Jump to content

User:Ajaslay/Transgenerational epigenetic inheritance

From Wikipedia, the free encyclopedia

Article Draft

[edit]

Lead

[edit]

Transgenerational epigenetic inheritance is the transmission of epigenetic markers and modifications from one generation to multiple subsequent generations without altering the primary structure of DNA.[1] Thus, the regulation of genes via epigenetic mechanisms can be heritable; the amount of transcripts and proteins produced can be mitigated by inherited epigenetic changes. In order for epigenetic marks to be heritable, however, they must occur in the gametes in animals, but since plants lack a definitive germline and can propagate, epigenetic marks in any tissue can be heritable.

It is important to note that the inheritance of epigenetic marks in the immediate generation is referred to as intergenerational inheritance.[2] In male mice, the epigenetic signal is maintained through the F1 generation.[3] In female mice, the epigenetic signal is maintained through the F2 generation as a result of the exposure of the germline in the womb.[3] Many epigenetic signals are lost beyond the F2/F3 generation and are no longer inherited, because the subsequent generations were not exposed to the same environment as the parental generations.[2] The signals that are maintained beyond the F2/F3 generation are referred to as transgenerational epigenetic inheritance (TEI), because initial environmental stimuli resulted in inheritance of epigenetic modifications.[4] There are several mechanisms of TEI that have shown to affect germline reprogramming, such as transgenerational increases in susceptibility to diseases, mutations, and stress inheritance. During germline reprogramming and early embryogenesis in mice, methylation marks are removed to allow for development to commence, but the methylation mark is converted into hydroxymethyl-cytosine so that it is recognized and methylated once that area of the genome is no longer being used, [5] which serves as a memory for that TEI mark. Therefore, under lab conditions, inherited methyl marks are removed and restored to ensure TEI still occurs. However, observing TEI in wild populations is still in its infancy, as laboratory studies allow for more tractable systems.[6]

Environmental factors can induce the epigenetic marks (epigenetic tags) for some epigenetically influenced traits.[1] These can include, but are not limited to, changes in temperature, resources availability, exposure to pollutants, chemicals, and endocrine disruptors.[7] The dosage and exposure levels can affect the extent of the environmental factors' influence over the epigenome and its effect on later generations. The epigenetic marks can result in a wide range of effects, including minor phenotypic changes to complex diseases and disorders.[7] The complex cell signaling pathways of multicellular organisms such as plants and humans can make understanding the mechanisms of this inherited process very difficult.[8]

The heritability of these epigenetic marks has increased the controversial idea that modern biology should no longer reject the inheritance of acquired characteristics (Lamarckism) as strongly as it once did.[2] Rather, there is an interplay between natural selection (Darwinism) and changes accrued during an organisms' lifetime that are passed down to progeny (Lamarckism).

Article body

[edit]

Epigenetic Categories

[edit]

There are mechanisms by which environmental exposures induces epigenetic changes by affecting regulation and gene expression. Four general categories of epigenetic modification are known.

