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Epigenetic Mechanisms of Abiotic Stress Response and Memory in Plants

  • Biology Centre, Czech Academy of Sciences, Ceske Budejovice, CZ

Abstract and Figures

Being sessile organisms, plants are exposed to multiple stimuli without possibility for escape. Therefore, plants have evolved to be able to adapt their developmental and physiological responses to the surrounding environment. Some environmental stresses will rarely occur during the life of the plant, but others, such as seasonal drought or heat, can be recurrent. Therefore, plant responses to these stresses can be transient to provide plants with the required tools to acclimate and survive, whereas others may promote a state that we will refer to as “memory” throughout the chapter, which predisposes the plant for a more efficient stress response upon next encounter of stress. The possibility of transferring this memory to the next generation has been also proposed, which implies a lack of resetting of the priming memory during sexual reproduction. Different epigenetic and chromatin-related modifications such as DNA methylation, histone modifications, and chromatin remodeling have been associated with the memory to both biotic and abiotic stresses. This chapter reviews how and which epigenetic processes are involved in remembering a past abiotic stress event and also forgetting it. Contradictory arguments concerning transgenerational memory and its implications in phenotypic variation are critically discussed. In addition, the stability of epigenetic modifications during asexual propagation and its impact on clonally propagated plants is addressed. Finally, we mention possible agricultural implications of the epigenetic mechanisms involved in plant memory and propose future applications for breeding of epigenetically modified crops considering new challenges arising from climate change.
Somatic and transgenerational memory induced by environmental stresses. Plants growing under naïve conditions can experience a first environmental stress that will promote transcriptional changes correlated with chromatin changes (i.e., DNA methylation, histone PTMs, DNA-dependent chromatin remodeling, deposition of new histone variants) of stress-responsive genes. This can result in sustained (type I) or temporal (type II) activation and/or repression of genes (Bäurle 2017) and addition and/or removal of specific chromatin modifications. However, for simplification, the figure focuses on transcriptional activation and addition of new chromatin modifications. Encountering the stress may also impair plant vigor. After the stress, the plant enters in a primed state in which transcription of stress-responsive genes may recover to original expression levels. Amplitude of the recovering phase varies depending on the environmental cue and on memory genes. Plant vigor also recovers, although a phenotypic cost may be applied. However, the new chromatin state of memory genes will be stably maintained. When the plant perceives a second stress, this triggers the response of memory genes. The triggered response can be faster, stronger, more sensitive, and/or different to the first one (Lämke and Bäurle 2017). Intensity and amplitude of the response also differs depending on experimental conditions. Although most of our current knowledge indicates that the primed state perdures for a finite period within the same generation (somatic memory) and resetting of the primed state occurs during sexual reproduction, in some cases the chromatin state linked to the stress memory may be inherited by the offspring (inter-/transgenerational memory). Although much less is known of this possibility (?), inheritance of the memory could provide the new plant generation with molecular tools to better cope with recurrent stresses
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1© Springer Nature Switzerland AG 2019
R. Alvarez-Venegas et al. (eds.), Epigenetics in Plants of Agronomic Importance:
Fundamentals and Applications,
Chapter 1
Epigenetic Mechanisms ofAbiotic Stress
Response andMemory inPlants
IvaMozgova, PawelMikulski, AlesPecinka, andSaraFarrona
Abstract Being sessile organisms, plants are exposed to multiple stimuli without
possibility for escape. Therefore, plants have evolved to be able to adapt their devel-
opmental and physiological responses to the surrounding environment. Some envi-
ronmental stresses will rarely occur during the life of the plant, but others, such as
seasonal drought or heat, can be recurrent. Therefore, plant responses to these
stresses can be transient to provide plants with the required tools to acclimate and
survive, whereas others may promote a state that we will refer to as “memory”
throughout the chapter, which predisposes the plant for a more efficient stress
response upon next encounter of stress. The possibility of transferring this memory
to the next generation has been also proposed, which implies a lack of resetting of
the priming memory during sexual reproduction. Different epigenetic and chromatin-
related modifications such as DNA methylation, histone modifications, and chroma-
tin remodeling have been associated with the memory to both biotic and abiotic
stresses. This chapter reviews how and which epigenetic processes are involved in
I. Mozgova
Institute of Microbiology of the Czech Academy of Sciences, Centre Algatech,
Trebon, Czech Republic
Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic
Biology Centre of the Czech Academy of Sciences, Institute of Plant Molecular Biology,
Ceske Budejovice, Czech Republic
P. Mikulski
Department of Cell and Developmental Biology, John Innes Centre, Norwich, UK
A. Pecinka
Institute of Experimental Botany of the Czech Academy of Sciences, Prague, Czech Republic
Centre of the Region Haná for Biotechnological and Agricultural Research,
Olomouc, Czech Republic
S. Farrona ()
Plant and AgriBiosciences Research Centre, Ryan Institute, NUI Galway, Galway, Ireland
remembering a past abiotic stress event and also forgetting it. Contradictory argu-
ments concerning transgenerational memory and its implications in phenotypic vari-
ation are critically discussed. In addition, the stability of epigenetic modifications
during asexual propagation and its impact on clonally propagated plants is addressed.
Finally, we mention possible agricultural implications of the epigenetic mechanisms
involved in plant memory and propose future applications for breeding of epigeneti-
cally modified crops considering new challenges arising from climate change.
1.1 Introduction
Crop production is deeply affected by the environmental conditions and current
models for climate change indicate that future conditions will become even more
challenging. Climate trends show that the Earth tends to be less cold with an increase
in temperatures in every season, especially for minimal temperatures, in most of the
crop producing regions, which is coupled to a major increase in the frequency of
temperature extremes (Alexander etal. 2006; Lobell etal. 2011; Lobell and Gourdji
2012). Although more difficult to predict, the numbers of drought periods have
shown a tendency to increase over the last 50years in some parts of the world (i.e.,
Africa, southern Europe, east and south Asia, and eastern Australia) and will become
much more frequent by the end of the twenty-first century, while the wet regions
will become even wetter (Skliris etal. 2016). There is, therefore, a complex inter-
connection between climate change and food security, which is at a risk due to the
effects of increasing temperatures, water-cycle changes, and higher CO2 levels on
plant yields. Indeed, a decline in the production and a subsequent price increase of
important crops (i.e., wheat—Triticum aestivum, maize—Zea mays, and barley—
Hordeum vulgare) has already been linked to global warming (Lobell etal. 2011;
Lobell and Gourdji 2012; Moore and Lobell 2015). Thus, understanding the pheno-
typic variation of plants and how food and feed production can be secured has taken
a central position in crop science.
Plants can efficiently respond to abiotic or biotic environmental conditions and
modify their development and physiology accordingly. In this review, we focus on
the response and memory of abiotic stresses such as extreme temperatures, drought,
and salinity. Stress can be considered as any situation that can alter plant fitness and
cause a substantial loss in yield. Abiotic stresses are major cause of food scarcity
being responsible for estimated 50% loss in staple crops (reviewed in Boyer 1982;
Bray etal. 2000). One of the main abiotic stresses that plants face are extreme tem-
peratures, both high and low. Heat will most probably increase in the future affect-
ing many countries, including developing countries where hunger is already an
issue (reviewed in Lobell and Gourdji 2012). Increase in temperature is particularly
dramatic during plant reproduction and seed filling, having a significant impact on
yield (reviewed in Kosina etal. 2007). As part of global warming, heat stress usually
comes in combination with water scarcity, which according to predictions will
become more acute, and with higher CO2 and UV radiation (reviewed in Williamson
I. Mozgova et al.
etal. 2014). On the other hand, floods, which will be more recurrent in other regions
of the globe, present also major agronomic constraints especially affecting yield and
grazing land and, in more extreme situation, causing plant death due to hypoxia
(reviewed in Jackson and Colmer 2005). Soil water content is directly linked to
other main stresses including salinity and nutrient availability. Soil salinization has
a strong impact on plant growth affecting the photosynthetic rate, absorbance of
nutrients, and increasing senescence (reviewed in Hanin etal. 2016). Chilling tem-
peratures also impair plant metabolism, germination, and reproduction, whereas
freezing temperatures additionally cause tissue and membranes damage and cell
dehydration (reviewed in Xin and Browse 2000).
An intricate network of processes involved in sensing and responding to the envi-
ronment, which implies massive changes in gene expression and nuclear organiza-
tion, aids the plant to cope with the stress (reviewed in Probst and Mittelsten Scheid
2015; Asensi-Fabado etal. 2017). However, plants will seldom be affected by indi-
vidual conditions and, hence, they usually respond to multiple stresses at the same
time. However, the challenge of simultaneously applying different stresses and ana-
lyzing their overlapping action still limits our understanding of the complexity of
plant responses to abiotic stresses. Therefore, for the breeding of new crop varieties
better adapted to future more severe climate conditions, multidimensional experi-
mental approaches more closely mimicking on-field conditions will be required
(reviewed in Mittler 2006; Ahuja etal. 2010; Qin etal. 2011).
Whereas some stresses occur occasionally, generating a temporal stress response
in the plant, many of the abiotic changes occur as daily (e.g., day and night changes)
or seasonal fluctuations (e.g., summer and winter seasons in temperate climates or
dry and humid seasons in tropical areas). Recurrent stresses can therefore induce a
cellular memory that poses or primes the plant for a faster and stronger response
upon repeated stress exposure. This stress memory is also known as priming or, in
the case of abiotic stress, as acclimation or hardening (reviewed in Bruce et al.
2007). Therefore, the priming of plants implies: (1) the action of a first stress condi-
tion that, in addition to inducing a stress response in the plant, may trigger the for-
mation of a molecular memory, (2) the end of this first stress condition, (3) a lapse
of time during which the memory can perdure in the absence of the stress that gener-
ated it, and (4) the occurrence of a second stress that will activate the recovery of the
stress memory to induce a new enhanced plant response. Furthermore, an additional
(5) step entails resetting the memory or maintaining it for transfer to the next
generation(s) through a process usually known as inter-/transgenerational memory
(Fig.1.1 and reviewed in Bruce etal. 2007; Pecinka and Mittelsten Scheid 2012;
Chen and Arora 2013; Kinoshita and Seki 2014; Avramova 2015; Crisp etal. 2016;
Hilker etal. 2016; Bäurle 2017; He and Li 2018). The second stress that retrieves
the memory can be of the same nature as the first one, but it seems that a different
abiotic stress, or even a biotic one, can activate the priming memory, indicating a
complex crosstalk between different types of stresses (reviewed in Hilker et al.
2016; Asensi-Fabado etal. 2017; Lämke and Bäurle 2017; Friedrich etal. 2018).
Eventually, primed plants will be readier to respond to a second stress showing an
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
Fig. 1.1 Somatic and transgenerational memory induced by environmental stresses. Plants grow-
ing under naïve conditions can experience a first environmental stress that will promote transcrip-
tional changes correlated with chromatin changes (i.e., DNA methylation, histone PTMs,
DNA-dependent chromatin remodeling, deposition of new histone variants) of stress-responsive
genes. This can result in sustained (type I) or temporal (type II) activation and/or repression of
genes (Bäurle 2017) and addition and/or removal of specific chromatin modifications. However,
for simplification, the figure focuses on transcriptional activation and addition of new chromatin
modifications. Encountering the stress may also impair plant vigor. After the stress, the plant enters
in a primed state in which transcription of stress-responsive genes may recover to original expres-
sion levels. Amplitude of the recovering phase varies depending on the environmental cue and on
memory genes. Plant vigor also recovers, although a phenotypic cost may be applied. However, the
new chromatin state of memory genes will be stably maintained. When the plant perceives a sec-
ond stress, this triggers the response of memory genes. The triggered response can be faster, stron-
ger, more sensitive, and/or different to the first one (Lämke and Bäurle 2017). Intensity and
amplitude of the response also differs depending on experimental conditions. Although most of our
current knowledge indicates that the primed state perdures for a finite period within the same gen-
eration (somatic memory) and resetting of the primed state occurs during sexual reproduction, in
some cases the chromatin state linked to the stress memory may be inherited by the offspring
(inter-/transgenerational memory). Although much less is known of this possibility (?), inheritance
of the memory could provide the new plant generation with molecular tools to better cope with
recurrent stresses
I. Mozgova et al.
improved phenotypic adaptation with minor fitness cost and, hence, survival and
yield. On the other hand, the priming stage increases plant sensitivity, affects
development and growth, and can be more cost-effective to reset than to maintain;
therefore, plants may employ mechanisms to elucidate whether to memorize or to
forget (reviewed in Avramova 2015; Crisp etal. 2016; Bäurle 2017).
Transcriptional reprogramming is a common feature of the primed state. Genes
that show a memory will modify their expression in response to both the first and
the second stress, but expression levels will be significantly different in the second
response. Considering that the primed state between the two stresses can last from
days to months (as in the case of somatic memory—see Sect. 1.2), or stress can even
recur in the subsequent generation(s) (as in intergenerational or transgenerational
memory—see Sect. 1.2, Fig.1.1), the transcriptional memory and molecular mech-
anisms that underlie it need to have the potential to be maintained and transmitted
through cell division and even sexual reproduction. These criteria are met by genetic
and epigenetic mechanisms. In fact, different epigenetic processes and chromatin-
related mechanisms have been involved in setting memory of passed environmental
events (Fig.1.1 and reviewed in Bruce etal. 2007; Chen and Arora 2013; Kinoshita
and Seki 2014; Avramova 2015; Crisp etal. 2016; Hilker etal. 2016; Bäurle 2017;
He and Li 2018). Other processes, such as stability and modification of proteins,
have also been involved in the priming memory (reviewed in Pastor etal. 2013).
Chromatin, the molecular complex containing DNA and nuclear proteins, mainly
histones, plays an essential role in transcriptional regulation. DNA and histones can
be modified by the addition of chemical groups, methyl group being by far the most
common in the case of DNA and variable chemical post-translational modifications
(PTMs) in case of histones (e.g., methyl, acetyl, phosphate, and ubiquitin groups
being most common). The presence of these chromatin marks or their combinations
acts to regulate gene expression by modifying the accessibility of DNA or the
recruitment of specific proteins to chromatin. Furthermore, chromatin marks pres-
ent on a gene may be stably transmitted through cell division contributing to the
maintenance of its transcriptional status. In addition to primary DNA sequence, this
adds a new layer of information that can be mitotically and/or meiotically transmit-
ted and underlies epigenetic inheritance (reviewed in Zentner and Henikoff 2013;
Du etal. 2015). Different pieces of evidence demonstrate that in the presence of a
stress that triggers transcriptional changes, epigenetic modifications will be added/
removed to/from specific key stress-response genes and create a stable chromatin
environment that will perdure even once the stress that induced it has passed. This
environment-triggered epigenetic memory will contribute to the phenotypic plastic-
ity of the plant in the event of a new stress. The implication of this long-lasting
chromatin-related memory has been subject of lively discussion due to the obvious
potential for improving crop adaptation and its relationship to Lamarck’s vision of
genetic inheritance (Pecinka and Mittelsten Scheid 2012).
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
1.2 Somatic, Inter- andTransgenerational Memory
Memory of stress experienced by plants can be somatic (or intra-generational), last-
ing for a varied period of time within the exposed plant generation after the immedi-
ate stress response. Intergenerational memory persists into the next generation of
progeny of the exposed plants and transgenerational memory is transmitted into
further generation(s) in the absence of stress (Fig. 1.1; reviewed in Heard and
Martienssen 2014; Lämke and Bäurle 2017). We will focus on the molecular mech-
anisms underlying stress memory and in particular on mechanisms connected to
modification of chromatin structure (chromatin-based memory) in model and crop
plants. At present, strong experimental support exists for somatic memory that per-
sists in the range of days to weeks following the initial stress treatment, while less
and often contradictory examples of intergenerational or transgenerational memory
are available.
