Molecular insights into the transgenerational inheritance of stress memory

Qian Zhang; Ye Tian

doi:10.1016/j.jgg.2021.11.015

Volume 49 Issue 2

Mar. 2022

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2022 > 49(2): 89-95

PDF( 926 KB)

Molecular insights into the transgenerational inheritance of stress memory

doi: 10.1016/j.jgg.2021.11.015

Qian Zhang^a,
Ye Tian^a,b,c

a State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China;
b University of Chinese Academy of Sciences, Beijing 100093, China;
c Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China

Funds:

This work was supported by the National Key R&

D Program of China (2017YFA0506400), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB39000000), and the National Natural Science Foundation of China (31930023, 31771333). Q.Z. was supported by the China National Postdoctoral Program for Innovative Talents (BX2021356).

Received Date: 2021-10-08
Accepted Date: 2021-11-22
Rev Recd Date: 2021-11-18
Publish Date: 2021-12-17

Abstract

Abstract

There is accumulating evidence to show that environmental stressors can regulate a variety of phenotypes in descendants through germline-mediated epigenetic inheritance. Studies of model organisms exposed to environmental cues (e.g., diet, heat stress, toxins) indicate that altered DNA methylations, histone modifications, or non-coding RNAs in the germ cells are responsible for the transgenerational effects. In addition, it has also become evident that maternal provision could provide a mechanism for the transgenerational inheritance of stress adaptations that result from ancestral environmental cues. However, how the signal of environmentally-induced stress response transmits from the soma to the germline, which may influence offspring fitness, remains largely elusive. Small RNAs could serve as signaling molecules that transmit between tissues and even across generations. Furthermore, a recent study revealed that neuronal mitochondrial perturbations induce a transgenerational induction of the mitochondrial unfolded protein response mediated by a Wnt-dependent increase in mitochondrial DNA levels. Here, we review recent work on the molecular mechanism by which parental experience can affect future generations and the importance of soma-to-germline signaling for transgenerational inheritance.

FullText(HTML)

References(89)

References

Badyaev, A. V., 2005. Stress-induced variation in evolution:From behavioural plasticity to genetic assimilation. Proc. R. Soc. B Biol. Sci. 272, 877-886

Baugh, L.R., Day, T., 2020. Nongenetic inheritance and multigenerational plasticity in the Nematode C. Elegans. Elife 9, e58498

Benedetti, C., Haynes, C.M., Yang, Y., Harding, H.P., Ron, D., 2006. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 174, 229-239

Berendzen, K.M., Durieux, J., Shao, L.W., Tian, Y., Kim, H. eui, Wolff, S., Liu, Y., Dillin, A., 2016. Neuroendocrine coordination of mitochondrial stress signaling and proteostasis. Cell 166, 1553-1563.e10

Burton, N.O., Riccio, C., Dallaire, A., Price, J., Jenkins, B., Koulman, A., Miska, E.A., 2020. Cysteine synthases CYSL-1 and CYSL-2 mediate C. elegans heritable adaptation to P. vranovensis infection. Nat. Commun. 11, 1741

Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Yunfang, Shi, J., Feng, G.H., Peng, H., Zhang, X., Zhang, Ying, Qian, J., Duan, E., Zhai, Q., Zhou, Q., 2016. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351, 397-400

Conine, C.C., Sun, F., Song, L., Rivera-Perez, J.A., Rando, O.J., 2018. Small RNAs Gained during Epididymal Transit of Sperm Are Essential for Embryonic Development in Mice. Dev. Cell 46, 470-480.e3

Cropley, J.E., Eaton, S.A., Aiken, A., Young, P.E., Giannoulatou, E., Ho, J.W.K., Buckland, M.E., Keam, S.P., Hutvagner, G., Humphreys, D.T., Langley, K.G., Henstridge, D.C., Martin, D.I.K., Febbraio, M.A., Suter, C.M., 2016. Male-lineage transmission of an acquired metabolic phenotype induced by grand-paternal obesity. Mol. Metab. 5, 699-708