  1. self-sustaining metabolic loops, in which an mRNA or protein product of a gene stimulates transcription of the gene; e.g. Wor1 gene in Candida albicans;
  2. Structural templating: structures are replicated using a template or scaffold structure of the parent. This can include, but is not limited to, the orientation and architecture of cytoskeletal structures, cilia and flagella. Ciliates provide a good example of this type of modification. In an experiment Beisson and Sonneborn in 1985, it was demonstrated in Paramecium that if a section of cilia was removed and inverted, then the progeny of that Paramecium would also display the modified cilia structure for several generations.[9] Another example is seen in prions, special proteins that are capable of changing the structure of normal proteins to match their own. The prions use themselves as a template and then edit the folding of normal proteins to match their own folding pattern. The changes in the protein folding results in an alteration in the normal protein's function. This transmission of programming can also alter the chromatin and histone of the DNA and can be passed through the cytosol from parent to offspring during meiosis.[9]
  3. Histone modifications in which the structure of chromatin and its transcriptional state is regulated. DNA is wrapped into a DNA-protein complex called chromatin in the nucleus of eukaryotic cells.[10] Chromatin is comprised of DNA and nucleosomes that comes together to form a histone octamer.[11] The N- and C- terminal of the histone proteins are post-translationally modified by the removal or addition of acetyl (acetylation), phosphate (phosphorylation), methyl (methylation), ubiquitin (ubiquitination), and ubiquitin-like modifier (SUMOylating) groups.[10] Histone modifications can be transgenerational epigenetic signals. For example, histone H3K4 trimethylation (H34me3) and a network of lipid metabolic genes interact to increase the transcription response to TEI obesogenic effects.[12] TEI can also be observed in Drosophila embryos through the exposure of heat stress over generations.[13] The induced heat stress resulted in the phosphorylation of ATF-2 (dATF-2) which is required for heterochromatin assembly. [14] This epigenetic event was maintained over multiple generations, but over time dATF-2 returned back to its normal state.[14]
  4. Non-coding and coding RNAs in which various classes of RNA is implicated in TEI through maternal stores of mRNA, translation of mRNA (miRNA), and small RNA strands interfering with transcription (piRNAs and siRNAs) via RNA interference pathways (RNAi).[2] There has been an increase in studies reporting noncoding RNA contributions to TEI. For example, altered miRNA in early trauma mice.[15] Early trauma mice with unpredictable maternal separation and maternal stress (MSUS) were used as a model to identify the effects of altered miRNA in sperm.[16] In MSUS mice, behavior responses were affected, insulin levels, and blood glucose levels were decreased.[16] Notably, these effects were more severe across the F2 and F3 generation. The expression of miRNA in MSUS mice was down regulated in the brain, serum, and sperm of the F1 generation.[16] However, the miRNA was not altered in the sperm of the F2 generation, and the miRNAs were normal in the F3 generation.[16] This provides supportive evidence that the initial alterations in miRNAs in sperm are transferred to epigenetic marks to maintain transmission.[17] In C.elegans, starvation is induced in which survival is dependent on the mechanisms of the RNAi pathway, repression of microRNAs, and regulation of small RNAs.[18] Thus, memorization of dietary history is inherited across generations.[18]

See also: Dutch famine of 1944–45

Although genetic inheritance is important when describing phenotypic outcomes, it cannot entirely explain why offspring resemble their parents. Aside from genes, offspring come to inherit similar environmental conditions established by previous generations. One environment that human offspring commonly share with their maternal parent for nine months is the womb. Considering the duration of the fetal stages of development, the environment of the mother’s womb can have long lasting effects on the health of offspring.

An example of how the environment within the womb can affect the health of an offspring is the Dutch hunger winter of 1944-45 and its causal effect on induced transgenerational epigenetic inherited diseases. During the Dutch hunger winter, the offspring exposed to famine conditions during the third trimester of development were smaller than those born the year before the famine. Moreover, the offspring born during the famine and their subsequent offspring were found to have an increased risk of metabolic diseases, cardiovascular diseases, glucose intolerance, diabetes, and obesity in adulthood. The effects of this famine on development lasted up to two generations.[8][19] The increased risk factors to the health of F1 and F2 generations during the Dutch hunger winter is a known phenomenon called “fetal programming,” which is caused by exposure to harmful environmental factors in utero.[19]

Inheritance of immunity

[edit]