1.2.1 Somatic Memory
Several molecular mechanisms that contribute to somatic memory of abiotic stress
have been identified (reviewed in Conrath etal. 2015; Avramova 2015; Crisp etal.
2016; Bäurle 2017; Lämke and Bäurle 2017). Somatic memory has been connected
to the persistence of stress-induced metabolites (Pastor etal. 2014; Balmer etal.
2015; Hu etal. 2016), to sustained expression of genes after the stress response ends
(Charng etal. 2006b; Stief etal. 2014), to stalling of RNA polymerase II that poten-
tiates transcription (Ding etal. 2012), to the accumulation of proteins (e.g., mitogen-
activated protein kinases—MPKs, Beckers et al. 2009), or to mitotic stability of
stress-induced chromatin changes (Ding etal. 2012; Sani etal. 2013; Singh etal.
2014; Weng etal. 2014; Lämke etal. 2016; Brzezinka etal. 2016, 2018; Feng etal.
2016; Liu etal. 2018b). Based on the transcription level of the stress-response
genes, chromatin-based transcriptional memory can be separated into type I, during
which transcriptional activity of stress-responsive genes persists, and type II, during
which the initial stress-induced transcription ceases but a second exposure to stress
can induce a modified response in comparison with the response of naïve plants
(reviewed in Bäurle 2017) (Fig. 1.1). Somatic memory of abiotic stresses seems
limited to several days or weeks (Bäurle 2017; Lämke and Bäurle 2017). Several
chromatin-based mechanisms have been shown to contribute to somatic memory.
These include nucleosome occupancy and remodeling, relative abundance of his-
tone PTMs, cytosine (DNA) methylation, and RNA interference, and we discuss
examples of the particular mechanisms in the respective sections. Although molecu-
lar aspects of somatic memory are best well studied in the short-lived annual
Arabidopsis (Arabidopsis thaliana), it may be of particular importance in long-lived
perennial species (Lafon-Placette etal. 2018; Le Gac etal. 2018). Its existence is
suggested by maintained changes of DNA methylation in the shoot apical meristem
I. Mozgova et al.
(SAM) of poplar (Populus spp.) trees that have grown under different water avail-
ability (Lafon-Placette et al. 2018). In addition, winter-dormant SAMs of trees
grown at different environmental conditions retain differentially methylated regions
at genes involved in abiotic stress response, SAM organization, and phytohormone
metabolism and signaling (Le Gac etal. 2018) suggesting that growth conditions
during vegetative phase can be reflected in cells that will produce organs in the next
vegetative season and may potentially influence performance and growth. It is of
note, however, that global DNA methylation level changes occur during bud dor-
mancy and break that are mediated by DNA demethylases (Conde etal. 2017), sug-
gesting that active reprogramming occurs. Whether environmentally induced
epialleles can escape the global DNA methylation reprogramming remains to be
1.2.2 Inter- andTransgenerational Memory
Transgenerational stress memory can be in principle mediated by transmission of
structural variation in the genome, inheritance of chromatin states (or epialleles),
and/or seed provisioning (or maternal effect) whereby different level of resources
such as mRNA, hormones, proteins, starch, lipids, or other reserve molecules are
stored in the seed based on the environmental conditions during growth of the
maternal plant (reviewed in Herman and Sultan 2011; Pecinka and Mittelsten
Scheid 2012; Pecinka etal. 2013; Heard and Martienssen 2014). Due to the diffi-
culty in separating maternal effects from heritability of epialleles, transgenerational
inheritance of acquired epialleles as means of environmental memory and its adap-
tive value has been debated (Boyko and Kovalchuk 2011; Mirouze and Paszkowski
2011; Paszkowski and Grossniklaus 2011; Pecinka and Mittelsten Scheid 2012;
Ganguly etal. 2017). Taking into consideration also maternal effects or possible
induced structural variation, intergenerational memory mechanisms can neverthe-
less contribute to adaptive transgenerational plasticity (Herman and Sultan 2011)
and to rapid environmental adaptation in plants (Franks and Hoffmann 2012).
Transmission of acquired epialleles between generations is prevented by active
resetting of chromatin states during sexual reproduction (reviewed in Paszkowski
and Grossniklaus 2011; Heard and Martienssen 2014; Kawashima and Berger 2014;
Iwasaki 2015). In mammals, extensive epigenetic reprogramming occurs during
germline formation and early embryogenesis during which DNA methylation and
histone PTMs are erased and thus examples of transgenerational inheritance of epi-
alleles are rare (reviewed in Heard and Martienssen 2014). On the contrary, several
features of plant development make plants more prone to transgenerational inheri-
tance of acquired epialleles. First is the late developmental origin of the germline
that forms from stem cells within the SAM, in which exposure of the somatic tissue
to environmental conditions can be reflected. Nevertheless, it needs to be consid-
ered that mechanisms which restrict responses affecting genome and epigenome
stability may operate with higher stringency in stem cells that give rise to the
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
germline than in vegetative tissue (Yadav 2009; Baubec etal. 2014). Second, stress-
induced epigenetic changes have a chance to be copied and maintained during plant
sexual reproduction. In plants, reprogramming (reduction) of DNA methylation
mainly occurs in the companion cells, the vegetative cell nucleus in pollen and the
central cell nucleus in the ovule, rather than in the nuclei (sperm cell and egg cell)
that will fuse to form the zygote during fertilization (reviewed in Kawashima and
Berger 2014). Still, considerable global epigenetic reprogramming does take place
during gametogenesis, connected to histone replacement (Ingouff etal. 2007; Schoft
etal. 2009; She etal. 2013; She and Baroux 2015) and DNA demethylation (Calarco
etal. 2012). Despite the constraint imposed by epigenetic reprogramming during
sexual reproduction for the transmission of acquired epialleles, examples of sexual
transmission of epialleles are more abundant in plants than in mammals suggesting
a higher potential for transgenerational epiallele inheritance (reviewed in Heard and
Martienssen 2014). Finally, it is important to note that plants possess an immense
capability of vegetative reproduction, which may increase the probability of epial-
lele retention and its later outgrowth into a sexually propagating individual. Memory During Sexual Reproduction
Despite sexual reprogramming and other mechanisms that actively limit transgen-
erational inheritance of epialleles (Iwasaki 2015), natural epialleles that can be sta-
ble over sexual plant generations exist in plants (Cubas etal. 1999; Manning etal.
2006; Martin etal. 2009; Stam 2009). Much information on the inheritance of
acquired and existing epialleles has been provided by genome-wide studies employ-
ing DNA methylation variation in natural accessions (ecotypes) (Dubin etal. 2015;
Kawakatsu etal. 2016), in mutation accumulation lines (Becker etal. 2011; Schmitz
etal. 2011), recombinant inbred lines (RILs) (Eichten etal. 2013; Schmitz etal.
2013), or the epigenetic RILs (epi-RILs) (Reinders etal. 2009; Teixeira etal. 2009;
Johannes et al. 2009). These studies demonstrated that natural as well as some
newly acquired DNA methylation epialleles can be inherited over several sexual
generations and that DNA methylation at some loci can be re-established in the
epiRILs to resemble the ancestral epiallelic states (Reinders etal. 2009; Teixeira
et al. 2009). Hence, DNA methylation-based epialleles can be stably inherited
mitotically and meiotically but are often reversible, especially if located close to
TEs and small RNA-producing loci (Becker etal. 2011).
Alternative epialleles could serve as a source of variation for breeding purposes
(Hofmeister etal. 2017). Indeed, epialleles can confer alternative transcription of
their respective gene loci (Becker etal. 2011; Schmitz etal. 2011) and alter pheno-
typic traits of plants (Roux etal. 2011; Zhang etal. 2013b; Cortijo etal. 2014).
Phenotypes associated with changes in chromatin states also affect traits that are of
potential agronomic importance, including stress tolerance (Kooke etal. 2015;
Verkest etal. 2015), disease resistance (Akimoto etal. 2007; Reinders etal. 2009),
plant stature (Miura etal. 2009; Reinders etal. 2009; Johannes etal. 2009), root
length (Soppe etal. 2000; Reinders etal. 2009; Johannes etal. 2009; Cortijo etal.
I. Mozgova et al.
2014), transition to flowering (Soppe etal. 2000; Reinders etal. 2009; Johannes
etal. 2009; Cortijo etal. 2014), senescence (He etal. 2018), flower sex determina-
tion (Martin etal. 2009), genetic incompatibility (Durand etal. 2012), fruit ripening
(Manning etal. 2006), or yield (Hauben etal. 2009; Ong-Abdullah et al. 2015).
However, the extent of purely epigenetic contribution to the observed phenotypes
must be interpreted with care as the studied plant lines are not completely isogenic
and genetic changes may accompany chromatin states connected to a particular
epiallele (Pecinka etal. 2013). In some cases, structural changes to the genome can
be induced by strong selective pressure imposed by stress (e.g., by chemical treat-
ment, as is frequent during evolution of herbicide resistance—reviewed in Markus
et al. 2018) or by activation of transposable elements (TEs) (discussed in Sect.
1.4.2). Even though combined effect of genetic and epigenetic change contributing
to the desired phenotypic traits is not necessarily an obstacle and may be exploited
for agricultural purposes (Yasuda etal. 2013), the nature of stress-induced epigen-
etic changes may be stochastic (Eichten and Springer 2015) and present an impedi-
ment to targeted crop improvement.
Transgenerational memory of abiotic stress observed in subsequent sexual gen-
erations of stress-exposed plants seems limited to one to two generations of
unstressed sexual progeny of stressed plants. Activation of TEs induced by heat
stress was only retained for maximum of several weeks in the treated plants but was
not observed in the progeny (Pecinka etal. 2010). In a more extensive study the
effect of several abiotic stress treatments was seen in the first or second generation
after the treatment, but the appearance was stochastic and could represent experi-
mental variation (Pecinka etal. 2009). Similarly, the resistance to several stresses
(including heat, cold, flood, and UV-C) was elevated in the progeny of plants when
both generations were subjected to stress but the effect was diminished in unstressed
progeny (Boyko etal. 2010). Recently, Wibowo etal. (2016) observed enhanced
resistance to hyperosmotic stress in the progeny of plants exposed to the stress for
at least two consecutive generations. In the absence of the stress, however, the
enhanced resistance was lost within two sexual generations (Wibowo etal. 2016),
demonstrating transient retention of stress memory. Interestingly, repetitive stress
over several generations does not always seem to correlate with improved pheno-
typic performance under stress. Arabidopsis plants subjected to drought conditions
during five generations did not show any growth advantage to control plants
(Ganguly etal. 2017). The only trait that showed significant memory through gen-
erations and perdured one generation after the stress was seed dormancy that was
increased by drought (Ganguly etal. 2017). Memory During Vegetative Reproduction
Epialleles can also be transmitted during vegetative propagation invitro. Multiple
economically important species are propagated vegetatively, producing large num-
bers of clonal progeny. Despite clonal origin, phenotypic variability occurs among
individuals of the progeny, a phenomenon called somaclonal variation. Even though
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
somaclonal variation can in principle contribute to the emergence of advantageous
traits and progeny improvement, it often leads to reduced plant vigor, and substan-
tial quality and yield losses (reviewed in Miguel and Marum 2011). Somaclonal
variation can be caused by different chromatin states, often associated with differ-
ences in DNA methylation (reviewed in Miguel and Marum 2011). Somaclonal
variation may also be connected to genome structural rearrangements, as tissue cul-
ture in several crop species including rice (Oryza sativa) or maize may promote
mobilization of TEs (reviewed in Negi etal. 2016), and other types of structural
changes including polyploidization, aneuploidy, chromosomal mutations or DNA
mutations (reviewed in Neelakandan and Wang 2012).
Three recent studies show that DNA methylation patterns can be maintained in
plants regenerated from tissue culture in Arabidopsis (Wibowo etal. 2018), rice
(Stroud etal. 2013), or maize (Stelpflug etal. 2014; Han etal. 2018). Importantly,
the altered epiallelic states were retained in sexual progeny of plants obtained from
these tissue cultures and DNA methylation changes were reflected in gene expres-
sion changes (Stroud et al. 2013; Han et al. 2018; Wibowo et al. 2018). In
Arabidopsis, plants were regenerated from somatic embryos induced from either
root or leaf and the original tissue-specific DNA methylation patterns persisted for
two generations of sexual progeny of the regenerated plants. Especially the leaf of
root-derived plants retained DNA methylation pattern of the original root tissue
(Wibowo etal. 2018). These results suggest that DNA methylation epialleles estab-
lished during tissue culture can be retained during regeneration and sexual propaga-
tion and that tissue of origin can be reflected in the regenerated plants and their
sexual progeny. Although it remains unclear to what extent the changes in DNA
methylation may be associated with genomic structural changes, these findings
raise important considerations for massive clonal propagation of plants.
Information regarding inheritance of other than DNA-methylation dependent
epialleles during vegetative propagation is scarce. Nevertheless, environmentally
induced epialleles that are known to be stable somatically, such as the repressed
form of the FLOWERING LOCUS C (FLC) (which will be discussed later in the
chapter), can be maintained during vegetative propagation invitro, changing the
phenotypic traits of the regenerated plants by promoting early flowering (Nakamura
and Hennig 2017). It is therefore possible that asexual propagation in tissue culture
may allow for retention of histone PTMs but much more work is required in the
future to gain more global insights.
In summary, epialleles (especially connected to alternative DNA methylation
states) can be transmitted over generations both during sexual and vegetative plant
propagation and can have an impact on plant phenotypes. The adaptive value of
purely epigenetic, but not structural, variation and its contribution to evolution of
populations under changing environmental conditions however remains to be deter-
mined (De Waele 2005; Franks and Hoffmann 2012).
I. Mozgova et al.
1.3 Abiotic Stresses: Physiological Perspective
Although environmental stresses are usually combined in nature, most research so
far has focused on application of a particular stress type. A compilation of major
abiotic stresses and plant responses in relation to plant memory is summarized in
the following section.
1.3.1 Drought andDesiccation
Drought is one of the factors limiting agricultural output that will be increasingly
important due to the predicted climate change in next decades (reviewed in IPCC
2013). Therefore, drought-induced responses and stress memory in crops attract
considerable attention in tackling negative effects of global warming.
In Arabidopsis, drought memory was studied by single or multiple desiccation
stress treatments, followed by recovery (re-watering) periods of varying duration. In
the seminal works from Avramova group (Ding etal. 2012, 2013; Liu etal. 2014a),
Arabidopsis seedlings were treated with air-dry desiccation/rehydration cycles
repeated up to four times. The samples were collected at pre-stress, stress, and
recovery phases and subjected to gene expression and chromatin analyses. As a
result, the group identified desiccation-responsive genes whose transcriptional and
chromatin status is changed by the stress. Importantly, a subset of drought- responsive
targets exhibited stress memory pattern, where response to subsequent stresses was
altered in relation to the priming stress (Ding etal. 2012). Interestingly, categorized
by the function, the biggest fraction of drought-memory genes is implicated also in
response to salt, cold/heat, light, and abscisic acid (ABA) (Ding etal. 2013), high-
lighting a crosstalk between different stress signaling pathways. Another example
of desiccation memory in Arabidopsis concerns drought tolerance induced at the
seed stage. Imbibed seeds were treated with polyethylene glycol (PEG) at different
developmental stages, followed by rehydration and growth/survival assessment dur-
ing post-germination development. Strikingly, improved survival in PEG-treated
plants was still present for at least 5–10days after rehydration. A microarray experi-
ment revealed significant subset of genes related to temperature- and hormone-
response upregulated 3 days after PEG-treatment demonstrating continuous
transcriptional response (Maia etal. 2011).
