Herbicide resistance in grass weeds: Epigenetic regulation matters too

. 2022 ; 13 () : 1040958. [epub] 20221110

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid36438151

Although herbicides have been successfully used for controlling weeds, their continuous use has developed in the evolution of resistance to all major herbicide modes of action worldwide. Reports suggest that the members of Poaceae family are more prone to developing herbicide resistance than other families. In plants, epigenetic mechanisms play critical roles by increasing their stress-adaptive potential in a rapidly changing environment. Epigenetic mechanisms involve alteration of the expression of genetic elements, but without any changes in the DNA sequence. Although the possible roles of epigenetic mechanisms in contributing to survival and fitness under various stresses are well documented in model plants and crops, their contribution to herbicide resistance in weeds is still in its infancy. A few studies with herbicides have shown differential expression of DNA methyltransferases, histone methyltransferases and DNA demethylases in response to the herbicides; however, no further studies were conducted. In the case of herbicide stress, exploring how these epigenetic processes affect the gene expression pattern in individual plants subjected to recurrent selection would be exciting. Hence, our mini-review will focus on the potential contributions of epigenetic mechanisms to the adaptive responses of grass-weedy species to herbicide stress. A better understanding of these epigenetic changes will add novel perceptions to our knowledge of herbicide resistance evolution in weeds enabling the development of herbicides with novel targets.

Zobrazit více v PubMed

Akhter Z., Bi Z., Ali K., Sun C., Fiaz S., Haider F. U., et al. . (2021. 1096). In response to abiotic stress, DNA methylation confers EpiGenetic changes in plants. Plants 10. doi: 10.3390/plants10061096 PubMed DOI PMC

Arıkan B., Özden S., Turgut-Kara N. (2018). DNA Methylation related gene expression and morphophysiological response to abiotic stresses in Arabidopsis thaliana . Environ. Exp. Bot. 149, 17–26. doi: 10.1016/j.envexpbot.2018.01.011 DOI

Arzate-Mejía R. G., Valle-García D., Recillas-Targa F. (2011). Signaling epigenetics: Novel insights on cell signaling and epigenetic regulation. IUBMB Life 63, 881–895. doi: 10.1002/iub.557 PubMed DOI

Ashapkin V. V., Kutueva L. I., Aleksandrushkina N. I., Vanyushin B. F. (2020. 7457). Epigenetic mechanisms of plant adaptation to biotic and abiotic stresses. Int. J. Mol. Sci. 21. doi: 10.3390/ijms21207457 PubMed DOI PMC

Aufsatz W., Stoiber T., Rakic B., Naumann K. (2007). Arabidopsis histone deacetylase 6: a green link to R.N.A. silencing. Oncogene 26, 5477–5488. doi: 10.1038/sj.onc.1210615 PubMed DOI

Baba S. A., Jain D., Ashraf N. (2019). “Role of chromatin assembly and remodeling in water stress responses in plants,” in Genetic enhancement of crops for tolerance to abiotic stress: Mechanisms and approaches, vol. I. Eds. Rajpal V. R., Sehgal D., Kumar A., Raina S. N. (Cham: Springer International Publishing; ), 167–182. doi: 10.1007/978-3-319-91956-0_7 DOI

Baba A., Ohtake F., Okuno Y., Yokota K., Okada M., Imai Y., et al. . (2011). PKA-dependent regulation of the histone lysine demethylase complex PHF2–ARID5B. Nat. Cell Biol. 13, 668–675. doi: 10.1038/ncb2228 PubMed DOI

Berndsen C. E., Denu J. M. (2008). Catalysis and substrate selection by histone/protein lysine acetyltransferases. Curr. Opin. Struct. Biol. 18, 682–689. doi: 10.1016/j.sbi.2008.11.004 PubMed DOI PMC

Bhar A., Chakraborty A., Roy A. (2022). Plant responses to biotic stress: Old memories matter. Plants 11, 84. doi: 10.3390/plants11010084 PubMed DOI PMC

Chauhan B. S. (2020). Grand challenges in weed management. Front. Agron. 1. doi: 10.3389/fagro.2019.00003 DOI

Cheung P., Tanner K. G., Cheung W. L., Sassone-Corsi P., Denu J. M., Allis C. D. (2000). Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5, 905–915. doi: 10.1016/S1097-2765(00)80256-7 PubMed DOI

Chinnusamy V., Zhu J. K. (2009). Epigenetic regulation of stress responses in plants. current. Opin. Plant Biol. 12, 133–139. doi: 10.1016/j.pbi.2008.12.006 PubMed DOI PMC

