TRPLSC 1805 No.

of Pages 16

Trends in Plant Science

Review

Coordination of ABA and Chaperone Signaling

in Plant Stress Responses
Victor P. Bulgakov, 1,2,* Hui-Chen Wu, 3 and Tsung-Luo Jinn 4

The abscisic acid (ABA) and chaperone signaling pathways are the central regu- Highlights
lators of plant stress defense. Despite their significance and potential overlap, The ABA signaling systems is the central
these systems have been described separately. In this review, we summarize regulator of plant stress defense and
contributes to the generation of plant
information about mechanisms by which the ABA and chaperone signaling path-
memory to abiotic stress. The interaction
ways might be coregulated. The central factors that join the ABA and chaperone of ABA signaling with SWI/SNF
signaling systems are the SWI/SNF chromatin-remodeling proteins, which are in- chromatin-remodeling factors is impor-
volved in stress memory. A benefit from coordination is that the signals sensed tant for establishing plant stress memory.

through both the ABA and chaperone signaling systems are perceived and SWI/SNF chromatin-remodeling factors
stored via chromatin-remodeling factors. For improving plant stress resistance, are considered among the main compo-
we propose new bioengineering strategies, which we term ‘bioengineering nents of chromatin-modifying mecha-
memory’. nisms in all eukaryotes. These factors
ensure dynamic epigenetic mechanisms
that control gene expression and induce
stress memory. Chaperones sense the
Interaction of the Two Main Stress-Responsive Subnetworks epigenetic environment and play an
Heat stress is considered to be the main factor that affects crop production [1]. Cold stress important role in this process.
also limits agriculture in many regions, and combinations of multiple stresses, including heat,
excessive light and lack of water, or cold and lack of water, affect crop productivity. Excessive
hydration that consequently floods crops also plays a significant role. For these situations, bioen-
gineering strategies are developed to improve plant resistance for individual types of stress and
multiple stresses [2]. However, these strategies are not based on a complete picture of stress
regulation, which involves a combination of different signaling pathways. We do not know the
impact of different signaling pathways on acute, chronic, or recurring stress exposure, and little
is known about transgenerational stress memory (see Glossary), although research in
these areas is now receiving a lot of attention [3,4]. Two main signal transduction pathways,
the abscisic acid (ABA) and heat shock protein (HSP)/chaperone pathways, have been studied
intensively in recent years in order to identify approaches that improve stress tolerance.
1
Federal Scientific Center of the East
The ABA signaling pathway includes hierarchically coordinated levels of regulation. Stress Asia Terrestrial Biodiversity (Institute of
induces ABA accumulation and binding to its receptors of the PYL family to inhibit protein Biology and Soil Science), Far Eastern
phosphatases 2C (PP2Cs). PP2C inactivation activates class 3 sucrose nonfermenting-1- Branch of the Russian Academy of
Sciences, 159 Stoletija Str., Vladivostok,
related protein kinases (SnRK2s), which phosphorylate ABA-responsive element binding factors 690022, Russia
(ABFs). Activated ABFs initiate expression of responsive genes by binding to the cis-acting ABA 2
Far Eastern Federal University,
response element (ABRE) [5–10]. Sukhanova Str. 8, 690950, Vladivostok,
Russia
3
Department of Biological Sciences and
The chaperone signaling system seems to be more complicated. With regards to stress, it com-
Technology, National University of
prises predominantly HSP/heat-shock factors (HSFs), and peptidyl-prolyl cis-trans isomerases Tainan, Tainan 70005, Taiwan
4
(PPIase), also called immunophilins [11–15]. The functional diversification of HSFs has been Department of Life Science and
Institute of Plant Biology, National
described in detail [2,16–21]. In brief, the transcription factors HsfA1abd and e (HsfA1s) activate
Taiwan University, Taipei 10617, Taiwan
the heat-stress response (HSR) by complex interaction with downstream HSFs. HsfA1s not only
ensure the basal thermotolerance but also initiate the acquisition of thermotolerance. HsfA1s bind
to heat-stress elements (HSEs) to activate transcription of HSP and HSF genes, mainly HsfA2, *Correspondence:
HsfA3, and HsfA7a, which collectively maintain a strong HSR during repetitive stress. Initially bulgakov@ibss.dvo.ru (V.P. Bulgakov).

