Epigenetic Modifications, Immune Control Processes, and Plant Responses to Nematodes
Abstract
:1. Introduction
2. Plant–Nematode Interaction
2.1. Environmental Factors in the Plant–Nematode Interaction
2.2. Transcription Factors in the Plant–Nematode Interaction
2.3. Epigenetics in Plant–Nematode Interaction
2.3.1. DNA Methylation
2.3.2. Non-Coding RNAs
2.3.3. Histone Modifications
2.4. Emerging Technologies in the Plant–Nematode Interaction
2.5. Endophytic Micro-Organisms in the Plant–Nematode Interaction
2.6. Plant Memory in the Plant–Nematode Interaction
3. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
ncRNAs | Non-coding RNAs |
SAR | Systemic acquired resistance |
RKNs | Root-knot nematodes |
PPNs | Plant parasitic nematodes |
GCs | Giant cells |
smRNAs | Small RNA |
dsRNA | Double-stranded RNA |
miRNAs | Micro RNAs |
Met1 | Methyl transferase 1 |
CMT3 | Chromomethylase 3 |
RdDM | RNA-directed DNA methylation |
PTI | Pattern-triggered immunity |
ETI | Effector-triggered immunity |
PAMP | Pathogen-associated molecular pattern |
DAMP | Damage-associated molecular pattern |
DRM | Domains rearranged methyltransferase |
ROS1 | Repressor of silencing 1 |
AGO | Argonaute |
lncRNAs | Long non-coding RNAs |
RISC | RNA-induced silencing complex |
UTR | Untranslated region |
JA | Jasmonic acid |
TCP4 | Teosinte branched1/cycloidea/proliferating cell factor |
ARF | Auxin response factors |
ATX | Arabidopsis trithorax |
5mC | 5-methylcytosine |
ChIP | Chromatin immunoprecipitation sequencing |
References
- Banihashemian, S.N.; Jamali, S.; Golmohammadi, M.; Ghasemnejad, M. Specific identification of root-knot nematode Meloidogyne incognita common in kiwifruit orchards of Guilan and Mazandaran provinces using sec-1 gene sequence. J. Appl. Res. Plant Prot. 2023, 11, 63–72. [Google Scholar] [CrossRef]
- Chavan, S.N.; Degroote, E.; De Kock, K.; Demeestere, K.; Kyndt, T. ARGONAUTE4 and the DNA demethylase REPRESSOR OF SILENCING 1C mediate dehydroascorbate-induced intergenerational nematode resistance in rice. Plant Physiol. 2025, 197, kiae598. [Google Scholar] [CrossRef]
- Donelson, J.M.; Salinas, S.; Munday, P.L.; Shama, L.N.S. Transgenerational plasticity and climate change experiments: Where do we go from here? Glob. Chang. Biol. 2018, 24, 13–34. [Google Scholar] [CrossRef]
- Chen, C.; Wang, M.; Zhu, J.; Tang, Y.; Zhang, H.; Zhao, Q.; Jing, M.; Chen, Y.; Xu, X.; Jiang, J. Long-term effect of epigenetic modification in plant–microbe interactions: Modification of DNA methylation induced by plant growth-promoting bacteria mediates promotion process. Microbiome 2022, 10, 36. [Google Scholar] [CrossRef]
- Siddique, S.; Coomer, A.; Baum, T.; Williamson, V.M. Recognition and response in plant–nematode interactions. Annu. Rev. Phytopathol. 2022, 60, 143–162. [Google Scholar] [CrossRef]
- Mendy, B.; Wang’ombe, M.W.; Radakovic, Z.S.; Holbein, J.; Ilyas, M.; Chopra, D.; Holton, N.; Zipfel, C.; Grundler, F.M.W.; Siddique, S. Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. PLoS Pathog. 2017, 13, e1006284. [Google Scholar] [CrossRef]
- Zipfel, C. Plant pattern-recognition receptors. Trends Immunol. 2014, 35, 345–351. [Google Scholar] [CrossRef]
- Goode, K.; Mitchum, M.G. Pattern-triggered immunity against root-knot nematode infection: A minireview. Physiol. Plant. 2022, 174, e13680. [Google Scholar] [CrossRef]
- Banihashemian, S.N.; Jamali, S.; Golmohammadi, M.; Ghasemnezhad, M. Management of root-knot nematode in kiwifruit using resistance-inducing Bacillus altitudinis. Trop. Plant Pathol. 2023, 48, 443–451. [Google Scholar] [CrossRef]
- Rani, P.; Singh, M.; Prashad, H.; Sharma, M. Evaluation of bacterial formulations as potential biocontrol agents against the southern root-knot nematode, Meloidogyne incognita. Egypt. J. Biol. Pest. Control 2022, 32, 29. [Google Scholar] [CrossRef]
- Pratx, L.; Rancurel, C.; Da Rocha, M.; Danchin, E.G.J.; Castagnone-Sereno, P.; Abad, P.; Perfus-Barbeoch, L. Genome-wide expert annotation of the epigenetic machinery of the plant-parasitic nematodes Meloidogyne spp., with a focus on the asexually reproducing species. BMC Genom. 2018, 19, 321. [Google Scholar] [CrossRef]