Epigenetics play a crucial role in regulation and development of the immune system.[20] In 2021, evidence of inheritance of trained immunity across generations to progeny of mice with a systemic infection of Candida albicans was provided.[21] The progeny of mice survived the Candida albicans infection via functional, transcriptional, and epigenetic changes linked to the immune gene loci.[21] The responsiveness of myeloid cells to the Candida albicans infection increased in inflammatory pathways, and resistance was increased to infections in the next generations.[21] Immunity in vertebrates can also be transferred from maternal through the passing of hormones, nutrients and antibodies.[22] In mammals, the maternal factors can be transferred via lactation or the placenta.[22] The transgenerational transmission of immune-related traits are also described in plants and invertebrates. Plants have a defense priming system which enables them to have an alternate defense response that can be accelerated upon exposure to stress actions or pathogens.[23] After the event of priming, priming stress clue information is stored, and the memory may be inherited in the offspring (intergenerational or transgenerational).[23] In studies, the progeny of Pseudomonas syringae infected Arabidopsis were primed during the expression of systemic acquired resistance (SAR).[24] The progeny showed to have resistance against (hemi)-biotrophic pathogens which is associated with salicylic dependent genes and the defense regulatory gene, non expressor of PR genes (NPR1).[24] Transgenerational SAR in the progeny was associated with increased acetylation of histone 3 at lysine 9, hypomethylation of genes, and chromatin marks on promoter regions of salicylic dependent genes.[24] Similarly in insects, the red flour beetle Trifolium castoreum is primed through the exposure of the pathogen Bacillus thuringiensis.[25] Double-mating experiments with the red flour beetle demonstrated that paternal transgenerational immune priming is mediated by sperm or seminal fluid which enhances survival upon exposure to pathogens and contribute to epigenetic changes.[25]

Feedback loops and TEI

[edit]

Positive and negative feedback loops are commonly observed in molecular mechanisms and regulation of homeostatic processes. There is evidence that feedback loops interact to maintain epigenetic modifications within one generation, as well as contributing to TEI in various organisms, and these feedback loops can showcase putative adaptations to environmental perturbances. Feedback loops are truly a repercussion of any epigenetic modification, since it results in changes in expression. Even more so, the feedback loops seen across multiple generations because of TEI showcases a spatio-temporal dynamic that is associated with TEI alone. For example, elevated temperatures during embryogenesis and PIWI RNA (piRNA) establishment are directly proportional, providing a heritable outcome for repressing transposable elements via piRNA clusters [26]. Furthermore, subsequent generations retain an active locus to continue establishing piRNA, which its formation was previously enigmatic [26]. In another case, it was suggested that endocrine disruption had a feedback loop interaction with methylation of varying genomic sites in Menidia beryllina, which may have been a function of TEI. [27] When exposure was removed, and M. beryllina F2 offspring still retained these methylation marks, which caused a negative feedback loop on expression of various genes. [27] In another example, hybridization of eels can lead to feedback loops contributing to transposon demethylation and transposable element activation. [28] Because TE's are typically silenced in the genome, their presence and potential expression creates a feedback loop to prevent hybrids from reproducing with other hybrids or non-hybrid species, which eliminates the proliferation of TE expression and prevents TEI in this context. This phenomenon is known as a form of post-zygotic reproductive isolation.


Examples of TEI

[edit]

See also: Contribution of epigenetic modifications to evolution

The relative importance of genetic and epigenetic inheritance is subject to debate. Though hundreds of examples of epigenetic modification of phenotypes have been published, few studies have been conducted outside of the laboratory setting. Therefore, the interactions of genes with the environment cannot be inferred despite the central role of environment in natural selection. Multiple epigenetic factors can influence the state of genes and alter the epigenetic state. Due to the multivariate nature of environmental factors, it is difficult for researchers to pinpoint the exact cause of epigenetic changes outside of a laboratory setting.[29]

In plants

[edit]

Examples of environmentally induced transgenerational epigenetic inheritance in plants has also been reported. In one case, rice plants that were exposed to drought-simulation treatments displayed increased tolerance to drought after 11 generations of exposure and propagation by single-seed descent as compared to non-drought treated plants. Differences in drought tolerance was linked to directional changes in DNA-methylation levels throughout the genome, suggesting that stress-induced heritable changes in DNA-methylation patterns may be important in adaptation to recurring stresses. In another study, plants that were exposed to moderate caterpillar herbivory over multiple generations displayed increased resistance to herbivory in subsequent generations (as measured by caterpillar dry mass) compared to plants lacking herbivore pressure. This increase in herbivore resistance persisted after a generation of growth without any herbivore exposure suggesting that the response was transmitted across generations. The report concluded that components of the RNA-directed DNA-methylation pathway are involved in the increased resistance across generations. Transgenerational epigenetic inheritance has also been observed in polyploid plants. Genetically identical reciprocal F1 hybrid triploids have been shown to display transgenerational epigenetic effects on viable F2 seed development.

