limitations originate from many different factors : too high or too low temperatures / water supply / light intensity , non - optimal mineral composition or soil contamination , mechanic inhibition , pathogen infestation , lack of symbiotic partners , interactions with other plants , parasites or herbivores .
these conditions can activate defense responses by which plants can minimize detrimental consequences of stressful conditions for their survival , growth , or propagation .
these mechanisms allow plants to occupy even extreme habitats , despite their sedentariness . under field conditions ,
different stress types usually occur concomitantly , like heat and drought , and the molecular responses can be difficult to separate .
response to one stress type can be also antagonistic to another , as adaptation to nutrient - poor substrates might reduce stress by competition .
therefore , mechanistic studies of stress effects are mostly performed under controlled laboratory conditions , applying one stress type and distinguishing biotic from abiotic stress . while this resulted in information about signaling cascades , transcription factors , and defense compounds ,
stress effects on the epigenetic level are expected to allow more permanent changes of gene expression and potentially long - term adaptation that could have evolutionary impact , as chromatin modifications can be mitotically or meiotically heritable .
this review will focus on the connection of stress with epigenetic regulation , separated in three levels .
investment into stress defense , alongside constitutive morphological and metabolic survival equipment and seasonal adaptations , expends plants general resources and therefore should be restricted to the actual occurrence of stressful situations .
plants use a range of different sensing and signaling mechanisms to induce dynamic stress responses only when challenged .
signaling includes mainly the hormones salicylic acid ( sa ) , jasmonic acid ( ja ) and ethylene upon biotic stress , and abscisic acid ( aba ) in case of abiotic stress ( reviewed in ) .
nevertheless , there is growing evidence that noncoding and sirnas and the proteins generating or binding them are involved in stress - signaling and can subsequently induce transcriptional or posttranscriptional gene silencing ( tgs or ptgs , respectively ) .
the recent identification of a mutated nrpd2 gene responsible for constitutive overexpression of a sa - inducible gene provided a mechanistic link between stress signaling and elements of the rna directed dna methylation ( rddm ) pathway , excluding only poliv .
some rddm mutants had a compromised immune response to pathogenic fungi correlated with a lack of gene induction by ja .
in contrast , resistance to a bacterial pathogen was increased , corresponding with elevated levels of salicylic acid - related defense genes and enriched activating chromatin marks h3k4me3 and h3k9ac at the promoter of the sa - inducible gene pr-1 .
this argues for the overlap between targets of rddm and sa - signaling and a role of rddm to relay stress signals to the nucleus .
stress can certainly induce the production of sirnas , either via antisense transcription of protein - coding or non - protein - coding sequences , or from inverted repeats .
an early example of naturally occurring antisense was the discovery that induction of the arabidopsis sro5 expression under salt stress creates a transcript partially complementary to that of the constitutively expressed p5cdh , resulting in dsrna as a substrate for dicer - like proteins and sirnas that are only present and effective under stress .
among 76 long non - protein - coding rnas ( npcrna ) in the arabidopsis genome , 26 had altered expression levels upon low phosphate , salt or drought stress .
some of them gave rise to 24  bp sirnas , and npc536 conferred improved root growth under salt stress .
by now , many pairs of potential antisense transcripts are identified , and natural cis - antisense sirnas ( nat - sirnas ) are defined as a separate class of the small rna family .
one example role of sirnas in extreme stress tolerance is a dehydration- and aba - inducible retroelement - derived sirna that regulates an adaptive response in the resurrection plant craterostigma plantagineum . applying tailor - made transcripts of inverted repeats ( irs )
is a routine technique to interfere with transcription of target genes with homology to the resulting sirnas , but similar sirna can also originate from transcripts of endogenous irs .
two arabidopsis repeats , ir71 and ir2039 , produce sirna of different size classes , of which some can silence a gfp - reporter in trans .
endogenous irs are highly variable in the genome of different ecotypes of arabidopsis , indicating fast evolution and rapid adaptive changes .
however , the actual response of ir - derived sirna to environmental factors and contribution to stress - adaptation is yet to be demonstrated .
responses of transposable elements ( te ) to stress are the topic of reviews by lisch ( this issue ) and bucher et al .