- Silva, A.C.; Ruiz-Ferrer, V.; Müller, S.Y.; Pellegrin, C.; Abril-Urías, P.; Martínez-Gómez, Á.; Gómez-Rojas, A.; Berenguer, E.; Testillano, P.S.; Andrés, M.F. The DNA methylation landscape of the root-knot nematode-induced pseudo-organ, the gall, in Arabidopsis, is dynamic, contrasting over time, and critically important for successful parasitism. New Phytol. 2022, 236, 1888–1907. [Google Scholar] [CrossRef]
- Ali, M.A.; Anjam, M.S.; Nawaz, M.A.; Lam, H.-M.; Chung, G. Signal transduction in plant–nematode interactions. Int. J. Mol. Sci. 2018, 19, 1648. [Google Scholar] [CrossRef]
- Morao, A.K.; Bouyer, D.; Roudier, F. Emerging concepts in chromatin-level regulation of plant cell differentiation: Timing, counting, sensing and maintaining. Curr. Opin. Plant Biol. 2016, 34, 27–34. [Google Scholar] [CrossRef]
- Zhou, J.; Xu, X.-C.; Cao, J.-J.; Yin, L.-L.; Xia, X.-J.; Shi, K.; Zhou, Y.-H.; Yu, J.-Q. Heat shock factor HsfA1a is essential for R gene-mediated nematode resistance and triggers H2O2 production. Plant Physiol. 2018, 176, 2456–2471. [Google Scholar] [CrossRef]
- Khan, M.; Khan, A.U. Plant parasitic nematodes effectors and their crosstalk with defense response of host plants: A battle underground. Rhizosphere 2021, 17, 100288. [Google Scholar] [CrossRef]
- Jones, J.D.G.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef]
- Fiorilli, V.; Catoni, M.; Lanfranco, L.; Zabet, N.R. Interactions of plants with bacteria and fungi: Molecular and epigenetic plasticity of the host. Front. Plant Sci. 2020, 11, 274. [Google Scholar] [CrossRef]
- Mirmajlessi, S.M.; Mostafavi, H.A. Application of Radiation and Genetic Engineering Techniques to Improve Biocontrol Agent. In Use of Gamma Radiation Techniques in Peaceful Applications; IntechOpen: London, UK, 2019; p. 129. [Google Scholar]
- Asgari, S. Epigenetic modifications underlying symbiont–host interactions. Adv. Genet. 2014, 86, 253–276. [Google Scholar]
- Bardgett, R.D.; Van Der Putten, W.H. Belowground biodiversity and ecosystem functioning. Nature 2014, 515, 505–511. [Google Scholar] [CrossRef]
- Li, Z.; Chen, X.; Li, J.; Liao, X.; Li, D.; He, X.; Zhang, W.; Zhao, J. Relationships between soil nematode communities and soil quality as affected by land-use type. Forests 2022, 13, 1658. [Google Scholar] [CrossRef]
- Barrios, E.; Delve, R.J.; Bekunda, M.; Mowo, J.; Agunda, J.; Ramisch, J.; Trejo, M.T.; Thomas, R.J. Indicators of soil quality: A South–South development of a methodological guide for linking local and technical knowledge. Geoderma 2006, 135, 248–259. [Google Scholar]
- Berkelmans, R.; Ferris, H.; Tenuta, M.; Van Bruggen, A.H.C. Effects of long-term crop management on nematode trophic levels other than plant feeders disappear after 1 year of disruptive soil management. Appl. Soil. Ecol. 2003, 23, 223–235. [Google Scholar]
- Quist, C.W.; Schrama, M.; de Haan, J.J.; Smant, G.; Bakker, J.; van der Putten, W.H.; Helder, J. Organic farming practices result in compositional shifts in nematode communities that exceed crop-related changes. Appl. Soil. Ecol. 2016, 98, 254–260. [Google Scholar] [CrossRef]
- Dutta, T.K.; Phani, V. The pervasive impact of global climate change on plant-nematode interaction continuum. Front. Plant Sci. 2023, 14, 1143889. [Google Scholar]
- Arraes, F.B.; Vasquez, D.D.; Tahir, M.; Pinheiro, D.H.; Faheem, M.; Freitas-Alves, N.S.; Moreira-Pinto, C.E.; Moreira, V.J.; Paes-de-Melo, B.; Lisei-de-Sa, M.E.; et al. Integrated omic approaches reveal molecular mechanisms of tolerance during soybean and Meloidogyne incognita interactions. Plants 2022, 11, 2744. [Google Scholar] [CrossRef]
- Petitot, A.-S.; Kyndt, T.; Haidar, R.; Dereeper, A.; Collin, M.; de Almeida Engler, J.; Gheysen, G.; Fernandez, D. Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots. Ann. Bot. 2017, 119, 885–899. [Google Scholar]
- Ali, M.A.; Abbas, A.; Kreil, D.P.; Bohlmann, H. Overexpression of the transcription factor RAP2. 6 leads to enhanced callose deposition in syncytia and enhanced resistance against the beet cyst nematode Heterodera schachtii in Arabidopsis roots. BMC Plant Biol. 2013, 13, 47. [Google Scholar]