In crops, drought leads to morphological (e.g., reduced germination, plant height,
plant biomass), physiological (e.g., reduced water content, photosynthetic activity,
pigment content, membrane integrity), biochemical (e.g., accumulation of osmo-
protectants like proline, sugars, antioxidants), and molecular (e.g., altered expres-
sion of stress-related genes) changes (reviewed in Farooq etal. 2012; Fahad etal.
2017). Rice, as submerged crop, is one of the most drought-sensitive species (Jaleel
and Llorente 2009), in which drought-induced yield losses can amount even to 92%
(Lafitte etal. 2007). Intermediate drought stress applied to rice seedlings causes
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
dehydration-induced oxidative cellular damage symptoms (Li etal. 2011). However,
rice seedlings pre-treated with mild drought and re-watered before intermediate
stress exhibited less pronounced oxidative damage as assessed by the levels of lipid
peroxidation and selective antioxidants (Li etal. 2011). The beneficial effect of pre-
treatment of rice seedlings suggests existence of drought memory mechanisms pro-
tecting against oxidative-stress caused by subsequently applied stronger drought.
Wheat seedlings acclimated by dehydration, re-watered, and exposed to further
water deficit showed limited membrane damage, retained water content, decreased
accumulation of reactive oxygen species (ROS), compared to non-acclimated con-
trols (Selote etal. 2004; Selote and Khanna-Chopra 2006, 2010). The authors cor-
related drought acclimation with levels of antioxidant enzymes that were induced
by pre-treatment and maintained over re-watering period and triggering stress event
(Selote and Khanna-Chopra 2006, 2010). In maize, drought memory was assessed
by studying response to repetitive dehydration/rehydration cycles in seedlings.
Plants exposed to multiple stress cycles exhibited improved water content in leaves
as compared to single-stress controls. By comparing transcriptomic responses in
maize and Arabidopsis, the authors identified not only conserved acclimation fea-
tures, but also species-specific gene regulation patterns, indicating not only evolu-
tionarily conservation but also divergence in drought stress response and memory
(Ding etal. 2014). In potato (Solanum tuberosum), drought stress acclimation was
shown to have positive effect on yield and overall plant growth. Plants exposed to
two mild dehydration cycles before two complete soil dehydration showed reduced
leaf wilting, cuticle accumulation, greater stem number and more open stomata
under stress, compared to non-acclimated controls. In contrast, the authors did not
observe acclimation effect on tuber weight and number under severe drought (Banik
etal. 2016).
1.3.2 Osmotic Stress andSalinity
High salinity is one of the most detrimental factors for agricultural production on
both, naturally saline soils and irrigated lands with high level of evaporation or
insufficient water management. Salt-induced osmotic stress impairs plant growth by
reduction of water uptake, stomatal closure, and decline in photosynthetic activity.
In turn, ionic stress caused by specific salts taken up at above-optimum concentra-
tions influences the homeostasis of essential ions, metabolic activity, and integrity
of plasma membranes (reviewed in Sudhir and Murthy 2004; Rasool etal. 2012).
Priming with mild salt treatment can increase the tolerance of model plants and dif-
ferent crop species to subsequent salt stress, improving the physiological and growth
parameters connected to plant vigor and fitness.
Memory in salinity and osmotic stress responses in Arabidopsis were studied at
both, somatic and trans-generational level. Regarding the somatic memory, Sani
etal. (2013) reported that plants primed with low NaCl concentration accumulate
less sodium in their shoots, have higher biomass and better survival after triggering
I. Mozgova et al.
stress than control plants. The memory of initial stress was retained for at least
10days and salinity-primed plants acquired tolerance also to drought, highlighting
the crosstalk between the two stresses. Importantly for biotechnology applications,
the plants did not exhibit obvious growth retardation effects after the priming stress,
suggesting that memory did not come with a cost of overall plant vigor (Sani etal.
2013). Response to salinity stress in Arabidopsis was also related to proline content
(Feng etal. 2016). Proline is an amino acid implicated in metal chelation, antioxida-
tion and signaling, and its accumulation is positively correlated with tolerance to
various stresses (Hayat etal. 2012). Arabidopsis plants primed by salt (NaCl) exhib-
ited increased proline content upon subsequent stresses than non-primed controls.
The effect was dependent on the transcription of the gene encoding the enzyme
Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1) that mediates the rate-limiting
step of proline biosynthesis pathway (Feng etal. 2016).
In wheat, priming of seedlings with low NaCl concentration led to increased
tolerance to subsequent treatment with high NaCl concentrations. Specifically,
primed plants exhibited efficiently reduced chlorotic symptoms, undisturbed photo-
synthetic activity, and improved osmotic potential upon high salt stress than non-
primed controls (Janda etal. 2016). Higher tolerance to salinity stress was achieved
in rice by pre-treatment of seedlings with sublethal NaCl dose. Primed plants
showed better control of ion absorption, improved ion transport to leaves, less
affected photosynthesis activity, and enhanced accumulation of osmolytes for
osmotic adjustment than non-pre-treated controls (Djanaguiraman etal. 2006). In
sorghum (Sorghum bicolor), priming of seedlings with NaCl led to improved growth
upon severe salt treatment (Amzallag etal. 1990). In maize, priming treatment with
low salt significantly reduced the detrimental effect of high salt stress manifested by
less decreased chlorophyll concentration, water content, and stomatal conductance
in comparison with non-primed plants (Pandolfi etal. 2016). Salt priming effect was
also observed in other crops like pea (Pisum sativum—Pandolfi etal. 2012), potato
(Etehadnia etal. 2010), or olive (Olea europaea—Pandolfi etal. 2017). In potato
and olive, salt tolerance and priming effect were related also to cultivar type. In
potato, the biggest effect of priming was seen for relatively salt-sensitive cultivars
(Etehadnia etal. 2010), while in olive, priming had overall similar effect in improv-
ing salt tolerance, but affected plant organs to different extent, depending on the
cultivar (Pandolfi etal. 2017).
1.3.3 Heat
Increase in temperatures is one of the major predictions from climate change mod-
els that will likely deeply impact on food security as it impairs plant growth, affects
plant reproduction and, therefore, final yield (reviewed in Bäurle 2016).
In Arabidopsis, heat stress memory was studied mostly at the seedling stage.
Current evidence suggests that heat stress memory in Arabidopsis seedlings can be
kept up to 3days after initial stress (Lämke et al. 2016; Brzezinka et al. 2016).
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
However, the memory strength may decay within hours of recovery (Charng etal.
Works on heat stress memory in Arabidopsis served as an aid for similar studies
in agronomic plant species. For example, an experimental setup established for
Arabidopsis (Charng etal. 2006a, b) was applied to rice seedlings where the dura-
tion of the memory differed between cultivars (Lin etal. 2014).
The crosstalk between different stress types in crops was studied for heat, as
priming stress, and cold or salinity as triggering stress. For example, barley plants
subjected to high salt stress exhibit impaired growth, as measured by root elonga-
tion (Faralli et al. 2015). However, this response can be prevented by acute heat
shock priming (Faralli etal. 2015). The beneficial effect of heat shock priming in
protection against cold stress-mediated damage was observed in tomato
(Lycopersicon esculentum). Harvested tomato fruits exposed to non-freezing cold
conditions exhibit signatures of chilling injury, i.e. aroma loss, electrolyte leakage,
failure to ripen, and oxidative stress (Malacrida et al. 2006; Biswas etal. 2016).
However, post-harvest treatment of tomato fruits with higher temperature results in
decreased chilling injury upon subsequent cold stress (Saltveit 1991; Zhang etal.
Heat-stress memory has been frequently linked also to the tolerance to subse-
quent heavy metal exposure in crops. In wheat, priming heat shock was shown to
mediate higher viability rate of seedlings upon subsequent injection of iron and
cadmium salts to leaf segments (Orzech and Burke 1988). In wild tomato
(Lycopersicon peruvianum L.) cell suspension cultures, acute heat shock prevented
cell membrane leakage upon treatment with cadmium (Neumann et al. 1994). In
rice, short-term heat pre-treatment led to reduced cadmium-induced chlorosis in
seedlings (Hsu and Kao 2007; Chao etal. 2009; Chao and Kao 2010; Chou etal.
2012). Heat-shock-induced accumulation of antioxidative compounds is suggested
to play a prominent role in protection against subsequent exposure to cadmium (Hsu
and Kao 2007; Chao etal. 2009; Chao and Kao 2010; Chou etal. 2012). These stud-
ies indicate that heat pre-treatment can be efficient for priming against heat but also
heavy metal, cold or salt stresses.
1.3.4 Cold
Low temperature is also one of the major factors determining locations of crop pro-
duction and is periodically responsible for losses in crop yields (reviewed in
Thomashow 1999). Exposure to low temperatures causes various phenotypic symp-
toms such as poor germination rate, chlorosis, reduced organ expansion, wilting,
and inhibited reproductive development (reviewed in Yadav 2009). Cold memory in
Arabidopsis can be triggered by persisting or oscillating low temperature stress
(reviewed in Thomashow 1999; Markovskaya etal. 2008), both of which have an
immense impact on plant fitness to seasonal and daily temperature changes in the
I. Mozgova et al.
Arabidopsis response to triggering cold stress was assessed after two different
priming stress types, short-term cold stress (STC) or long-term cold stress (LTC),
both followed by a 5 day-long recovery phase. Only LTC plants showed higher
effective quantum yields of photosystem II and higher photochemical quenching
after triggering stress, in contrast to STC plants (van Buer etal. 2016). The results
indicate that long-term, but not short-term, priming allows better energy dissipation
through photosystem II in response to cold.
Cold stress memory was studied in a number of chilling-sensitive agronomic
species. Here, exposure to moderate temperatures before cold alleviates cold-
induced negative effects on plant growth and development. For example, in rice,
cold-priming prevents cold-induced impaired water uptake in roots, leaf wilting,
and color bleaching (Ahamed etal. 2012). Priming of maize was shown to protect
the photosynthetic apparatus from cold-induced damage. The authors used maize
inbred lines of different cold-sensitivity to demonstrate a crucial role of cold prim-
ing in chilling-resistant high cold-tolerant varieties (Sobkowiak etal. 2016). Cold
priming effect on different varieties was also studied in wheat (Charest and Ton
Phan 1990). Cold treatment led to increased soluble protein content, decreased
water content, and accumulation of proline even 30days after cold. Most impor-
tantly, such cold memory effect was more pronounced in winter than in spring
wheat cultivars. Cold priming has an effect in tolerance to subsequent exposure to
freezing temperatures in winter wheat and also in winter and spring cultivars of
canola (Trischuk etal. 2014).
Similar to heat priming, cold priming treatment was shown to increase resistance
to further exposure to stress of other types. For example, cold priming results in
better survival and growth of mustard seedlings exposed to salt and drought (Hossain
etal. 2013), in alleviated photoinhibition and oxidative cellular damage caused by
cadmium, copper or high light intensity in pea (Streb etal. 2008) and in increasing
resistance to heat stress (Zhang etal. 2006a; Wan etal. 2009).
1.3.5 Ultraviolet (UV-B) Radiation
UV-B is one of the types of ultraviolet light and a natural component of solar radia-
tion. Increased UV-B intensities are especially detrimental for plants due to their
sessile lifestyle and obligatory requirement for sunlight. UV-B stress can be divided
into low- and high-dose, and short-term (acute, seconds to hours) or long-term
(chronic, hours to days) exposure (reviewed in Brown and Jenkins 2007; Lang-
Mladek etal. 2012; Hideg etal. 2013). Whereas acute, high dose radiation causes
severe detrimental effects and results ultimately in programmed cell death, chronic,
low-dose UV-B causes effective activation of defense mechanisms and acclimation
to UV stress (reviewed in Hideg etal. 2013).
Arabidopsis plants exposed to long-term low-dose UV-B exhibited stress mem-
ory even after 9days of recovery period and showed morphological changes such as
decreased rosette diameter, reduced inflorescence height, increased number of flow-
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
ering stems, and stimulated axillary branching (Hectors etal. 2007). However, such
stress did not affect photosynthesis efficiency—increased pigment content compen-
sated reduced leaf area, preventing substantial growth impairment (Hectors et al.
2007). Arabidopsis plants treated with a 2-h pulse for several days showed increased
flavonoid content that eventually reaches a steady-state (Hectors etal. 2014). Such
result suggests a role of flavonoids in long-term UV memory and acclimation.
The response to low-dose UV treatment and the UV stress memory was studied
also in crops. Beneficial effect of low-dose UV-B was observed on morphological,
physiological, and metabolic levels. Plant species showing long-term beneficial
effect after UV-B stress range from crops (wheat, maize, rice) to commonly culti-
vated Brassicaceae (cabbage—Brassica oleracea, rapeseed—B. napus) and legumes
(mungo bean—Vigna radiata, kidney bean—Phaseolus vulgaris, cowpea—Vigna
unguiculata, soybean—Glycine max) (Thomas and Puthur 2017). Crop seeds
treated with UV-B exhibit, i.e. increased germination, faster growth rate, elevated
pigment content, and increased tolerance to other stresses (i.e., salinity, pathogens).
For example, increased germination rate as a result of UV-B treatment was seen for
maize (Wang etal. 2010); increased content of pigments for cabbage, beet (Beta
vulgaris), kidney bean (Kacharava etal. 2009), soybean (Yanqun etal. 2003), mash
bean (Vigna mungo—Shaukat et al. 2013), and rice (Olsson et al. 1998); and
increased biomass for tartary buckwheat (Fagopyrum tataricum Gaertn.—Yao etal.
2007). Increased chlorophyll or carotenoid content was reported for UV-treated
seedlings of rice (Xu and Qiu 2007), cowpea (Mishra etal. 2008), and bitter gourd
(Momordica charantia L.—Mishra etal. 2009).
1.3.6 Chemical Agents
Instead of applying initial mild abiotic stress, stress memory in plants can be also
induced by treatment with chemical compounds in a process called chemical prim-
ing. Such chemicals can be synthetic or of natural origin and include, i.e. amino
acids, hormones, nutrients, pesticides, reactive oxygen-nitrogen-sulfur species
(RONSS) (reviewed in Jisha etal. 2013; Savvides etal. 2016; Antoniou etal. 2016;
Lutts etal. 2016). One of the advantages of using chemical agents to prime plants
against environmental stresses is the robustness, enhancing plant resilience against
many different stress types.
Chemical priming on Arabidopsis was assessed in a number of studies. Pre-
treatment of Arabidopsis seedlings with the non-protein amino acid β-aminobutyric
acid (BABA) 1day before, either high salt or drought treatment showed improved
tolerance to subsequent stresses—lower wilting rate and water loss (Jakab etal.
2005). Interestingly, BABA is also a commonly used agent enhancing systemic
acquired resistance (SAR) for pathogen protection, indicating that the compound
triggers activation of a pathway common for biotic and abiotic stresses. Arabidopsis
plants pre-treated with melatonin showed better growth following cold stress, mani-
fested in fresh weight, root length and shoot length increase (Bajwa etal. 2014).
I. Mozgova et al.
Melatonin increased expression of cold-inducible genes at different timepoints dur-
ing stress (Bajwa etal. 2014), suggesting that the compound triggered a similar
primed state at the transcriptomic level as a mild cold pre-treatment (van Buer etal.
