants
(Ding et al., 2011b). These results indicate that ATX1, but not its H3K4
trimethylation activity, is required at promoters for PIC assembly and
transcription initiation, whereas ATX1-generated H3K4me3 is essential
for transcriptional elongation. Another aspect of gene expression
subject to regulatory control is mRNA splicing. Successful mRNA splicing
requires a 5'-cap, which is recognized and protected by a nuclear mRNA
cap-binding complex (CBC; Calero et al., 2002). In Arabidopsis, the CBC
was shown to interact with ATX and an H3K36 methyltransferase,
indicating that trimethylation of both H3K4 and H3K36 is required for
CBC-mediated 5'-cap preservation and mRNA splicing at ATX1 targets (Z.
Li et al., 2016). Taken together these results demonstrate that H3K4me3
plays key roles in multiple aspects of gene regulation, including
initiation, elongation, and mRNA splicing (Figure 1).

H3K4me3 has been implicated in the regulation of a number of
developmental and environmental responses, and the associated mechanisms
are subject to many functional considerations that are position- and/or
context-dependent (Figure 2). In addition to the promoter versus
promoter-proximal determinacy of ATX1 function described above, H3K4me3
at the transcription end site (TES) may play a role in antisense
transcriptional control as observed for some mammalian genes (Cui et
al., 2012). In this capacity, H3K4me3 may indirectly repress sense
transcription by promoting antisense transcription. Further study is
needed to determine the role of TES-localized H3K4me3 at plant genes.
Another positional consideration of H3K4me3 function is the breadth of
its distribution (i.e. peak width). A number of studies have suggested
that relatively broad H3K4me3 peaks facilitate gene expression by
reducing transcriptional noise or by promoting Pol II pausing (Park,
Kim, Kwon, \& Lee, 2020). Also, genes marked by broad H3K4me3 domains
tend to be responsive (i.e. with non-housekeeping functions) and exhibit
cell type-specific functions. For example, Zhang et al. (2016), showed
that broad H3K4me3 domains in chromatin isolated from human primary
monocytes were biased at immune-responsive genes linked to the
autoimmune disease, lupus. In Arabidopsis, H3K4me3 distribution at some
dehydration stress-responsive genes was broader than at unresponsive
genes (van Dijk et al., 2010). Therefore, broad H3K4me3 domains may
recruit extensive, but paused, Pol II at stress-responsive genes,
poising them for a robust transcriptional response upon induction.

In addition to positional considerations, H3K4me3 functions are also
context-dependent. A study in yeast revealed that after cessation of
transcription, H3K4me3 remained at promoter regions of several inducible
genes and inhibited their reactivation (B. O. Zhou \& Zhou, 2011).
Additionally, a more rapid transcriptional repression was observed at a
number of genes previously repressed by carbon-source shifts, a
phenomenon termed transcriptional repression memory (TREM; B. B. Lee et
al., 2018). Induction of TREM is promoted by histone deacetylation via
interaction between Rpd3L histone deacetylase (HDAC) and H3K4me3 (B. B.
Lee et al., 2018). In Arabidopsis, H3K4me3 plays a role in the
transcriptional memory of genes related to drought (Ding, Fromm, \&
Avramova, 2012) and heat stress (Lämke, Brzezinka, Altmann, \& Bäurle,
2016). H3K4me3 levels significantly increased at response genes under
re-exposure to stress treatments and displayed quicker and/or stronger
transcriptional responses. In a related phenomenon, H3K4me3 accumulates
at some defense-response genes during chemical priming. For example,
exogenous application of the phytohormone salicylic acid (SA), or
certain synthetic SA analogs, is sufficient to induce tolerance to a
subsequent pathogen challenge (i.e. priming), and H3K4me3 appears to be
involved in poising the primed defense-responsive genes for enhanced
transcription (Kohler, Schwindling, \& Conrath, 2002; Mozgova et al.,
2015a, 2015b).

Perhaps the foremost context-dependent consideration for the function of
any chromatin mark is its interaction with other chromatin
modifications. ``Bivalent'' nucleosomes or domains contain both
activating and repressive marks, with the pairing of H3K4me3 and
H3K27me3 in particular, is a prominent example (B. E. Bernstein et al.,
2006). In mammalian H3K4me3-H3K27me3 bivalent domains, H3K4me3 poises
genes for activation, whereas H3K27me3 represses transcription (B. E.
Bernstein et al., 2006; Vastenhouw \& Schier, 2012). In Arabidopsis,
H3K4me3-H3K27me3 bivalent domains were present at some genes required
for gametophyte development (Berr et al., 2010), flowering time
regulation (Qian et al., 2018), and at some dehydration stress-induced
genes (N. Liu, Fromm, \& Avramova, 2014). Recently, a large number of
genes in potato (\emph{Solanum tuberosum} ) tubers up- or down-regulated
by cold treatment were shown to contain the H3K4me3-H3K27me3 bivalent
mark, suggesting it increases chromatin accessibility and facilitates
recruitment of regulatory proteins necessary for either gene induction
or repression (Zeng et al., 2019). More discussion on the interactions
between H3K4me3 and other marks, as well as how H3K4me3 functions relate
to specific developmental and environmental responses is presented in
the sections below.