- Zhang, M.; Zhang, H.; Tan, J.; Huang, S.; Chen, X.; Jiang, D.; Xiao, X. Transcriptome analysis of eggplant root in response to root-knot nematode infection. Pathogens 2021, 10, 470. [Google Scholar] [CrossRef]
- Xu, X.; Fang, P.; Zhang, H.; Chi, C.; Song, L.; Xia, X.; Shi, K.; Zhou, Y.; Zhou, J.; Yu, J. Strigolactones positively regulate defense against root-knot nematodes in tomato. J. Exp. Bot. 2019, 70, 1325–1337. [Google Scholar]
- Huang, H.; Zhao, W.; Qiao, H.; Li, C.; Sun, L.; Yang, R.; Ma, X.; Ma, J.; Song, S.; Wang, S. SlWRKY45 interacts with jasmonate-ZIM domain proteins to negatively regulate defense against the root-knot nematode Meloidogyne incognita in tomato. Hortic. Res. 2022, 9, uhac197. [Google Scholar] [PubMed]
- Ribeiro, C.; de Melo, B.P.; Lourenço-Tessutti, I.T.; Ballesteros, H.F.; Ribeiro, K.V.G.; Menuet, K.; Heyman, J.; Hemerly, A.; de Sá, M.F.G.; De Veylder, L. The regeneration conferring transcription factor complex ERF115-PAT1 coordinates a wound-induced response in root-knot nematode induced galls. New Phytol. 2024, 241, 878–895. [Google Scholar]
- Suzuki, R.; Yamada, M.; Higaki, T.; Aida, M.; Kubo, M.; Tsai, A.Y.-L.; Sawa, S. PUCHI regulates giant cell morphology during root-knot nematode infection in Arabidopsis thaliana. Front. Plant Sci. 2021, 12, 755610. [Google Scholar]
- Kumar, A.; Sichov, N.; Bucki, P.; Miyara, S.B. SlWRKY16 and SlWRKY31 of tomato, negative regulators of plant defense, involved in susceptibility activation following root-knot nematode Meloidogyne javanica infection. Sci. Rep. 2023, 13, 14592. [Google Scholar]
- Nie, W.; Liu, L.; Chen, Y.; Luo, M.; Feng, C.; Wang, C.; Yang, Z.; Du, C. Identification of the regulatory role of SlWRKYs in tomato defense against Meloidogyne incognita. Plants 2023, 12, 2416. [Google Scholar] [CrossRef]
- Chinnapandi, B.; Bucki, P.; Fitoussi, N.; Kolomiets, M.; Borrego, E.; Braun Miyara, S. Tomato SlWRKY3 acts as a positive regulator for resistance against the root-knot nematode Meloidogyne javanica by activating lipids and hormone-mediated defense-signaling pathways. Plant Signal. Behav. 2019, 14, 1601951. [Google Scholar]
- Meresa, B.K.; Matthys, J.; Kyndt, T. Biochemical Defence of Plants against Parasitic Nematodes. Plants 2024, 13, 2813. [Google Scholar] [CrossRef]
- Miah, M.; Mezei, M.; Mujtaba, S. Epigenetic Mechanisms in Bacteria Bridge Physiology, Growth and Host–Pathogen Interactions. In Handbook of Epigenetics; Elsevier: Amsterdam, The Netherlands, 2023; pp. 201–213. [Google Scholar]
- Escobar, C.; Brown, S.; Mitchum, M.G. Transcriptomic and proteomic analysis of the plant response to nematode infection. In Genomics and Molecular Genetics of Plant-Nematode Interactions; Springer: Dordrecht, The Netherlands, 2011; pp. 157–173. [Google Scholar]
- Gómez-Díaz, E.; Jorda, M.; Peinado, M.A.; Rivero, A. Epigenetics of host–pathogen interactions: The road ahead and the road behind. PLoS Pathog. 2012, 8, e1003007. [Google Scholar]
- Kaushal, R.; Peng, L.; Singh, S.K.; Zhang, M.; Zhang, X.; Vílchez, J.I.; Wang, Z.; He, D.; Yang, Y.; Lv, S. Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation. Microbiome 2021, 9, 57. [Google Scholar] [CrossRef]
- Vílchez, J.I.; Varotto, S.; Jung, H.W. Epigenetic regulation behind plant-microbe interactions. Front. Plant Sci. 2024, 15, 1385356. [Google Scholar]
- Ramirez-Prado, J.S.; Abulfaraj, A.A.; Rayapuram, N.; Benhamed, M.; Hirt, H. Plant immunity: From signaling to epigenetic control of defense. Trends Plant Sci. 2018, 23, 833–844. [Google Scholar] [CrossRef] [PubMed]
- Jaubert-Possamai, S.; Noureddine, Y.; Favery, B. MicroRNAs, new players in the plant–nematode interaction. Front. Plant Sci. 2019, 10, 1180. [Google Scholar] [CrossRef]
- Hassanaly-Goulamhoussen, R.; de Carvalho Augusto, R.; Marteu-Garello, N.; Péré, A.; Favery, B.; Da Rocha, M.; Danchin, E.G.J.; Abad, P.; Grunau, C.; Perfus-Barbeoch, L. Chromatin landscape dynamics in the early development of the plant parasitic nematode Meloidogyne incognita. Front. Cell Dev. Biol. 2021, 9, 765690. [Google Scholar] [CrossRef] [PubMed]
- Bennett, M.; Hawk, T.E.; Lopes-Caitar, V.S.; Adams, N.; Rice, J.H.; Hewezi, T. Establishment and maintenance of DNA methylation in nematode feeding sites. Front. Plant Sci. 2023, 13, 1111623. [Google Scholar] [CrossRef]