Cropley, J.E., Suter, C.M., Beckman, K.B., Martin, D.I.K., 2006. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proc. Natl. Acad. Sci. U. S. A. 103, 17308-17312

Cubas, P., Vincent, C., Coen, E., 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157-161

de Castro Barbosa, T., Ingerslev, L.R., Alm, P.S., Versteyhe, S., Massart, J., Rasmussen, M., Donkin, I., Sjogren, R., Mudry, J.M., Vetterli, L., Gupta, S., Krook, A., Zierath, J.R., Barres, R., 2016. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol. Metab. 5, 184-197

Devanapally, S., Ravikumar, S., Jose, A.M., 2015. Double-stranded RNA made in C. Elegans neurons can enter the germline and cause transgenerational gene silencing. Proc. Natl. Acad. Sci. U. S. A. 112, 2133-2138

Dias, B.G., Ressler, K.J., 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 17, 89-96

Duempelmann, L., Skribbe, M., Buhler, M., 2020. Small RNAs in the Transgenerational Inheritance of Epigenetic Information. Trends Genet. 36, 203-214

Durieux, J., Wolff, S., Dillin, A., 2011. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144, 79-91

Fullston, T., Palmer, N.O., Owens, J.A., Mitchell, M., Bakos, H.W., Lane, M., 2012. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum. Reprod. 27, 1391-1400

Galloway, L.F., Etterson, J.R., 2007. Transgenerational plasticity is adaptive in the wild. Science 318, 1134-1136

Gapp, K., Soldado-Magraner, S., Alvarez-Sanchez, M., Bohacek, J., Vernaz, G., Shu, H., Franklin, T.B., Wolfer, D., Mansuy, I.M., 2014. Early life stress in fathers improves behavioural flexibility in their offspring. Nat. Commun. 5, 5466

Grandjean, V., Fourre, S., De Abreu, D.A.F., Derieppe, M.A., Remy, J.J., Rassoulzadegan, M., 2015. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci. Rep. 5, 18193

Greer, E.L., Maures, T.J., Hauswirth, A.G., Green, E.M., Leeman, D.S., Maro, G.S., Han, S., Banko, M.R., Gozani, O., Brunet, A., 2010. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 466, 383-387

Greer, E.L., Maures, T.J., Ucar, D., Hauswirth, A.G., Mancini, E., Lim, J.P., Benayoun, B.A., Shi, Y., Brunet, A., 2011. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479, 365-371

Harvey, S.C., Orbidans, H.E., 2011. All eggs are not equal:The maternal environment affects progeny reproduction and developmental fate in Caenorhabditis elegans. PLoS One 6, e25840

Haynes, C.M., Petrova, K., Benedetti, C., Yang, Y., Ron, D., 2007. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 13, 467-480

Hercus, M.J., Loeschcke, V., Rattan, S.I.S., 2003. Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress. Biogerontology 4, 149-156

Hibshman, J.D., Hung, A., Baugh, L.R., 2016. Maternal Diet and Insulin-Like Signaling Control Intergenerational Plasticity of Progeny Size and Starvation Resistance. PLoS Genet. 12, e1006396

Houri-Zeevi, L., Rechavi, O., 2017. A Matter of Time:Small RNAs Regulate the Duration of Epigenetic Inheritance. Trends Genet. 33, 46-57

Huypens, P., 2016. Epigenetic germline inheritance of diet-induced obesity and insulin resistance. Nat. Genet. 48, 497-499

Igosheva, N., Abramov, A.Y., Poston, L., Eckert, J.J., Fleming, T.P., Duchen, M.R., McConnell, J., 2010. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5, e10074

Jawaid, A., Jehle, K.L., Mansuy, I.M., 2021. Impact of Parental Exposure on Offspring Health in Humans. Trends Genet. 37, 373-388