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© 2019 Elsevier Ltd. All rights reserved.
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described as related to heat stress, the chaperone signaling system is presently considered to be Glossary
linked to multiple stresses. At the level of gene transcription, ABA and HSF signaling have intrinsic BRM: SWI2/SNF2-type ATPase;
regulatory relationships [2,19,21], but at the level of protein–protein interactions, these links have central subunit of SWI/SNF complex.
just started to be explored. Here, we present a systematic study of these relationships (Box 1). BSH: SNF5-type core subunit of
Arabidopsis SWI/SNF.
Epigenetic landscape: an integrated
Significant progress has been achieved in the investigation of epigenetic regulation of stress
state of epigenetic modifications
responses, including DNA methylation, ATP-dependent chromatin remodeling, histone modifica- determined by developmental cues and
tion, and long noncoding RNAs [1,3,4]. In this review, we will concentrate on the role of environmental influences.
chromatin-remodeling factors. Chromatin-remodeling proteins exploit energy derived from ATP Epigenetic mechanism: a stable and
heritable (through cell divisions) change
hydrolysis to change the accessibility of the core DNA; they can form 11 potential SWI/SNF
in gene expression that is independent
core complexes, the so-called SWI/SNF chromatin-remodeling complexes (CRCs) [17,18]. In of DNA sequence changes.
plants, SWI/SNF CRCs play a critical role in transcriptional control of growth, developmental Priming: phenomenon through which a
processes, and stress responses [4,22–37]. SWI/SNF CRCs regulate hormone signaling transient stress cue leads to modified
defense responses upon exposure to a
pathways [23] and control the RNA-mediated transcriptional silencing [37].
recurring stress.
Stress memory: phenomenon through
Connecting Two Main Stress-Responsive Subnetworks which information on a past stress cue is
SNF2/BRAHMA-type Chromatin-Remodeling Proteins Join Two Main Stress-Responsive retained and results in a modified
Subnetworks response upon a recurring stress.
SWI/SNF CRC: switch/sucrose
We analyzed the information about protein–protein interactions to identify proteins that could
nonfermenting; ATP-dependent
connect the ABA and chaperone signaling subnetworks. We found such interactions between chromatin-remodeling complex.
PP2Cs and SWI3B, HSFs and SWI3B, BRM and SnRK2.2/2.3 kinases, and HsfA1d and SYD: SWI2/SNF2-type ATPase; central
MUTE (Figure 1). The potential role of the bHLH transcriptional factor MUTE (which is a potent subunit of Arabidopsis SWI/SNF.
Transcriptional memory: sustained
inducer of stomatal differentiation) in stress response is described below. Here we will differential response in gene expression
concentrate on the SWI/SNF chromatin-remodeling proteins, which emerge as virtually the only after an exogenous cue. Transcriptional
candidates for network joining. memory can be evident from either
sustained changes in expression or from
a modified response after a second cue.
Several Scenarios of Interpathway Regulation
Transgenerational stress memory: a
We propose three models of ABA and HSF signaling integration through SWI/SNF (Figure 2B, stress imprint that extends from one
Key Figure). The links ABA → SWI/SNF CRC and ABA ↔ SWI/SNF CRC are well documented. stressed generation of organisms to at
Saez et al. [25] were probably the first group to describe the interaction of SWI/SNF chromatin- least the first stress-free offspring
generation.
remodeling proteins with ABA signaling. They identified the physical interaction of HAB1
and SWI3B in the nucleus and showed that HAB1 regulates a SWI/SNF complex targeted to
ABA-responsive promoters. Han et al. [28] discovered that plants with mutated BRM acquired
ABA hypersensitivity and increased drought resistance. BRM repressed ABI3 and ABI5 expres-
sion, depending on the growth phase. The authors suggested that the physiological role of BRM
is to help plants avoid stress responses in the absence of stress. BRM is considered a key
element in determining the allocation of resources between drought tolerance and growth [28].

Peirats-Llobet et al. [33] showed that components of the ABA signaling pathway, such as PP2Cs
and SnRK2s, physically interact with BRM and control its activity by (de)phosphorylation. BRM
is located downstream of SnRK2s in the signaling pathway. BRM phosphorylation by SnRK2s

Box 1. Visualizing Protein–Protein Interactions

To help the reader more clearly understand the protein–protein interactions discussed in this review, we have visualized the
interactions using the program Cytoscape [78], as previously described [68]. The data loaded into the program were
obtained from PAIR version 3.3 [79] (http://www.cls.zju.edu.cn/pair/). The protein–protein interactions presented in PAIR
were supplemented with data from BioGRID [80] (http://thebiogrid.org/), UniProtKB (https://www.uniprot.org/), TAIR [81]
(https://www.arabidopsis.org/), IntAct (https://www.ebi.ac.uk/intact/interactors/), and STRING (https://string-db.org/)
databases. These studies are necessary for the development of any complex networks of protein interactions, since it is
impossible to keep the interaction in memory without visualization. The STRING database also provides possible
protein–protein interactions (shown in Figure 1 in main text as dashed lines); this database is often used in the analysis
and prediction of poorly studied protein modules.

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Figure 1. General View of the Network that Joins the ABA and HSP/Chaperone Signaling Systems. The bottom left is the ABA signaling system (protein
kinases highlighted in light blue and ABF proteins in rose); the HSP/chaperone system is presented at top right. The central module that joins both systems is BRM-
SWI3B-SWI3C. Besides ABA- and chaperone-related proteins, this module is connected with numerous proteins presented in Table 1. The connectivity of the network
with other signaling systems is also presented: with auxin signaling (via ETT, ARF18, and IAA11), calcium signaling (via CRK1), and light signaling (PHYB, CO, and
RHL41). Unbroken lines represent protein–protein interactions presented in PAIR, IntAct, and BioGRID, and dashed lines represent possible interactions taken from
STRING. Dotted lines represent transcriptional regulation. Red lines show inhibition as a result of protein–protein interactions (see also details in Figure 2).
Abbreviations: ABA, abscisic acid; ABFs, abscisic acid responsive elements-binding factors (short name: ABRE-binding factors); ABI5, protein abscisic acid-insensitive
5; BRM, ATP-dependent helicase BRAHMA; CO, CONSTANS; CRK1, CDPK-related kinase 1; DREBs, dehydration-responsive element-binding proteins; HOS1, E3
ubiquitin-protein ligase HOS1; HSFs, heat-shock factors; HSPs, heat-shock proteins; ICE1, inducer of CBF expression 1; MUTE, transcription factor MUTE; NAC032,
NAC domain containing protein 32; PHYB, phytochrome B; RHL41, high light responsive zinc-finger protein ZAT12 (synonym: zinc finger protein ZAT12); SnRK2s,
sucrose nonfermenting related protein kinases 2; SWI3A, SWI/SNF complex subunit SWI3A; SWI3B, SWI/SNF complex subunit SWI3B; SWI3C , SWI/SNF complex
subunit SWI3C; ZF2, zinc-finger protein 2.

releases BRM-mediated repression of ABI5 expression, whereas PP2C-mediated BRM dephos-

phorylation maintains the repressive function of BRM on ABA response [33]. ABA promotes shut-
tling of the E3 ubiquitin ligase RGLG1 to induce degradation of nuclear PP2CA [38]. Additionally,
nuclear localization of PYL8 is induced by ABA, and this receptor inhibits several PP2Cs [8].
Therefore, non-cell autonomous and ligand stabilization-based mechanisms targeted to inhibit
nuclear PP2C activity can further contribute to plant stress memory. In general, these findings
mean that ABA responses are linked to dynamic chromatin changes that can be mitotically
heritable. In most cases, the model ABA ↔ SWI/SNF CRC is probably working.