- Hewezi, T. Epigenetic mechanisms in nematode–plant interactions. Annu. Rev. Phytopathol. 2020, 58, 119–138. [Google Scholar] [CrossRef]
- Law, J.A.; Jacobsen, S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11, 204–220. [Google Scholar] [CrossRef]
- Matzke, M.A.; Mosher, R.A. RNA-directed DNA methylation: An epigenetic pathway of increasing complexity. Nat. Rev. Genet. 2014, 15, 394–408. [Google Scholar] [CrossRef]
- Pavet, V.; Quintero, C.; Cecchini, N.M.; Rosa, A.L.; Alvarez, M.E. Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae. Mol. Plant-Microbe Interact. 2006, 19, 577–587. [Google Scholar] [PubMed]
- Rambani, A.; Rice, J.H.; Liu, J.; Lane, T.; Ranjan, P.; Mazarei, M.; Pantalone, V.; Stewart, C.N., Jr.; Staton, M.; Hewezi, T. The methylome of soybean roots during the compatible interaction with the soybean cyst nematode. Plant Physiol. 2015, 168, 1364–1377. [Google Scholar] [CrossRef]
- Ruiz-Ferrer, V.; Cabrera, J.; Martinez-Argudo, I.; Artaza, H.; Fenoll, C.; Escobar, C. Silenced retrotransposons are major rasiRNAs targets in Arabidopsis galls induced by Meloidogyne javanica. Mol. Plant Pathol. 2018, 19, 2431–2445. [Google Scholar] [CrossRef]
- Hewezi, T.; Pantalone, V.; Bennett, M.; Neal Stewart, C.; Burch-Smith, T.M. Phytopathogen-induced changes to plant methylomes. Plant Cell Rep. 2018, 37, 17–23. [Google Scholar] [CrossRef] [PubMed]
- Hewezi, T.; Lane, T.; Piya, S.; Rambani, A.; Rice, J.H.; Staton, M. Cyst nematode parasitism induces dynamic changes in the root epigenome. Plant Physiol. 2017, 174, 405–420. [Google Scholar] [CrossRef] [PubMed]
- López Sánchez, A.; Stassen, J.H.M.; Furci, L.; Smith, L.M.; Ton, J. The role of DNA (de) methylation in immune responsiveness of Arabidopsis. Plant J. 2016, 88, 361–374. [Google Scholar] [PubMed]
- Leonetti, P.; Molinari, S. Epigenetic and metabolic changes in root-knot nematode-plant interactions. Int. J. Mol. Sci. 2020, 21, 7759. [Google Scholar] [CrossRef]
- Ji, H.; Gheysen, G.; Denil, S.; Lindsey, K.; Topping, J.F.; Nahar, K.; Haegeman, A.; De Vos, W.H.; Trooskens, G.; Van Criekinge, W. Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots. J. Exp. Bot. 2013, 64, 3885–3898. [Google Scholar]
- Borges, F.; Martienssen, R.A. The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 2015, 16, 727–741. [Google Scholar] [CrossRef]
- Huang, L.; Dong, H.; Zhou, D.; Li, M.; Liu, Y.; Zhang, F.; Feng, Y.; Yu, D.; Lin, S.; Cao, J. Systematic identification of long non-coding RNA s during pollen development and fertilization in Brassica rapa. Plant J. 2018, 96, 203–222. [Google Scholar]
- Rai, M.I.; Alam, M.; Lightfoot, D.A.; Gurha, P.; Afzal, A.J. Classification and experimental identification of plant long non-coding RNAs. Genomics 2019, 111, 997–1005. [Google Scholar]
- Liu, X.; Hao, L.; Li, D.; Zhu, L.; Hu, S. Long non-coding RNAs and their biological roles in plants. Genom. Proteom. Bioinform. 2015, 13, 137–147. [Google Scholar] [CrossRef]
- Nejat, N.; Mantri, N. Emerging roles of long non-coding RNAs in plant response to biotic and abiotic stresses. Crit. Rev. Biotechnol. 2018, 38, 93–105. [Google Scholar] [CrossRef]
- Kyndt, T. Loss of susceptibility, an underexplored approach for durable resistance to plant-parasitic nematodes. J. Exp. Bot. 2023, 74, 5422–5425. [Google Scholar] [PubMed]
- Datta, R.; Paul, S. Long non-coding RNAs: Fine-tuning the developmental responses in plants. J. Biosci. 2019, 44, 77. [Google Scholar]
- Khoei, M.A.; Karimi, M.; Karamian, R.; Amini, S.; Soorni, A. Identification of the complex interplay between nematode-related lncRNAs and their target genes in Glycine max L. Front. Plant Sci. 2021, 12, 779597. [Google Scholar]
- Yang, F.; Zhao, D.; Fan, H.; Zhu, X.; Wang, Y.; Liu, X.; Duan, Y.; Xuan, Y.; Chen, L. Functional analysis of long non-coding RNAs reveal their novel roles in biocontrol of bacteria-induced tomato resistance to Meloidogyne incognita. Int. J. Mol. Sci. 2020, 21, 911. [Google Scholar] [CrossRef]