\textbf{5. H3K4me3 and Developmental Processes}

\textbf{5.1 Flowering Time and Flower Development}

Flowering is one of the most vital and regulated developmental processes
in higher plants. Plants have evolved complex signaling pathways to
ensure appropriate transition to the reproductive phase in accordance
with developmental and environmental cues. In Arabidopsis, a number of
components, including FLOWERING LOCUS C (FLC), the key floral repressor,
its activator, FRIGIDA (FRI), and its downstream target, FLOWERING LOCUS
T (FT), are involved in these pathways (I. Lee, Michaels, Masshardt, \&
Amasino, 1994). Investigations of the molecular mechanisms of flowering
have revealed the involvement of many H3K4 trimethyltransferases,
largely through their role in modulating \emph{FLC} expression. Indeed,
mutation of either of the \emph{ATX1} , \emph{ATX2} , \emph{ATXR7} ,
or\emph{ATXR3} /\emph{SDG2} HKMTs directly or the COMPASS-like
components,\emph{ASH2R} or \emph{RbBP5} , resulted in reductions in
H3K4me3 levels and transcription at \emph{FLC} , along with an early
flowering phenotype (Berr et al., 2009; D. Jiang et al., 2011; Michaels
\& Amasino, 1999; Pien et al., 2008; Tamada et al., 2009; Yun, Tamada,
Kang, \& Amasino, 2012). Notably, ATX1, ATXR7 and ASH2R were shown to
directly bind the\emph{FLC} locus at the TSS. Since the expression level
of \emph{FLC} is low in the native Colombia ecotype because of the
absence of FRI, the function of H3K4 methyltransferases (\emph{ATX1} ,
\emph{ATX2} ,\emph{ATXR7} and \emph{SDG2} ) in \emph{FLC} activation
were investigated in a Colombia background containing an active FRI
allele. The activation of \emph{FLC} by FRI was shown to be associated
with H3K4me3 abundance and required \emph{ATX1} , \emph{ATX2} ,
\emph{ATXR7} and \emph{ATXR3}activity (Pien, Fleury et al. 2008, Tamada,
Yun et al. 2009, Yun, Tamada et al. 2012). Thus, COMPASS-like and H3K4
trimethylation are required for proper \emph{FLC} expression and the
vegetative to reproductive transition. Recently, characterization of the
plant-specific protein, SHORT LIFE (SHL), revealed a flowering time
regulatory mechanism that involves H3K4me3-H3K27me3 bivalent domains
(Qian et al., 2018). SHL is capable of binding both H3K4me3 and
H3K27me3, but in an independent and mutually exclusive manner. SHL
negatively regulates the floral activator, SUPPRESSOR OF OVEREXPRESSION
OF CONSTANS 1 (SOC1), likely by interacting with H3K4me3 and recruiting
HISTONE DEACETYLASE 6 (HDA6) (Lopez-Gonzalez et al., 2014).
Interestingly, the presence of H3K27me3 at the \emph{SOC1} locus is also
necessary for SHL-mediated repression (Qian et al., 2018). Therefore SHL
appears to be a central regulatory component in flowering time that
mediates the switch between active and repressive states of \emph{SOC1}
, and likely other floral integrator genes. Given that overexpression or
antisense-knockdown of \emph{SHL}resulted in a pleiotropic phenotype,
including perturbations in growth, senescence, and flower and seed
formation (Mussig, Kauschmann, Clouse, \& Altmann, 2000), SHL is likely
to modulate a number of distinct developmental pathways.

Further evidence for a role of H3K4me3 in flowering time regulation has
been determined through investigations of demethylases. JMJ15 and JMJ18
contribute to floral activation by decreasing H3K4me3 and expression
of\emph{FLC} , whereas JMJ14 is implicated in floral repression by
decreasing H3K4me3 and expression of \emph{FT} (Jeong et al., 2009; Ning
et al., 2015; H. Yang, Han, et al., 2012; H. Yang, Mo, et al., 2012; W.
Yang, Jiang, Jiang, \& He, 2010). However, two additional studies showed
that mutation of \emph{JMJ14} caused changes in the expression levels of
multiple floral regulator-encoding genes, including \emph{FT}
,\emph{SOC1} , \emph{LFY} , and \emph{AP1} , without corresponding
changes in H3K4me3 levels (Falong Lu, Cui, Zhang, Liu, \& Cao, 2010;
Ning et al., 2015). Additional studies are needed to resolve the
mechanistic details of JMJ14 function at floral regulator genes. JMJ14
appears to influence flowering, in part, via physical interaction with
two NAC (NAM, ATAF1, and CUC1/CUC2) transcriptional repressors, NAC050
and NAC052 (Ning et al., 2015). Mutation of \emph{JMJ14} or RNAi
knock-down of \emph{NAC050} and \emph{NAC052} led to an early flowering
phenotype, as well as up-regulation and enhanced H3K4 trimethylation at
a number of target genes. Therefore, JMJ14 and NAC050/NAC052 interact
and co-regulate a number of genes via H3K4 demethylation and
transcriptional repression, including genes that influence flowering
time control.

H3K4me3 is also required for proper flowering time in rice. The
H3K4me3/H3K27me3 ratio and expression levels for a number of genes were
correlated during transition from the shoot apical meristem (SAM) to the
inflorescence meristem (IM; X. Liu et al., 2015). Specifically, the
H3K4me3/H3K27me3 ratio was relatively high and low at up- and
down-regulated genes, respectively. Also, mutations in
\emph{OsSDG711}(H3K27 methyltransferase) or \emph{OsJMJ703} (H3K4
demethylase) were found to reduce induction in the levels of H3K27me3 at
many genes in the IM. H3K4me3 and H3K27me3 levels were increased and
decreased, respectively, in both the \emph{osjmj703} and \emph{ossdg711}
single mutants at the CKX2/Gn1a locus, a gene expressed in IM related to
panicle size. The \emph{ossdg711 osjmj703} double mutant showed strong
induction of H3K4me3 and reduction of H3K27me3, suggesting that OsSDG711
and OsJMJ703 function to control the H3K4me3/H3K27me3 ratio (Liu, Zhou
et al. 2015). A recent study utilizing cell-type specific analysis with
stem cells and non-stem cells found that within the SAM, H3K4me3 and
H3K27me3 levels changed during floral transition, with an increase in
H3K4me3 corresponding to an increase in gene expression (You et al.,
2017). However, the results of this study suggest that the level of
H3K27me3 does not predict levels of gene expression in the SAM as a
result of flowering. OsTrx1 and OsSDG701, rice orthologs of ATX1 and
ATXR3/SDG2, respectively\emph{,} also play roles in regulating flowering
time. OsTrx1 binds to \emph{Early Heading Date 3} (\emph{Ehd3} ), which
induces flowering through downregulation of \emph{Heading Date
7}(\emph{Ghd7} ; Choi et al., 2014). In addition, OsSDG723\emph{/}
OsTrx1\emph{/} OsSET33 Interaction Protein 1 (SIP1) recruits OsTrx1 to
\emph{Ehd1} where it impacts H3K4me3 levels and expression (P. Jiang et
al., 2018). Ehd1, in turn, regulates the florigen-encoding genes,
\emph{Heading Date 3a (Hd3a)} and \emph{Rice Flowering Locus T1}
(\emph{RFT1} ). In \emph{ossdg701} mutants, the expression of all three
genes was downregulated, and H3K4me3 levels were reduced at \emph{Hd3a}
and \emph{RFT1} , but not \emph{Ehd1} (K. Liu et al., 2017). This
indicates that OsSDG701 is necessary for the transition to flowering,
apparently through direct and indirect interactions with floral
regulators.

Three studies have investigated the roles of H3K4 demethylases (OsSe14
and OsJMJ703) in rice flowering and development (Q. Chen et al., 2013;
T. Song et al., 2018; Yokoo et al., 2014). Mutation of
\emph{osse14}caused early flowering, increased levels of H3K4me3 at
\emph{RFT1} , and induced \emph{RFT1} expression (Yokoo, Saito et al.
2014). A more recent study showed that mutation of \emph{OsJMJ703}
caused early flowering, and overexpression of \emph{OsJMJ703} changed
the structure of the panicle (T. Song et al., 2018). The levels of
H3K4me3 were measured in both mutant and overexpression lines, and the
developmental defects were associated with higher and lower levels of
H3K4me3, respectively.