( this issue ) , but te activation raises the interesting potential of te - derived small rnas that target stress - related protein - coding genes   and thereby represent an indirect stress signaling pathway .
stress signaling leads to stress - adapted gene expression and also affects chromatin structure at responsive genes , directly or indirectly [ 1114 ] . the changes can affect dna methylation , histone tail modifications , exchange of histone variants , or nucleosome occupancy and larger chromatin configuration , as documented in the following examples ( figure 1 ) .
double - stranded viral transcripts can induce methylation at homologous sequences , which led to the discovery of the rddm phenomenon .
some sirnas associated with virus infection can be complementary to regions of the host genome , especially to regulatory sequences containing retro - elements evolved from ancient integration events , and can exert stable gene silencing on such  off - targets. the same principle could apply to other endogenous sirnas that match with promoter regions and could affect stress - related genes .
for example , repeat elements in the promoter of a sodium transporter gene are methylation targets and determine salt stress tolerance .
a plausible correlation is also the dna methylation of two genes controlling stomata development , their transcriptional repression , and a reduced number of stomata in arabidopsis plants grown under low humidity .
methylation changes that appear non - targeted or not yet associated with stress gene targets are induced by salt stress in arabidopsis , or in roots of rice plants , to different degree depending on the salt sensitivity of the cultivars
. these could be secondary effects due to stress - induced activity changes of epigenetic regulators .
multiple methylation changes were also observed associated with herbivore and pathogen attack in dandelions , and between mangroves or rubber trees growing in different habitats .
higher resistance to pathogens of arabidopsis mutants with defects in dna methyltransferases inspired a genome - wide analysis after infection with a bacterial pathogen , revealing methylation changes in all sequence contexts and at multiple loci , including defense - related genes , transposons and repeats .
there are several reports of stress - induced histone tail modifications and altered stress resistance in mutants lacking histone - modifying enzymes .
installation of activating marks can result in increased transcription levels of stress genes but may also simply poise target genes for faster or stronger response upon a more serious attack later .
aba and salt change h3 phosphorylation and h4 acetylation in cell cultures of tobacco and arabidopsis .
activation of a gene for an immune receptor protein ( r ) gene in arabidopsis depends on a histone methyltransferase installing h3k36me3 .
a prominent target is also the pr-1 ( pathogen - related 1 ) gene involved in initiating defense or stress adaptation where h3k4me2 , h3k4me3 and h3ac levels increase upon sa treatment or pathogens .
pr1 expression is negatively regulated by two wrky transcription factors , which both interact with histone deacetylase 19 ( hda19 ) .
deacetylation reduces active marks , and the induction of hda19 upon bacterial infection could be a chromatin - based way to weaken the plant defense system , among many other strategies .
another histone deacetylase , hda6 , is required for freezing tolerance in arabidopsis , although the link to histone acetylation at a specific target gene is missing .
a histone ubiquitin ligase determines the resistance to necrotrophic fungi , and the growing number of identified modification types makes it likely that more of them will also be connected with stress regulation .
the histone methylation at h3k27 under control of the polycomb / trithorax complexes and its response to environmental signals are described in detail elsewhere .
msi1 , a member of the prc2 as well as the caf1 complex , contributes to drought stress resistance by controlling the expression of aba - responsive genes and proline synthesis .
lower h3k27me3 levels at abscisic acid - responsive genes upon downregulation of the cell cycle regulator retinoblastoma - related ( rbr ) , and induction of several stress - related genes before deregulation of the cell cycle machinery   indicate a tight and complex connection between stress factors that modify chromatin features and developmental regulation .
histone variant h2a.z associated with the 5end of many genes is relevant for repression of pathogen response , as mutants lacking subunits of the swr1 complex that installs h2a.z show increased resistance to bacterial infections . a clear connection of this variant also with abiotic stress is evident from its eviction by heat exposure .
lack of arp6 , one swr1 subunit , mimics the transcriptional changes even at ambient temperatures .
further , a plant - specific linker histone h1 variant is expressed under drought stress in arabidopsis , and its downregulation in tomato revealed its importance in water stress response .
dna damaging stress is followed by incorporation of h2a.x , which becomes phosphorylated and attracts dna repair complexes and transcriptional activators .
however , many more chromatin components might be involved in enabling dna repair and recombination .
lastly , the association of nucleosomes with dna can be modified in response to stress .
indirect evidence came from analyzing mutants with defects in putative or proven chromatin remodeling factors in response to stress ( e.g. ) .
a protein phosphatase 2c and aba co - receptor , hypersensitive to aba1 ( hab1 ) can interact with a subunit of the atp - dependent chromatin remodeling complex swi3b , and swi3b mutants show reduced aba responses .