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Key Figure
SWI/SNF CRC, ABA, and Chaperone Signaling.

Trends in Plant Science

Figure 2. (A) Generalized presentation of signaling pathways that combine ABA and chaperone signaling systems. In nonstress conditions, PP2C (A-type
protein phosphatases) block activity of SnRK2 (class 3 sucrose nonfermenting-1-related protein kinases) that prevents ABA pathway activation. A stress
signal induces the ABA pathway via PYR/PYL ABA receptors and SnRK2-mediated phosphorylation of ABF/AREB transcription factors that activate
downstream gene expression through the cis-acting ABA response element (ABRE). These core ABA signaling components, including PYR/PYL ABA recep-
tors, clade A PP2Cs, and SnRK2s, play roles in controlling chromatin regulatory proteins. SnRK2 phosphorylates BRM to release BRM-mediated repression
of ABI5 expression, whereas PP2C-mediated BRM dephosphorylation maintains the repressive function of BRM on ABA response. AREB/ABF transcription
factors (such as ABF1, ABF2, ABF3, and ABF4; see Figure 4 and Table 1) in turn interact with BRM and SWI3C chromatin-remodeling proteins at the DNA
template. Cis-regulatory modules perform their function by integrating active transcription factors [such as ABFs, dehydration-responsive element-binding
(DREB) proteins, and HSFs] on the DNA templates that carry ABRE, DRE, and HSE (heat shock element). For cooperation of these response elements,
see also [2]. BRM maintains high occupancy of the + 1 nucleosome to instruct time-dependent transcription [28]. As a result, nucleosomes are displaced
in the coding region and RNA Pol II starts transcription. Thus, the SWI/SNF CRC can integrate ABA and chaperone signals to generate appropriate con-
ditions for transcription of response genes. The mechanism for generating memory through these interactions may be realized via the ABA pathway [52],
where ABREs recruit the SWI/SNF CRC to the chromatin template via ABFs, and via the HSF interaction with SWI/SNF CRC, histone-modifying enzymes,
and other cofactors (as described for eukaryotic models by [40]). (B) Possible signal transmission pathways. Abbreviations: ABA, abscisic acid; ABFs, abscisic acid
responsive elements-binding factors (short name: ABRE-binding factors); BRM, ATP-dependent helicase BRAHMA; CRC, chromatin-remodeling complex; HSF,
heat-shock factor.

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With regards to potential SWI/SNF CRC → HSF or SWI/SNF CRC ↔ HSF signaling, the picture
is more complex and almost unknown for plants. The SWI/SNF CRC–HSF interactions
(e.g., SWI3B–HsfA3) was revealed by Efroni et al. [30] using the two-hybrid assay. Reyes [32]
pointed to the importance of these observations and the need for their in vivo experimental
confirmation, but so far, no new data have been published. Thus, we need to examine research
in non-plant models to adapt the knowledge to plants.

In Caenorhabditis elegans, the chromatin-remodeling factor ISW-1 is involved in controlling

nuclear and mitochondrial stress and integrates organism responses through chromatin re-
modeling [39]. In the author’s model, different stressors reorganize the epigenetic landscape
to modulate transcriptional programs. Miozzo et al. [40] provided a detailed analysis of the
relationship between SWI/SNF CRCs and HSFs and noted that HSFs play a pivotal role in
rearranging the epigenetic landscape. In yeast, flies, and mammals, HSF1 contributes to
reshaping the chromatin environment on HSP genes by interacting with SWI/SNF remodeling
complexes, histone-modifying enzymes, and other factors. Upon heat stress, HSF1 recruits
and attracts an SWI/SNF remodeling complex to the DNA template to allow transcription of
HSP genes [40].

The presence of dynamic nucleosomes upstream of the transcription start site is coordi-
nated by both chromatin-remodeling proteins and so-called pioneer factors (a subset
of transcription factors that remains bound to mitotic chromatin during cell division [41]. In
animals, HSF1 and HSF2, as pioneer factors, are involved in the initiation of embryogenesis
and cell reprogramming. HSF2 mediates memory of past stress exposure through cell
generations [40]. In our opinion, the term ‘rearranging the epigenetic landscape’ is a key
to understanding how chromatin regulatory proteins work to integrate the ABA and chaper-
one systems.

Considering the ancient origin and high conservation of chromatin remodelers, as well as the
HSF/HSP chaperone machinery in different living organisms, the most realistic integration
model appears to be: ABA ↔ SWI/SNF CRC ↔ HSF. If we accept this model, we can attempt
to explain how it works by the process known as ‘stress memory’ or ‘priming of organismal
responses to stress’. Priming plant responses to stress describes the phenomenon by which a
short-term stress stimulus modifies a plant for future stress exposure [4].

How Do SWI/SNF CRCs work?

The chromatin-remodeling mechanism was explained in most detail for yeast (Saccharomyces
cerevisiae). The fundamental units of chromatin are the nucleosomes, which consist of histone
octamers (histones H2A, H2B, H3, and H4), around which a 147-bp fragment of DNA is wrapped
in almost two turns. Binding of the yeast chromatin-remodeling complex (RSC) to the nucleo-
some releases the DNA from the histone surface and initiates DNA translocation. Further ATP
binding completes translocation and ATP hydrolysis reorganizes the system [42]. RSC primarily
translocates DNA around the nucleosome. At the sites where DNA enters the nucleosome,
the DNA moves along its canonical wrapping path. Therefore, the movement of DNA across
the nucleosome is directly linked to DNA translocation by the ATPase at its binding site inside
the nucleosome [43].