In addition to a role in regulating flowering time, H3K4me3 dynamics
have been linked to flower development. Mutation of
Arabidopsis\emph{ATXR3} /\emph{SDG2} resulted in floral defects
including severe male and female reproductive organ abnormalities, as
well as inability to maintain indeterminate growth of the IM, resulting
in a terminal flower (Guo et al., 2010b). Similarly, mutation of
Arabidopsis\emph{ATX1} led to defects in floral organ development and
identity (Alvarez-Venegas et al., 2003). \emph{In situ} hybridization
assays showed a correlation between \emph{ATX1} expression and floral
organ initiation. Additionally, the expression of three homeotic
genes,\emph{APETALA} (\emph{AP1} , \emph{AP2} ), and \emph{AGAMOUS}
(\emph{AG} ) were reduced in \emph{atx1} mutants. Dynamic change of
H3K4me3 was found to be a strong indicator for changes in gene
expression over flower development, moreso than H3K27me3, although
several genes were found to be marked differentially by these two
modifications throughout development (Engelhorn et al., 2017). During
flower initiation, changes in H3K4me3 occurred sooner and exhibited a
stronger correlation with expression relative to H3K27me3. It is likely
that bivalent domains containing both H3K4me3 and H3K27me3 marks
modulate expression of many genes in accordance with developmental cues.

\textbf{5.2 Root and Shoot Development}

Trimethylation of H3K4 is required for proper root and shoot
development, which is exemplified by the pleiotropic phenotypes of HKMT
mutants. In addition to many floral defects, Arabidopsis \emph{sdg2}
and\emph{atx1} mutants exhibit small shoot and root organs
(Alvarez-Venegas \& Avramova, 2005; Guo et al., 2010b;
Napsucialy-Mendivil, Alvarez-Venegas, Shishkova, \& Dubrovsky, 2014;
Yao, Feng, Yu, Dong, \& Shen, 2013). Detailed characterization showed
that loss of SDG2 function and reduction of H3K4me3 levels in root cells
led to a smaller root apical meristem (RAM), disorganized root stem cell
niche, and as a consequence, halted meristem activity in both primary
and lateral roots (Yao et al., 2013). In addition to loss of cell
identity and stem cell function, there was no observable auxin gradient
in the root quiescent center within \emph{sdg2} mutants. More
similarities between \emph{sdg2}and \emph{atx1} mutants include delayed
primary root growth, decreased RAM size and activity, and attenuated
lateral root emergence . Interestingly, the transition from cell
proliferation to cell elongation in the RAM was impaired in mutants of
\emph{ATX1} , but not \emph{SDG2} , revealing non-redundant requirements
of ATX1 for root development (Napsucialy-Mendivil et al., 2014).

Evidence suggests H3K4me3 is involved in shoot development by regulating
the expression of the repressive shoot developmental
genes,\emph{MIR156A} and \emph{MIR156C} (Xu, Leichty, Hu, \& Poethig,
2018). Transition from juvenile to adult vegetative phase is controlled
by induction of \emph{SQUAMOSA PROMOTER BINDING PROTEIN-LIKE}
(\emph{SPL} ) expression, which is negatively regulated by miR156A and
miR156C (Poethig, 2010; Yu et al., 2013). In wild-type plants at
the\emph{MIR156A} and \emph{MIR156C} genes, H3K4me3 levels decreased
gradually during shoot development whereas H3K27me3 levels increased (Xu
et al., 2018). Mutation in \emph{ACTIN-RELATED PROTEIN 6}(\emph{ARP6}
)\emph{,} which facilitates deposition of the H2A.Z variant, reduced the
level of H3K4me3 at both genes, whereas nucleosome occupancy and
H3K27me3 increased at only \emph{MIR156A} (Xu et al., 2018).
Additionally, expression levels of \emph{MIR156A} and \emph{MIR156C}were
reduced in \emph{arp6} mutants. These results indicate that genes
regulated by H2A.Z-assisted deposition of H3K4me3 are required for shoot
development in Arabidopsis (Xu et al., 2018).

H3K4me3 dynamics have also been implicated in tissue identity and plant
regeneration. For example, Arabidopsis ATX4 was shown to regulate shoot
identity genes required for successful transition from callus to shoot
tissue (K. Lee, Park, Choi, \& Seo, 2019). In rice, H3K4me3 was found to
be important for stem elongation and growth. Mutants of
\emph{OsJMJ703}exhibited semi-dwarf phenotypes due to slower cell
division and cytokinin deficiency, apparently as a result of increased
H3K4me3 at the promoter of \emph{CYTOKININ OXIDASE} (\emph{CKX} ) and
induction of\emph{CKX} expression (Q. Chen et al., 2013).

\textbf{5.3 Sporophyte and Gametophyte Development}

Berr et al. (2010) reported on the involvement of ATXR3/SDG2 in
sporophyte and gametophyte development in Arabidopsis. Results indicated
that leaf sizes were reduced during the vegetative phase in
the\emph{sdg2} mutant because of impaired cell division and cell
expansion. Sterility of the \emph{sdg2} mutants was caused by defective
anther and pollen development along with short stamens and misregulated
microgametogenesis. In addition, megagametogenesis was halted in
most\emph{sdg2} mutant ovules, leading to degenerate megaspore nuclei
and defective embryo sacs. The expression levels
of\emph{SPOROCYTELESS/NOZZLE} (\emph{SPL/NZZ} ) and \emph{MALE
STERILITY1}(\emph{MS1} ), two essential genes for male and/or female
gametophyte development, were drastically reduced in \emph{sdg2}
mutants. In wild-type plants, \emph{SPL/NZZ} and \emph{MS1} contain
H3K4me3-H3K27me3 bivalent nucleosomes. In \emph{sdg2} mutants, the
levels of H3K4me3, but not H3K27me3, were decreased. Therefore,
SDG2-mediated H3K4me3 deposition regulates expression of two essential
developmental genes, controlling molecular mechanisms for gametophyte
development. More recently, SDG2 was shown to play a role in postmeiotic
gametogenesis by promoting chromatin decondensation, mitotic cell
division, and activation of the ATLANTYS1 retrotransposon (Pinon, Yao,
Dong, \& Shen, 2017). At the tricellular stage, \emph{sdg2} pollen
grains contained only two sperm nuclei per pollen. Also, chromatin was
more condensed in the \emph{sdg2} mutant as compared to wild type. This
elevated chromatin compaction in \emph{sdg2} resulted in defects in
\emph{ATLANTYS1}activity, pollen germination, and pollen tube
elongation, which were accompanied by a reduction of H3K4me3 and
reorganization of H3K9me2.

