Various epigenetic modulators and their functions.
Abstract
Plants being organisms that lack locomotion and vocabulary, they are not privileged to escape and communicate during unfavourable conditions of biotic/abiotic stresses, like their animal counterparts. Therefore, plants have evolved with higher adaptive skills that tune them during unfavourable conditions. In this context, regulation of gene expression plays a crucial role in controlling the cellular pathways required for survival during unfavourable conditions. This chapter is about the epigenetic regulation of plant defence during biotic stress. Researchers have taken various approaches to understand the epigenetic regulation of plant defences and these approaches are described here. Epigenetic regulation also has the potential to be inherited and this phenomenon has aided plants for better adaption. Such reports on transgenerational memory during biotic stress in plants are also compiled. A deeper understanding of epigenetic regulation of defence pathways during biotic stress, and identification of epigenetic marks on the genomes, can aid the development of crop improvement strategies. With the recent advancement in epigenome editing, it should become possible to develop epigenetically improvised plants, devoid of genetic modification.
Keywords
- epigenetic regulation
- epigenetic modification
- biotic stress
- plant defence
- heritable epigenetic changes
- methylation
1. Introduction
Regulation of gene expression is the ultimate criteria that decide the role of each player in all cellular pathways. Gene regulation occurs in the nucleus and cytoplasm at multiple levels such as chromatin conformation, transcription regulation, post-transcription regulation, regulation of translation, protein modification, and protein degradation. Regulation at transcription is one of the prominent mechanisms as it involves the so called ‘switching-on and switching-off’ of genes. Gene regulation is required for organisms not only for their routine growth and maintenance but also for survival during unfavourable conditions. In this context, epigenetic regulation is of much significance because it not only offers adaptive skills to the organisms under stress but also has the potential to be heritable, thereby contributing to transgenerational memory. Owing to lack of locomotion and vocabulary in plants, like their animal counter parts, it is imperative for them to survive in unfavourable conditions such as biotic and abiotic stress. Therefore, plants have evolved with an elaborate mechanism of gene regulation, especially epigenetic regulation. Researchers have deduced gene functions by adopting various approaches and the key findings in epigenetic regulation and transgenerational memory in plants during biotic stress are described in this chapter.
2. Promoters, the switches for perceiving stress-induced communications
Promoters serve the function of a switch as they are the site for the binding of RNA polymerase and other transcription regulators. Promoters harbour
3. Epigenetic modifications
Epigenetic changes refer to all modifications or influences on the chromatin, except for changes in the DNA sequence [4, 5]. These changes if occurred in promoters or other regulatory regions can result in altered gene expression, thereby contributing to phenotype plasticity. Multiple factors can lead to epigenetic changes (Figure 1). Nucleotides in DNA, especially cytosine, undergo methylation/demethylation. In addition to methylation, histones can undergo other chemical modifications such as acetylation, phosphorylation, ubiquitylation, and sumoylation. Non-coding RNAs are involved in altering chromatin organisation and/or methylation of chromatin [6]. Replacement of histones by histone variants such as H3.3, H2A.X, and H2A.Z also influence chromatin organisation and gene expression [7, 8].
4. Different approaches taken to understand epigenetic regulation of plant defences
Discoveries in various aspects of epigenetic regulation in plants provided a deeper perception of various pathways, including defence. Different approaches taken by researchers include the study of epigenetic regulation of defence genes directly under pathogen stress, whole epigenome analysis, and understanding of the regulation of epigenetic regulators and their influence on disease (Figure 2). In this chapter, the research done in understanding different aspects of epigenetic regulation during plant-pathogen interaction and defence is described. Epigenetic changes have the potential to be retained after multiple cell divisions of both mitosis and meiosis. Therefore, heritable epigenetic changes lead to an interesting phenomenon of transgenerational memory. Epigenetic changes play a crucial role in plants as they not only lack locomotion, but also the vocabulary mode of communication. Biotic/abiotic stress-induced epigenetic changes have often generated plants and even their offsprings, with enhanced stress resistance. Such aspects are also elaborated in this chapter.
4.1 Biotic stress-induced epigenetic modulation of defence genes
Pathogen stress is well known to alter the expression of numerous genes, belonging to several pathways, including those involved in defence, in plants. Interestingly, there are reports revealing the involvement of pathogen stress in altering the epigenetic status of various defence genes. For example, infection by
Though regulation of defence genes was known to be modulated by many TFs as mentioned earlier in this chapter, it is interesting to note that epigenetic regulation is involved in modulating these modulators. For example, promoters of three WRKY TFs, WRKY29, WRKY6, and WRKY53 underwent histone methylation and acetylation under biotic stress conditions and some of these modifications facilitated gene expression in primed plants [13].