It should be noted that chromatin regulators stochastically instruct time-dependent control of

transcription (so-called ‘duration-dependent fractional control’), whereas transcription factors
ensure their function in a graded and nonrandom manner [44]. Target gene transcription may
be dependent on short, repetitive cycles of nucleosome mobilization that reduces transcriptional
noise and ensures a homogeneous response of a cell population to stress [45].

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These events allow chromatin remodelers to control the expression levels of a number of target
genes. BRM occupies numerous sites in Arabidopsis genome (Arabidopsis thaliana) [46] and
has overlapping roles with other chromatin-remodeling proteins. Nevertheless, BRM is a specific
regulator of transcription and controls the expression of a relatively small number of targets [22].
Unfortunately, CRC formation in plants is only beginning to be studied and their functional role is
unknown for different stress types [32].

BRM and SYD are the best-described chromatin remodelers in plants. In Figure 3, we present a
set of plant chromatin remodelers, including BRM, SYD, SWI3A, SWI3B, SWI3C, SWI3D, and
BSH, joined in a small network. Of these, BRM, SWI3B, and SWI3C are involved in defense reac-
tions against abiotic stress. SYD and BRM have overlapping functions [22] but regulate specific
stress signaling pathways. SYD is involved in biotic stress response [36] but has not been clearly
linked to abiotic stress. The S1760 and S1762 residues of BRM, located between the C terminal
bromodomain and AT-hook, and required for interaction with acetylated histones, were identified
as putative SnRK2 phosphorylation sites [33]. BRM is required to maintain high occupancy of
the + 1 nucleosome at the 5′ region of the ABI5 locus, but BRM is not involved in ABA-
dependent restructuring the –1 nucleosome at promoters of the ABA response genes [28,30].

Basic HSF Mechanisms and Acclimated State

Under nonstress conditions, HSPs repress HsfA1 activity. Heat shock activates HsfA1s and
induces transcription factor expression, including dehydration-responsive element-binding 2A
(DREB2A), multiprotein bridging factor 1C (MBF1C), and HSFs, to regulate heat-stress-
inducible gene expression. The complex interaction between these factors is necessary to fine-
tune tolerance to abiotic stress responses, especially to heat stress [2,20,47]. After the stress
stimulus, the expression of HSFs and HSPs is different from the background. The quantity and
the type of HSFs and HSPs determine the acclimated status [2].

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Figure 3. Connectivity of the SWI/SNF Chromatin-Remodeling Proteins as Presented in the PAIR (Unbroken
Lines) and STRING Databases (Dashed Lines). BRM and SYD are SWI/SNF-type SNF2-ATPases, BUSHY (BSH) is a
SNF5-type protein, and SWI3A, B, and C are SWI3-like proteins. In total, 11 SWI/SNF CRCs can be potentially formed [22].
Each CRC consists of the central chromatin-remodeling ATPase (SYD or BRM), two SWI3 subunits (SWI3), and one SNF5
subunit (BSH) [22,23]. For BRM, three core complexes are possible: BRM-BSH-SWI3B/SWI3C, which is the most likely
candidate for combining ABA and chaperone signaling systems (links between these proteins are highlighted with red
lines), BRM-BSH-SWI3A/SWI3B, and BRM-BSH-SWI3A/SWI3C. Note that the interactions marked with dashed lines
indicate data on coexpression and interaction of putative homologs in other species. Abbreviations: ABA, abscisic acid;
BRM, ATP-dependent helicase BRAHMA; BSH, chromatin structure-remodeling complex protein BSH; CRC, chromatin-
remodeling complex; SYD, chromatin structure-remodeling complex protein SYD.

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HsfA3 and HsfA6a

In contrast to yeast, flies, and mammals, Arabidopsis HsfA1s do not cooperate with CRC pro-
teins (at least, such interactions have not been described yet). Since HsfA3 and HSFA6a proteins
are located in the center of the constructed network, which joins chromatin-remodeling factors
with ABA and chaperone signaling (Figure 1), we will describe these HSFs in more detail. Both
proteins interact physically with three main factors, namely BRM, SWI3B, and SWI3C.

HsfA3 transcript levels increase under heat stress and excessive light, and an hsfA3 mutant
reduces thermotolerance, while HsfA3 overexpression increases thermotolerance [48]. Heat
shock induces HsfA3 transcription through DREB2A, and HsfA3, in turn, regulates HSP gene
expression [49]. HsfA3 is one of the crucial factors regulating ascorbate peroxidase 2 (APX2)
expression in diverse stress conditions [48,50]. HsfA3-overexpressing transgenic plants exhibit
increased oxidative stress tolerance [51]. Reactive oxygen species (ROS) induces HsfA3 tran-
scription in seedlings, a finding that indicates the involvement of HsfA3 in ROS metabolism and
detoxification.

In Arabidopsis, HsfA6a expression is low and induced by ABA, salt, and water deficit; in turn,
the plants, overexpressing HsfA6a, show activation of various defense genes [21]. The HsfA6a
gene acts as activator of stress-responsive genes via the ABA signaling pathway because
ABRE-binding proteins regulate HsfA6a expression [21]. Likewise, the closest homolog of
HsfA6a, HsfA6b, is also involved in the ABA-dependent signaling pathway [19]. HsfA3 and
HsfA6s are potent activators of HSP genes [19,21,49]. Overall, both HsfA3 and HsfA6s are
uniquely involved in stress reactions, but their role in interaction with chromatin remodelers
is not clear. Considering the data from yeast, flies, and mammals [40], we propose a similar
mechanism in Arabidopsis. According to this mechanism, interactions between HSFs, such as
HsfA6a and HsfA3, and chromatin remodelers could harmonize the chromatin changes that
drive HSF-mediated activation of HSP genes.