\textbf{5.4 Circadian Clock}

Rhythmic transition from activation to repression of oscillator genes
within the circadian clock is influenced by H3K4me3 dynamics. Both the
expression of Arabidopsis oscillator genes responsible for circadian
clockwork and the levels of H3K4me3 at those genes are dependent on SDG2
(Malapeira, Khaitova, \& Mas, 2012). A decrease in H3K4me3 levels by
nicotinamide treatment showed an induction in the binding of a clock
transcriptional repressor, PSEUDO-RESPONSE REGULATOR 5 (PRR5), to its
target genes, causing repression. In wild type, the enrichment of
H3K4me3 and H3K56ac was higher at evening-expressed oscillator genes at
Zeitgeber Time 15 (ZT15), whereas a reduction in the level of both
histone modifications was observed at morning-expressed oscillatory
genes at ZT15. The opposite was true for ZT3, with H3K4me3 and H3K56ac
increasing at morning-expressed oscillator genes, while decreasing at
the evening genes. A time course analysis showed that H3K4me3 had a
delayed accumulation when compared to H3K56ac, suggesting a difference
in accrual could be specific to time-related activating functions. In
addition, H3K4me2 levels were high at the time H3K56ac was low and vice
versa, whereas the coexistence of H3K4me3 and H3K4me2 was also detected.
This suggests a sequential accumulation of first H3K56ac, then H3K4me3,
and finally H3K4me2, which is temporally associated with the expression
of oscillator genes through the circadian cycle (Malapeira et al.,
2012).

\textbf{5.5 Leaf Senescence}

The dynamics of several histone marks, including H3K4me3, H3K27me3, and
H3K9ac, have been implicated in the regulation of gene expression during
leaf senescence. Genome-wide investigation showed in older leaves of
Arabidopsis a positive correlation between H3K4me3 and transcript
levels, as well as a negative correlation between H3K27me3 and
transcript levels (Brusslan et al., 2012). Only a limited portion (5\%)
of differentially expressed genes showed changes in both H3K4me3 and
H3K27me3, suggesting the importance of H3K4me3-H3K27me3 bivalent domains
in the developmental transition of senescing leaves may be minimal
(Brusslan et al., 2012). In a subsequent study, a stronger positive
correlation between H3K4me3 levels and gene expression was shown during
leaf senescence (Brusslan et al., 2015). Around 56\% of increased
H3K4me3 genes and 63\% of decreased H3K4me3 genes were up- and
down-regulated, respectively, during leaf senescence, whereas a moderate
positive correlation was observed between H3K9ac and gene expression.
Recently, Liu et al. (2019) investigated the mechanism of how
age-dependent induction of senescence-associated genes (SAGs) are
associated with high levels of H3K4me3. Rice \emph{osjmj16} mutants
displayed a premature senescence phenotype, as well as an increase in
both H3K4me3 abundance and expression levels of several SAGs, such
as\emph{WRKY53} and \emph{SAG201} . In addition, \emph{OsJMJ16}
expression decreased in the later stages of leaf development. Thus,
OsJMJ16 appears to negatively controls leaf senescence, in part, by
repressing the expression of \emph{WRKY53} and \emph{SAG201} .

\textbf{6. H3K4me3 and Stress Responses}

\textbf{6.1 Drought Stress}

Drought is one of the most prominent and growth-limiting abiotic
stressors encountered by crop plants. In response to dehydration, plants
initiate signaling pathways aimed at enhancing tolerance to drought via
molecular, biochemical, and physiological responses. More than a decade
ago, H3K4me3 was first implicated in regulating plant responses to
drought. By examining chromatin marks specifically at four
drought-inducible genes in Arabidopsis (\emph{RD29A} , \emph{RD29B}
,\emph{RD20} , and \emph{RAP2.4} ) Kim et al. (2008) showed that H3K4me3
abundance, along with transcript levels, increased at all four genes in
response to drought stress (Kim et al., 2008). Subsequent genome-wide
studies in Arabidopsis (van Dijk et al., 2010) and rice (Zong, Zhong et
al. 2013) showed a similar trend in which many genes up- or
down-regulated by dehydration exhibited increased and decreased H3K4me3
abundance, respectively.

Examination of transgenic lines exhibiting altered expression of
methylases and demethylases suggest direct involvement of H3K4me3
dynamics in controlling responses to drought stress. Mutation
of\emph{ATX1} in Arabidopsis (Ding, Avramova, \& Fromm, 2011a) or
overexpression of \emph{OsJMJ703} in rice (Song, Zhang et al. 2018) each
led to transgenic lines that exhibited increased sensitivity to drought
stress. Consistently, RNAi knockdown of \emph{OsJMJ703} conferred
enhanced drought tolerance (Song, Zhang et al. 2018). On the other hand,
in wild-type plants, \emph{OsJMJ703} expression was reduced by drought
stress, whereas \emph{ATX1} expression was unaffected (Ding et al.,
2009). This suggests different roles for H3K4me3 methyltransferases and
demethylases in drought stress responses, such that the catalytic
activity of methyltransferases (e.g. ATX1) is responsive to stress, but
demethylases (e.g. OsJMJ703) respond to stress through increases in
their gene expression.

Detailed characterization of Arabidopsis \emph{atx1} mutants revealed
that the increased sensitivity of drought conferred by loss
of\emph{ATX1} was in part due to reduced biosynthesis of abscisic acid
(ABA), an important phytohormone that modulates osmotic stress pathways
in plants (Ding et al., 2011a). Specifically, dehydration stress
increased transcription and H3K4me3 abundance at the \emph{NCED3} ABA
biosynthetic gene, which required recruitment of ATX1 to the\emph{NCED3}
locus. ATX1, in turn, increased the amount of Pol II bound to
\emph{NCED3} . Therefore, ATX1 influences drought-stress pathways by
upregulating \emph{NCED3} transcription and ABA production (Ding et al.,
2011a).

Characterization of the \emph{NCED3} locus also highlights two distinct
functions of ATX1 in Arabidopsis (Ding et al., 2011a). In the promoter,
ATX1 aids in transcription initiation by recruiting TBP and Pol II. Upon
transition to a transcriptional elongation state, phosphorylation occurs
at Ser5 of Pol II's carboxy-terminal domain (CTD). ATX1 is recruited to
Ser5P-containing regions, which peak at around +300 bp downstream of the
TSS, at which it catalyzes H3K4 trimethylation. Additional
transcriptional elongation leads to the predominantly Ser2P form of CTD,
resulting in loss of ATX1. These data indicate that ATX1 plays distinct
roles in Pol II recruitment and H3K4 trimethylation, both of which
appear to be involved in the regulation of \emph{NCED3} during drought
stress. The observation that the level of H3K4me3 was established only
after Pol II accumulation at two drought-responsive genes
(\emph{RD29A}and \emph{RAP2.4} ) further supports a model in which
Ser5P-dependent H3K4 trimethylation occurs subsequently to Pol II
recruitment in the promoter (Kim et al., 2008).