Spermine is a natural polyamine synthesized in eukaryotic cells and it was
reported to accumulate, along with the other polyamines, under abiotic stress condi-
tions (reviewed in Rhee etal. 2007). Pre-treated Arabidopsis seedlings with exoge-
nously applied spermine exhibited attenuated chlorosis in cotyledons compared to
controls. The crucial impact of spermine on heat acclimation was also confirmed by
genetic approaches—transgenic plants overexpressing spermine biosynthetic genes
showed less inhibited growth upon heat shock, whereas knock-out mutants were
hypersensitive to a high temperature (Sagor etal. 2013).
The exogenous application of chemical compounds on crops has frequently been
used for seed priming, because seeds can be more easily treated and with a minor
cost than the adult plants (reviewed in Jisha etal. 2013; Savvides etal. 2016; Lutts
etal. 2016). Confirmed for a big range of various agronomic plants, chemical pre-
treatment of seeds can increase the rate and percentage of seed germination. In
addition, it can have a beneficial effect in the longer term by improving seedling
vigor, especially during growth under stress conditions (reviewed in Savvides etal.
2016; Lutts etal. 2016). However, there are also reports showing priming effect of
chemicals, when applied at later developmental stages. The application of the chem-
ical on a specific organ, for instance roots, leaves, or stems, or at specific develop-
mental stage, such as seedlings, promoted a systemic response that will spread to
protect other parts of the plant and not only the organs that were treated in different
crops such as wheat (Hasanuzzaman etal. 2011; Shan etal. 2011; Turk etal. 2014),
rice (Uchida et al. 2002; Saleethong etal. 2013; Mostofa etal. 2014), maize (Li
etal. 2013), tomato (øúeri etal. 2013; Amooaghaie and Nikzad 2013), strawberry
(Fragaria sp.—Christou et al. 2013, 2014a, b), oil rapeseed (YÕldÕz etal. 2013;
Xiong etal. 2018), or tangerine (Citrus sp.—Shi etal. 2010).
1.4 Epigenetic Mechanisms ofAbiotic Stress Response
Responses to stress result in genome-wide changes to chromatin structure and gene
transcription or can be even associated with modifications to genomic sequence.
Exposure to stress induces alterations at all levels of chromatin structure, including
DNA methylation, nucleosome occupancy and composition, presence of histone
variants as well as histone PTMs and global chromatin arrangement. Uncoupling
the direct effects of stress on chromatin structure and nuclear architecture from its
effects on gene transcription is very challenging, making a large part of evidence
describing mechanisms of stress-induced changes correlative. In addition, even
though the connections between chromatin rearrangement and response to various
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
stresses are well established, the inheritance of the stress-induced chromatin struc-
ture is less well understood.
1.4.1 Global Changes toChromatin Structure
Various abiotic stresses lead to cytologically detected heterochromatin de-
condensation and release of transcriptional gene silencing (TGS) from TEs and
ribosomal RNA genes (rDNA) in different plant species. In Arabidopsis, prolonged
heat stress causes decompaction of centromeric repeats and 5S rDNA and TGS
release from specific TEs, hallmarked by the COPIA78 family (Pecinka etal. 2010).
Heat treatment of cold acclimated plants results in general de-repression of hetero-
chromatic (centromeric and pericentromeric) repetitive elements (Tittel-Elmer etal.
2010) and heat or UV-B stress releases TGS of transgenes as well as endogenous
loci (Lang-Mladek etal. 2010). Similarly, de-condensation of 45S rDNA clusters
follows salinity and heat stress in rice (Santos etal. 2011) or heat stress in rye
(Tomás etal. 2013), and loss of tandem repeat transcriptional silencing in hetero-
chromatin knobs follows cold treatment in maize (Hu etal. 2012). De-condensation
of heterochromatic regions and release of TGS may be a shared response to several
types of abiotic stresses. One possibility is that this may represent increased need
for ribosomal RNAs to support changes in protein synthesis or transcriptional repro-
gramming in specific genomic regions. The effects seem to be generally transient
(Pecinka etal. 2009, 2010; Lang-Mladek etal. 2010; Hu etal. 2012; Iwasaki and
Paszkowski 2014a) and may provide a time window that allows complex epigenetic
and gene expression changes in response to stress (Pecinka etal. 2010). Interestingly,
stress-induced TGS release is not necessarily connected to reduction of repressive
chromatin marks at the affected loci (such as DNA methylation, H3K9me2—
dimethylation of lysine 9 of histone 3—or H3K27me) (Lang-Mladek etal. 2010;
Pecinka etal. 2010; Tittel-Elmer etal. 2010) and can be associated with transient
reduction in nucleosome occupancy (Pecinka etal. 2010). Restoration of TGS to
naïve state requires factors such as the nucleosome chaperone CHROMATIN
ASSEMBLY FACTOR 1 (CAF-1) (Pecinka etal. 2010), the chromatin remodeler
MOLECULE 1 (MOM1) (Iwasaki and Paszkowski 2014a), and components of the
RNA-directed DNA methylation (RdDM) pathway (discussed in more detail in
Sect. 1.4.2). Global alterations to chromatin structure in response to stress resemble
chromatin changes during developmental transitions and may suggest functional
connection between developmental and stress-induced reprogramming (reviewed in
Probst and Mittelsten Scheid 2015). Even though the causal connection between the
triggering stress, global chromatin architecture change and stress-induced gene
transcription change is often unclear, strong correlative association is well docu-
mented. Exposure to abiotic stress factors such as salt, water availability, tempera-
ture, or UV-light results in global changes to histone modifications marks (for
example, van Dijk etal. 2010; Hu etal. 2012; Sani etal. 2013; Forestan etal. 2018)
I. Mozgova et al.
and/or DNA methylation (for example, Colaneri and Jones 2013; Secco etal. 2015;
Wang etal. 2015b, 2016a; Eichten and Springer 2015; Wibowo etal. 2016; Ganguly
etal. 2017) and is connected to global gene expression changes (for example, van
Dijk etal. 2010; Sani etal. 2013; Eichten etal. 2013; Ding etal. 2013, 2014; Secco
etal. 2015; Forestan etal. 2016; Wang etal. 2016a; Wibowo etal. 2016).
1.4.2 DNA Methylation Changes andtheRole ofTEs
inResponse toAbiotic Stress
Transcriptional activity of genes and especially TEs is affected by DNA methyla-
tion. In mammals, DNA methylation is found almost exclusively in the CG sequence
context during somatic development. In plants, however, any cytosine can be meth-
ylated and three functional sequence contexts are distinguished. Cytosines in the
symmetrical CG or CHG contexts as well as the non-symmetrical CHH (where H
represents A, T, or C) context can undergo methylation (reviewed by Law and
Jacobsen 2010; Du etal. 2015; Zhang etal. 2018a). Presence of DNA methylation
in all contexts generally contributes to TGS.Genome-wide distribution of DNA
methylation in plant genomes strongly correlates with the density of TEs where
DNA methylation safeguards the genome from unwanted activity of repetitive ele-
ments (Kato etal. 2003; Zhang etal. 2006b; Lister etal. 2008; Cokus etal. 2008;
Mirouze etal. 2009; Ito etal. 2011). In contrast, presence of only CG methylation,
typically in the bodies of moderately transcribed genes, does not have repressive
function in plants (reviewed in Bewick and Schmitz 2017). DNA methylation is
catalyzed by three classes of DNA methyltransferases in plants. DNA
METHYLTRANSFERASE 1 (MET1) is an evolutionarily conserved DNA-
replication- coupled maintenance CG methyltransferase. CHROMOMETHYLASE
(CMT) family harbors plant specific DNA methyltransferases, where CMT3 and
CMT2 act as CHG and CHH maintenance and de novo DNA methyltransferases
whose activities are coupled to the presence of H3K9me2 (Stroud etal. 2013;
Zemach et al. 2013). Finally, DOMAINS REARRANGED
METHYLTRANSFERASES (DRMs) are guided to the target sites by RdDM.In
RdDM, 24nt siRNAs are produced following transcription of target loci from a
double-stranded RNA precursor by the joint action of the plant-specific DNA-
dependent RNA polymerase IV (RNA pol IV, NRPD), RNA-DEPENDENT RNA
POLYMERASE 2 (RDR2) and DICER-LIKE3 (DCL3). The siRNAs are loaded
into ARGONAUTE 4 (AGO4)-containing complex and paired with another plant
specific DNA-dependent RNA polymerase V (RNA pol V, NRPE)-produced nascent
transcripts, recruiting chromatin modifier complexes including DRMs (reviewed by
Law and Jacobsen 2010; Du etal. 2015; Zhang etal. 2018a). RdDM is a pathway
that provides a backup for other methylation pathways and can largely restore origi-
nal methylation patterns if necessary (Teixeira etal. 2009; Baubec etal. 2014).
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
A large number of studies have addressed DNA methylation and gene expression
changes induced by abiotic stresses in different model and crop plants. In general,
exposure to abiotic stresses induces global changes in DNA methylation amount
and distribution in different plant species. The changes affect not only the exposed
plant generation but, in some cases, also their progeny (Bilichak etal. 2012; Boyko
etal. 2010; Colaneri and Jones 2013; Eichten and Springer 2015; Jiang etal. 2014;
Secco etal. 2015; Steward et al. 2002; Wang et al. 2015b; Wibowo et al. 2016;
Yong- Villalobos etal. 2015). Whether a particular stress induces targeted changes
to DNA methylation is not clear. In Arabidopsis, it was suggested that DNA meth-
ylation changes may be stress-type-specific (Wibowo etal. 2016). However, analy-
sis of DNA methylation in individual maize plants exposed to various abiotic
stresses showed that DNA methylation changes in response to abiotic stress are
stochastic and unrelated to particular stress-type (Eichten and Springer 2015).
Additionally, upon drought stress in five generations of Arabidopsis, only stochastic
changes in DNA methylation without epiallele accumulation were observed
(Ganguly etal. 2017), supporting the idea of DNA methylation changes observed
during stress being mostly stochastic.
DNA methylation machinery may nevertheless represent an integral component
of abiotic stress responses and memory. For example, expression of DNA methyl-
transferase genes is modulated by inorganic phosphate (Pi) availability in
Arabidopsis and mutants in the methyltransferases DRM1, DRM2 and CMT3 or
RNAi MET1 plants display impaired response and hypersensitivity to Pi starvation
(Yong-Villalobos etal. 2015). Similarly, Arabidopsis nrpd2 mutants are hypersensi-
tive to heat-stress (Popova etal. 2013). Transcription of RdDM and DNA demeth-
ylation genes responds to hyperosmotic stress (Wibowo et al. 2016) and
intergenerational memory of stress-response genes is affected in nrpd1a, cmt3, and
DNA demethylase mutants (Wibowo etal. 2016). Stress-induced changes in DNA
methylation can affect the expression of stress-responsive genes (Colaneri and
Jones 2013; Wibowo etal. 2016). In contrast, correlation between DNA methylation
and gene expression of plants treated with drought stress was not observed (Ganguly
etal. 2017). Additionally, stress-induced transcriptional changes at methylated loci
are not always accompanied by DNA methylation changes (for example, Lang-
Mladek etal. 2010; Pecinka etal. 2010; Tittel-Elmer etal. 2010; Song etal. 2012b).
Thus, the connection between DNA methylation and stress-induced transcriptional
changes is not uniform.
Direct effects of DNA methylation on gene expression (Fig.1.2) can stem from
the change of chromatin state at an affected locus or from altered properties of regu-
latory regions—over 75% transcription factors are affected by DNA methylation for
their binding to DNA (O’Malley etal. 2016). Negative correlation between DNA
methylation with gene expression in response to abiotic stress is mainly observed.
For instance, cold treatment of maize seedlings induces hypomethylation at the
genomic fragment ZmMI1 in roots which correlates with its elevated transcription
(Steward et al. 2002). Salt stress in soybean leads to the hypomethylation of
promoter regions and transcriptional activation of several salt-responsive transcrip-
tion factor genes (Song etal. 2012b). In contrast, increase in DNA methylation on
I. Mozgova et al.
Protein coding gene - sense
lncRNA - antisense
No stress
Hyperosmotic stress
21nt - PTGS
no transcription
activator sequence
small RNA
element present or not
intron or intergenic region
Fig. 1.2 Stress-induced changes to gene expression connected to DNA methylation and transpos-
able elements (TEs). (a) The role of DNA methylation and TEs in affecting gene expression in
response to stress. (i) Upon stress, global DNA methylation distribution and level can be changed,
potentially affecting gene expression. Stress-induced changes in DNA methylation and associated
gene expression are often connected to the presence of TEs or their residual sequences in the
upstream regions of affected genes and to general release of transcriptional gene silencing (TGS)
from TEs and other repetitive elements. This is associated with the production of 24 nt small
RNAs. Silent (methylated) state can be re-established by RNA-directed DNA methylation
(RdDM). (ii) TEs can affect genomic loci in-trans. (iii) TEs can be a source of 21nt small RNAs
that mediate post-transcriptional gene silencing (PTGS) in trans (McCue etal. 2012, 2013). (iv)
Alternatively, upon very severe stress (and/or in combination with deficient RdDM), TEs can
transpose and their de novo integration can disrupt regulatory regions or gene bodies, impairing the
expression of a gene (for example, Ito etal. 2016). Alternatively, (v) TEs can integrate into gene
regulatory regions, introducing novel stress-responsive elements that they carry (for example,
Cavrak etal. 2014). By TE integration to the upstream region, the target gene can also become
silenced by the in-trans activity of RdDM (vi). (b) Stress-induced gene expression can induce
DNA methylation at adjacent TEs. This may serve as a mechanism that protects TE-rich genomes,
such as in rice (Secco etal. 2015). (c) Gene expression can be downregulated upon stress by the
loss of DNA methylation at downstream loci, which correlates with the transcriptional activation
of antisense long non-coding RNAs (lncRNAs) (Wibowo etal. 2016)
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
stomata- specifying transcription factor genes SPEECHLESS (SPCH) and FAMA in
response to low humidity was observed, corresponding with their downregulation
and decrease in relative number of stomata (Tricker etal. 2012). DNA-methylation-
coupled changes in gene expression can be connected to the presence of TEs or their
partial sequences in the proximity or within protein-coding genes (Fig.1.2a). TE
transposition can be induced by some severe abiotic treatments including gamma-
irradiation (Nakazaki etal. 2003) or hydrostatic pressure (Lin etal. 2006), potentiat-
ing the emergence of novel insertion sites. However, TE transposition does not seem
to be a common response to abiotic stresses (reviewed in Negi et al. 2016). In
Arabidopsis, heat stress-induced TE mobilization was observed only in mutants of
the RdDM pathway (Mirouze etal. 2009; Ito etal. 2011, 2016), indicating stringent
control of TE mobility. More frequently, abiotic stresses including salinity, flood-
ing, heat, cold, or UV-light stress cause general release of TGS of endogenous
repetitive sequences including TEs and can also increase the frequency of homolo-
gous recombination in Arabidopsis (Molinier etal. 2006; Pecinka etal. 2009, 2010;
Boyko etal. 2010; Tittel-Elmer et al. 2010). Transcriptional activation of TEs in
response to various abiotic stresses also occurs in different crop species, including
maize (Makarevitch etal. 2015), oat (Avena sativa) (Kimura etal. 2001), durum
wheat (Triticum durum) (Woodrow etal. 2010), or blood oranges (Citrus sinensis)
(Butelli etal. 2012). In maize plants subjected to various abiotic stresses including
heat, cold, UV-light, and high salt, activation of 20–30% of stress-responsive genes
is associated with TGS release of proximal TEs that act as local enhancers
(Makarevitch etal. 2015). In Arabidopsis subjected to hyperosmotic treatment, dif-
ferentially methylated regions overlapping with genes that harbor proximal TEs
were identified. Approximately 30% of these genes changed their expression in
response to osmotic stress (Wibowo et al. 2016). In several rice varieties, the
inverted-repeat TE miniature Ping (mPing) can locate into regions inducing the
expression of genes responding to cold or salt stress (Naito etal. 2009; Yasuda etal.