Cokus S. J., Feng S., Zhang X., Chen Z., Merriman B., Haudenschild C. D., et al. . (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219. doi: 10.1038/nature06745 PubMed DOI PMC

Délye C. (2013). Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: A major challenge for weed science in the forthcoming decade. Pest Manage. Sci. 69, 176–187. doi: 10.1002/ps.3318 PubMed DOI

Délye C., Duhoux A., Pernin F., Riggins C. W., Tranel P. J. (2015). Molecular mechanisms of herbicide resistance. Weed Sci. 63, 91–115. doi: 10.1614/WS-D-13-00096.1 DOI

De Melo B. P., Lourenço-Tessutti I. T., Paixão J. F. R., Noriega D. D., Silva M. C. M., de Almeida-Engler J., et al. . (2020). Transcriptional modulation of AREB-1 by CRISPRa improves plant physiological performance under severe water deficit. Sci. Rep. 10, 16231. doi: 10.1038/s41598-020-72464-y PubMed DOI PMC

De Santa F., Totaro M. G., Prosperini E., Notarbartolo S., Testa G., Natoli G. (2007). The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130, 1083–1094. doi: 10.1016/j.cell.2007.08.019 PubMed DOI

Gaines T. A., Duke S. O., Morran S., Rigon C. A. G., Tranel P. J., Küpper A., et al. . (2020) 295(20):10307–30. Mechanisms of evolved herbicide resistance. J. Biol. Chem. doi: 10.1074/jbc.REV120.013572 PubMed DOI PMC

Ghanizadeh H., Harrington K. C. (2017). Non-target site mechanisms of resistance to herbicides. Crit. Rev. Plant Sci. 36, 24–34. doi: 10.1080/07352689.2017.1316134 DOI

Grob S. (2022). “Tough tissue Hi-c,” in Spatial genome organization: Methods and protocols methods in molecular biology. Ed. Sexton T. (New York, NY: Springer US; ), 35–50. doi: 10.1007/978-1-0716-2497-5_3 PubMed DOI

Grunau C., Clark S. J., Rosenthal A. (2001). Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res. 29, e65. doi: 10.1093/nar/29.13.e65 PubMed DOI PMC

Gupta D., Bhattacharjee O., Mandal D., Sen M. K., Dey D., Dasgupta A., et al. . (2019). CRISPR-Cas9 system: A new-fangled dawn in gene editing. Life Sci. 232, 116636. doi: 10.1016/j.lfs.2019.116636 PubMed DOI

Halabian R., Arshad V., Ahmadi A., Saeedi P., Azimzadeh Jamalkandi S., Alivand M. R. (2021). Laboratory methods to decipher epigenetic signatures: a comparative review. Cell Mol. Biol. Lett. 26, 46. doi: 10.1186/s11658-021-00290-9 PubMed DOI PMC

Jacinto F. V., Ballestar E., Esteller M. (2008). Methyl-DNA immunoprecipitation (MeDIP): Hunting down the DNA methylome. BioTechniques 44, 35–43. doi: 10.2144/000112708 PubMed DOI

Jogam P., Sandhya D., Alok A., Peddaboina V., Allini V. R., Zhang B. (2022). A review on CRISPR/Cas-based epigenetic regulation in plants. Int. J. Biol. Macromolecules 219, 1261–1271. doi: 10.1016/j.ijbiomac.2022.08.182 PubMed DOI

Kim G., Clarke C. R., Larose H., Tran H. T., Haak D. C., Zhang L., et al. . (2017). Herbicide injury induces DNA methylome alterations in arabidopsis. PeerJ 5, e3560. doi: 10.7717/peerj.3560 PubMed DOI PMC

Kinoshita T., Seki M. (2014). Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 55, 1859–1863. doi: 10.1093/pcp/pcu125 PubMed DOI

Kong S., Zhang Y. (2019). Deciphering Hi-c: from 3D genome to function. Cell Biol. Toxicol. 35, 15–32. doi: 10.1007/s10565-018-09456-2 PubMed DOI

Kreiner J. M., Stinchcombe J. R., Wright S. I. (2018). Population genomics of herbicide resistance: Adaptation via evolutionary rescue. Annu. Rev. Plant Biol. 69, 611–635. doi: 10.1146/annurev-arplant-042817-040038 PubMed DOI