Jobson, M.A., Jordan, J.M., Sandrof, M.A., Hibshman, J.D., Lennox, A.L., Baugh, L.R., 2015. Transgenerational Effects of Early Life Starvation on Growth, Reproduction, and Stress Resistance in Caenorhabditis elegans. Genetics 201, 201-212

Jordan, J.M., Hibshman, J.D., Webster, A.K., Kaplan, R.E.W., Leinroth, A., Guzman, R., Maxwell, C.S., Chitrakar, R., Bowman, E.A., Fry, A.L., Hubbard, E.J.A., Baugh, L.R., 2019. Insulin/IGF Signaling and Vitellogenin Provisioning Mediate Intergenerational Adaptation to Nutrient Stress. Curr. Biol. 29, 2380-2388.e5

Kaletsky, R., Moore, R.S., Vrla, G.D., Parsons, L.R., Gitai, Z., Murphy, C.T., 2020. C. elegans interprets bacterial non-coding RNAs to learn pathogenic avoidance. Nature 586, 445-451

Kishimoto, S., Uno, M., Okabe, E., Nono, M., Nishida, E., 2017. Environmental stresses induce transgenerationally inheritable survival advantages via germline-to-soma communication in Caenorhabditis elegans. Nat. Commun. 8, 14031

Klosin, A., Casas, E., Hidalgo-Carcedo, C., Vavouri, T., Lehner, B., 2017. Transgenerational transmission of environmental information in C. elegans. Science 356, 320-323

Kumsta, C., Chang, J.T., Schmalz, J., Hansen, M., 2017. Hormetic heat stress and HSF-1 induce autophagy to improve survival and proteostasis in C. Elegans. Nat. Commun. 8, 14337

Latorre-Pellicer, A., Moreno-Loshuertos, R., Lechuga-Vieco, A.V., Sanchez-Cabo, F., Torroja, C., Acin-Perez, R., Calvo, E., Aix, E., Gonzalez-Guerra, A., Logan, A., Bernad-Miana, M.L., Romanos, E., Cruz, R., Cogliati, S., Sobrino, B., Carracedo, A., Perez-Martos, A., Fernandez-Silva, P., Ruiz-Cabello, J., Murphy, M.P., Flores, I., Vazquez, J., Enriquez, J.A., 2016. Mitochondrial and nuclear DNA matching shapes metabolism and healthy ageing. Nature 535, 561-565

Liu, Y., Samuel, B.S., Breen, P.C., Ruvkun, G., 2014. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature 508, 406-410

Ma, J.Y., Li, S., Chen, L.N., Schatten, H., Ou, X.H., Sun, Q.Y., 2020. Why is oocyte aneuploidy increased with maternal aging? J. Genet. Genomics 47, 659-671

Ma, C., Niu, R., Huang, T., Shao, L.W., Peng, Y., Ding, W., Wang, Y., Jia, G., He, C., Li, C.Y., He, A., Liu, Y., 2019. N6-methyldeoxyadenine is a transgenerational epigenetic signal for mitochondrial stress adaptation. Nat. Cell Biol. 21, 319-327

Martinus, R.D., Garth, G.P., Webster, T.L., Cartwright, P., Naylor, D.J., Hoej, P.B., Hoogenraad, N.J., 1996. Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome. Eur. J. Biochem. 240, 98-103

Maxwell, C.S., Antoshechkin, I., Kurhanewicz, N., Belsky, J.A., Baugh, L.R., 2012. Nutritional control of mRNA isoform expression during developmental arrest and recovery in C. elegans. Genome Res. 22, 1920-1929

Merkwirth, C., Jovaisaite, V., Durieux, J., Matilainen, O., Jordan, S.D., Quiros, P.M., Steffen, K.K., Williams, E.G., Mouchiroud, L., Tronnes, S.U., Murillo, V., Wolff, S.C., Shaw, R.J., Auwerx, J., Dillin, A., 2016. Two conserved histone demethylases regulate mitochondrial stress-induced longevity. Cell 165, 1209-1223