- Xu, P.; Li, H.; Wang, X.; Zhao, G.; Lu, X.; Dai, S.; Cui, X.; Yuan, M.; Liu, Z. Integrated analysis of the lncRNA/circRNA-miRNA-mRNA expression profiles reveals novel insights into potential mechanisms in response to root-knot nematodes in peanut. BMC Genom. 2022, 23, 239. [Google Scholar] [CrossRef] [PubMed]
- Luo, X.; Jin, Y.; Shen, F.; Zhang, W. Integrated Analysis of the lncRNA-miRNA-mRNA Expression Profiles in Response to Meloidogyne incognita in Radish (Raphanus sativus L.). Agronomy 2024, 14, 1603. [Google Scholar] [CrossRef]
- Li, X.; Xing, X.; Xu, S.; Zhang, M.; Wang, Y.; Wu, H.; Sun, Z.; Huo, Z.; Chen, F.; Yang, T. Genome-wide identification and functional prediction of tobacco lncRNAs responsive to root-knot nematode stress. PLoS ONE 2018, 13, e0204506. [Google Scholar]
- Khanna, K.; Ohri, P.; Bhardwaj, R. Genetic toolbox and regulatory circuits of plant-nematode associations. Plant Physiol. Biochem. 2021, 165, 137–146. [Google Scholar]
- Legüe, M.; Calixto, A. RNA language in Caenorhabditis elegans and bacteria interspecies communication and memory. Curr. Opin. Syst. Biol. 2019, 13, 16–22. [Google Scholar] [CrossRef]
- Kasschau, K.D.; Fahlgren, N.; Chapman, E.J.; Sullivan, C.M.; Cumbie, J.S.; Givan, S.A.; Carrington, J.C. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 2007, 5, e57. [Google Scholar]
- Zhang, L.; Zhu, Q.; Tan, Y.; Deng, M.; Zhang, L.; Cao, Y.; Guo, X. Mitogen-activated protein kinases MPK3 and MPK6 phosphorylate receptor-like cytoplasmic kinase CDL1 to regulate soybean basal immunity. Plant Cell 2024, 36, 963–986. [Google Scholar] [PubMed]
- Medina, C.; Da Rocha, M.; Magliano, M.; Raptopoulo, A.; Marteu, N.; Lebrigand, K.; Abad, P.; Favery, B.; Jaubert-Possamai, S. Characterization of siRNAs clusters in Arabidopsis thaliana galls induced by the root-knot nematode Meloidogyne incognita. BMC Genom. 2018, 19, 943. [Google Scholar]
- da Costa, G.S.; Cerqueira, A.F.; de Brito, C.R.; Mielke, M.S.; Gaiotto, F.A. Epigenetics Regulation in Responses to Abiotic Factors in Plant Species: A Systematic Review. Plants 2024, 13, 2082. [Google Scholar] [CrossRef] [PubMed]
- Lisch, D.; Bennetzen, J.L. Transposable element origins of epigenetic gene regulation. Curr. Opin. Plant Biol. 2011, 14, 156–161. [Google Scholar] [PubMed]
- Wei, L.; Gu, L.; Song, X.; Cui, X.; Lu, Z.; Zhou, M.; Wang, L.; Hu, F.; Zhai, J.; Meyers, B.C. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc. Natl. Acad. Sci. USA 2014, 111, 3877–3882. [Google Scholar]
- Cabrera, J.; Barcala, M.; García, A.; Rio-Machín, A.; Medina, C.; Jaubert-Possamai, S.; Favery, B.; Maizel, A.; Ruiz-Ferrer, V.; Fenoll, C. Differentially expressed small RNA s in Arabidopsis galls formed by Meloidogyne javanica: A functional role for miR390 and its TAS 3-derived tasi RNA s. New Phytol. 2016, 209, 1625–1640. [Google Scholar]
- Margis, R.; Fusaro, A.F.; Smith, N.A.; Curtin, S.J.; Watson, J.M.; Finnegan, E.J.; Waterhouse, P.M. The evolution and diversification of Dicers in plants. FEBS Lett. 2006, 580, 2442–2450. [Google Scholar] [PubMed]
- Yang, F.; Wu, X.; Chen, L.; Qi, M. The Tomato lncRNA47258-miR319b-TCP Module in Biocontrol Bacteria Sneb821 Induced Plants Resistance to Meloidogyne incognita. Pathogens 2025, 14, 256. [Google Scholar] [CrossRef]
- Palatnik, J.F.; Wollmann, H.; Schommer, C.; Schwab, R.; Boisbouvier, J.; Rodriguez, R.; Warthmann, N.; Allen, E.; Dezulian, T.; Huson, D. Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev. Cell 2007, 13, 115–125. [Google Scholar] [CrossRef]
- Zhao, W.; Li, Z.; Fan, J.; Hu, C.; Yang, R.; Qi, X.; Chen, H.; Zhao, F.; Wang, S. Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J. Exp. Bot. 2015, 66, 4653–4667. [Google Scholar]
- Medina, C.; Da Rocha, M.; Magliano, M.; Ratpopoulo, A.; Revel, B.; Marteu, N.; Magnone, V.; Lebrigand, K.; Cabrera, J.; Barcala, M. Characterization of microRNAs from Arabidopsis galls highlights a role for miR159 in the plant response to the root-knot nematode Meloidogyne incognita. New Phytol. 2017, 216, 882–896. [Google Scholar] [CrossRef] [PubMed]
- Tian, B.; Wang, S.; Todd, T.C.; Johnson, C.D.; Tang, G.; Trick, H.N. Genome-wide identification of soybean microRNA responsive to soybean cyst nematodes infection by deep sequencing. BMC Genom. 2017, 18, 572. [Google Scholar] [CrossRef]