Krueger F., Kreck B., Franke A., Andrews S. R. (2012). DNA Methylome analysis using short bisulfite sequencing data. Nat. Methods 9, 145–151. doi: 10.1038/nmeth.1828 PubMed DOI

Lee J. S., Smith E., Shilatifard A. (2010). The language of histone crosstalk. Cell 142, 682–685. doi: 10.1016/j.cell.2010.08.011 PubMed DOI PMC

Li Z., Li D., Li Y., Guo X., Yang R. (2022). Deciphering the regulatory code of histone modifications in plants. J. Genet. Genomics. doi: 10.1016/j.jgg.2022.07.003 PubMed DOI

Lo W. S., Trievel R. C., Rojas J. R., Duggan L., Hsu J. Y., Allis C. D., et al. . (2000). Phosphorylation of serine 10 in histone H3 is functionally linked In vitro and In vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5, 917–926. doi: 10.1016/S1097-2765(00)80257-9 PubMed DOI

Lu Y. C., Feng S. J., Zhang J. J., Luo F., Zhang S., Yang H. (2016). Genome-wide identification of DNA methylation provides insights into the association of gene expression in rice exposed to pesticide atrazine. Sci. Rep. 6, 18985. doi: 10.1038/srep18985 PubMed DOI PMC

Margaritopoulou T., Tani E., Chachalis D., Travlos I. (2018). Involvement of epigenetic mechanisms in herbicide resistance: The case of Conyza canadensis . Agriculture 8, 17. doi: 10.3390/agriculture8010017 DOI

Markus C., Pecinka A., Karan R., Barney J. N., Merotto A. (2018). Epigenetic regulation – contribution to herbicide resistance in weeds? Pest Manage. Sci. 74, 275–281. doi: 10.1002/ps.4727 PubMed DOI

Markus C., Pecinka A., Merotto A. (2021. 3314). Insights into the role of transcriptional gene silencing in response to herbicide-treatments in Arabidopsis thaliana . Int. J. Mol. Sci. 22. doi: 10.3390/ijms22073314 PubMed DOI PMC

Mohn F., Weber M., Schübeler D., Roloff T. C. (2009). “Methylated DNA immunoprecipitation (MeDIP),” in DNA Methylation: Methods and protocols methods in molecular biology. Ed. Tost J. (Totowa, NJ: Humana Press; ), 55–64. doi: 10.1007/978-1-59745-522-0_5 PubMed DOI

Molina-Serrano D., Schiza V., Kirmizis A. (2013). Cross-talk among epigenetic modifications: lessons from histone arginine methylation. Biochem. Soc. Trans. 41, 751–759. doi: 10.1042/BST20130003 PubMed DOI

Molinier J., Ries G., Zipfel C., Hohn B. (2006). Transgeneration memory of stress in plants. Nature 442, 1046–1049. doi: 10.1038/nature05022 PubMed DOI

Mozgova I., Mikulski P., Pecinka A., Farrona S. (2019). “Epigenetic mechanisms of abiotic stress response and memory in plants,” in Epigenetics in plants of agronomic importance: Fundamentals and applications. Eds. Alvarez-Venegas R., De-la-Peña C., Casas-Mollano J. A. (Cham: Springer International Publishing; ), 1–64. doi: 10.1007/978-3-030-14760-0_1 DOI

Munshi A., Ahuja Y. R., Bahadur B. (2015). “Epigenetic mechanisms in plants: An overview,” in Plant biology and biotechnology: Volume II: Plant genomics and biotechnology. Eds. Bahadur B., Rajam M.V., Sahijram L., Krishnamurthy K. V. (New Delhi: Springer India; ), 265–278. doi: 10.1007/978-81-322-2283-5_12 DOI

Murfett J., Wang X.-J., Hagen G., Guilfoyle T. J. (2001). Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13, 1047–1061. doi: 10.1105/tpc.13.5.1047 PubMed DOI PMC

Nardemir G., Agar G., Arslan E., Aygun Erturk F. (2015). Determination of genetic and epigenetic effects of glyphosate on Triticum aestivum with RAPD and CRED-RA techniques. Theor. Exp. Plant Physiol. 27, 131–139. doi: 10.1007/s40626-015-0039-1 DOI

Ni P., Huang N., Nie F., Zhang J., Zhang Z., Wu B., et al. . (2021. 5976). Genome-wide detection of cytosine methylations in plant from nanopore data using deep learning. Nat. Commun. 12. doi: 10.1038/s41467-021-26278-9 PubMed DOI PMC