Moore, R.S., Kaletsky, R., Lesnik, C., Cota, V., Blackman, E., Parsons, L.R., Gitai, Z., Murphy, C.T., 2021. The role of the Cer1 transposon in horizontal transfer of transgenerational memory. Cell 184, 4697-4712.e18

Moore, R.S., Kaletsky, R., Murphy, C.T., 2019. Piwi/PRG-1 argonaute and TGF-β mediate transgenerational learned pathogenic avoidance. Cell 177, 1827-1841.e12

Nargund, A.M., Fiorese, C.J., Pellegrino, M.W., Deng, P., Haynes, C.M., 2015. Mitochondrial and nuclear accumulation of the transcription factor ATFS-1 promotes OXPHOS recovery during the UPRmt. Mol. Cell 58, 123-133

Nargund, A.M., Pellegrino, M.W., Fiorese, C.J., Baker, B.M., Haynes, C.M., 2012. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 337, 587-590

Natt, D., Kugelberg, U., Casas, E., Nedstrand, E., Zalavary, S., Henriksson, P., Nijm, C., Jaderquist, J., Sandborg, J., Flinke, E., Ramesh, R., Orkenby, L., Appelkvist, F., Lingg, T., Guzzi, N., Bellodi, C., Lof, M., Vavouri, T., Ost, A., 2019. Human sperm displays rapid responses to diet. PLoS Biol. 17, 1109-1122

Nono, M., Kishimoto, S., Sato-Carlton, A., Carlton, P.M., Nishida, E., Uno, M., 2020. Intestine-to-Germline Transmission of Epigenetic Information Intergenerationally Ensures Systemic Stress Resistance in C. elegans. Cell Rep. 30, 3207-3217.e4

Norouzitallab, P., Baruah, K., Vandegehuchte, M., Stappen, G. Van, Catania, F., Bussche, J. Vanden, Vanhaecke, L., Sorgeloos, P., Bossier, P., 2014. Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model. FASEB J. 28, 3552-3563

Painter, R.C., Osmond, C., Gluckman, P., Hanson, M., Phillips, D.I.W., Roseboom, T.J., 2008. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG An Int. J. Obstet. Gynaecol. 115, 1243-1249

Perez, M.F., Francesconi, M., Hidalgo-Carcedo, C., Lehner, B., 2017. Maternal age generates phenotypic variation in Caenorhabditis elegans. Nature 552, 106-109

Perez, M.F., Lehner, B., 2019. Intergenerational and transgenerational epigenetic inheritance in animals. Nat. Cell Biol. 21, 143-151

Posner, R., Toker, I.A., Antonova, O., Star, E., Anava, S., Azmon, E., Hendricks, M., Bracha, S., Gingold, H., Rechavi, O., 2019. Neuronal small RNAs control behavior transgenerationally. Cell 177, 1814-1826.e15

Quadrana, L., Colot, V., 2016. Plant Transgenerational Epigenetics. Annu. Rev. Genet. 50, 467-491

Radford, E.J., Ito, M., Shi, H., Corish, J.A., Yamazawa, K., Isganaitis, E., Seisenberger, S., Hore, T.A., Reik, W., Erkek, S., Peters, A.H.F.M., Patti, M.E., Ferguson-Smith, A.C., 2014. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345, 6198

Rechavi, O., Houri-Ze'Evi, L., Anava, S., Goh, W.S.S., Kerk, S.Y., Hannon, G.J., Hobert, O., 2014. Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158, 277-287

Remy, J.J., 2010. Stable inheritance of an acquired behavior in Caenorhabditis elegans. Curr. Biol. 20, R877-R878

Robert A., W., Randy L., J., 2003. Transposable Elements:Targets for Early Nutritional Effects on Epigenetic Gene Regulation. Mol. Cell. Biol. 15, 5293-5300

Rodgers, A.B., Morgan, C.P., Bronson, S.L., Revello, S., Bale, T.L., 2013. Paternal stress exposure alters sperm MicroRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33, 9003-9012