- Kaur, P.; Shukla, N.; Joshi, G.; VijayaKumar, C.; Jagannath, A.; Agarwal, M.; Goel, S.; Kumar, A. Genome-wide identification and characterization of miRNAome from tomato (Solanum lycopersicum) roots and root-knot nematode (Meloidogyne incognita) during susceptible interaction. PLoS ONE 2017, 12, e0175178. [Google Scholar] [CrossRef]
- Lee, H.J.; Park, Y.J.; Kwak, K.J.; Kim, D.; Park, J.H.; Lim, J.Y.; Shin, C.; Yang, K.-Y.; Kang, H. MicroRNA844-guided downregulation of cytidinephosphate diacylglycerol synthase3 (CDS3) mRNA affects the response of Arabidopsis thaliana to bacteria and fungi. Mol. Plan Microbe Interact. 2015, 28, 892–900. [Google Scholar] [CrossRef]
- Fan, J.W.; Hu, C.L.; Zhang, L.N.; Li, Z.L.; Zhao, F.K.; Wang, S.H. Jasmonic acid mediates tomato’s response to root knot nematodes. J. Plant Growth Regul. 2015, 34, 196–205. [Google Scholar] [CrossRef]
- Nahar, K.; Kyndt, T.; De Vleesschauwer, D.; Höfte, M.; Gheysen, G. The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol. 2011, 157, 305–316. [Google Scholar] [CrossRef] [PubMed]
- Schommer, C.; Palatnik, J.F.; Aggarwal, P.; Chételat, A.; Cubas, P.; Farmer, E.E.; Nath, U.; Weigel, D. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 2008, 6, e230. [Google Scholar] [CrossRef]
- Marin, E.; Jouannet, V.; Herz, A.; Lokerse, A.S.; Weijers, D.; Vaucheret, H.; Nussaume, L.; Crespi, M.D.; Maizel, A. miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 2010, 22, 1104–1117. [Google Scholar] [CrossRef] [PubMed]
- Díaz-Manzano, F.E.; Cabrera, J.; Ripoll, J.; Del Olmo, I.; Andrés, M.F.; Silva, A.C.; Barcala, M.; Sánchez, M.; Ruíz-Ferrer, V.; de Almeida-Engler, J. A role for the gene regulatory module microRNA172/TARGET OF EARLY ACTIVATION TAGGED 1/FLOWERING LOCUS T (mi RNA 172/TOE 1/FT) in the feeding sites induced by Meloidogyne javanica in Arabidopsis thaliana. New Phytol. 2018, 217, 813–827. [Google Scholar] [CrossRef]
- Zhang, B.; Wang, L.; Zeng, L.; Zhang, C.; Ma, H. Arabidopsis TOE proteins convey a photoperiodic signal to antagonize CONSTANS and regulate flowering time. Genes. Dev. 2015, 29, 975–987. [Google Scholar] [CrossRef]
- Ramazi, S.; Allahverdi, A.; Zahiri, J. Evaluation of post-translational modifications in histone proteins: A review on histone modification defects in developmental and neurological disorders. J. Biosci. 2020, 45, 135. [Google Scholar]
- Lawrence, M.; Daujat, S.; Schneider, R. Lateral thinking: How histone modifications regulate gene expression. Trends Genet. 2016, 32, 42–56. [Google Scholar] [CrossRef] [PubMed]
- Jha, R.K.; Levens, D.; Kouzine, F. Mechanical determinants of chromatin topology and gene expression. Nucleus 2022, 13, 95–116. [Google Scholar] [CrossRef] [PubMed]
- Yetgin, A. Exploring the Role of Epigenetics in Plant Adaptation to Environmental Stress. J. Epigenetics 2023, 4, 10–21. [Google Scholar]
- Berger, S.L. The complex language of chromatin regulation during transcription. Nature 2007, 447, 407–412. [Google Scholar] [CrossRef]
- De Santa, F.; Totaro, M.G.; Prosperini, E.; Notarbartolo, S.; Testa, G.; Natoli, G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 2007, 130, 1083–1094. [Google Scholar]
- Tie, F.; Banerjee, R.; Stratton, C.A.; Prasad-Sinha, J.; Stepanik, V.; Zlobin, A.; Diaz, M.O.; Scacheri, P.C.; Harte, P.J. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 2009, 136, 3131–3141. [Google Scholar]
- Boyer, L.A.; Plath, K.; Zeitlinger, J.; Brambrink, T.; Medeiros, L.A.; Lee, T.I.; Levine, S.S.; Wernig, M.; Tajonar, A.; Ray, M.K. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441, 349–353. [Google Scholar]
- Bracken, A.P.; Dietrich, N.; Pasini, D.; Hansen, K.H.; Helin, K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes. Dev. 2006, 20, 1123–1136. [Google Scholar]
- Battle, S.L.; Jayavelu, N.D.; Azad, R.N.; Hesson, J.; Ahmed, F.N.; Overbey, E.G.; Zoller, J.A.; Mathieu, J.; Ruohola-Baker, H.; Ware, C.B. Enhancer chromatin and 3D genome architecture changes from naive to primed human embryonic stem cell states. Stem Cell Rep. 2019, 12, 1129–1144. [Google Scholar]
- Zhou, D.-X.; Hu, Y.; Zhao, Y. Epigenomics. In Genetics and Genomics of Rice; Springer: Berlin/Heidelberg, Germany, 2013; pp. 129–143. [Google Scholar]