Pan L., Guo Q., Wang J., Shi L., Yang X., Zhou Y., et al. . (2022). CYP81A68 confers metabolic resistance to A.L.S. and ACCase-inhibiting herbicides and its epigenetic regulation in Echinochloa crus-galli . J. Hazardous Materials 428, 128225. doi: 10.1016/j.jhazmat.2022.128225 PubMed DOI

Park P. J. (2009). ChIP–seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10, 669–680. doi: 10.1038/nrg2641 PubMed DOI PMC

Pellegrini M., Ferrari R. (2012). “Epigenetic analysis: ChIP-chip and ChIP-seq,” in Next generation microarray bioinformatics: Methods and protocols methods in molecular biology. Eds. Wang J., Tan A. C., Tian T. (Totowa, NJ: Humana Press; ), 377–387. doi: 10.1007/978-1-61779-400-1_25 PubMed DOI

Powles S. B., Yu Q. (2010). Evolution in action: Plants resistant to herbicides. Annu. Rev. Plant Biol. 61, 317–347. doi: 10.1146/annurev-arplant-042809-112119 PubMed DOI

Radwan D. E. M. (2012). Salicylic acid induced alleviation of oxidative stress caused by clethodim in maize (Zea mays l.) leaves. Pesticide Biochem. Physiol. 102, 182–188. doi: 10.1016/j.pestbp.2012.01.002 DOI

Sahu P. P., Pandey G., Sharma N., Puranik S., Muthamilarasan M., Prasad M. (2013). Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep. 32, 1151–1159. doi: 10.1007/s00299-013-1462-x PubMed DOI

Schatz M. C. (2017). Nanopore sequencing meets epigenetics. Nat. Methods 14, 347–348. doi: 10.1038/nmeth.4240 PubMed DOI

Sen M. K., Hamouzová K., Mikulka J., Bharati R., Košnarová P., Hamouz P., et al. . (2021). Enhanced metabolism and target gene overexpression confer resistance against acetolactate synthase-inhibiting herbicides in Bromus sterilis . Pest Manage. Sci. 77, 2122–2128. doi: 10.1002/ps.6241 PubMed DOI

Shin H., Choi W. L., Lim J. Y., Huh J. H. (2022). Epigenome editing: targeted manipulation of epigenetic modifications in plants. Genes Genom 44, 307–315. doi: 10.1007/s13258-021-01199-5 PubMed DOI

Sulewska A., Niklinska W., Kozlowski M., Minarowski L., Naumnik W., Niklinski J., et al. . (2007). Detection of DNA methylation in eucaryotic cells. Folia Histochemica Cytobiologica 45, 315–324. Available at: https://journals.viamedica.pl/folia_histochemica_cytobiologica/article/view/4502. PubMed

Sun L., Jing Y., Liu X., Li Q., Xue Z., Cheng Z., et al. . (2020. 1886). Heat stress-induced transposon activation correlates with 3D chromatin organization rearrangement in Arabidopsis . Nat. Commun. 11(1), 1–13. doi: 10.1038/s41467-020-15809-5 PubMed DOI PMC

Tanić M. (2020). “Epigenome-wide association study (EWAS): Methods and applications,” in Epigenetics methods (Elsevier; ), 591–613. doi: 10.1016/B978-0-12-819414-0.00029-X DOI

Wang J., Wang C., Long Y., Hopkins C., Kurup S., Liu K., et al. . (2011). Universal endogenous gene controls for bisulphite conversion in analysis of plant DNA methylation. Plant Methods 7, 39. doi: 10.1186/1746-4811-7-39 PubMed DOI PMC

Yaish M. W., Colasanti J., Rothstein S. J. (2011). The role of epigenetic processes in controlling flowering time in plants exposed to stress. J. Exp. Bot. 62, 3727–3735. doi: 10.1093/jxb/err177 PubMed DOI

Yu Q., Ahmad-Hamdani M. S., Han H., Christoffers M. J., Powles S. B. (2013). Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity 110, 220–231. doi: 10.1038/hdy.2012.69 PubMed DOI PMC

Yuan L., Lui X., Luo M., Yang S., Wu K. (2013). Involvement of histone modifications in plant abiotic stress responses. Journal of Integrative Plant BiologyJournal of Integrative Plant Biology 55(10): 892–901. doi: 10.1111/jipb.12060 PubMed DOI

Zhang H., Lang Z., Zhu J. K. (2018). Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489–506. doi: 10.1038/s41580-018-0016-z PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...