It has been demonstrated in wild radish plants (Raphanus raphanistrum) that TEI can be induced when the plants are exposed to predators such as Pieris rapae, the cabbage white caterpillar. The radish plants will increase production of bristly leaf hairs and toxic mustard oil in response to caterpillar predation. The increased levels will also be seen in the next generation. Decreased levels of predation also results in decreased leaf hairs and toxins produced in the current and subsequent generations.[30]

In Animals

[edit]

It is difficult to trace TEI in animals due to the reprogramming of genes during meiosis and embryogenesis, especially in wild populations that are not reared in a lab setting. Further studies must be conducted to strengthen the documentation of TEI in animals. However, a few examples do exist.

Induced transgenerational epigenetic inheritance has been demonstrated in animals, such as Daphnia cucullata. These tiny crustaceans will develop protective helmets as juveniles if exposed to kairomones, a type of hormone, secreted by predators while they are in utero. The helmet acts as a method of defense by decreasing the ability of predators to capture the Daphnia, thus induction of helmet presence will lower mortality rates. D. cucullata will develop a small helmet if no kairomones are present. However, depending upon the level of predator kairomones, the length of the helmet will almost double. The next generation of Daphnia will display a similar helmet size. If the kairomone levels decrease or disappear, then the third generation will revert to the original helmet size. These organisms display adaptive phenotypes that will affect the phenotype in the subsequent generations.[31]

Genetic analysis of coral reef fish, Acanthochromis polyacanthus, has proposed TEI in response to climate change. As climate change occurs, the ocean water temperature increases. When A. polyacanthus is exposed to higher water temperatures of up to +3°C from normal ocean temperatures, the fish express increased DNA methylation levels on 193 genes, resulting in phenotypic changes in the function of oxygen consumption, metabolism, insulin response, energy production, and angiogenesis. The increase in DNA methylation and its phenotypic affects were carried over to multiple subsequent generations.[32]

Possible TEI has been studied in guinea pigs (Cavia aperea) by exposing males to increased ambient temperature for two months. In the lab, the males were allowed to mate with the same female before and after the heat exposure to determine if the high temperatures affected the offspring. Since it serves as a thermoregulatory organ, samples of the liver were studied in the father guinea pigs (F0 generation) and liver and testes of the male offspring (F1 generation). The F0 males experienced an immediate epigenetic response to the increase in temperature. The F1 generation also displayed the different methylated epigenetic response in their liver and testes, indicating that they could potentially pass on the epigenetic marks to the F2 generation.[33]