- Alvarez-Venegas, R.; Abdallat, A.A.; Guo, M.; Alfano, J.R.; Avramova, Z. Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2007, 2, 106–113. [Google Scholar] [CrossRef] [PubMed]
- Chavan, S.N.; De Kesel, J.; Desmedt, W.; Degroote, E.; Singh, R.R.; Nguyen, G.T.; Demeestere, K.; De Meyer, T.; Kyndt, T. Dehydroascorbate induces plant resistance in rice against root-knot nematode Meloidogyne graminicola. Mol. Plant Pathol. 2022, 23, 1303–1319. [Google Scholar] [CrossRef] [PubMed]
- Zang, C.; Schones, D.E.; Zeng, C.; Cui, K.; Zhao, K.; Peng, W. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 2009, 25, 1952–1958. [Google Scholar] [CrossRef] [PubMed]
- Oda, H.; Okamoto, I.; Murphy, N.; Chu, J.; Price, S.M.; Shen, M.M.; Torres-Padilla, M.E.; Heard, E.; Reinberg, D. Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol. Cell. Biol. 2009, 29, 2278–2295. [Google Scholar]
- Wu, Z.; Sun, W.; Zhou, S.; Zhang, L.; Zhao, X.; Xu, Y.; Wang, W. Genome-wide Analysis of Histone Modifications Distribution using the Chromatin Immunoprecipitation Sequencing Method in Magnaporthe oryzae. J. Vis. Exp. (JoVE) 2021, e62423. [Google Scholar] [CrossRef]
- Weinhouse, C.; Truong, L.; Meyer, J.N.; Allard, P. Caenorhabditis elegans as an emerging model system in environmental epigenetics. Environ. Mol. Mutagen. 2018, 59, 560–575. [Google Scholar]
- SIROHI, A.; DUTTA, T.K. Genome Engineering for Nematode Management. Indian J. Nematol. 2024, 53, 114–121. [Google Scholar]
- Alonso, C.; Ramos-Cruz, D.; Becker, C. The role of plant epigenetics in biotic interactions. New Phytol. 2019, 221, 731–737. [Google Scholar]
- Mirmajlessi, S.M.; Radhakrishnan, R. Biostimulants in Plant Science; Intechopen: London, UK, 2020; ISBN 1838801618. [Google Scholar]
- Mostafavi, H.A.; Mirmajlessi, S.M.; Fathollahi, H. The potential of food irradiation: Benefits and limitations. Trends Vital. Food Control Eng. 2012, 5, 43–68. [Google Scholar]
- De Palma, M.; Salzano, M.; Villano, C.; Aversano, R.; Lorito, M.; Ruocco, M.; Docimo, T.; Piccinelli, A.L.; D’Agostino, N.; Tucci, M. Transcriptome reprogramming, epigenetic modifications and alternative splicing orchestrate the tomato root response to the beneficial fungus Trichoderma harzianum. Hortic. Res. 2019, 6, 5. [Google Scholar] [CrossRef]
- Desmedt, W.; Kudjordjie, E.N.; Chavan, S.N.; Desmet, S.; Nicolaisen, M.; Vanholme, B.; Vestergård, M.; Kyndt, T. Distinct chemical resistance-inducing stimuli result in common transcriptional, metabolic, and nematode community signatures in rice root and rhizosphere. J. Exp. Bot. 2022, 73, 7564–7581. [Google Scholar] [CrossRef] [PubMed]
- Elnahal, A.S.M.; El-Saadony, M.T.; Saad, A.M.; Desoky, E.-S.M.; El-Tahan, A.M.; Rady, M.M.; AbuQamar, S.F.; El-Tarabily, K.A. The use of microbial inoculants for biological control, plant growth promotion, and sustainable agriculture: A review. Eur. J. Plant Pathol. 2022, 162, 759–792. [Google Scholar] [CrossRef]
- Bind, S.; Bind, S.; Sharma, A.K.; Chaturvedi, P. Epigenetic modification: A key tool for secondary metabolite production in microorganisms. Front. Microbiol. 2022, 13, 784109. [Google Scholar]
- Gupta, S.; Kulkarni, M.G.; White, J.F.; Van Staden, J. Epigenetic-based developments in the field of plant endophytic fungi. S. Afr. J. Bot. 2020, 134, 394–400. [Google Scholar]
- Banihashemian, S.N.; Jamali, S.; Golmohammadi, M.; Ghasemnezhad, M. Isolation and identification of endophytic bacteria associated with kiwifruit and their biocontrol potential against Meloidogyne incognita. Egypt. J. Biol. Pest. Control 2022, 32, 1–12. [Google Scholar] [CrossRef]
- Patel, J.S.; Kumar, G.; Bajpai, R.; Teli, B.; Rashid, M.; Sarma, B.K. PGPR formulations and application in the management of pulse crop health. In Biofertilizers; Elsevier: Amsterdam, The Netherlands, 2021; pp. 239–251. [Google Scholar]
- Maier, T.R.; Hewezi, T.; Peng, J.; Baum, T.J. Isolation of whole esophageal gland cells from plant-parasitic nematodes for transcriptome analyses and effector identification. Mol. Plant Microbe Interact. 2013, 26, 31–35. [Google Scholar] [CrossRef]