The Significance of Chromatin Remodelers in the Cooperation of ABA and

Chaperone Regulatory Mechanisms
Chromatin remodelers appear to be significant in the coordination of ABA and chaperone
defense mechanisms through memory generation. One manifestation of memory is a modified
transcriptional response, during which the priming stimulus induces sustained changes in gene
expression. Other mechanisms include post-translational mechanisms that influence SWI/SNF
CRC protein stability or protein modifications [4]. Apparently, all these mechanisms can play a
role in ABA ↔ SWI/SNF CRC ↔ HSF interactions.

Such cooperation provides a significant benefit in that the signals sensed through ABA and chap-
erone signaling systems can be perceived, stored, and later retrieved via chromatin-remodeling
factors (Figure 4). It is easy to see that changes in BRM and SWI3B conformation or modification,
mediated by interactions with SnRK2s/PP2Cs or ABRE-binding factors ABF/AREB, as well
as HSFs, will ultimately lead to changes in gene expression of the same HSFs, in addition to
downstream responsive genes, including DREB2A. It is noteworthy that self-regulating loops
might be established, such as HsfA3-HsfA6a → DREB2A → HsfA3. This loop, or others
that are yet unknown, will work under different backgrounds (different dynamics of chromatin
modification), depending on the accumulated memory. The summarized picture of ABA and
chaperone system integration is presented in Figure 2.

This scenario is most realistic, considering the data from plants and animals. Virlouvet et al. [52]
found that the SnRK2 and ABF/AREB factors of the ABA signaling pathway are necessary but

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Figure 4. Protein–Protein Interactions and Transcriptional Regulation at the Core of the ABA ↔ SWI/SNF
CRC ↔ HSF Module. SWI3C was not shown to simplify the figure. Unbroken and dashed lines represent physical
protein–protein interactions and dotted lines represent transcriptional regulation. ABF/AREB proteins specifically bind to
the HsfA6s (HsfA6a and HsfA6b) promoters and positively regulate HsfA6s transcription [19,21]. In turn, HsfA6s activates
transcription of genes that encode dehydration-responsive element binding proteins, such as DREB2A [19,21]. Further,
DREB2A induces HsfA3 transcription [49] with subsequent HSP activation. BRM and SWI3B interact with HSFs (HsfA6a
and HsfA3). At the same time, BRM and SWI3B interact with different components of the ABA signaling pathway that
indicates two levels of regulation at the interface of SWI/SNF chromatin-remodeling proteins and ABA signaling. The first
level of regulation is post-translational modification of the SWI/SNF proteins by (de)phosphorylation; the second level is the
change in SWI/SNF protein conformation by physical interaction with ABFs and HSFs. Abbreviations: ABA, abscisic acid;
ABFs, abscisic acid responsive elements-binding factors; ABI1, protein phosphatase 2C 56; ABI2, protein phosphatase
2C 77; BRM, ATP-dependent helicase BRAHMA; DREB2A, dehydration-responsive element-binding protein 2A; HAB1,
protein phosphatase 2C 16; HSFs, heat-shock factors; HSPs, heat-shock proteins.

not sufficient for the transcriptional memory during dehydration stress; they searched for
an unknown component. RD29B was used as a marker memory gene. They showed that ABA,
or an initial dehydration stress, primes a memory factor and hypothesized that ABF2, ABF3, and
ABF4 recruit the transcriptional memory components to the chromatin template [52]. The authors’
hypothesis came very close to our model, since they considered protein modification and protein
interaction with unknown memory factors as essential processes in the priming memory response.
BRM, SWI3B, and SWI3C are best suited for such memory factors.

Studying transcriptional activities of the ‘revised-response’ memory genes during dehydration

stress (expression of these genes are different during the first and second stress signals), Liu
et al. [53] proposed the existence of an ABA-independent memory mechanism for revised-
response transcriptional behavior. They showed that ABF/AREB factors were not sufficient to

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induce revised-response memory genes [53]. The authors concluded that transcriptional
activities of a given transcription factor are insufficient to predict the transcriptional activity of its
target genes under repeated stress.

Considering the Drosophila Polycomb/Trithorax system as a basis for reconstruction of similar

mechanisms in plants, Buzas [54] proposed that histone modification (trimethylation of lysine
27 on histone H3; H3K27me3) confers dehydration stress memory and manifests peculiar
RD29B expression. Since there were no substantial changes in H3K27me3 at the RD29B
locus during dehydration treatments [53], and considering the observation that swi3b mutants
show reduced RD29B expression [25], we tend to favor the chromatin-modifying mechanism
realized through SWI3B.

Similar chromatin-modifying mechanism exists in animals, where heat acclimation-mediated

cross-tolerance (HACT) is based on both post-translational histone modification and altered
levels of chromatin modifiers [55]. Dynamic epigenetic mechanisms that control gene expres-
sion induce HACT and acclimation memory, and HSPs play an important role in this process.
Although SWI/SNF CRCs are considered among the main components of chromatin-modifying
mechanisms in all eukaryotes, the majority of the attention and publications are devoted to
post-translational histone modification. It is now generally accepted that these mechanisms
work in a coordinated manner to provide the necessary chromatin assembly.