the deregulation of epigenetically controlled genes and repetitive sequences upon heat stress [ 4648 ] is associated with transient loss of dna - bound nucleosomes at transcribed and non - transcribed genomic regions , and with substantial heterochromatin de - condensation . a role for nucleosome occupancy
is further suggested by delayed re - silencing of heat stress - activated repeats in mutants with impaired chromatin assembly factor 1 ( caf-1 ) subunits .
nucleosome eviction , together with histone tail modifications were also observed at target genes of stress - induced transcription factors in the green alga chlamydomonas .
extreme stress can result in a complete growth arrest , but , after limited damage , plants can recover and resume growth and development .
this is in part exerted by activation of replication- and cell cycle checkpoints that prohibit amplification and transmission of damaged dna .
it is tempting to propose the existence of a similar epigenetic checkpoint control that senses detrimental alterations in the epigenome and halts growth until these alterations are repaired .
similarly , epigenetic mutations with lethal consequences in animals are often less severe in plants , which could indicate a less stringent  quality control of epigenetic integrity .
many plants proliferate partially or even exclusively by vegetative propagation , circumventing epigenetic reprogramming during gamete formation and sexual reproduction as observed in mammals . however
, if such  resetting occurs in plants , it seems to be at least not as extensive , and mitotic and meiotic transmission of stress - induced epigenetic disruptions is therefore conceivable .
these could even be beneficial if they make exposed plants and/or their progeny more resistant upon recapitulated challenges .
the concept of priming plants with a certain stress , resulting in a faster and more pronounced response later , is exemplified by systemic acquired resistance ( sar ) , in which soluble and/or volatile signaling molecules can spread within an individual or be transmitted between plants .
several stress types were reported to induce a priming effect that can be assayed also in subsequent generations [ 5257 ] . in some cases , the lack of epigenetic components , mainly in the rddm pathway , was shown to reduce or eliminate the transmission to the progeny   or mimic the primed state .
however , the effects did not last more than one or two generations , and concomitant chromatin changes were connected only in one case with the primed state of stress - specific genes .
seemingly transgenerational responses can also originate from parental stress affecting embryo development , seed germination or early growth of the progeny , independent or dependent from chromatin - regulated components .
although a role of chromatin in priming is widely assumed [ 5860 ] , proof of strong causal epigenetic changes affecting traits with adaptive values , without concomitant genetic changes or long - living signaling components transmitted through the cytoplasm of gametes , would be desirable .
this is not meant to discourage further studies : on the contrary , the wealth of interesting phenomena that could indicate transgenerational epigenetic inheritance , together with the growing toolbox for thorough genome - wide genetic and epigenetic analysis , make it a very interesting field of research .
analysis of dna methylation in individuals , between generations or populations from different habitats indicates a range of epigenetic diversity that might by far exceed genetic diversity , as described in the contribution of becker and weigel ( this issue ) .
but it is also clear that many epigenetic changes are triggered by genetic mutations , especially transposon movements , in the vicinity .
so far , these genetically triggered epigenetic changes are those with the most relevant and drastic consequences , as exemplified by the development of genetic incompatibility . on the other hand , many transposons are under epigenetic control , as reviewed by bucher et al .
( this issue ) , which makes the question of a direct or indirect epigenetic stress memory an interesting , but difficult - to - investigate chicken - and - egg problem .
stress and epigenetic regulation meet at many different levels from which only a few aspects are documented so far .
current information about the connection resembles a few fragments of a jigsaw puzzle for which neither the number of parts nor the dimensions of the picture are known .
it is very likely that epigenetic variation contributes to the adaptation potential of plants and , like genetic diversity , is under selection by environmental conditions .
whether epigenetic responses to stress can serve as adaptive traits remains a matter of debate .
surprisingly few primary publications have addressed the issue , while many reviews discuss this possibility . adding another one will not shift this imbalance but we hope to stimulate more work in the field .
papers of particular interest , published within the period of review , have been highlighted as: of special interest of outstanding interest  of special interest  of outstanding interest
 highlights epigenetic control is involved in stress signaling and stress responses . 
  stress can modify epigenetic regulation at many different levels . 
  epigenetic and genetic components of stress responses are connected . 
  epigenetic diversity might be an important factor in stress adaptation and evolution . 
Introduction
Level 1: epigenetic components of stress signaling
Level 2: stress etching on chromatin
Level 3: potential for lasting adaptation
Conclusions
References and recommended reading