In addition to general TGS release of TEs upon stress, specific stress-mediated
activation of TEs can be conferred by stress-responsive elements present within the
TE sequence itself. Heat, drought, and ABA-response elements are found in the
proximity and within a TE-derived repetitive sequence upstream of Arabidopsis
heat-responsive genes (Popova etal. 2013). The heat-responsive Ty1/Copia-type
retrotransposon ONSEN (COPIA78) contains a target site for the plant heat-
responsive transcription factor HFSA2, exploiting the plant’s innate heat-stress
response system for its activation (Cavrak et al. 2014). The transcription factor
binding site is evolutionary conserved in COPIA78 transposons and several other
transposon families, making it apparently possible to trick the host genome in a
similar way (Pietzenuk etal. 2016). Different TE families can be associated with
different stress responses (Beguiristain etal. 2001; Makarevitch etal. 2015), sup-
porting the notion that selective transcriptional activation of TEs in the upstream
regulatory regions of stress-responsive genes may be an integral part of stress-type-
specific responses in plants.
I. Mozgova et al.
The interplay between stress-induced changes in gene expression and TE meth-
ylation can also act in an opposite direction (Fig.1.2b). Stress-induced changes in
DNA methylation at TE loci can follow altered transcription of neighboring stress-
responsive genes, as is the case in Pi-starved rice plants (Secco etal. 2015). Here,
the newly deposited DNA methylation in TEs does not restrict the expression of the
neighboring genes but may serve as a protective measure against reactivation of TEs
located close to highly transcribed genes. Interestingly, this response is species spe-
cific, not observed in Arabidopsis, perhaps reflecting the different genome organiza-
tion in the two species, in particular the relatively low abundance of TEs in
Arabidopsis compared to rice (Secco etal. 2015; Yong-Villalobos etal. 2015).
Due to mechanisms of DNA methylation maintenance and re-establishment fol-
lowing DNA replication (reviewed in Du etal. 2015), stress-induced DNA methyla-
tion changes have the potential to be maintained somatically and also inter- or
transgenerationally. The maintenance of stress-induced DNA methylation changes
over sexual generations, however, seems limited either to the generation of stress-
exposed plants (somatic memory) or to the first generation of their progeny (inter-
generational), being progressively reset to the pre-treatment state in the absence of
stress (Pecinka etal. 2009; Boyko et al. 2010; Secco etal. 2015; Wibowo etal.
2016; Ganguly etal. 2017). This has been attributed to epigenetic reprogramming
mainly in the male germline (Wibowo etal. 2016) and active resetting of DNA
methylation by RdDM (Ito etal. 2011; Popova etal. 2013). In wild-type plants, the
heat-induced transcription of ONSEN decreases during recovery after the stress but
in plants carrying mutations in genes of the RdDM pathway, including NRPD2,
ONSEN activity persists and retrotransposition occurs (Ito etal. 2011). NRPD2 is
also required for the re-establishment of heat-released TGS and restoration of CHH
methylation at RdDM target loci during resetting of heat stress-induced genes
(Popova etal. 2013). RdDM therefore seems to be a key pathway involved in the
resetting of the pre-stress DNA methylation patterns. DNA methylation may how-
ever be implicated also in stress memory, as intergenerational increase of resistance
to hyperosmotic stress and transcriptional memory also depend on the NRPD1a,
CMT3, or DNA demethylation (Wibowo etal. 2016).
In summary, stress-induced changes to DNA methylation and associated stress
responses are mostly reversible in the absence of the initial stress. Somatic and
intergenerational resetting of DNA methylation is in large governed by RdDM and
sexual transmission of acquired chromatin states is mitigated by global epigenetic
reprogramming in the germline. Nevertheless, TE mobilization potentiates trans-
generational stability of altered DNA methylation connected with structural changes
to the genome (Fig.1.2a).
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
1.4.3 The Role ofSmall RNAs inPost-Transcriptional
Regulation ofStress-Responsive Genes
Abiotic stresses including cold, drought, salt, nutrient deficiency, and oxidative
stress induce the production of long non-coding RNAs and small RNAs of different
classes (reviewed in Borges and Martienssen 2015) that affect the expression of
stress-responsive genes (reviewed in Shukla etal. 2008; Sunkar etal. 2012; Kumar
2014; Zhao etal. 2016a) in Arabidopsis (Sunkar 2004; Zhou etal. 2008; Amor etal.
2009) and in crops including wheat or barley (reviewed in Alptekin etal. 2017),
maize (Wang etal. 2014; Lunardon etal. 2016), rice (Liu etal. 2017), Brachypodium
distachyon (Wang etal. 2015a), foxtail millet (Setaria italica—Wang etal. 2016b),
or legumes (Trindade etal. 2010).
MicroRNAs (miRNAs) modulate stress-responsive gene expression through
post-transcriptional gene silencing (PTGS). In PTGS 20–22nt long miRNAs origi-
nating from RNA polymerase II-mediated transcription of miRNA-coding genes and
processing of their transcripts by DCL1 incorporate into AGO1-containing RNA-
induced silencing complex (RISC) that mediates cleavage of miRNA-targeted tran-
scripts (reviewed in Borges and Martienssen 2015). The expression of
stress-responsive miRNAs can be both upregulated or downregulated, affecting the
expression of their target genes negatively or positively, respectively. For example,
in Arabidopsis, drought reduces the expression of miR169 that targets a drought
response-activating transcription factor NFYA5, increasing the abundance of the
NFYA5 and contributing to drought resistance (Li etal. 2008). On the contrary,
several conserved miRNAs are upregulated in response to drought stress in
Medicago truncatula (Trindade etal. 2010). Among those are the miRNAs miR398
and miR408, whose upregulation by drought suppresses the abundance of their tar-
get transcripts, which code for proteins involved in copper homeostasis (Trindade
etal. 2010). miR398 is upregulated in response to abiotic stresses targeting the cop-
per metabolic genes in several species (Sunkar et al. 2012). Interestingly in
Arabidopsis, where miR398 targets the genes Zn/Cu SUPEROXIDE DISMUTASE 1
(CCS1), it is downregulated under oxidative stress but upregulated in response to
copper deprivation, regulating these genes in an opposing manner to fine-tune their
dosage in response to abiotic conditions (Sunkar etal. 2006; Yamasaki etal. 2007;
Beauclair etal. 2010).
In addition to miRNAs, other classes of small RNAs have been implicated in
regulation of abiotic stress responses. For example, 21 and 24nt natural antisense
siRNAs (natsiRNAs) produced from overlapping transcripts of convergent gene
pairs SIMILAR TO RCD ONE 5 (SRO5) and a gene encoding Δ1-pyrroline-5-
carboxylate dehydrogenase (P5CDH) establish salt stress tolerance in Arabidopsis
(Borsani etal. 2005). Interestingly, in addition to affecting gene expression in-cis
TEs can influence stress-responsive gene expression also post-transcriptionally in-
trans (Fig.1.2c). This is demonstrated by the effect of TGS release of the GYPSY-
type LTR retrotransposon ATHILA6 following heat stress in Arabidopsis. Upon
I. Mozgova et al.
transcriptional activation, 21–22nt trans-acting siRNA (tasiRNA854) is produced
from the ATHILA6 locus that targets the transcript of UBP1b, encoding a stress
granule-formation protein (McCue etal. 2012). Several other genes regulated in a
similar fashion were identified, suggesting a more general mechanism of in-trans
regulation of gene transcription following stress-induced release of TGS of TEs
(McCue etal. 2013). In contrast to the traditional role in PTGS, 21nt small RNAs
in concert with AGO1 can also participate in the transcriptional activation of stress
and hormone-responsive genes. AGO1 interacts with SWI3 and BSH, subunits of
the SWI/SNF chromatin remodelers, and guided by the different classes of 21nt
RNAs (including miRNAs and tasiRNAs), the complex can be recruited to activate
the target genes. The number of AGO1 targeted regions is enhanced by different
biotic and abiotic triggers, including cold stress, and these are enriched for the
stress-specific genes, indicating targeted effect (Liu etal. 2018a). In addition, in B.
distachyon, stress-induced siRNAs target regulatory intronic regions, possibly
affecting splicing (Wang etal. 2015a).
Interestingly, miRNAs can also be involved in the memory of abiotic stresses.
Heat stress induces the expression of miR156, which correlates with the downregu-
(SPL) transcription factor genes. Maintained level of miR156 is required for the
memory of recurring heat stress and miR156, an evolutionarily conserved miRNA
in plants, may mediate crosstalk between responses to environmental conditions
and plant development (Stief etal. 2014; Cui etal. 2014).
Antisense long non-coding RNAs (lncRNA) have been implicated in hyperos-
motic stress response and memory (Wibowo etal. 2018) (Fig.1.2c). Upon stress-
induced hypomethylation, antisense lncRNA is transcribed from the locus encoding
a metabolic sensing gene CARBON/NITROGEN INSENSITIVE 1 (CNI1). This acti-
vation inversely correlates with the sense transcription of CNI1 through a yet
unknown mechanism. Interestingly, regions differentially methylated upon stress
were enriched with proximal hyperosmotic stress-responsive antisense lncRNAs,
indicating that this may be a more general mechanism of interplay between DNA
methylation stress-response gene control (Wibowo etal. 2018).
Together, non-coding RNAs are emerging as integral components of stress
response but also memory pathways. Overexpression of transgenic miRNAs has
been used in Arabidopsis as well as crop species to successfully modulate sensitiv-
ity to various abiotic stresses (reviewed in Zhang 2015). The use of transgenic miR-
NAs or artificial miRNAs may present a promising approach to future crop
improvement. At the same time however, more research is needed to decipher the
mechanism of function of stress-response-associated miRNAs, to identify broader
gene regulatory networks that are affected by the respective miRNAs and to distin-
guish general and tissue- or species-specific effects of miRNA expression (reviewed
in Zhang 2015).
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
1.4.4 Modifications ofHistone–DNA Interactions
byChromatin Remodelers
ATP-dependent chromatin remodelers use the energy of ATP hydrolysis to alter
DNA–histone interactions and modify the accessibility to the genetic information.
This action can have both positive and negative effects on the regulation of gene
expression (reviewed in Clapier and Cairns 2009; Narlikar etal. 2013; Reyes 2014;
Han etal. 2015). DNA-dependent ATPases of the SNF2 family act as the enzymatic
subunit of large SWI/SNF (SWItch/Sucrose Non-Fermentable) multi-subunit com-
plexes that have been involved in the alteration of nucleosome position and assem-
bly (reviewed in Narlikar etal. 2013). SNF2 proteins were first discovered in yeast
(Egel etal. 1984; Neigeborn and Carlson 1984), but they are conserved in animals
(Flaus etal. 2006) and plants (Hu and Lai 2015; reviewed in Knizewski etal. 2008;
Sarnowska etal. 2016). Plants have larger SNF2 families with more than 40 mem-
bers (Flaus etal. 2006; reviewed in Knizewski etal. 2008; Hu and Lai 2015). Plant
SWI/SNF complexes have been involved in the cellular reprogramming triggered
by diverse abiotic stresses. Three of the four members of the SNF2 subfamily in
Arabidopsis have been implicated in the regulation of stress responses and in the
control of plant development upon abiotic stress. CHR12/MINUSCULE 1 (MINU1)
is required to arrest plant development in response to moderate heat, salinity, or
water deficiency stresses (Mlynárová etal. 2007) and the reduced germination phe-
notype of both MINU1 and CHR23/MINU2 overexpressing plants was enhanced
under mild salt or mild temperature stress conditions (Leeggangers etal. 2015).
BRAHMA (BRM) has an important role in the ABA-mediated post-germination
growth arrest under water scarcity stress and is involved in repressing early stress
responses during germination (Han etal. 2012; Peirats-Llobet et al. 2016). BRM
directly represses the expression of the gene ABA INSENSITIVE 5 (ABI5) and many
of the phenotypes observed in brm mutants are due to an overactive stress response.
These results also indicate the intricated link between environmental stress and
development, as most of the brm developmental phenotypes were mitigated in the
double brm abi5 mutant. BRM direct repressive action upon ABI5 was related with
positioning of a nucleosome at the transcription start site (TSS) of this gene which
may block initiation of transcription (Han etal. 2012). BRM and SWI3B, another
subunit of the SWI/SNF complex in Arabidopsis (Sarnowski etal. 2002), are able to
interact with HYPERSENSITIVE TO ABA1 (HAB1), a type 2C phosphatase that
negatively mediates ABA signaling. However, brm and swi3b mutants showed
opposite phenotypes to ABA, whereas swi3c mutant plants are ABA hypersensitive
similarly to brm plants (Saez etal. 2008; Han etal. 2012). A possible scenario is that
SWI3B contributes to the ABA response as part of a different complex (reviewed in
Asensi-Fabado etal. 2017). BRM also interacts with ABA-activated Sucrose non-
fermenting 1-Related protein Kinases (SnRKs) (Saez etal. 2008; Peirats-Llobet
etal. 2016). Therefore, the current model proposes that ABA-induced phosphoryla-
tion of BRM by SnRKs and dephosphorylation by HAB1 may rapidly regulate the
activity of the BRM-associated SWI/SNF complex without the requirement to evict
I. Mozgova et al.
it from the chromatin of stress-related genes (Peirats-Llobet etal. 2016). However,
BRM has been directly involved in activation and repression of many different
stress-responsive genes (Archacki etal. 2016) and, therefore, more molecular data
will be required to understand if phosphorylation/dephosphorylation of BRM is a
rule in the transcriptional reprogramming mediated by its associated complex in
response to abiotic stress conditions. In addition to ABA-mediated responses, BRM
has also been involved in the regulation to heat stress through repression of a subset
of heat-responsive genes (Buszewicz etal. 2016). The Rolled Fine Striped (RFS)
gene of rice encodes a member of the Mi-2 subfamily (Cho etal. 2018). In rfs-2
plants, essential genes involved in ROS scavenging are downregulated correlating
with changes in particular histone modifications. However, it is still unknown if the
changes in the covalent marks were directly or indirectly due to RFS. Although
ROS accumulation occurs as a result of abiotic stresses, the possible role of RFS in
the regulation of stress responses has not been elucidated yet (Cho etal. 2018).
Alkaline Tolerance 1 (ALT1) is a rice protein that belongs to the Ris1 subfamily,
which is a SWI2/SNF2 specific group of plants and fungi (Hu etal. 2013; reviewed
in Knizewski etal. 2008). alt1 mutants and ALT1-iRNA plants showed decreased
sensitivity to alkaline stress probably due to an impairment of ROS homeostasis
induced by this stress (Guo etal. 2014). Considering that alkaline salts have a more
severe effect on crop growth and yield than neutral salts (Zhang etal. 2017), it will
be very interesting to fully understand the molecular roles of plant-specific ALT1-
like proteins as a way to improve plant resistance. The role of SWI2/SNF2 ATPases
in the regulation of an environmental-induced molecular memory was indirectly
revealed through its association to another DNA-dependent ATPase called
FORGETTER 1 (FGT1) (Brzezinka etal. 2016). FGT1 is the single Arabidopsis
member of a different family of chromatin remodelers called Strawberry Notch
(Sno) (Majumdar et al. 1997; Brzezinka et al. 2016; Watanabe et al. 2017).