The H3K4me3 distribution profile at some dehydration stress-responsive
genes has been shown to be broader than unresponsive genes, although
these profiles are present during both control and dehydration stress
conditions (van Dijk et al., 2010). At human tumor-suppressor genes,
broad H3K4me3 peaks were linked to increased transcription elongation
(K. Chen et al., 2015). Although the relevance of H3K4me3 breadth is not
completely clear, the broad H3K4me3 peaks at drought-responsive genes
(and possibly other stress-responsive genes) may reflect extensive
gene-body H3K4 trimethylation, and perhaps extensive Ser5P Pol II, to
ensure a transcriptionally poised state in preparation for stress
induction.

A particularly striking phenomenon that has been revealed through
investigations of H3K4me3 in drought stress responses is its
contribution to transcriptional memory. Based on their expression
pattern during reoccurring drought stress, four dehydration-inducible
marker genes, \emph{RD29A} , \emph{RD29B} , \emph{RAB18} ,
and\emph{COR15A} , were designated `trainable' or `non-trainable' (Ding,
Fromm, et al., 2012). Transcripts of trainable genes (\emph{RD29B}
,\emph{RAB18} ) were greater during recurring stress relative to their
levels upon the initial stress; however, transcript levels of
non-trainable genes (\emph{RD29A} , \emph{COR15A} ) were induced at the
same level during each stress. Despite this difference, expression of
both trainable and non-trainable genes returned to initial levels during
the recovery states. For non-trainable genes, the degree of H3K4me3
enrichment was similar after each stress treatment, but in trainable
genes, H3K4me3 was significantly increased in repetitive stress
treatments. In the recovery states, the levels of H3K4me3 and Ser5P Pol
II remained high in trainable genes even with the low level of
transcription, showing Ser5P Pol II was stalled. These data suggest that
the presence of H3K4me3 may be necessary for elongation but does not
guarantee the transition from initiation to elongation. H3K4me3 behaves
as an adjustable chromatin mark which is correlated with transcription
levels in non-trainable genes, but acts as an epigenetic memory mark
that is not removed during recovery states in trainable genes (Ding,
Fromm, et al., 2012).

\textbf{6.2 Temperature Stress}

Another example of H3K4me3-mediated transcriptional memory occurs during
heat stress. Plants exposed to moderate heat stress acquire
thermotolerance, acclimating them to a subsequent high temperature
stress that is lethal to non-acclimated plants (Mittler, Finka, \&
Goloubinoff, 2012). The acquired thermotolerance is maintained for
several days after a return to non-stress temperatures, a phenomenon
termed heat-stress memory. Transcriptomic analysis identified a number
of putative heat-stress memory genes based on their persistent elevated
transcription for several days after the heat stress (Stief et al.,
2014). These genes contrast with heat stress-induced genes whose
expression declines relatively quickly (i.e. heat-stress non-memory
genes). Investigating the levels of H3K4me2/3 at the representative
heat-inducible memory and non-memory genes, \emph{HEAT SHOCK
PROTEIN}(\emph{HSP} ) \emph{22.0} and \emph{70} , respectively, showed
that these marks play a role in heat-stress memory (Lämke et al., 2016).
Relatively soon after an acclimatizing heat stress, the non-memory gene
(\emph{HSP70} ) exhibited a moderate increase in H3K4me3 that declined
over the next several days. In contrast, the memory gene (\emph{HSP22.0}
) showed a dramatic increase in H3K4me3 that remained for several days.
Also, H3K9 acetylation (H3K9ac) was highly enriched early at both loci,
and declined rapidly at \emph{HSP70} , but declined relatively slowly at
\emph{HSP22.0} , maintaining appreciable levels for several days.
Further, \emph{HSP70} exhibited no changes in H3K4me2, whereas H3K4me2
levels increased at \emph{HSP22.0} , but only at the later time points
of the experiment. These patterns of H3K4me2/3 and H3K9ac dynamics at
the \emph{HSP22.0} memory gene are reminiscent of the mechanism that
establishes transcriptional memory at some yeast genes, such as
\emph{INO1} , which encodes inositol-1-phosphate synthase. Inositol
starvation induces transcription of \emph{INO1} , which is accompanied
by increases in H3/H4 acetylation and H3K4 di- and trimethylation
(D'Urso et al., 2016). As memory is induced, levels of acetylated H3/H4
and H3K4me3 decline, whereas H3K4me2 levels persist. The shift in H3K4
methylation results from a remodeled version of the COMPASS complex that
catalyzes H3K4 mono- and demethylation, but not trimethylation.
Interestingly, the sustained accumulation of H3K4me2/3 at Arabidopsis
\emph{HSP22.0} required HSFA2, a transcription factor necessary for
heat-stress memory, but not heat-stress responses in naïve plants. These
findings support a model for plant transcriptional memory in which
stress-specific transcriptional activators such as HSFA2 bind memory
genes and help modulate H3/H4 acetylation and H3K4me di- and
trimethylation dynamics similar to those at yeast memory genes.

A recent study investigated the impact of cold stress on the chromatin
environment of potato by comparing maps of DNase I hypersensitive sites
(DHSs) for tubers stored at room temperature or cold
(4\textsuperscript{o}C) conditions (Zeng et al., 2019). DHSs are
indicative of relatively accessible genomic regions that contain active
cis-regulatory DNA elements. In response to cold stress, a large number
of DHSs were induced at genic regions associated with
temperature-responsive genes. Interestingly, the H3K4me3-H3K27me3
bivalent mark was present in the gene bodies of many of these genes, and
those that were up-regulated were linked to stress responses, whereas
those down-regulated were linked to developmental processes. This
suggests that the H3K4me3-H3K27me3 bivalent mark facilitates enhanced
accessibility during stress and allows for the recruitment of activators
or repressors in a gene-function dependent manner.

\textbf{6.3 Salt Stress}

Investigations of a number of stress-responsive genes in Arabidopsis
have shown that several chromatin marks impact the responsiveness of
ABA- and salt-induced genes. Both ABA and salt stress led to enrichment
of H3K4me3 and H3K9K14 acetylation, but decreased H3K9me2 at a subset of
ABA- and salt stress-responsive loci (L.-T. Chen, Luo, Wang, \& Wu,
2010). Mutation of \emph{HISTONE} \emph{DEACETYLASE}
\emph{6}(\emph{HDA6} ) led to increased H3 acetylation at
ABA/salt-inducible genes compared to wild type under control conditions.
In response to ABA, wild type, but not \emph{HDA6} mutants, exhibited
enriched H3 acetylation at ABA-induced loci. Interestingly, mutation of
\emph{HDA6}also abolished the enrichment of H3K4me3 exhibited at
ABA-induced genes in wild type. This suggests that H3 deacetylation by
HDA6 is necessary for H3K4me3 enrichment at ABA-induced loci. (L.-T.
Chen et al., 2010). Similarly, in soybean, three salt-stress inducible
genes encoding transcription factors showed induction in H3K4me3 and
reduction in both H3K9me2 and DNA methylation in response to salinity
stress (Y. Song et al., 2012).

