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