References

[edit]
  1. ^ a b Moore, David Scott (2015). The developing genome : an introduction to behavioral epigenetics. Oxford. ISBN 978-0-19-992235-2. OCLC 899240120.{{cite book}}: CS1 maint: location missing publisher (link)
  2. ^ a b c d Heard, Edith; Martienssen, Robert A. (2014-03-27). "Transgenerational Epigenetic Inheritance: Myths and Mechanisms". Cell. 157 (1): 95–109. doi:10.1016/j.cell.2014.02.045. ISSN 0092-8674. PMC 4020004. PMID 24679529.{{cite journal}}: CS1 maint: PMC format (link)
  3. ^ a b Fitz-James, Maximilian H.; Cavalli, Giacomo (2022-06). "Molecular mechanisms of transgenerational epigenetic inheritance". Nature Reviews Genetics. 23 (6): 325–341. doi:10.1038/s41576-021-00438-5. ISSN 1471-0064. {{cite journal}}: Check date values in: |date= (help)
  4. ^ Fitz-James, Maximilian H.; Cavalli, Giacomo (2022-06). "Molecular mechanisms of transgenerational epigenetic inheritance". Nature Reviews Genetics. 23 (6): 325–341. doi:10.1038/s41576-021-00438-5. ISSN 1471-0056. {{cite journal}}: Check date values in: |date= (help)
  5. ^ Iqbal, Khursheed; Jin, Seung-Gi; Pfeifer, Gerd P.; Szabó, Piroska E. (2011-03). "Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine". Proceedings of the National Academy of Sciences. 108 (9): 3642–3647. doi:10.1073/pnas.1014033108. ISSN 0027-8424. PMC 3048122. PMID 21321204. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link)
  6. ^ Husby, Arild (2022-02-09). "Wild epigenetics: insights from epigenetic studies on natural populations". Proceedings of the Royal Society B: Biological Sciences. 289 (1968): 20211633. doi:10.1098/rspb.2021.1633. ISSN 0962-8452. PMC 8826306. PMID 35135348.{{cite journal}}: CS1 maint: PMC format (link)
  7. ^ a b Ho, Shuk-Mei; Johnson, Abby; Tarapore, Pheruza; Janakiram, Vinothini; Zhang, Xiang; Leung, Yuet-Kin (2012-12). "Environmental Epigenetics and Its Implication on Disease Risk and Health Outcomes". ILAR Journal. 53 (3–4): 289–305. doi:10.1093/ilar.53.3-4.289. ISSN 1084-2020. PMC 4021822. PMID 23744968. {{cite journal}}: Check date values in: |date= (help); line feed character in |title= at position 73 (help)
  8. ^ a b Emmanuel, DROUET (2016-09-30). "Epigenetics: How the environment influences our genes". Encyclopedia of the Environment. Retrieved 2023-02-22.
  9. ^ a b Jablonka, Eva; Raz, Gal (2009-06). "Transgenerational Epigenetic Inheritance: Prevalence, Mechanisms, and Implications for the Study of Heredity and Evolution". The Quarterly Review of Biology. 84 (2): 131–176. doi:10.1086/598822. ISSN 0033-5770. {{cite journal}}: Check date values in: |date= (help)
  10. ^ a b Li, Dong; Yang, Yan; Li, Youping; Zhu, Xiaohua; Li, Zeqin (2021-07-01). "Epigenetic regulation of gene expression in response to environmental exposures: From bench to model". Science of The Total Environment. 776: 145998. doi:10.1016/j.scitotenv.2021.145998. ISSN 0048-9697.
  11. ^ "DNA Packaging: Nucleosomes and Chromatin | Learn Science at Scitable". www.nature.com. Retrieved 2023-02-26.
  12. ^ Wan, Qin-Li; Meng, Xiao; Wang, Chongyang; Dai, Wenyu; Luo, Zhenhuan; Yin, Zhinan; Ju, Zhenyu; Fu, Xiaodie; Yang, Jing; Ye, Qunshan; Zhang, Zhan-Hui; Zhou, Qinghua (2022-02-09). "Histone H3K4me3 modification is a transgenerational epigenetic signal for lipid metabolism in Caenorhabditis elegans". Nature Communications. 13 (1): 768. doi:10.1038/s41467-022-28469-4. ISSN 2041-1723. PMC 8828817. PMID 35140229.{{cite journal}}: CS1 maint: PMC format (link)