A recent study by Zheng et al. (2019) showed that salt stress alters the
distribution of H3K4me3 in a tissue specific manner. In response to
salt, rice seedlings exhibited H3K4me3 decreases and increases in exons
and introns, respectively, whereas only exonic decreases in H3K4me3 were
observed in roots (Zheng et al., 2019). Notably, a chromatin state
defined by containing H3K3me3-H3K27me3 bivalent marks correlated with
both up- and down-regulated genes in seedlings, but only down-regulated
genes in roots. In potato tubers the H3K3me3-H3K27me3 bivalent mark was
enriched at genes both up- and down-regulated by cold stress (Zeng et
al., 2019). Together these observations may reflect a stronger and more
biased cessation of developmental processes in salt-stressed roots
relative to whole seedlings.

H3K4me3 association with salt stress was further demonstrated by
studying H3K4 demethylases in Arabidopsis (Shen et al., 2014). During
salt stress, \emph{JMJ15} expression increased, whereas \emph{JMJ14}
and\emph{JMJ18} expression decreased. Analysis of \emph{jmj15} mutants
showed a reduction in salt stress tolerance, whereas\emph{JMJ15}
-overexpression led to increased tolerance. Examination of global
H3K4me1/2/3 data showed that a majority of genes down-regulated by
\emph{JMJ15} -overexpression were marked with H3K4 di- and
trimethylation, but up-regulated genes did not show the same H3K4me2/3
bias. This suggests that JMJ15 represses gene expression at
salt-responsive genes via H3K4 demethylation.

\textbf{6.4 Submergence Stress}

In rice, submergence stress induced changes in the levels of H3K4
methylation at the submergence-inducible genes, \emph{ADH1}
and\emph{PDC1} (Tsuji et al., 2006). Specifically, during submergence,
the levels of H3K4me3 and H3K4me2 increased and decreased, respectively,
at both 5\selectlanguage{english}' and 3\selectlanguage{english}' genic regions. This finding suggests submergence
stress results in conversion of H3K4me2 to H3K4me3, which may recruit
Pol II and lead to increased transcript levels. In addition, during
submergence stress, the level of H3 acetylation showed a gradual
increase that occurred after the levels of Pol II and transcripts
increased. This suggests an important temporal interaction between H3
methylation and acetylation dynamics that modulates the response to
submergence stress.

\textbf{6.5 Nutrient Stress}

Studies investigating responses to phosphate (Pi) starvation and high
nitrogen have indicated a role for H3K4me3 in plant nutrient
homeostasis. A recent report on chromatin dynamics in Pi-starved rice
shoots showed that over 40\% of protein-coding genes exhibited a low-Pi
change in chromatin states (CSs) defined by differing levels of H3K4me3,
H2A.Z, and nucleosome occupancy at their TSS (Foroozani et al., 2019).
Genes marked by H3K4me3 and H2A.Z that exhibited decreases in both marks
in response to Pi starvation were enriched among low-Pi induced genes.
This suggests that combined loss of H3K4me3 and H2A.Z accompanies
de-repression of some Pi-starvation inducible genes. On the other hand,
genes marked by H3K4me3 and H2A.Z that exhibited a decrease in only
H3K4me3 were enriched among both up- and down-regulated genes. This
suggests a possible dual role of H3K4me3 in modulating expression of
this subset of Pi-responsive genes, of which a majority were linked to
cell wall and lipid remodeling pathways. A third subset of genes, which
included many translation-related loci including ribosomal protein
genes, suggested a pair of distinct CS transitions at the +1 and -1
nucleosomes. Under control conditions, these genes contained low H2A.Z
and high H3K4me3 at the -1 nucleosome, but high levels of both marks at
the +1 nucleosome. Pi starvation led to specific losses of H3K4me3 at
the -1 nucleosome and H2A.Z from the +1 nucleosome. Interestingly,
mutation of the yeast COMPASS component Spp1 results in substantial
decreases in global H3K4me3, but the genes that retain
disproportionately high H3K4me3 levels are enriched in ribosomal protein
genes and other translation-related genes (F. S. Howe et al., 2014).
This suggests that in rice, as in yeast, multiple COMPASS-like complexes
with different subunit compositions target distinct subsets of genes.

A role for H3K4me3 in Pi-starvation responses was also demonstrated in
Arabidopsis with the characterization of the \emph{ALFIN-LIKE
6}(\emph{AL6} ) gene, which encodes an H3K4me3-binding protein (W. Y.
Lee, Lee, Chung, \& Kwon, 2009). Mutation of \emph{AL6} resulted in a
pleiotropic phenotype including inhibition of low-Pi induced root hair
elongation (Chandrika, Sundaravelpandian, Yu, \& Schmidt, 2013).
Predicted targets of AL6 include \emph{ENHANCER OF TRY and
CPC1}(\emph{ETC1} ), which encodes a transcriptional activator of
Pi-responsive root hair elongation genes (Chandrika et al., 2013). Thus,
AL6 appears to regulate \emph{ETC1} through its interaction with H3K4me3
by promoting transcription elongation and/or mRNA maturation.

To maintain optimal nitrogen levels, plants repress root nitrate uptake
in response to high nitrogen conditions. The characterization of
the\emph{high nitrogen-insensitive 9} (\emph{hni9} ) mutant revealed
that\emph{HNI9} encodes INTERACT WITH SPT6 (IWS1), a conserved component
of the Pol II complex (Widiez et al., 2011). In response to high
nitrogen supply, the transcription of the \emph{NRT2.1} nitrate
transporter gene was repressed, which was associated with
HNI9/IWS1-dependent H3K27 trimethylation across the NRT2.1 locus from
promoter to 3' region. This increase in H3K27me3 coincided with a
decrease in H3K4 trimethylation across the gene body, but not at the
promoter, where H3K4me3 levels were unchanged. Recently, HNI9/IWS1 was
also shown to influence nitrogen homeostasis by modulating the
detoxification of reactive oxygen species (ROS) induced by high nitrogen
(Bellegarde et al., 2019). Mutation of\emph{HNI9} /\emph{IWS1} blocked
the high-nitrogen induction of a number of ROS-detoxification genes.
Interestingly, H3K4me3 levels were lower at these genes in the
\emph{hni9} mutant relative to wild type, whereas levels of H3K27me3,
H3K36me3, and H3K9ac were unchanged. This suggests that HNI9/IWS1
induces detoxification genes in order to quench high nitrogen-induced
ROS by facilitating H3K4me3 accumulation. HNI9/ISW1 is known to interact
with brassinosteroid-related factors that facilitate demethylation of
H3K27me3 and trimethylation of H3K36, thereby acting as a
transcriptional switch from a repressed to active state (Crevillen et
al., 2014; Y. Li et al., 2015; F. Lu, Cui, Zhang, Jenuwein, \& Cao,
2011). In a similar mechanism, HNI9/ISW1 may interact with factors to
increase the H3K4me3/H3K27me3 ratio at ROS detoxification genes in
response to high nitrogen.