4.2 Epigenetic modulators under biotic stress
About 130 genes are known to be involved in epigenetic regulation in plants [14]. We selected 60 genes involved in DNA and histone methylation (Table 1) and looked whether there are any previous reports on their expressions in the eFP Browser (
No. | Genes names and category | Function | References | |
---|---|---|---|---|
1. | Plant DNA methyltransferase | [15] | ||
2. | Maintenance of CHH methylation | |||
3. | A chromomethylase involved in methylating cytosine at non-CG sites | |||
4. | Gene silencing and maintenance of DNA methylation | |||
5. | Phosphate (Pi) homeostasis during DNA and histone methylation | [16] | ||
6. | Maintenance of CG and CHG methylation | [17] | ||
7. | Acts along with DME | |||
8. | Catalyses the release of 5-methylcytosine (5-meC) from DNA by a glycosylase/lyase mechanism | |||
9. | Maintains DNA methylation in CHG context | [18] | ||
10. | Major trans acting locus affecting DNA methylation | |||
11. | Link between responses to DNA damage and epigenetic gene silencing | [19] | ||
12. | DNA repair and meiotic recombination | |||
13. | High level delays flowering unless treated with prolonged cold | [20] | ||
14. | Encodes a histone 3 lysine 9 specific methyltransferase involved in the maintenance of DNA methylation | |||
15. | Required for posttranscriptional gene silencing | [21] | ||
16. | Normal RNA directed DNA methylation at non CG methylation sites and transgene silencing | |||
17. | Prevents the transmission of stress-induced transcriptional changes to progeny of the stressed plants | |||
18. | Prevents ectopic 3′ end processing of mRNA in atypically long introns containing T-DNA sequences | [22] | ||
19. | Encodes RNA-dependent RNA polymerase that is required for endogenous siRNA (but not miRNA) formation | |||
20. | Encodes a ribonuclease III family protein that is required for endogenous RDR2-dependent siRNA formation | |||
21. | SiRNA mediated gene silencing, CpNpG and CpHpH methylation | |||
22. | encodes a shared subunit of RNA polymerase IV and V | |||
23. | A putative DNA methyl transferase with rearranged catalytic domains | |||
24. | Important for DNA methylation and transcriptional gene silencing | |||
25. | Encodes a Dicer-like protein that functions in the antiviral silencing response | |||
26. | Encodes an RNaseIII-like enzyme that catalyses processing of trans-acting siRNA precursors | |||
27. | Encodes transcriptional regulator that promotes the transition to flowering, T DNA shows high methylation | |||
28. | Required for epigenetic maintenance of the vernalized state | [23] | ||
29. | Encodes a SET domain protein that is involved in epigenetic regulation | |||
30. | Has a SET domain for methyltransferase activity and is involved in the stable transcriptional silencing of target genes | |||
31. | Involved in centromere heterochromatisation, CG methylation | [24] | ||
32. | Activates the expression of AtWRKY70 epigenetically by nucleosomal histone H3K4 trimethylations | [25] | ||
33. | ATX1 leads to nucleosomal histone H3K4 trimethylations that activate AtWRKY70, which in turn activates | |||
34. | Histone methylations at the AtWRKY40 promoter activate the SA-dependent pathway to control plant immunity | |||
35. | Epigenetically influences systemic-acquired-resistance induced expression of AtWRKY29 and AtWRKY6 through histone modifications at their promoters | |||
36. | Leads to H3K4me2 and H3K4me3 methylation that epigenetically regulates AtWRKY53 to mediate leaf senescence responses | [26] | ||
37. | Histone methyl transferase activity and maintenance of H3 mK9 | |||
38. | Binds to methylated cytosine of CG, CNN, CNG | |||
39. | Control of replication of transposable elements and repeated sequences | [27] | ||
40. | Control of replication of transposable elements and repeated sequences | |||
41. | Maintains vegetative development, encodes a putative transcriptional regulator | [28] | ||
42. | Maintains vegetative development, encodes a polycomb group | |||
43. | Maintains gene silencing via histone modification | |||
44. | Maintains gene silencing via histone modification | |||
45. | Epigenetic maintenance of reproductive development | [29] | ||
46. | Gene involved in plant response to pathogen | [9] | ||
47. | Histone methyltransferase involved in di and tri-methylation of ‘Lys-36’ of histone H3 (H3K36me2 and H3K36me3) | |||
48. | Histone-lysine N-methyl transferase activity | |||
49. | Contributes to plant fitness like biomass, carbon fixation by influencing circadian clock period. | [21] | ||
50. | Essential component of a temperature-sensitive circadian system | |||
51 | Essential component of a temperature-sensitive circadian system | |||