  13. ^ Fitz-James, Maximilian H.; Cavalli, Giacomo (2022-06). "Molecular mechanisms of transgenerational epigenetic inheritance". Nature Reviews Genetics. 23 (6): 325–341. doi:10.1038/s41576-021-00438-5. ISSN 1471-0064. {{cite journal}}: Check date values in: |date= (help)
  14. ^ a b Seong, Ki-Hyeon; Li, Dong; Shimizu, Hideyuki; Nakamura, Ryoichi; Ishii, Shunsuke (2011-06-24). "Inheritance of Stress-Induced, ATF-2-Dependent Epigenetic Change". Cell. 145 (7): 1049–1061. doi:10.1016/j.cell.2011.05.029. ISSN 0092-8674. PMID 21703449.
  15. ^ Sen, Rwik; Barnes, Christopher (2021-06). "Do Transgenerational Epigenetic Inheritance and Immune System Development Share Common Epigenetic Processes?". Journal of Developmental Biology. 9 (2): 20. doi:10.3390/jdb9020020. ISSN 2221-3759. {{cite journal}}: Check date values in: |date= (help)CS1 maint: unflagged free DOI (link)
  16. ^ a b c d Gapp, Katharina; Jawaid, Ali; Sarkies, Peter; Bohacek, Johannes; Pelczar, Pawel; Prados, Julien; Farinelli, Laurent; Miska, Eric; Mansuy, Isabelle M. (2014-05). "Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice". Nature Neuroscience. 17 (5): 667–669. doi:10.1038/nn.3695. ISSN 1546-1726. PMC 4333222. PMID 24728267. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link)
  17. ^ Rodgers, Ali B.; Morgan, Christopher P.; Leu, N. Adrian; Bale, Tracy L. (2015-11-03). "Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress". Proceedings of the National Academy of Sciences. 112 (44): 13699–13704. doi:10.1073/pnas.1508347112. ISSN 0027-8424. PMC 4640733. PMID 26483456.{{cite journal}}: CS1 maint: PMC format (link)
  18. ^ a b Rechavi, Oded; Houri-Ze’evi, Leah; Anava, Sarit; Goh, Wee Siong Sho; Kerk, Sze Yen; Hannon, Gregory J.; Hobert, Oliver (2014-07-17). "Starvation-Induced Transgenerational Inheritance of Small RNAs in C. elegans". Cell. 158 (2): 277–287. doi:10.1016/j.cell.2014.06.020. ISSN 0092-8674. PMC 4377509. PMID 25018105.{{cite journal}}: CS1 maint: PMC format (link)
  19. ^ a b Stein, A. D (2004-07-28). "Intrauterine famine exposure and body proportions at birth: the Dutch Hunger Winter". International Journal of Epidemiology. 33 (4): 831–836. doi:10.1093/ije/dyh083. ISSN 1464-3685.
  20. ^ Sen, Rwik; Barnes, Christopher (2021-05-12). "Do Transgenerational Epigenetic Inheritance and Immune System Development Share Common Epigenetic Processes?". Journal of Developmental Biology. 9 (2): 20. doi:10.3390/jdb9020020. ISSN 2221-3759. PMC 8162332. PMID 34065783.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  21. ^ a b c Katzmarski, Natalie; Domínguez-Andrés, Jorge; Cirovic, Branko; Renieris, Georgios; Ciarlo, Eleonora; Le Roy, Didier; Lepikhov, Konstantin; Kattler, Kathrin; Gasparoni, Gilles; Händler, Kristian; Theis, Heidi; Beyer, Marc; van der Meer, Jos W. M.; Joosten, Leo A. B.; Walter, Jörn (2021-11). "Transmission of trained immunity and heterologous resistance to infections across generations". Nature Immunology. 22 (11): 1382–1390. doi:10.1038/s41590-021-01052-7. ISSN 1529-2916. {{cite journal}}: Check date values in: |date= (help)
  22. ^ a b Eggert, Hendrik; Kurtz, Joachim; Diddens-de Buhr, Maike F. (2014-12-22). "Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring". Proceedings of the Royal Society B: Biological Sciences. 281 (1797): 20142089. doi:10.1098/rspb.2014.2089. ISSN 0962-8452. PMC 4240996. PMID 25355479.{{cite journal}}: CS1 maint: PMC format (link)
  23. ^ a b Emerging Trends in Plant Pathology. doi:10.1007/978-981-15-6275-4.