Rodgers, A.B., Morgan, C.P., Leu, N.A., Bale, T.L., 2015. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl. Acad. Sci. U. S. A. 112, 13699-13704

Rompala, G.R., Simons, A., Kihle, B., Homanics, G.E., 2018. Paternal preconception chronic variable stress confers attenuated ethanol drinking behavior selectively to male offspring in a pre-stress environment dependent manner. Front. Behav. Neurosci. 12, 257

Sakano, H., 2020. Developmental regulation of olfactory circuit formation in mice. Dev. Growth Differ. 62, 199-213

Sarker, G., Sun, W., Rosenkranz, D., Pelczar, P., Opitz, L., Efthymiou, V., Wolfrum, C., Peleg-Raibstein, D., 2019. Maternal overnutrition programs hedonic and metabolic phenotypes across generations through sperm tsRNAs. Proc. Natl. Acad. Sci. U. S. A. 116, 10547-10556

Schuster, A., Skinner, M.K., Yan, W., 2016. Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs. Environ. Epigenetics 2, 787-790

Senaldi, L., Smith-Raska, M., 2020. Evidence for germline non-genetic inheritance of human phenotypes and diseases. Clin. Epigenet. 12, 136

Seong, K.H., Li, D., Shimizu, H., Nakamura, R., Ishii, S., 2011. Inheritance of stress-induced, ATF-2-dependent epigenetic change. Cell 145, 1049-1061

Shao, L.W., Niu, R., Liu, Y., 2016. Neuropeptide signals cell non-autonomous mitochondrial unfolded protein response. Cell Res. 26, 1182-1196

Sharma, U., 2019. Paternal contributions to offspring health:Role of sperm small rnas in intergenerational transmission of epigenetic information. Front. Cell Dev. Biol. 7, 215

Sharma, U., Conine, C.C., Shea, J.M., Boskovic, A., Derr, A.G., Bing, X.Y., Belleannee, C., Kucukural, A., Serra, R.W., Sun, F., Song, L., Carone, B.R., Ricci, E.P., Li, X.Z., Fauquier, L., Moore, M.J., Sullivan, R., Mello, C.C., Garber, M., Rando, O.J., 2016. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351, 391-396

Shi, J., Zhang, Yunfang, Tan, D., Zhang, X., Yan, M., Zhang, Ying, Franklin, R., Shahbazi, M., Mackinlay, K., Liu, S., Kuhle, B., James, E.R., Zhang, L., Qu, Y., Zhai, Q., Zhao, W., Zhao, L., Zhou, C., Gu, W., Murn, J., Guo, J., Carrell, D.T., Wang, Y., Chen, X., Cairns, B.R., Yang, X. lei, Schimmel, P., Zernicka-Goetz, M., Cheloufi, S., Zhang, Ying, Zhou, T., Chen, Q., 2021. PANDORA-seq expands the repertoire of regulatory small RNAs by overcoming RNA modifications. Nat. Cell Biol. 23, 424-436

Siklenka, K., Erkek, S., Godmann, M., Lambrot, R., McGraw, S., Lafleur, C., Cohen, T., Xia, J., Suderman, M., Hallett, M., Trasler, J., Peters, A.H.F.M., Kimmins, S., 2015. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350, aab2006

Skvortsova, K., Iovino, N., Bogdanovic, O., 2018. Functions and mechanisms of epigenetic inheritance in animals. Nat. Rev. Mol. Cell Biol. 19, 774-790

Stark, R., Grzelak, M., Hadfield, J., 2019. RNA sequencing:the teenage years. Nat. Rev. Genet. 20, 631-656

Tauffenberger, A., Parker, J.A., 2014. Heritable Transmission of Stress Resistance by High Dietary Glucose in Caenorhabditis elegans. PLoS Genet. 10, e1004346

Tetreau, G., Dhinaut, J., Gourbal, B., Moret, Y., 2019. Trans-generational immune priming in invertebrates:Current knowledge and future prospects. Front. Immunol. 10, 1938