- Noon, J.B.; Baum, T.J. Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients. BMC Evol. Biol. 2016, 16, 1–16. [Google Scholar] [CrossRef]
- Kim, K.H.; An, D.R.; Song, J.; Yoon, J.Y.; Kim, H.S.; Yoon, H.J.; Im, H.N.; Kim, J.; Kim, D.J.; Lee, S.J. Mycobacterium tuberculosis Eis protein initiates suppression of host immune responses by acetylation of DUSP16/MKP-7. Proc. Natl. Acad. Sci. USA 2012, 109, 7729–7734. [Google Scholar]
- Gallusci, P.; Agius, D.R.; Moschou, P.N.; Dobránszki, J.; Kaiserli, E.; Martinelli, F. Deep inside the epigenetic memories of stressed plants. Trends Plant Sci. 2023, 28, 142–153. [Google Scholar] [CrossRef]
- Crisp, P.A.; Ganguly, D.; Eichten, S.R.; Borevitz, J.O.; Pogson, B.J. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2016, 2, e1501340. [Google Scholar] [CrossRef]
- Kambona, C.M.; Koua, P.A.; Léon, J.; Ballvora, A. Stress memory and its regulation in plants experiencing recurrent drought conditions. Theor. Appl. Genet. 2023, 136, 26. [Google Scholar] [PubMed]
- Xu, P.; Chen, H.; Hu, J.; Cai, W. Potential evidence for transgenerational epigenetic memory in Arabidopsis thaliana following spaceflight. Commun. Biol. 2021, 4, 835. [Google Scholar]
- Pissolato, M.D.; Martins, T.S.; Fajardo, Y.C.G.; Souza, G.M.; Machado, E.C.; Ribeiro, R.V. Stress memory in crops: What we have learned so far. Theor. Exp. Plant Physiol. 2024, 36, 535–565. [Google Scholar]
- Liu, H.; Able, A.J.; Able, J.A. Priming crops for the future: Rewiring stress memory. Trends Plant Sci. 2022, 27, 699–716. [Google Scholar]
- Lämke, J.; Bäurle, I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017, 18, 124. [Google Scholar]
- Kang, H.; Fan, T.; Wu, J.; Zhu, Y.; Shen, W.-H. Histone modification and chromatin remodeling in plant response to pathogens. Front. Plant Sci. 2022, 13, 986940. [Google Scholar]
- Mauch-Mani, B.; Baccelli, I.; Luna, E.; Flors, V. Defense priming: An adaptive part of induced resistance. Annu. Rev. Plant Biol. 2017, 68, 485–512. [Google Scholar]
- Buswell, W.; Schwarzenbacher, R.E.; Luna, E.; Sellwood, M.; Chen, B.; Flors, V.; Pétriacq, P.; Ton, J. Chemical priming of immunity without costs to plant growth. New Phytol. 2018, 218, 1205–1216. [Google Scholar]
- Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, D.L. Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 2018, 9, 1473. [Google Scholar] [CrossRef]
- Deshe, N.; Eliezer, Y.; Hoch, L.; Itskovits, E.; Ben-Ezra, S.; Zaslaver, A. Inheritance of associative memories in C. elegans nematodes. bioRxiv 2020. [Google Scholar] [CrossRef]
- Mierziak, J.; Wojtasik, W. Epigenetic weapons of plants against fungal pathogens. BMC Plant Biol. 2024, 24, 175. [Google Scholar] [CrossRef] [PubMed]
- Catoni, M.; Alvarez-Venegas, R.; Worrall, D.; Holroyd, G.; Barraza, A.; Luna, E.; Ton, J.; Roberts, M.R. Long-lasting defence priming by β-aminobutyric acid in tomato is marked by genome-wide changes in DNA methylation. Front. Plant Sci. 2022, 13, 836326. [Google Scholar]
- Wojtasik, W.; Boba, A.; Preisner, M.; Kostyn, K.; Szopa, J.; Kulma, A. DNA methylation profile of β-1, 3-glucanase and chitinase genes in flax shows specificity towards Fusarium oxysporum strains differing in pathogenicity. Microorganisms 2019, 7, 589. [Google Scholar] [CrossRef] [PubMed]
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Banihashemian, S.N.; Mirmajlessi, S.M. Epigenetic Modifications, Immune Control Processes, and Plant Responses to Nematodes. Agriculture 2025, 15, 742. https://doi.org/10.3390/agriculture15070742
Banihashemian SN, Mirmajlessi SM. Epigenetic Modifications, Immune Control Processes, and Plant Responses to Nematodes. Agriculture. 2025; 15(7):742. https://doi.org/10.3390/agriculture15070742
Chicago/Turabian StyleBanihashemian, Seyedeh Najmeh, and Seyed Mahyar Mirmajlessi. 2025. "Epigenetic Modifications, Immune Control Processes, and Plant Responses to Nematodes" Agriculture 15, no. 7: 742. https://doi.org/10.3390/agriculture15070742
APA StyleBanihashemian, S. N., & Mirmajlessi, S. M. (2025). Epigenetic Modifications, Immune Control Processes, and Plant Responses to Nematodes. Agriculture, 15(7), 742. https://doi.org/10.3390/agriculture15070742