\textbf{6.6 Biotic Stress}

In addition to a role for H3K4me3 in a number of abiotic stress
responses, this histone mark has also been implicated in responses to
biotic stress, particularly during plant-pathogen interactions. During
pathogen exposure, H3K4me3 levels have been shown to increase at
defense-related genes. For example, \emph{Botrytis cinerea} infection in
both Arabidopsis and tomato plants resulted in increased levels of
H3K4me3 at up-regulated genes (Alonso, Ramos\selectlanguage{english}-Cruz, \& Becker, 2019;
Roberts \& Sanchez, 2019). In contrast, the level of H3K4me3 was not
significantly altered at down-regulated genes.

Analyses of H3K4 methyltransferase and demethylases have further
demonstrated a role for H3K4me3 in plant defense responses.\emph{WRKY70}
, a transcription factor involved in plant defense responses, was shown
to be a direct target of ATX1, while also being positively regulated by
ATX1-generated H3K4me3 (Alvarez-Venegas, Abdallat, Guo, Alfano, \&
Avramova, 2007). Mutation of another Arabidopsis HKMT, \emph{ATXR7} ,
led to greater sensitivity to the pathogen, \emph{Hyaloperonospora
arabidopsidis} (Xia et al., 2013). A suppressor screen for the
\emph{suppressor of npr1} -\emph{1} ,\emph{constitutive 1} (\emph{snc1}
) mutant, which exhibits constitutive activation of plant defense
responses, identified \emph{modifier of snc1,9} (\emph{mos9} ). MOS9 was
shown to directly interact with ATXR7, and \emph{mos9} mutants exhibited
reductions in H3K4me3 and transcript levels at \emph{SNC1} and another
defense response gene,\emph{RECOGNITION OF PERONOSPORA PARASITICA 4}
(\emph{RPP4} ). Thus, interaction between MOS9 and ATXR7 induces
defense-related gene expression via H3K4me3 deposition (Xia et al.,
2013). Studies of two demethylases, Rice OsJMJ704 and Arabidopsis JMJ14,
indicate that demethylation of H3K4me3 can play different roles in plant
defense responses. Under \emph{Xanthomonas oryzae pv. Oryzae} (Xoo)
infection, transcription levels of \emph{OsJMJ704} were induced in rice
plants and\emph{osjmj704} mutants were more sensitive to Xoo infection.
The expression of negative defense regulator genes (\emph{NRR, OsWRKY62
and Os-11N3} ,) and the ratio of H3K4me2/H3K4me3 at these genes was
increased in the \emph{osjmj704} mutant, suggesting a positive role for
OsJMJ704 in rice bacterial defense by repressing negative
defense-related genes through regulation of H3K4me2/H3K4me3 levels (Hou
et al., 2015). In Arabidopsis, \emph{jmj14} mutants were more sensitive
to the Pst DC3000 bacterial pathogen. Under normal conditions, the
transcript levels of positive defense-related genes (\emph{PR1, ALD1,
FMO1, and WRKY70} ) were not significantly changed in \emph{jmj14}
mutants, but negative defense-related genes (e.g. \emph{SNI1} ) were
up-regulated. H3K4me3 levels in \emph{jmj14} and wild-type plants at
these genes positively correlated with the levels of gene expression;
induced \emph{SNI1} in\emph{jmj14} had higher levels of H3K4me3 at the
TSS, and positive defense-related genes showed no changes in either
transcripts or H3K4me3. After pathogen infection, the expression of
positive defense-related genes were induced to a lesser degree in
mutants compared to wild type, and H3K4me3 abundance at these genes was
lower in\emph{jmj14} mutants, suggesting JMJ14 is involved in H3K4me3
enrichment at specific genes during defense responses. Considering the
H3K4 demethylase activity of JMJ14, a positive role of JMJ14 in
enrichment of H3K4me3 at positive defense-related genes was unexpected.
The identification of JMJ14 interacting partners and the genes directly
targeted by JMJ14 during pathogen infection should help to resolve the
roles of H3K4me3 demethylases during defense responses (D. Li et al.,
2019).

Exogenous application of the phytohormone salicylic acid (SA), or
certain synthetic SA analogs, is sufficient to induce resistance to a
subsequent pathogen challenge, a phenomenon known as chemical priming
(Kohler et al., 2002). The priming of defense genes poises them for a
stronger transcriptional response to future pathogens relative to
non-exposed plants. Interestingly, H3K4me3 levels increase at some
defense genes during priming and persist after the removal of the
initial stress signal (Jaskiewicz et al., 2011). This is similar to the
transcriptional memory function described for trainable
drought-responsive genes (Ding, Fromm, et al., 2012). Priming is
negatively regulated by CHROMATIN ASSEMBLY FACTOR 1 (CAF1), which
appears to antagonize H3K4me3 deposition at the TSS of defense genes
(Mozgova et al., 2015a). Therefore, CAF1 may prevent ectopic defense
gene activation.

\textbf{7. H3K4me3 Interactions with other Chromatin Modifications}

A central aspect of H3K4me3 function is its interaction with other
factors, especially histone variants and other histone modifications.
Among them, the H2A.Z histone variant and H3K27me3 have been
well-studied and show distinct functional correlations with H3K4me3.
H2A.Z is a conserved variant among eukaryotes that plays multiple roles
in chromatin structure and gene expression (Jackson, Falciano, \&
Gorovsky, 1996; Jarillo \& Pineiro, 2015). Genome-wide analyses showed
that H2A.Z is preferentially associated with H3K4me3, while showing
partial association with H3K27me3, in rice shoots, callus, and seedlings
(Foroozani et al., 2019; K. Zhang et al., 2017). In addition, the
combination of H2A.Z with either H3K4me3 or H3K27me3 correlated with
differences in gene expression (K. Zhang et al., 2017). Co-localization
of H2A.Z and H3K4me3 in genic regions has also been demonstrated in
Arabidopsis (Dai et al., 2017; Sequeira-Mendes et al., 2014). On the
other hand, activity of enhancers was repressed by H2A.Z through
promoting H3K27me3 and antagonizing H3K4me3 deposition at enhancer
regions (Dai et al., 2017). Interestingly, Arabidopsis H2A.Z appeared to
facilitate H3K4 trimethylation at miR156 loci (Xu et al., 2018) but
antagonize it at some anthocyanin biosynthetic genes (Cai et al., 2019),
reflecting divergent and context-dependent interactions between H2A.Z
and H3K4me3.