  24. ^ a b c Luna, Estrella; Ton, Jurriaan (2012-06). "The epigenetic machinery controlling transgenerational systemic acquired resistance". Plant Signaling & Behavior. 7 (6): 615–618. doi:10.4161/psb.20155. ISSN 1559-2324. {{cite journal}}: Check date values in: |date= (help)
  25. ^ a b Eggert, Hendrik; Kurtz, Joachim; Diddens-de Buhr, Maike F. (2014-12-22). "Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring". Proceedings of the Royal Society B: Biological Sciences. 281 (1797): 20142089. doi:10.1098/rspb.2014.2089. ISSN 0962-8452. PMC 4240996. PMID 25355479.{{cite journal}}: CS1 maint: PMC format (link)
  26. ^ a b Casier, Karine; Delmarre, Valérie; Gueguen, Nathalie; Hermant, Catherine; Viodé, Elise; Vaury, Chantal; Ronsseray, Stéphane; Brasset, Emilie; Teysset, Laure; Boivin, Antoine (2019-03-15). Nilsen, Timothy W; Manley, James L (eds.). "Environmentally-induced epigenetic conversion of a piRNA cluster". eLife. 8: e39842. doi:10.7554/eLife.39842. ISSN 2050-084X.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  27. ^ a b Major, Kaley M.; DeCourten, Bethany M.; Li, Jie; Britton, Monica; Settles, Matthew L.; Mehinto, Alvine C.; Connon, Richard E.; Brander, Susanne M. (2020). "Early Life Exposure to Environmentally Relevant Levels of Endocrine Disruptors Drive Multigenerational and Transgenerational Epigenetic Changes in a Fish Model". Frontiers in Marine Science. 7. doi:10.3389/fmars.2020.00471/full. ISSN 2296-7745.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  28. ^ Liu, Shenglin; Tengstedt, Aja Noersgaard Buur; Jacobsen, Magnus W.; Pujolar, Jose Martin; Jónsson, Bjarni; Lobón‐Cervià, Javier; Bernatchez, Louis; Hansen, Michael M. (2022-08). "Genome‐wide methylation in the panmictic European eel ( Anguilla anguilla )". Molecular Ecology. 31 (16): 4286–4306. doi:10.1111/mec.16586. ISSN 0962-1083. {{cite journal}}: Check date values in: |date= (help); no-break space character in |first4= at position 5 (help)
  29. ^ Day, Jeremy J. (2014-09-30). "New approaches to manipulating the epigenome". Dialogues in Clinical Neuroscience. 16 (3): 345–357. doi:10.31887/DCNS.2014.16.3/jday. ISSN 1958-5969. PMC 4214177. PMID 25364285.{{cite journal}}: CS1 maint: PMC format (link)
  30. ^ Sobral, Mar; Sampedro, Luis; Neylan, Isabelle; Siemens, David; Dirzo, Rodolfo (2021-08-17). "Phenotypic plasticity in plant defense across life stages: Inducibility, transgenerational induction, and transgenerational priming in wild radish". Proceedings of the National Academy of Sciences. 118 (33): e2005865118. doi:10.1073/pnas.2005865118. ISSN 0027-8424. PMC 8379918. PMID 34389664.{{cite journal}}: CS1 maint: PMC format (link)
  31. ^ Agrawal, Anurag A.; Laforsch, Christian; Tollrian, Ralph (1999-09-02). "Transgenerational induction of defences in animals and plants". Nature. 401 (6748): 60–63. doi:10.1038/43425. ISSN 0028-0836.
  32. ^ Ryu, Taewoo; Veilleux, Heather D.; Donelson, Jennifer M.; Munday, Philip L.; Ravasi, Timothy (2018-04-30). "The epigenetic landscape of transgenerational acclimation to ocean warming". Nature Climate Change. 8 (6): 504–509. doi:10.1038/s41558-018-0159-0. ISSN 1758-678X.
  33. ^ Hu, J.; Barrett, R. D. H. (2017-07-20). "Epigenetics in natural animal populations". Journal of Evolutionary Biology. 30 (9): 1612–1632. doi:10.1111/jeb.13130. ISSN 1010-061X.
Retrieved from "https://en.wikipedia.org/w/index.php?title=User:Ajaslay/Transgenerational_epigenetic_inheritance&oldid=1150769385"