Arabidopsis fgt1 mutant plants were not able to maintain the expression of heat-
shock memory genes after a heat shock stress and, subsequently, showed a decreased
memory to passed heat shock events. FGT1 binds to heat-shock memory genes
before application of the stress and its binding increases just after the stress correlat-
ing with an upregulation of target genes (Fig.1.3). FGT1 interacts with BRM and
CHR11 and CHR7 in planta. CHR11 and CHR7 are the two members of the
Imitation Switch (ISWI) subfamily, which also belongs to the SNF2-group (reviewed
in Knizewski etal. 2008; Li etal. 2017). In Arabidopsis, they regulate gametogen-
esis and have been involved in regulation of nucleosome spacing (Huanca-Mamani
etal. 2005; Li etal. 2014b). Single brm and chr11 mutants and the double chr11/;
chr7+/ were also impaired in heat-shock acclimation and, as in fgt1 plants, high
heat-shock related gene expression was not sustained after heat shock (Brzezinka
etal. 2016). Genome-wide analyses in nonstressed plants demonstrated that binding
of BRM overlaps with FGT1 binding in heat-shock memory genes and transcrip-
tional analyses had already pointing out a role of BRM in regulating the expression
of heat-responsive genes (Brzezinka etal. 2016; Buszewicz etal. 2016). Considering
the nature of FGT1 and its interaction with other main chromatin remodelers, an
obvious possibility was that this protein acts in nucleosome remodeling at target
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
genes. To confirm this hypothesis, fgt1, brm, and chr11/;chr7+/ mutant plants
showed an increase in nucleosomes at the TSS of heat-shock memory genes without
stress conditions and in fgt1 plants recovery of nucleosome DNA at the TSS during
acclimation was faster than in WT plants. Therefore, FGT1 might be involved in
poising target genes into a more easy-to- activate state and has been proposed that
could act as a linker between SWI/SNF and ISWI remodeling complexes (Brzezinka
etal. 2016). Why does heat-stress memory require the concerted action of different
Fig. 1.3 Chromatin changes associated with transcriptional stress memory. The first encounter of
stress (priming stress) induces initial transcriptional onset of stress response genes that is associ-
ated with modification of the naïve-state repressive chromatin structure towards accessible tran-
scriptionally active structure (type I memory) or accessible transcriptionally inactive structure
(poised—type II memory). Both these states predispose enhanced transcriptional response upon
triggering stress. Type I memory is marked by continuous transcriptional activity of stress-response
genes. This is, for example, connected to the recruitment of a putative helicase FORGETTER 1
(FGT1) to the transcription start sites (TSSs) of heat-response genes and recruitment of chromatin
remodelers (CF-R, such as the SWI/SNF—Brzezinka etal. 2016). Type II memory is associated
with chromatin changes that are uncoupled from elevated gene transcription. Type II memory can
be mediated by different sets of factors. First, the stress-response transcription factors (TFs) that
are responsible for the initial transcriptional activation during priming response. Second, the
“memory factors” (MF) (such as the heat-shock factor HSFA2) Lämke etal. 2016) or the transcrip-
tion factor HY5 (Feng etal. 2016) that are not required for the initial transcriptional activation but
ensure the establishment and/or maintenance of heritable accessible chromatin structure, puta-
tively by recruiting chromatin modifiers (CF-H, such as histone methyltransferase complexes—
HMT). Type II memory chromatin is associated with RNA polymerase II phosphorylated on serine
5 (Ser5 pol II—Ding etal. 2012) and histone PTMs H3K4me3 but also H3K4me2 or H3ac
I. Mozgova et al.
chromatin remodelers? and are these complexes involved in the memory to other
stresses? are still unaddressed questions that will require further analysis.
1.4.5 Histone Variants andNucleosome Assembly
As one of the main components of the chromatin, histones play a very important
role in transcriptional regulation. Different histone variants are described: canonical
histones and other histone variants. While synthesis of canonical histones, and its
incorporation to chromatin is mostly coupled to DNA replication, other histone
variant genes are expressed independently of cell division and their exchange occurs
in connection to transcription. The turnover of histones contributes to the regulation
of gene expression enabling fast cellular reprogramming that occurs, for instance,
during the response to environmental stresses (Deal and Henikoff 2011; Henikoff
and Smith 2015; Jiang and Berger 2017; Talbert and Henikoff 2017). The structure
and function of a nucleosome containing histone variants differs from that contain-
ing canonical histones. Further, canonical and histone variants can contribute to
recruit specific proteins to chromatin (Koyama and Kurumizaka 2018). So far, most
described histone variants belong to H3 and H2A families. Besides the canonical
H2A, there are three other H2A variants: H2A.X and H2A.Z, also present in ani-
mals, and H2A.W, a plant-specific variant. The sequence diversity among these four
H2A versions affects the DNA–histone and histone–histone interactions impacting
chromatin stability (Deal and Henikoff 2011; Jiang and Berger 2017; Talbert and
Henikoff 2017; Osakabe etal. 2018). H2A.Z fulfills an important role in transcrip-
tional regulation; and, although its exact role is not fully clear yet, it seems to coun-
teract DNA methylation (Zilberman etal. 2007). In Arabidopsis, H2A.X plays a
role in DNA repair in euchromatic regions (Lorkoviü et al. 2017; Osakabe etal.
2018). H2A.W is abundant at heterochromatic TE-enriched regions and acts in
DNA repair at heterochromatic regions (Yelagandula et al. 2014; Lorkoviü etal.
2017; Osakabe et al. 2018). H3.1 is the canonical H3, whereas the transcription-
coupled H3.3 (Deal and Henikoff 2011; Jiang and Berger 2017; Talbert and Henikoff
2017), sperm cell-specific H3.10 (or MALE GAMETE-SPECIFIC HISTONE3,
MGH3) (Okada etal. 2005; Ingouff etal. 2007, 2010), and the centromeric CenH3
(Lermontova etal. 2006; Ravi etal. 2011) are variants of H3. H3.3 is the closest
related to canonical H3.1 that are differently targeted by chromatin modifying
enzymes and deposited at distinct genomic loci (Stroud etal. 2012; Jacob etal.
2014). The bulk of information about histone variants comes from Arabidopsis and,
for example, histone variants of cereals display some special features (Waterborg
1991; Shan etal. 2011; Cui etal. 2015; Hu and Lai 2015). Future studies in crops
and other plant species are foreseen to reveal the conservation of histone variants
and their functions in plants.
Current knowledge of the involvement of histone variants in responses to the
environment comes from analyses of histone chaperone mutants. Histone chaper-
one complexes are usually well conserved among different organisms and are key in
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
depositing histones for nucleosome assembling dependently or separately of DNA
replication (Deal and Henikoff 2011; Henikoff and Smith 2015; Jiang and Berger
2017; Talbert and Henikoff 2017). Among these complexes, the chromatin remodel-
ing complex SWI2/SNF2-Related 1 (SWR1), highly conserved in eukaryotes, con-
tributes to the replacement of H2A by H2A.Z at target genes. H2A.Z and components
of the SWR1 complex modulate response to ambient temperature in monocot and
eudicot plants coupling this response to developmental plasticity and yield (Kumar
and Wigge 2010; Boden etal. 2013; Cortijo etal. 2017). Sensitivity of plants to
increases in ambient temperature (i.e., still below stress threshold) relates to the
presence of H2A.Z in specific genes. Thus, H2A.Z has been proposed as a key com-
ponent of the thermosensory machinery in plants. At low temperature H2A.Z is
enriched genome-wide, posing the target genes to dynamically respond to tempera-
ture increase. Upon temperature rise, the Heat Shock Factor A1 (HSFA1) family of
TFs is recruited to chromatin and promotes removal of H2A.Z, increase in chroma-
tin accessibility, and induction of transcriptional activation of temperature-
responsive genes (Kumar and Wigge 2010; Cortijo etal. 2017). In addition to this
role in perception of an environmental cue, H2A.Z also has a role in response to
heat stress that is particularly harmful during seed development, strongly impacting
plant yield. Using B. distachyon, Boden etal. (2013) showed a differential sensitiv-
ity of vegetative and reproductive organs in response to moderate heat stress that
was associated with higher thermostability of H2A.Z nucleosomes in vegetative
tissue and the transcriptome of SWR1-RNAi grains resembled that of wild-type
grains under high temperatures (Boden etal. 2013). H2A.Z may also play a role in
response to nutrient starvation. In SWR1 complex mutant plants, the decrease of
H2A.Z in specific genes mimicked the phenotypes of plants grown under low Pi
concentrations (Zahraeifard et al. 2018). In Arabidopsis, depletion of
H2A.Z-containing nucleosomes from the chromatin of the AtMYB44 gene has been
correlated with the strong induction of this gene in plants grown under salt stress
conditions (Nguyen and Cheong 2018). h2a.z mutants showed genome-wide mis-
regulation of stress-responsive genes, indicating a broad contribution of H2A.Z to
stress responses (Coleman-Derr and Zilberman 2012) and, indeed, in response to
stress a genome-wide decrease of H2A.Z is observed (Kumar and Wigge 2010; Sura
et al. 2017). In addition to the H2A.Z variant, a wheat histone variant called
TaH2A.7, closely related to H2A.W of Arabidopsis, plays a specific role in drought
tolerance. The expression of TaH2A.7 is strongly induced under drought conditions
and when overexpressed in Arabidopsis increases drought resistance (Xu et al.
2016). Therefore, further analyses in other plant species will be required to fully
understand the roles of H2A.W-like variants in response to water deficiency. Another
group of histone chaperone involved in stress responses is the Nucleosome Assembly
Protein (NAP)-family. NAPs work as H2A and H2B chaperones, but are also
involved in the assembly of H3/H4 dimers into the nucleosome and in assisting
SWR1 in the deposition of H2A.Z (Dong et al. 2003; Jiang and Berger 2017).
Arabidopsis mutants affected in the three constitutive NAP1 genes were affected in
their response to salt stress (Liu etal. 2009). OsNAPL6, proposed to encode a H3/
H4 specific chaperone, has been related to resistance to different stresses in rice and
I. Mozgova et al.
when overexpressed results in biomass and yield improvement under drought or
salinity stress (Tripathi etal. 2016).
Three histone variants for the linker H1 (H1.1, H1.2, and H1.3) have been
described and, among them, H1.3 seems to play a prominent role in the regulation
of stress responses. H1.3 protein has shorter N- and C-termini which may affect its
interaction with DNA (Over and Michaels 2014; Jiang and Berger 2017). Water
deficiency induces the expression of the His1.3 gene in Arabidopsis, levant cotton
(Gossypium herbaceum L.), and tomato (Ascenzi and Gantt 1997; Scippa etal.
2000, 2003; Trivedi etal. 2012), but, interestingly, not in tobacco (Nicotiana taba-
cum L.—Przewloka etal. 2002). Low light conditions alone or in combination with
water deficiency also increases expression of His1.3 in Arabidopsis and lack of
H1.3 impairs developmental adaptations to these combined stresses (Rutowicz etal.
2015). ABA-mediated induction of the His1.3 gene during stress signaling has been
proposed (Cohen etal. 1991; Bray etal. 1999). Although still not fully clear, H1.3
may play a role during the response to stress by competing with other H1 variants
and destabilizing chromatin structure (Rutowicz etal. 2015).
Despite the demonstrated role of histone variants in immediate stress response,
there is not much evidence connecting them to stress memory. Several examples
nevertheless suggest involvement of histone variants and their chaperones in mem-
ory. ANTI-SILENCING FUNCTION 1 (ASF1) is a conserved histone H3-H4 chap-
erone that has been associated with both the sensitivity and memory of heat stress
in Arabidopsis. Double mutant affected in the two orthologous Arabidopsis ASF1
genes, AtASF1a and AtASF1b, was more sensitive to a first priming heat stress
shock than wild-type plants and showed decreased priming response to a second
more severe heat shock. Interestingly, the impairment of heat priming was more
pronounced under long recovery lag periods, indicating a role of AtASF1in mem-
ory maintenance. Expression and chromatin analyses demonstrated that AtASF1A/B
may induce nucleosome disassembly at specific Heat Shock Factor (HSF) genes
upon priming for heat stress, which creates an acclimated chromatin environment
for higher and faster induction of the stress-responsive genes after a second stress
treatment (Weng etal. 2014). In Arabidopsis, the H3.3 chaperone Histone Regulator
A (HIRA) partially compensates the loss of CAF-1 (Duc etal. 2015; Muñoz-Viana
etal. 2017) and it is plausible that other plant histone variants and chaperones aside
ASF1 and CAF-1 play a role in the inheritance of transcriptional states. For instance,
BRUSHY (BRU1)/TONSOKU/MGOUN3 is a nuclear protein of unknown molecu-
lar function that has been related not only to DNA damage repair, but also to stable
transmission of chromatin and transcriptional states (Takeda etal. 2004; Brzezinka
etal. 2018). bru1 mutant developmental phenotypes resembled mutants affected in
components of the DNA replication-coupled histone H3/H4 chaperone complex
CAF-1 (Takeda etal. 2004). Furthermore, bru1 mutants show defects in the mainte-
nance of thermotolerance, a function that may be independent of CAF-1 and its
activity on DNA repair (Brzezinka etal. 2018). Although it has been suggested that
BRU1 could be involved in the inheritance of chromatin structure from mother to
daughter cells through DNA replication, further evidence will be necessary to sup-
port this model (Takeda etal. 2004; Brzezinka etal. 2018).
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
1.4.6 Histone Modifications
Histone PTMs have a key role in regulating gene expression. Mainly N-terminal
histone tail PTMs are currently implicated in transcription—some PTMs act as
marks for transcriptional activation and others for repression (Zhao and Garcia
2015) but for some, the function in transcriptional modulation is still unclear.
Histone PTMs affect chromatin structure (1) by altering nucleosome compaction
and (2) by mediating or interfering with the recruitment of other proteins to the
chromatin, among them chromatin remodelers (Bannister and Kouzarides 2011;
Lawrence etal. 2016). PTMs can be highly dynamic or stably transmitted through
cell division and multiple proteins involved in adding, removing, and reading them
have been described (Hyun etal. 2017; Zhao etal. 2018). A single amino acid resi-
due can be modified by different number of groups (e.g., lysine mono-, di- or tri-
methylation) or PTM types (e.g., lysine methylation and acetylation) and different
PTMs can co-exist on the same histone or on different histones of the same nucleo-
some. In summary, all these possibilities add an extraordinary level of complexity
to histone PTMs and their impact on gene expression (Bannister and Kouzarides
2011; Zhao and Garcia 2015; Lawrence etal. 2016). Acetylation andDeacetylation ofHistones DuringResponses
toAbiotic Stress
The activity of histone acetyltransferases (HATs) and deacetylases (HDACs) is sig-
nificantly involved in the responses to different abiotic stresses (Kim etal. 2015;
Luo etal. 2017; Lämke and Bäurle 2017). Acetylation is a highly dynamic PTM and
therefore chromatin of stress-related genes whose acetylation changed in response
to abiotic stress may rapidly recover its naïve state (Kim etal. 2012; Friedrich etal.
2018). Histone acetylation is usually correlated with transcriptional activation and
histone deacetylation with gene repression (Loidl 1994).
Transcriptomic analysis in different plant species indicates that HAT genes
expression is regulated by ABA, salinity or drought stresses (i.e., rice (Fang etal.
2014); barley (Papaefthimiou etal. 2010); maize (Li etal. 2014a)). In Arabidopsis
plants under drought stress a gradual increase in H3 acetylation in stress-responsive
loci correlated with enhanced transcription (Kim etal. 2008). In addition, ADA2b,
5 (GCN5) HAT complex, may also act in the response to high salt (Kaldis etal.