Tian, Y., Garcia, G., Bian, Q., Steffen, K.K., Joe, L., Wolff, S., Meyer, B.J., Dillin, A., 2016. Mitochondrial stress induces chromatin reorganization to promote longevity and UPRmt. Cell 165, 1197-1208

Valtonen, T.M., Kangassalo, K., Polkki, M., Rantala, M.J., 2012. Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster. PLoS One 7, e31611

Wahba, L., Hansen, L., Fire, A.Z., 2021. An essential role for the piRNA pathway in regulating the ribosomal RNA pool in C. elegans. Dev. Cell 56, 2295-2312.e6

Wan, Q.L., Meng, X., Dai, W., Luo, Z., Wang, C., Fu, X., Yang, J., Ye, Q., Zhou, Q., 2021. N6-methyldeoxyadenine and histone methylation mediate transgenerational survival advantages induced by hormetic heat stress. Sci. Adv. 7, eabc3026

Webster, A.K., Jordan, J.M., Hibshman, J.D., Chitrakar, R., Ryan Baugh, L., 2018. Transgenerational effects of extended dauer diapause on starvation survival and gene expression plasticity in Caenorhabditis elegans. Genetics 210, 263-274

Willis, A.R., Zhao, W., Sukhdeo, R., Wadi, L., El Jarkass, H.T., Claycomb, J.M., Reinke, A.W., 2021. A parental transcriptional response to microsporidia infection induces inherited immunity in offspring. Sci. Adv. 7, eabf3114

Wu, L.L., Russell, D.L., Wong, S.L., Chen, M., Tsai, T.S., St John, J.C., Norman, R.J., Febbraio, M.A., Carroll, J., Robker, R.L., 2015. Mitochondrial dysfunction in oocytes of obese mothers:Transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Dev. 142, 681-691

Zhang, Y., Lu, H., Bargmann, C.I., 2005. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438, 179-184

Zhang, Q., Wang, Z., Zhang, W., Wen, Q., Li, X., Zhou, J., Wu, X., Guo, Y., Liu, Y., Wei, C., Qian, W., Tian, Y., 2021. The memory of neuronal mitochondrial stress is inherited transgenerationally via elevated mitochondrial DNA levels. Nat. Cell Biol. 23, 870-880

Zhang, Q., Wu, X., Chen, P., Liu, L., Xin, N., Tian, Y., Dillin, A., 2018. The mitochondrial unfolded protein response is mediated cell-non-autonomously by retromer-dependent Wnt signaling. Cell 174, 870-883.e17

Zhang, Y., Zhang, X., Shi, J., Tuorto, F., Li, X., Liu, Yusheng, Liebers, R., Zhang, L., Qu, Y., Qian, J., Pahima, M., Liu, Ying, Yan, M., Cao, Z., Lei, X., Cao, Y., Peng, H., Liu, S., Wang, Y., Zheng, H., Woolsey, R., Quilici, D., Zhai, Q., Li, L., Zhou, T., Yan, W., Lyko, F., Zhang, Ying, Zhou, Q., Duan, E., Chen, Q., 2018. Dnmt2 mediates intergenerational transmission of paternally acquired metabolic disorders through sperm small non-coding RNAs. Nat. Cell Biol. 20, 535-540

Zhao, T., Zhan, Z., Jiang, D., 2019. Histone modifications and their regulatory roles in plant development and environmental memory. J. Genet. Genomics 46, 467-476

Zhu, D., Wu, X., Zhou, J., Li, X., Huang, X., Li, J., Wu, J., Bian, Q., Wang, Y., Tian, Y., 2020. NuRD mediates mitochondrial stress-induced longevity via chromatin remodeling in response to acetyl-CoA level. Sci. Adv. 6, eabb2529

Zu, W., Zhang, H., Lan, X., Tan, X., 2020. Genome-wide evolution analysis reveals low CpG contents of fast-evolving genes and identifies antiviral microRNAs. J. Genet. Genomics 47, 49-60

Relative Articles

Supplements(0)

Cited By

Proportional views