52 | Necessary component for bacterial resistance. | |||
53. | One of the four closely related | [24] | ||
54. | Putative role in cell fate determination. Involved in the control of leaf morphogenesis. | |||
55. | Has a SET domain for methyltransferase activity and is involved in the stable transcriptional silencing of target genes. | |||
56. | Encodes a polycomb group of protein | |||
57. | Contains a SET domain which is known to be involved in modification of histone tails by methylation | |||
58. | SET domain, histone methylation | |||
59. | Encodes a type I protein arginine methyltransferase | |||
60. | Encodes a type I protein arginine methyltransferase |
4.3 Regulators of epigenetic modifications that influence defence genes
Like any other pathway in organisms, epigenetic regulation is also maintained by many key players. There are reports that many such epigenetic regulators are directly associated with the expression of many defence genes as, observed in various loss-of-function mutant plants. JmjC DOMAIN-CONTAINING PROTEIN 27 (JMJ27), an
Using the
4.4 Epigenetic regulators that provide immunity/resistance/susceptibility
There are several reports confirming that various epigenetic regulators are directly involved in either providing immunity to plants or, to render the plants susceptible to various stresses. For instance, studies on
4.5 Biotic stress-induced epigenomic changes
Biotic stress such as microbes and herbivory have induced loci-specific as well global epigenetic changes, both at DNA and histone levels. Infection of
Nematode-associated molecular patterns from different nematode species and bacterial pathogen-associated molecular pattern flg22 induced global DNA hypomethylation in rice and tomato plants [50]. Hypomethylation was more common at CHH and not CG or CHG nucleotides in these plants. While herbivory due to an insect
Open chromatin is an indication of epigenetic changes such as histone acetylation, which loosen chromatin. About 10,129 open chromatin sites associated with about 3025 genes, most of which also had enhanced expression, were induced in
A comparison of whole epigenomes in various
The beneficial fungus
4.6 Heritable epigenetic biotic stress-induced responses
There are several reports revealing the heritable nature of pathogen-induced epigenetic changes in plants [55, 56]. For example,
The epiRILs lines of
Similarly, to pathogens, herbivory also induced transgenerational responses. For example herbivory due to caterpillars in
The close influence of pathogen stress on epigenetic modification of plant defence system and transgenerational memory offers an entire new array of promises for crop improvement. Approaches of whole epigenome studies under various conditions of biotic stress and resistance would unravel more aspects of the epigenetic regulation of host mechanisms. New avenues of epimutagenic studies that could serve as alternatives for methods that involve gene manipulations/mutations seem to be promising.
5. External application of chemicals or external factors that induce epigenetic changes
There are observations where application of certain chemicals such as SA, JA, methyl jasmonate, systemin, paraquat, abscisic acid, azelaic acid, and pipecolic acid on plants had resulted in enhanced resistance against pathogens, which could even be heritable [62, 63]. Even conditions of altered salinity, light, drought, and temperature had induced similar results [63]. Reports indicate that the action of some of these external factors involve epigenetic modifications in plants. For example, application of 1-isothiocyanato-4-methylsulfinylbutane on
6. Conclusions
While understanding of the DNA sequence conveyed what information is there in the genome and expression analysis conveyed what information is disseminated, research on epigenetics conveyed how the information is disseminated. While the entire genome of an organism needs to be sequenced only once to get the sequence information, epigenome has to be sequenced and studied multiple times, with multiple approaches, based on the regulatory aspects of relevance. Owing to the dynamic and reversible nature of epigenetic regulation and, phenotypic plasticity, epigenetic regulation can play a crucial role in improvising traits of agronomic importance, including plant defence. Functions of more epigenetic modulators need to be analysed that can tune the plants towards a favourable trait. The function of more epialleles needs to be identified for their application in developing enhanced resistance in plants. With the recent development of non-transgenic method of epigenome editing, epialleles of agronomic importance can be generated and deployed.
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