The Role of PPIases in Stress Memory

Immunophilins constitute a large family of proteins that possess PPIase activity and include such
classes as cyclophilins, FK506-binding protein class (FKBPs), and parvulins [56,57]. Certain
immunophilin-drug (cyclosporins and FK506) complexes block T cell activation in animals,
showing immunosuppressive activity. They perform diverse functions in plants through their
foldase, scaffolding, and chaperone activities. In both plants and animals, cyclophilins alter
gene transcription by changing chromatin structure via recruiting chromatin- and histone-
modifying enzymes [15].

It has been previously noted that little is known about the functional connection of chaperones,
such as HSPs and PPIases in plants [58], although in animal and human studies these investiga-
tions are of high importance [14]. Do these connections have the same importance for plant
biology and, in particular, for understanding the development of stress resistance and stress
memory?

Meiri and Breiman [11] discovered the important role of the ROF1 rotamase, a FK506-binding-
protein class PPIase, in thermotolerance modulation by interaction with Hsp90.1 and accumula-
tion of HsfA2-regulated small HSPs. The role of ROF1 has been proposed in thermotolerance
prolongation. A homologous rotamase, ROF2, joins the complex ROF1-Hsp90.1-HsfA2 via
interaction with ROF1 and participates in long-term acquired thermotolerance [59]. It is interesting
to note that HsfA2 interacts with Hsp90.1 but not with ROF1 [11]. The physical interaction HsfA2-
ROF1, with a reference to this article, is shown in the STRING database. However, ROF1 interacts
only with the HsfA2-Hsp90.1 complex [11]. ROF2 overexpression confers tolerance to intracellu-
lar acidification. Since intracellular acidification is a common consequence of many stresses,
the mechanism by which ROFs modulate pH homeostasis may be necessary for stress resis-
tance [60].

Animal data confirm the involvement of PPIases in HSP regulation. Immunophilins (FKBPs and
cyclophilins) participate in the assembly of the Hsp90-receptor complex. FKBP52 replaces
FKPB51 in activated receptors and promotes translocation to the nucleus. Further, the complex

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Trends in Plant Science

dissociates, and the hormone receptor binds DNA and regulates transcription [15]. In turn,
FKPB51 expression is regulated by the SWI/SNF complex BRM subunit in human cultured
cells [61]. It will be interesting to see whether immunophilin interactions with other proteins in
plants can be regulated in a ligand-dependent manner or by receptor complexes, as in mammals
(such possibility provides an additional regulatory level of stress memory). There are examples of
such regulations by 12-oxo-phytodienoic acid [62] or through the NLR family immune receptors
[63]; but in general, these studies are just beginning [13].

In principle, the involvement of cyclophilins and FKBPs in stress defense reactions is well docu-
mented for plants [64–67]. An intriguing investigation was published that demonstrated that over-
expression of alpine haircap moss PaFKBP12 in Arabidopsis ensured stress tolerance and better
plant growth than the wild type [67]. However, it is unclear whether cyclophilins and FKBPs
interacted with HSFs/HSPs or SWI/SNF CRCs in these examples, and thus whether they are
related to stress memory.

SWI/SNF Chromatin-Remodeling ATPases at the Interface of Development and

Stress Responses
Ten years ago, seven SWI3B-interacting proteins were described, namely BRM, BSH, SWI3A,
SYD, SWI3C, SWI3D, and FCA; presently, 72 interacting proteins are known (BioGRID annota-
tion; htttps://thebiogrid.org/). For BRM and SWI3C, 179 and 149 interactions are described,
respectively (BioGRID). Among them, we present numerous proteins involved in the control of
plant growth and development (Table 1). Reyes [32] suggested that SWI3C and BRM are in
the same SWI/SNF complex, but SWI3B might be in different complexes. This hypothesis is
probably true for developmental processes, given that proteins that participate in floral induction
and organ formation are similar among BRM- and SWI3C-interacting proteins (Table 1). SWI3B
and SWI3C might perform different functions in SWI/SNF complexes that interact with ABA-
related protein phosphatases, because SWI3B interacts with ABI1, ABI2, HAB1, and PP2CA,
but BRM and SWI3C with ABI3. BRM, SWI3B, and SWI3C are probably in the same complex,
which interacts with HsfA3 and HsfA6a (see also reconstruction of complexes in Figure 2 and
Figure 3).

Developing their ‘trade-offs’ hypothesis [28], which regards the resource allocation decision
between growth and drought tolerance, Han and Wagner [31] postulated a role for remodeling
enzymes at the nexus of growth versus stress response pathways, realized by modulation of
developmental programs and accurate and timely changes in gene expression. Indeed, BRM
controls floral organ identity by interacting with the MADS-box transcription factor SEPALLATA3
and transcription factor LEAFY, which activates expression of floral homeotic regulators
APETALA3 and AGAMOUS [29]. The BRM role in leaf maturation is mediated by cycloidea and
PCF transcription factor 4 (TCP4). TCP4 and BRM are bound to the promoter of an inhibitor of
cytokinin responses (ARR16) and induce its expression, thus ensuring modification of cytokinin
responses [30]. Reyes [32] noted that SWI/SNF complexes play a dual role in flower develop-
ment: they activate floral-specific transcription factors and they assist these factors to regulate
downstream genes. Such a dual role also occurs in the interactions of SWI/SNF complexes
and hormonal signaling pathways, namely ABA-, auxin-, cytokinin-, gibberellin-, and
jasmonate-dependent pathways [23]. In some cases, proteins of the SWI/SNF complexes inter-
act with a protein and simultaneously regulate expression of its corresponding gene. For BRM
and SWI3C, those examples are ABI3 and ABI3 (ABA pathway); for BRM and SWI3B, they are
MYC2 and MYC2 from the jasmonate signaling pathway [23] (Table 1).