2011). Strikingly, it has been recently shown that under salinity stress GCN5 directly
binds and increases H3 and H4 acetylation at genes involved in the biosynthesis of
cell wall components and, hence, contributes to cell integrity under high salt condi-
tions (Zheng etal. 2018). In peanut (Arachis hypogaea) activation of AhDREB1, an
APETALA2/Ethylene Respond Factor (AP2/ERF2) involved in the activation of
different stress pathways through acetylation under osmotic stress, has been pro-
posed to enhance drought resistance (Zhang etal. 2018b).
I. Mozgova et al.
GCN5 and ADA2b are also involved in the activation of COLD-REGULATED
(COR) genes (Vlachonasios etal. 2003). A more recent paper from the same group
showed that although cold-triggered induction of COR relies on GCN5 and ADA2b
and correlates with elevated acetylation, the chromatin changes did not depend on
ADA2b or GCN5 (Pavangadkar etal. 2010). This suggests that other HATs may be
involved in this process. Increase in histone acetylation together with expression of
specific stress-related genes has been shown to be induced by cold stress in rice and
maize and specifically at repetitive sequences in maize (Hu etal. 2011, 2012; Roy
etal. 2014). Considering that HATs are well conserved in different plant species,
orthologs of these proteins could serve similar functions in crop species (Pandey
etal. 2002; Aquea etal. 2010; Papaefthimiou etal. 2010; Liu et al. 2012; Aiese
Cigliano etal. 2013; Fang etal. 2014).
In Arabidopsis, HATs mediate response to UV-B light (Fina etal. 2017), corre-
lating with histone hyperacetylation at targets of the UV-B photoreceptor UVR8
(Velanis etal. 2016). Arabidopsis ASF1A/B has been implicated in H3K56ac cou-
pled to nucleosome removal and stalled RNA PolII at specific HEAT SHOCK
PROTEIN (HSP) loci under heat stress in Arabidopsis (Weng etal. 2014). Histone
acetylation is also coupled to waterlogging stress response in rice (Tsuji etal. 2006).
HDACs are also very well conserved in different plant species (Luo etal. 2017)
and can be induced (e.g., in barley—Demetriou etal. 2009) or repressed (e.g., in
Arabidopsis—Sridha and Wu 2006; Luo etal. 2012a, b—or in rice—Fu etal. 2007)
by ABA and salt. For instance, one of the HDACs in rice, the HDAC OsSRT701,
modified H3K9ac levels on stress genes, whereas overexpression of OsHDT701,
which encodes for another HDAC, increases resistance to high salinity and drought
and overexpression of OsHDA705, results in lower resistance to salt and ABA
(Zhong etal. 2013; Zhao etal. 2015, 2016b). HD2C overexpression in Arabidopsis
has been related with drought and salinity stress resistance (Sridha and Wu 2006;
Luo etal. 2012a). HD2D overexpression also conferred higher resistance to drought,
high salt stresses and cold in Arabidopsis (Han etal. 2016). HDA9 may repress the
response to high salt and drought, as in the hda9 mutant many drought-related genes
were upregulated and showed increased H3K9ac at the promoter of salt and drought-
responsive genes (Zheng etal. 2016; Chen etal. 2016; Kim etal. 2016). Arabidopsis
HDC1 interacts with HDA6 and HDA19 to form a putative complex able to deacet-
ylate H3 invitro (Perrella etal. 2013). Overexpression of HDC1 reduces sensitivity
to high salt and ABA reducing H3 acetylation levels and expression of salinity
stress-related genes (Perrella etal. 2013). On the contrary, mutations in HDA6,
HDA19, or HDC1 result in plants more sensitive to high salt and ABA and decreased
expression of salinity stress genes (Chen etal. 2010; Chen and Wu 2010; Perrella
etal. 2013). HDA6 was also shown to play a role in drought tolerance (Kim etal.
2017), whereas HDA19 could help to increase plant resistance to different abiotic
stresses (Ueda et al. 2018). In addition, HDA19 and HDC1 interact with
MULTICOPY SUPPRESSOR OF IRA 1 (MSI1) (Derkacheva etal. 2013; Mehdi
etal. 2015), which is a subunit of at least two different complexes, CAF-1 and
POLYCOMB REPRESSIVE COMPLEX 2 (PRC2) (Hennig et al. 2005). The
HDA19-MSI1 complex reduces the level of H3 acetylation at ABA receptor genes
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
(Mehdi etal. 2015). MSI1 has also been shown to repress ABA responses in plants
and its downregulation to enhance drought tolerance. The role of MSI1in drought
tolerance is probably independent of PRC2 and CAF1 (Alexandre etal. 2009).
Thus, these results highlight the flexibility of chromatin-related proteins to form
part of different complexes and contribute to different outputs.
HDA6 has also been related to the response to cold stress by freezing tempera-
tures (To etal. 2011). HDA9 and its interactor POWERDRESS (PWR) have been
involved in regulating developmental changes under high temperatures. PWR was
required to promote H3K9ac in thermomorphogenic genes. In addition, transcrip-
tional analyses demonstrated a link between PWR and H2A.Z (Tasset etal. 2018).
Another example of interplay is the interaction between HD2C and SWI/SNF com-
plex in the regulation of the response to heat stress (Buszewicz etal. 2016). HOS15
(for high expression of osmotically responsive genes) interacts with HD2C and
together directly represses the expression of COR genes. Low temperatures induce
HOS15-dependent HD2C degradation, probably through the recruitment of an E3
ligase complex, and decreases H3 acetylation of COR genes (Park etal. 2018). In
maize cold treatment promotes the decrease of different acetylation marks correlat-
ing with upregulation of several HDACs (Hu etal. 2011). Although expression pat-
terns of HDACs under abiotic stresses have also been analyzed in other crops (Luo
etal. 2017), further data will be required to link these changes with transcriptional
changes due to acetylation status of stress-related genes. Methylation andDemethylation ofHistones DuringResponses
toAbiotic Stress
Although methylation can occur on any histone, the bulk of our knowledge for the
role of this PTM in the modification of gene expression comes from the methylation
of a few H3 residues (i.e., K4, K9, K27, and K36). The impact of histone methyla-
tion on transcription varies: H3K4me3, H3K9me3, and H3K36me3 are involved in
activation; H3K27me3 switches off genes; H3K9me2 and H3K27me1 are enriched
in stably repressed regions and usually related to DNA methylation (Roudier etal.
2011; Sequeira-Mendes et al. 2014). Histone methyltransferases (HMTs) are
responsible for adding this PTM and histone demethylases (HDMs) for its active
removal (Hyun etal. 2017). Therefore, methylation of histones is also a dynamic
mark, despite showing a slower turnover than histone acetylation (Asensi-Fabado
etal. 2017; Hyun etal. 2017), which may affect relative contribution to memory by
these two PTMs.
Most HMTs are characterized by the presence of a conserved SET (Su(var), E(z),
and Thritorax) domain that has allowed the identification of components of this
family in different plant species, including important crops (Ng et al. 2007;
Pontvianne etal. 2010; Aquea etal. 2011; Huang etal. 2011, 2016; Lei etal. 2012;
Yadav etal. 2016). In maize, class V of SET genes, which is related to H3K4 meth-
ylation, was differentially expressed in response to osmotic stress (Qian etal. 2014).
Analysis of the SET family in foxtail millet (Setaria italica), a millet crop cultivated
I. Mozgova et al.
in arid regions and highly resistant to stress, demonstrated that most SiSET genes
were upregulated under cold stress and several also responded to salt and dehydra-
tion stress (Yadav etal. 2016). In Gossypium raimondii, a putative contributor to
allotetraploid cotton, three SET genes (GrKMT1A;1α, GrKMT3;3, and GrKMT6B;1)
were induced by heat stress (Huang etal. 2016).
Arabidopsis plants subjected to drought stress showed an increase of H3K4me3
coupled to transcriptional activation on specific drought-stress related genes.
Enrichment of this PTM followed RNA polymerase II (RNA Pol II) accumulation,
indicating that in this case H3K4me3 was probably a consequence of high transcrip-
tional rate (Kim etal. 2008). Although H3K4me3 decreased on stress genes during
rehydration, low levels of this mark still above naïve levels were maintained. These
results indicated a role of H3K4me3 as epigenetic mark for drought-responsive
genes (Kim etal. 2012).
Genome-wide analyses of histone PTMs in Arabidopsis subjected to water depri-
vation showed changes in H3K4me3 enrichment that correlated with gene expres-
sion levels. However, stress-responsive genes showed broader H3K4me3 distribution
not only after applying the stress, but also under unstressed conditions (van Dijk
etal. 2010). The meaning of the differential H3K4me3 distribution along the bodies
of stress-responsive genes is unknown, but it is tempting to speculate that it may
mark specific stress genes for a prompt response under inductive conditions.
Genome-wide analyses of rice plants grown under control and water scarcity condi-
tions showed that only a small percentage of genes that showed different H3K4me3
enrichment under stress was differentially expressed. Therefore, changes in this
mark were not necessarily coupled to changes in gene expression. As expected how-
ever, in stress-responsive genes that showed a change in both H3K4me3 and expres-
sion, the increase in H3K4me3 positively correlated with expression levels (Zong
etal. 2013). Upon waterlogging in rice, changes in PTMs, including increase in
H3K4me3, correlated with gene activation (Tsuji etal. 2006). Hence, these changes
in PTMs during waterlogging may mirror transcriptional state of stress-responsive
genes and are unlikely to be involved in priming.
the deposition of H3K4me3 and is key in the regulation of drought- and ABA-
related genes (Ding etal. 2009, 2011). atx1 mutants are hypersensitive to water
deficiency (Ding et al. 2009, 2011) and show decreased ABA levels under both
naïve and water stress (Ding et al. 2011). ATX1 binds to NINE-CIS-
EPOXYCAROTENOID DIOXYGENASE 3 (NCDE3), which plays an important role
in ABA biosynthesis (Qin and Zeevaart 1999), and its binding to this gene increases
under drought stress correlating with higher H3K4me3. Expression analyses showed
that ATX1 is involved in both activation of ABA-dependent and -independent dehy-
dration stress genes through H3K4me3 enrichment, but that may not be the only
HMT involved in this regulation (Ding etal. 2011). ATX1 belongs to class III SET
domain proteins, with ATX2 being its closest homolog (Pontvianne etal. 2010). It
will be very interesting to see in future works whether ATX1 homologs also play a
role in stress responses. Arabidopsis JMJ15, a Jumonji-family HDM, mediates
response to salt stress. Overexpression of JMJ15 increases salt resistance and leads
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
to downregulation of H3K4me2/me3 marked genes, many of which are stress-
related genes (Shen etal. 2014). JMJ and other HDM proteins are well conserved in
plants (Zhou and Ma 2008; Qian etal. 2015). However, our understanding of HDMs
is limited and future works will be paramount to fully understand the activity of
these proteins in different processes such as responses to stress.
In addition to H3 methylation, H4R3 symmetric dimethylation (H3K4sme2) has
been shown to act as a repressive mark for gene expression during stress responses
in Arabidopsis. Specifically, H4R3sme2 plays a role in calcium signaling in the
(SKB1) is a H4R3 HMT able to directly repress the expression of CALCIUM
SENSOR (CAS) that acts in detection of external cellular calcium. Increase of exter-
nal calcium concentration induces a reduction in CAU1 and subsequently reduction
of H4R3sme2 at CAS and activation of this gene. This cascade results in stomata
closure to reduce water-loss through transpiration (Fu etal. 2013). A very recent
paper from the same lab has shown a CAU1/PRMT5/SKB1 novel activity indepen-
dent of CAS, which also promotes drought resistance indirectly inducing accumula-
tion of proline (Fu etal. 2018). PRMTs are well conserved in rice and OsPRMT5
can also induce H3K4sme2 invitro (Ahmad et al. 2011); therefore, a plausible
hypothesis is that the molecular activity of this protein in dehydration tolerance is
also conserved in crops. Other PTMs Involved inAbiotic Stress Responses
Compared to acetylation and methylation, our knowledge about the role of other
PTMs in gene expression and, in particular, in transcriptional regulation under stress
conditions is limited. For instance, proteomic analyses of sumoylated proteins under
different conditions indicated that heat stress induces H2B sumoylation. In addition,
other important chromatin-related factors (e.g., SWI/SNF components, HMTs,
GCN5, etc.) were also sumoylated after stress, suggesting that sumoylation may
develop a more complex role in the regulation of chromatin-mediated stress
responses (Miller etal. 2010).
In Arabidopsis, HISTONE MONOUBIQUITINATION 1 and 2 (HUB1/2), which
encode C3HC4 RING-type E3 ubiquitin ligases responsible for H2Bub1 (Cao etal.
2008), were induced under salt stress. Single hub1 and hub2 mutants and the respec-
tive double mutant were intolerant to high salt. H2Bub1 is required for microtubule
de-polymerization in response to high salt stress through the activation of genes that
mediate in this process. In addition, H2Bub1 was also required for activation of
MAP KINASE PHOSPHATE 3 and 6 (MAP 3/6) genes that play a central role in
stress signaling (Zhou etal. 2017). Recently, the overexpression of Arabidopsis
HUB2 in transgenic cotton (Gossypium hirsutum) increased the performance of
plants under drought conditions through H2Bub1 of drought-responsive genes,
while decreased expression of GsHUB2 increased water deficiency intolerance
(Chen etal. 2018).
I. Mozgova et al.
H3T3 phosphorylation (H3T3ph) levels increased in pericentromeric regions
under drought stress and mutants affected in the kinases that phosphorylate this resi-
due were sensitive to osmotic stress (Wang et al. 2015c). Using Arabidopsis and
tobacco cell lines, Sokol etal. demonstrated that application of cold or salinity
stress transiently induced H3S10ph in both cell types. This increase was followed
up by H3 and H4 acetylation. These chromatin changes correlated with differential
expression of stress-related genes (Sokol etal. 2007).
In summary, these data highlight not only the importance of other PTMs in defin-
ing stress responses, but also how far we still are to have the full picture of the
contribution of PTMs to the capacity of plants to adapt to the environment. Histone Modifications andMemory
At present, histone PTMs have mainly been implicated in somatic rather than inter-
generational memory of abiotic stresses. Chromatin-related mechanisms of stress-
induced gene transcription memory are subject of intense research (for recent
reviews, see Bäurle 2017; Lämke and Bäurle 2017; Friedrich etal. 2018). Currently
available results indicate that histone PTM-associated transcriptional memory is of
relatively short duration in the range of 3–10days following the initial abiotic stress
treatment (Ding etal. 2012; Sani etal. 2013; Singh etal. 2014; Lämke etal. 2016).
Most studies that focus on molecular mechanisms of transcriptional memory were
performed using Arabidopsis seedlings, in which the range of several days may
nevertheless represent a substantial number of cell divisions, indicating that histone
PTMs can be mitotically transmitted and contribute to improved stress tolerance
under conditions of recurring stress (Lämke and Bäurle 2017). Molecular mecha-
nism of vernalization in Arabidopsis provides a well-studied example of how his-
tone PTM-based chromatin state can be stably transmitted somatically and, if not
reset, even inter-generationally. FLC encodes a MADS-box transcription factor
serving as flowering repressor in Arabidopsis. During vernalization, upon sufficient
time of cold treatment, repressive chromatin marked by the PRC2-deposited
H3K27me3 forms at the FLC locus (Michaels 1999; Sheldon 2000; Bastow etal.
2004; De Lucia etal. 2008). The repressive chromatin is then transmitted during
mitotic cell divisions for the rest of the plant life regardless of ambient temperature.