In plants, Polycomb Repressive Complex 2 (PRC2) is a methyltransferase
responsible for the deposition of H3K27me3, which acts antagonistically
to H3K4me3 (Engelhorn et al., 2017; X. Zhang et al., 2009). Although the
distribution and interactions between these two modifications have been
investigated, a conclusive pattern remains elusive. Genome-wide analysis
of both marks within Arabidopsis seedlings seems to indicate a mutually
exclusive relationship (X. Zhang et al., 2009). However, when
considering specific dehydration stress-induced memory genes, H3K27me3
and H3K4me3 are found to be independent of one another, showing the
capability of occurring at the same gene at the same time (N. Liu et
al., 2014). Similarly, H3K4me3 and H3K27me3 have been found to
co-localize at bivalent domains in cold stress-responsive genes in
potato (Zeng et al., 2019), as well as in rice genes
differentially-expressed by ionizing radiation (Pan et al., 2017) or
salt stress (Zheng et al., 2019). In each case, the correlation existed
for both up- and down-regulated genes, consistent with H3K4me3/H3K27me3
bivalent domains allowing for greater access of transcriptional
regulators (i.e. activators or repressors) in response to stress. Our
recent work in rice suggests that H3K4me3/H3K27me3 bivalent nucleosomes
also interact with H2A.Z to modulate both up- and down-regulation of
phosphate-starvation response genes (Foroozani et al., 2019). In
addition to modulating responses to stress, H3K4me3-H3K27me3 bivalent
domains also play a role in developmental processes in Arabidopsis,
including gametophyte development (Berr et al., 2010), flowering time
regulation (Qian et al., 2018), and seed germination (Molitor, Bu, Yu,
\& Shen, 2014), and possibly in xylem tissue development
in\emph{Eucalyptus grandis} (Hussey, Mizrachi, Groover, Berger, \&
Myburg, 2015).

In addition to associations with other histone modifications and histone
variants, H3K4me3 function is influenced by DNA methylation. Three DNA
methylation pathways exist in plants to methylate DNA in distinct
sequence contexts: CG, CHH, and CHG (X. Zhang et al., 2009). In
Arabidopsis, CHG and CHH methylation were depleted in H3K4
mono/di/trimethylated genomic regions, whereas CG methylation was
enriched at H3K4me1 regions (X. Zhang et al., 2009). The mutually
exclusive relationship between DNA methylation and H3K4me2/3 was further
demonstrated in studies of demethylase mutants. In \emph{jmj14} plants,
genes targeted by the RNA-directed DNA methylation (RdDM) pathway, which
is responsible for de novo DNA methylation and maintenance of CHH and
CHG methylation, exhibited reduced DNA methylation and elevated H3K4me3
levels (Deleris et al., 2010). Also, target genes of LDL1 and LDL2
demethylases exhibited increased expression and decreased non-CG DNA
methylation in \emph{ldl1} \emph{ldl2} double mutants (D. Jiang et al.,
2007). Compared to the \emph{ldl1} \emph{ldl2} double mutant,
a\emph{jmj14} \emph{ldl1} \emph{ldl2} triple mutant showed an even
greater reduction in DNA methylation, which was accompanied by increased
levels of H3K4me2/3 (Greenberg et al., 2013). Together these studies
indicate that H3K4me3 influences gene expression, in part, by
antagonizing CHG and CHH methylation.

\textbf{8. Concluding Remarks}

The distribution of H3K4me3 at genic regions, particularly at the 5' end
of genes, is conserved among species and implicates this histone
modification in the regulation of gene expression. Based on evidence
from a number of studies, H3K4me3 plays key roles in development and
stress responses in plants. Elucidating the extent to which H3K4me3
directly regulates a given biological pathway, and by what mechanisms,
has been challenging, although some patterns have emerged. The formation
of the ATX1-containing COMPASS-like complex at the promoter is important
for transcription initiation, whereas H3K4me3 deposited at the
promoter-proximal and gene body regions facilitates transcription
elongation and mRNA maturation, which are influenced by the breadth of
H3K4me3 distribution. Therefore, ATX1 and H3K4me3 likely play important
roles in the fundamental aspects of transcription for numerous genes.
The expression of many genes is sensitive to developmental and/or
environmental cues, and H3K4me3 also plays a role in integrating these
signals. In particular, H3K4me3 associated with H3K27me3 in bivalent
domains modulates expression of many genes that regulate developmental
transitions, such as flowering (e.g. \emph{SOC1} and \emph{FLC} ), shoot
maturation (e.g. \emph{MIR156A} and \emph{MIR156C} ), and gametophyte
development (e.g. \emph{SPL} /\emph{NZZ} and \emph{MS1} ). Notably, the
SHL protein exhibits dual recognition of both H3K4me3 and H3K27me3, and
likely functions during many developmental transitions. H3K4me3-H3K27me3
bivalent domains serve as an integrator of not only developmental cues
but also environmental signals. Although possibly a central part of
virtually all stress-response pathways, H3K4me3-H3K27me3 bivalent
domains have been shown to influence stress-responsive genes related to
cold stress, ionizing radiation, and salt stress. Finally H3K4me3
dynamics have been linked to transcriptional memory of stress-responsive
genes related to drought and heat stress, as well as transcriptional
priming of pathogen-responsive genes. As with H3K4me3-H3K27me3 bivalent
domains, H3K4me3-mediated memory is likely to be fundamental to many
environmental stressors. As sessile organisms with sophisticated
signaling networks that guide developmental processes and stress
adaptations, plants represent an ideal system for further investigation
into H3K4me3-dependent transcriptional and memory phenomena. Future
studies can be strengthened by a number of considerations, including the
use of single cell types, quantification of many marks simultaneously,
particularly H3K4me2, H3K4me3 and H3K27me3, and at multiple genic
regions, as well as temporal examination at conditions before, during,
and after reversal of the stimulus. The continued identification and
characterization of binding partners of HKMTs and JMJs, as well as
factors that confer target-gene specificity are also necessary. These
efforts will shed light on key unanswered questions such as the extent
to which H3K4me3-mediated mechanisms are causal or effectual, and
whether these mechanisms exhibit differences among diverse environmental
stressors, distinct cell types, and different species.

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