Besides proteins that participate in developmental processes, several SWI/SNF CRC-interacting

proteins (MYC2, TCP3, TT8, and MYB12; see Table 1) are interesting for evaluating the memory-

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Trends in Plant Science

Table 1. A List of Proteins that Interact with the SWI/SNF Proteinsa

SWI3B BRM SWI3C
Chromatin structure-remodeling SWI3B, SWI3C BRM, SWI3A, SWI3B
proteins: BRM, SWI3A, SWI3C, BSH,
CHB3 (SWI3D)
ABA-related protein phosphatases: ABI3 ABI3
ABI1, ABI2, HAB1, PP2CA
Heat stress transcription factors: HSFA3, HSFA6A HSFA3, HSFA6A
HSFA3, HSFA6A
CBF4 CBF4 –
dehydration-responsive element-binding
protein 1D
ABA-responsive element-binding factors ABF1, ABF3 ABF1
Auxin response transcription factors: ETT, ARF18, IAA11 ETT, ARF18
ETT
MADS box transcription factors AGL39, AGL92, AGL99 AGL92
(Floral development)
Ethylene-responsive transcription factors RAP2.1, TOE2 RAP2.1, TOE2
RAP2.1
– AN3 (ANGUSTIFOLIA 3) –
(leaf development)
– AP1 (floral homeotic protein APETALA 1) –
Two-component response regulators ARR11, RR10 (ARR10) ARR11, RR10 (ARR10)
– BIM1 (transcription factor BIM1) –
(brassinosteroid signaling)
Basic leucine-zipper proteins BZIP2, BZIP3, BZIP7, BZIP19, BZIP42, BZIP4, BZIP7, BZIP19.
BZIP52, BZIP70 BZIP42, BZIP52, BZIP70
Zinc finger proteins: CONSTANS (CO) and COL2, COL5 CO, COL2, COL5
CONSTANS-like proteins (light signaling)
– DegP protease 4 (DEGP4) DP-E2F-like 2 (DEL2)
– Embryo sac development arrest protein EDA31
31 (EDA31)
Flowering time control protein (FCA) – –
(flower development, thermal adaptation)
– GPRI1 (transcription activator GLK1) –
(chloroplast organization)
– – HAM2 (protein LOST
MERISTEM 2)
(shoot stem cell
proliferation)
Homeobox proteins: KNAT1, KNAT3, HB-1, HB40, HB20, HB21 KNAT3, HB-1, HB21,
KNAT3, HB-1, HB40 HB53 HB53
HEC1 transcription factor HEC1, HEC2 HEC1
(carpel formation)
– HSI2 (B3 domain-containing transcription HSI2
repressor VAL1) (seed germination,
regulation of seed
maturation)
IDD16 (shoot gravitropism5-like protein) IDD16 IDD16
– LGO –
cyclin-dependent protein kinase inhibitor
SMR1
(continued on next page)

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Table 1. (continued)
SWI3B BRM SWI3C
LBD29 LOB domain-containing proteins LOB domain-containing
(lateral root formation) (ASYMMETRIC LEAVES): proteins:
LBD1, LBD10, LBD35, LBD29, LBD39 LBD1, LBD10, LBD22,
LBD35, LBD38
LBD40
– LFY
LEAFY protein (flower development)
MYB transcription factors: MYB12, MYB15, MYB26, MYB41, MYB12, MYB15,
MYB26, MYB41, MYB60, MYB92, MYB46, MYB49, MYB53, MYB60. MYB26, MYB46,
MYB122 MYB74 MYB53 MYB60,
MYB86, MYB96, MYB101, MYB102, MYB74, MYB86,
MYB109, MYB121, MYB122, AS1/MYB91 MYB92, MYB96,
MYB101, MYB122
MYC2 transcription factor MYC2 –
NAC domain containing protein 32 NAC-domain transcription factors: –
(NAC032) NAC3, NAC038, NAC046, NAC074,
(multicellular organismal development) NAC080, NAC083, NAC097
– B3 domain-containing transcription –
factors
NGA2, NGA4
NF-YA5 nuclear transcription factors NF-YB8 NF-YA5, NF-YC4,
– NF-YB8
– OCS-element binding factor 5 (OBF5) OBF5
(disease resistance)
– PCL1 PCL1
PHYTOCLOCK 1
(circadian rhythm)
– PIF3 transcription factor
– Retarded growth of embryo 1 (RGE1) RGE1
DELLA proteins RGA1, RGL2, RGL3
RSL1 (RHD SIX-LIKE 1) RSL1, RSL2, RSL4 RSL1, RSL2, RSL4
(control of root hair initiation and elongation)
– SPT (SPATULA transcription factor) SPT
(circadian rhythm; flower development;
response to cold; response to red light)
TEOSINTE BRANCHED 1, cycloidea, TCP1, TCP3, TCP4, TCP5, TCP16, TCP1, TCP3, TCP4,
and PCF transcription factors: TCP20 TCP5, TCP13, TCP16
TCP3, TCP16, TCP20 TCP20
TDF1 (defective in meristem TDF1 TDF1
development and function 1) (microgametogenesis)
TGA4 transcription factor TGA3, TGA4 TGA3, TGA4
(response to cold)
TT8 transcription factor TT8 (flavonoid biosynthetic process) TT8
WRKY transcription factors: WRKY6, WRKY31, WRKY46, WRKY53 WRKY61
TTG2/WRKY44 WRKY61
WRKY53
UNE12 transcription factor UNE12 (regulation of defense response) UNE12
Zinc-finger proteins ZF2, ZFP7 ZFN1, CZF1

a
The data are taken from BioGRID and interacting proteins are grouped according to their function (noted in parentheses
where appropriate).