Permissive chromatin state at FLC is only reset during embryogenesis by active
removal of H3K27me3 mediated by the histone demethylase EARLY FLOWERING
6 (ELF6) which enables FLC activation and inhibition of precocious flowering in
the next generation (Sheldon etal. 2008; Choi etal. 2009; Crevillen etal. 2014). The
fact that in the absence of ELF6 the elevated amount of H3K27me3 is maintained
inter-generationally (Crevillen etal. 2014) suggests that, in the lack of active reset-
ting mechanisms, there is potential for sexual transmission of repressive histone
Such a long-lasting somatic memory has not been observed in connection to
abiotic stress and most examples come from transcriptional activation rather than
repression of stress-responsive genes. Somatic stress memory can be mediated by
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
sustained expression of stress-responsive genes (type I memory—Figs. 1.1 and 1.3;
reviewed in Bäurle 2017). An example is provided by the HSP gene Hsa32 that is
induced by heat in several plant species including Arabidopsis, rice (Charng etal.
2006a) and tomato (Liu etal. 2006). In contrast to other HSP genes (Scharf etal.
2012) whose expression declines quickly after the immediate stress response, the
transcription of Hsa32 declines at a slower rate. Hsa32 is not required for the imme-
diate stress response but it is needed for the retention of acquired thermotolerance
in plants after 2–3days following a first heat exposure (Charng etal. 2006b). Similar
to Hsa32, 40 other genes were identified in Arabidopsis whose transcription is
induced following heat stress and remains elevated for another 2–3days in the
absence of the stress, defining a set of heat-stress memory genes (Stief etal. 2014).
Abiotic stress transcriptional memory can also be independent of continuously
elevated transcriptional activity of genes, but initial transcriptional activation may
induce a state that allows for altered gene activation upon repeated exposure to
stress (type II memory—Figs. 1.1 and 1.3; reviewed in Bäurle 2017). Most often,
memory of active transcription seems connected with the maintenance of elevated
levels of H3K4me3 (Ding etal. 2012; Lämke etal. 2016), which correlates not only
with the duration of heat-stress memory (Liu etal. 2018b) but also with H3K9 acet-
ylation and H3K4me2 (Singh etal. 2014; Lämke etal. 2016; Liu etal. 2018b). High
H3K4me3 occupancy and presence of RNA Pol II phosphorylated on serine 5
(Ser5P Pol II—PTM-associated with transcriptional initiation/early elongation and
stalling of RNA Pol II) marks several dehydration-responsive genes in Arabidopsis
that display higher transcriptional activity upon repeated exposure to dehydration
but are not upregulated during periods of stress recovery (rehydration) (Ding etal.
2012). These were termed “trainable genes” and using the same experimental setup,
two genome-wide studies identified extended sets of dehydration memory genes
that displayed progressive up- or downregulation, loss of induction or loss of repres-
sion in response to repeated dehydration stress in Arabidopsis and in maize (Ding
etal. 2013, 2014). While the memory of transcriptional activity correlated with high
H3K4me3 and Ser5P Pol II (Ding etal. 2012; Liu etal. 2014b), the mechanisms and
histone PTMs imposing memory of repression remain less clear. Similarly, heat-
responsive memory genes in Arabidopsis are marked by increased levels of not only
H3K4me3, but also H3K4me2 and H3K9ac (Lämke etal. 2016; Liu etal. 2018b).
Chromatin at these genes is established by the action of the heat shock transcription
factor HFSA2 (Lämke et al. 2016). HFSA2 is activated by heat but, similarly to
Hsa32, it is not required for the immediate response to heat but for the retention of
thermotolerance (Charng etal. 2006a). HSFA2 transiently binds to the promoter of
the heat-stress responsive genes at early timepoints after exposure to heat stress but
is dissociated from the promoters at later timepoints when elevated levels of
H3K4me2/3 and transcription of the target genes persist. HFSA2 was therefore
proposed to act as a “hit-and-run” transcription factor that is not required for the
initial transcriptional activation, but recruits chromatin modifiers and promotes the
establishment of active PTMs that are retained even after HFSA2 has dissociated
from the locus (Lämke etal. 2016). High levels of H3Kac, H3K4me2, and H3K4me3
also mark cold, heat, or salt-primed genes (Singh etal. 2014) and retention of ele-
I. Mozgova et al.
vated H3K4me3 is required for salt stress memory (Feng etal. 2016). During salt
stress, the proline biosynthetic enzyme-encoding gene P5CS1 is activated and the
locus is marked by sustained high levels of H3K4me3 even during stress recovery.
Interestingly, the maintenance of H3K4me3 during the recovery phase—but not the
initial salt-induced transcriptional activation of P5CS1—requires light-dependent
binding of the transcription factor ELONGATED HYPOCOTYL 5 (HY5) to a C/A-
box element in the promoter of P5CS1 that was found to be essential for the stress
memory. These results support a model where the salt-responsive transcription fac-
tor mediates the initial stress-related gene activation but light-dependent HY5-
mediated recruitment of H3K4me3 histone methyltransferase mediates the
maintenance of the chromatin state as a part of the memory (Feng etal. 2016).
Similar uncoupling of stress-response gene activation and memory was observed in
the case of the drought-response gene RD29B, which depends on ABA-response
binding factors (ABFs) for the priming (transcriptional memory) but also requires
additional factors for its repeated induction (Ding etal. 2012; Virlouvet etal. 2014).
This suggests that combination of environmental cues (light and salt stress) and
distinct transcription factors may be implemented in initial gene activation, stress
memory, and repeated induction of the genes.
Apart from gaining chromatin marks associated with accessible chromatin struc-
ture, genes that display enhanced activation upon stress exposure in primed plants
may also lose repressive PTMs (Sani etal. 2013). Genome-wide profiling of several
histone PTMs (H3K4me2, H3K4me3, H3K9me2, and H3K27me3) in roots of
Arabidopsis seedlings primed by mild hyperosmotic treatment revealed shortening
and fragmentation of H3K27me3 regions and limited changes to other PTMs, which
were not globally reflected by changes in gene expression. Changes to H3K27me3
distribution persisted for another 10days after the stress suggesting mitotic inheri-
tance of the modified chromatin. The priming treatment enhanced the plant toler-
ance to subsequent stress exposure and the reduction of H3K27me3in primed plants
corresponded to elevated transcription of the root sodium transporter gene HKT1
during subsequent stress exposure (Sani etal. 2013), suggesting direct functional
connection between level of H3K27me3 and primed state.
In summary, abiotic stress memory mediated by histone PTMs seems to have a
limited duration of several days. It is often associated with elevated levels of
H3K4me3 that persist even during stress recovery and correlate with the duration of
the memory. Histone methylation may be a PTM suitable to contribute to memory
of past stress events considering its relatively slow turnover compared to other
highly dynamic modifications such as acetylation that also commonly marks mem-
ory genes. Initial stress-response gene activation and establishment and/or mainte-
nance of memory may require cooperation of distinct factors for full execution. It
remains to be determined whether stress-induced transcriptional activation and
memory establishment are two separated molecular phases governed by different
subsets of factors in general, or whether different modes of memory establishment
and maintenance exist.
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
1.5 Summary andPerspectives
Ongoing climate change and quickly growing world’s population represent chal-
lenges for sustainability of agriculture and food production in many, often underde-
veloped, regions (Adams et al. 1998; Mendelsohn 2008). The climatic and the
demographic models predict even a greater challenge in the future (Tol 2018).
Plants are one of the important factors that can help to mitigate negative effects of
the climatic changes by reducing weather extremes and binding atmospheric CO2.
Furthermore, plants feed the world as the major source of carbon and energy for
humans and domestic animals (Conway and Toenniessen 1999; Borlaug 1997).
Therefore, understanding plant stress responses and developing new strategies
allowing sustainable agricultural production under wide range of less predictable
conditions is one of the big challenges in plant biology. In order to succeed, the
strategies will need to involve a battery of measures, including modifications of the
farming style and breeding new crop varieties with high yield under stress. Many
breeding strategies are being discussed, ranging from the classical breeding to the
possible use of genome editing techniques (Moose and Mumm 2008; Belhaj etal.
2015; Bortesi and Fischer 2015).
One way to prepare plants for the new challenges could be through the epigenetic
modifications of DNA and histones in a transient or permanent manner and result-
ing in memory. Stress responses are accompanied by changes in gene expression,
many of which were shown to be underlined by modifications at the chromatin level
(reviewed in Chinnusamy and Zhu 2009; Iwasaki and Paszkowski 2014b; Avramova
2015). Most of the chromatin changes appear short lived. However, there are some
which can last for days and in some cases even into the next generation(s). There is
an ongoing discussion to what extent these changes could be influenced by other
experimental factors, whether they are stochastic or specific response to stresses
(Pecinka and Mittelsten Scheid 2012; Iwasaki and Paszkowski 2014b; Quadrana
and Colot 2016; Ganguly etal. 2017). Evidence exists for both possibilities. Well-
documented cases of beneficial plant memory include priming, which allows to
prepare plants for the future stress conditions by application of a lower stress dose
and/or activation of stress defense pathways by, e.g., chemical treatment (reviewed
in Conrath etal. 2015; Bäurle 2016). Priming is already applied in agriculture and
helps reducing economic losses. We foresee that the development of new priming
methods and/or understanding molecular basis of priming will open new possibili-
ties towards plant protection and can reduce economic losses due to stress. However,
application of a recurrent stress during several generations does not always correlate
with improved plant vigor and, therefore, memory may be only linked to specific
traits (Ganguly etal. 2017).
It is very attractive to think about transgenerational reprogramming of plants to
withstand many types of stress. However, success of such attempts is greatly limited
by the endogenous machineries resetting any changes to the basic (pre-stress) situ-
ation through the checkpoint centers localized in the meristematic tissues and repro-
ductive organs (Baubec etal. 2014; Iwasaki 2015). One possible way how a plant
I. Mozgova et al.
could maintain epigenetic changes is through vegetative propagation. In addition,
successful transmission of gained activation can be hampered for some loci upon
genetic interaction with the repressed allele as demonstrated in multiple examples
of paramutation (reviewed in Chandler and Stam 2004; Chandler and Alleman
2008). Evolutionary significance of (trans)generational stress memory is unknown.
On the one hand, exposure to periodically occurring stress probably led to evolution
of specific mechanisms, which became part of plant developmental program and
possibly allowed colonizing new niches. The best described example is vernaliza-
tion, which involves extensive and complex epigenetic regulation by multiple epi-
genetic pathways (reviewed in Song etal. 2012a). On the other hand, many stresses
occur stochastically and it is impossible to predict them even using modern moni-
toring methods. Furthermore, multiple studies demonstrated that activation of stress
response pathways requires energy and slows down growth, and, in case of severe
and/or long-lasting stress, also yield (Fig.1.1; reviewed in, e.g., Bechtold and Field
2018). Prophylactic long-term activation of the stress memory may lead to selective
disadvantage compared to the less sensitive peers. Therefore, plants may constantly
search for a balance between too little and too much stress responses. Epigenetic
regulation is a perfect candidate, which could control both the duration and the
amplitude of such response (reviewed in Lämke and Bäurle 2017). In addition,
stress-induced epigenetic variation among individuals and their offspring may rep-
resent a bet-hedging strategy, where the variation increases the chances that at least
some of the individuals will be programmed in the right way.
At present, most stresses are applied separately and in high doses in laboratory
conditions. This is a perfect approach to pin down components of individual path-
ways and to understand their functions. However, such experimental setups may be
very different from natural conditions where stresses occur in lower doses for longer
time (chronic stress) and often in combinations, e.g. heat, drought, and high UV
during a hot summer day. Therefore, understanding combinatorial effects of multi-
ple stresses applied in natural-like conditions on plant performance, physiology, and
epigenomes remains to be deciphered. It is also clear that the studies using different
species may give different answers. While most of the early and also current infor-
mation on plant memory comes from Arabidopsis, which allows accurate and fast
testing of many hypotheses and still is essential in this aspect, not all trends could
be confirmed in other species and various crops show also new epigenetic phenom-
ena (Chandler and Stam 2004; Jablonka and Raz 2009; Quadrana and Colot 2016).
The toolbox for analysis of plant epigenetic changes and memory contains a
continuously growing number of tools (Spillane and McKeown 2014). Recently,
multiple ultrasensitive methods for analyzing transcriptome, DNA methylation, his-
tone modifications and variants, chromatin packaging, etc. have been developed and
can be directly applied to any species with existing genome assembly. Furthermore,
the ongoing boom of the new technologies for genome editing offers great possibili-
ties for modifications of the systems towards epigenome editing or directing specific
modifications into the genomic regions of interest (Belhaj etal. 2015; Puchta 2015,
2017). The most promising approach is based on the CRISPR system, where Cas9
nuclease is guided by a specific RNA molecule to the target locus containing homol-
1 Epigenetic Mechanisms ofAbiotic Stress Response andMemory inPlants
ogous sequence (Herrmann etal. 2015). Upon removing Cas9 nuclease activity and
fusing Cas9 with epigenetic modifiers, potentially any genomic region could be
targeted with chromatin modifications of interest (Gallego-Bartolomé etal. 2018).
Current systems require stable transformation of the fusion construct. It is foresee-
able that the development will be directed towards transient transformation systems,
and even delivery of the ready-made modifier proteins, which will speed up the
whole process for induction of epigenetic variation in plants. Along with these tech-
nical advancements, both the risks (if any) and the benefits in use of such systems
need to be discussed with the public. General acceptance of the new technologies is
an essential step, which needs to be achieved before applying such methods in agri-
cultural production.
Acknowledgement Work of Ales Pecinka on this publication was supported by Purkyne fellow-
ship from the Czech Academy of Sciences and INTER-COST grant LTC18026 from the Ministry
of Youth, Education and Sports of the Czech Republic. Work of Iva Mozgova was supported by the
Czech Science Foundation (GACR 16-08423Y) and the National Programme of Sustainability
(LO1416). Work of Sara Farrona was supported by the College of Science (NUI Galway) and by
Science Foundation Ireland grant No. 16/TIDA/3980. All authors were supported by the COST
action CA16212 “Impact of Nuclear Domains On Gene Expression and Plant Traits (INDEPTH).”
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... In addition, priming has been shown to be effective at different stages of the plant life cycle, from seed (i.e., seed priming) to seedlings and to subsequent adult stages. However, while much is known about the physiological consequences of priming in the adaptability of the plant and hence its applications-products that boost plant vigour through priming are available from different agricultural companies-much less is known about the molecular mechanisms that establish, regulate, and even erase this molecular memory [179][180][181][182]. Although metabolic and physiological pathways have been shown to play a role in priming, it has been proposed that a long-lasting process able to be transmitted through cell division, such as epigenetics, could be key in establishing the primed memory [183][184][185][186]. ...
... Although metabolic and physiological pathways have been shown to play a role in priming, it has been proposed that a long-lasting process able to be transmitted through cell division, such as epigenetics, could be key in establishing the primed memory [183][184][185][186]. More recently, the molecular evidence supporting this hypothesis in diverse plant species has brought a novel focus on this field [179,180,187]. ...
... Isabel Bäurle, who has extensively contributed to our understanding of heat stress priming in Arabidopsis, has proposed that memory genes can be classified considering their transcriptional response to the stress. In type I memory genes, the epigenetic changes induced by the stress will induce the maintenance of the new transcriptional state posed by the stress during a certain period of time, while in type II memory genes, epigenetic marks that are established on the chromatin of the gene during this first encounter, will induce a modified transcriptional response to a second stress, usually stronger and faster than the first one [179,180]. For intra-generational memory, the lapse of time between the repeated stresses seems to be limited to a few days or, occasionally, several weeks [188,189]. ...