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Trends in Plant Science

dependent regulation of stress-related polyphenols (for example, anthocyanins, which play a Outstanding Questions
widespread protective role in defense of Photosystem II against high light stress). These pro- What heat shock factors, besides
teins play the central role in anthocyanin biosynthesis regulation [68]. Liu et al. [53] particularly HsfA6a and HsfA3, interact with
emphasized the role of MYC2 in the revised-response transcription memory. Considering the chromatin-remodeling proteins and
what are the interaction dynamics
general role of MYC2 in hormone signaling pathway regulation, the most interesting compo- in vivo? Do members of the HsfA1 family
nents are the MYC2-JAZ-COI1 module, MYC2-interacting DELLA proteins, and MYC2-EIN3 interact with chromatin-remodeling
and MYC2-AHP5 interactions [68]. Other significant players are HY5 and PIFs that form a proteins?
dynamic activation–suppression transcriptional module PIF1/PIF3-HY5, which is responsive
What is the contribution of each signaling
to temperature stress and serves as a rheostat to tune ROS signaling pathways [69]. Special system to memory generation? It is nec-
attention is required to evaluate the roles of NAC proteins, which interact with BRM essary to study how the basic, conserva-
and SWI3B, and play a role in ABA-induced drought stress tolerance and leaf senescence tive mechanism of the HSF-SWI/SNF
CRC interaction is combined with the
[70,71]. Specifically, NAC032, in concert with the WRKY6 transcription factor, participates in
mechanism of ABA-SWI/SNF CRC
ROS detoxification [72]. interaction.

Other SWI/SNF CRC-interacting proteins, which are of interest for in-depth study, are zinc-finger Do post-translational mechanisms in
proteins, such as ZF2, ZFP7, and ZFN1. Zinc-finger proteins negatively regulate the ABA signal- plants influence SWI/SNF CRC protein
ing and are involved in plant growth inhibition under abiotic stress conditions, specifically by stability or protein modifications, de-
pending on incoming signals of abscisic
repressing various genes, including osmotic stress and ABA-repressive genes [73]. Thus, we acid and chaperones?
listed groups of proteins potentially suitable for the design of ‘bioengineering memory’, that is,
those involved in plant development, hormonal signaling, and acting at the interface between
stress and development.

Inducer of CBF Expression 1 (ICE1)-MUTE-HsfA1d Interactions

Besides SWI/SNF chromatin-remodeling proteins, we uncovered the ICE1-MUTE-HsfA1d
interaction that connects ABA and HSF signaling (Figure 1). The bHLH transcriptional factor
ICE1 is a crucial component in cold signaling [74,75]. The ICE1-MUTE interaction was revealed
by the two-hybrid assay and indicated a possible link between transcriptional regulation of stress
adaptation and development [76]. The MUTE-HsfA1d interaction was demonstrated by the new
multiplexed yeast two-hybrid method [77] and represented in the IntAct database. The function of
this interaction is presently unknown. Therefore, the role of the ICE1-MUTE-HsfA1d module in the
connectivity of ABA and HSF signaling remains to be elucidated.

Concluding Remarks and Future Perspectives

From the information presented above, it is clear that a growing body of evidence points to the
existence of a link between ABA and chaperone signaling, and these interactions appear to
be mediated by chromatin-remodeling proteins. Conformation changes or modification of
chromatin-remodeling proteins, mediated by interactions with SnRK2s/PP2Cs or ABF/AREB
as well as HSFs, may be used for bioengineering purposes. Han and Wagner [31] noted that
the ability to modulate chromatin regulator activity (via targeted post-translational modifications)
would allow exploitation of their general reprogramming ability.

We propose several areas of research for the design of ‘bioengineering memory’ in regard to
stress resistance:
• Investigation and modification of self-regulating loops, such as HSFA3-HSFA6a → DREB2A →
HSFA3, activity from which may be perceived and stored via chromatin-remodeling factors.
• Simultaneous engineering of ABA- and HSF-signaling components that interact with SWI/SNF
complexes.
• Modulation of SWI/SNF component activity that interacts with a protein and simultaneously
regulates expression of its corresponding gene, for example, ABI3 and ABI3 in the ABA
pathway.
• Memory-dependent regulation of stress-related polyphenols.

Trends in Plant Science, Month 2019, Vol. xx, No. xx 13

Trends in Plant Science

• Regulation of MYC2-dependent signal transduction pathways (especially the MYC2-JAZ-COI1

module, which plays a major role in jasmonic acid signaling and crosstalk with the ABA, ethyl-
ene, gibberellin, and light signaling pathways).
• Engineering of the PIF1/PIF3-HY5 signaling module to tune ROS signaling pathways.

We should emphasize that in bioengineering plant stress responses, one must adhere to mild
methods of action that are as close as possible to natural adaptation. It is unclear whether direct
or indirect modifications of ‘instructive’ chromatin regulators would allow enhanced primary or
heritable stress tolerance without loss of yield. Currently, this is almost unexplored territory for
plant biotechnologists, but it is an engaging approach to coordinate protective processes and
growth. It is obvious that when trying to modify ABA or HSF signaling pathways, it will be neces-
sary to pay attention to and consider the epigenetic landscape when planning an experiment (see
Outstanding Questions).

Author Contributions
V.P.B.: conception, data analysis, manuscript writing. H.-C.W.: analysis and interpretation of data, revising for important
intellectual content, final approval. T.-L.J.: analysis and interpretation of data, revising for important intellectual content,
final approval.

Acknowledgments
This work was carried out as part of a joint project of the Russian Science Foundation and the Ministry of Science and
Technology, Taiwan. Financial support was provided by the Russian Science Foundation, Grant No. 18-44-08001
(V.P.B.), and the Ministry of Science and Technology, Taiwan, Grant Nos. 105-2311-B-002-033-MY3 and 107-2923-B-
002-003-MY3 (T-L.J.).

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