Epigenetic Regulation of Stress-Induced Extracellular Matrix Remodeling in Plants: Mechanisms, Memory, and Applications

Xiaochen Liu

doi:10.47297/taposatWSP2633-456951.20250608

PDF
Export
Share
Collection
Album

Epigenetic Regulation of Stress-Induced Extracellular Matrix Remodeling in Plants: Mechanisms, Memory, and Applications

Volume 6, Issue 8

Views: 0 Downloads: 0

Epigenetic Regulation of Stress-Induced Extracellular Matrix Remodeling in Plants: Mechanisms, Memory, and Applications
Epigenetic Regulation of Stress-Induced Extracellular Matrix Remodeling in Plants: Mechanisms, Memory, and Applications
School of Science, The University of Melbourne, Parkville, Melbourne, Vic, 3010, Australia
Vol. 6, Issue 8, Pages: 268-274(2025)
Published：30 August 2025
DOI：10.47297/taposatWSP2633-456951.20250608
Accepted：

Scan QR Code

Liu Xiaochen.Epigenetic Regulation of Stress-Induced Extracellular Matrix Remodeling in Plants: Mechanisms, Memory, and Applications[J].Theory and Practice of Science and Technology,2025,06(08):268-274.
DOI：

Liu Xiaochen.Epigenetic Regulation of Stress-Induced Extracellular Matrix Remodeling in Plants: Mechanisms, Memory, and Applications[J].Theory and Practice of Science and Technology,2025,06(08):268-274. DOI： 10.47297/taposatWSP2633-456951.20250608.

摘要

Abstract

The plant extracellular matrix (ECM)

mostly comprised of the cell wall and connected polymers

offers an active interface between growth and defense as well as environmental alterations. While ECM architecture remodeling is characteristic for stress responses

mechanistic relationships between nuclear epigenetic regulation and extracellular remodeling are not clearly defined. This work aims to construct a mechanistic framework correlating chromatin-level epigenetics with stress-induced ECM remodeling. By incorporating recent evidence and mechanistic dissection

four hierarchically organized layers of epigenetic regulation are defined: (i) DNA methylation

as a switch for cellulose and lignin biosynthetic genes; (ii) histone modifications

such as H3K4me3

H3K27me3

and histone acetylation

governing transcriptional activation and repression of wall-associated loci; (iii) chromatin remodeling complexes such as SWI/SNF

governing promoter accessibility of cell wall genes; and (iv) small RNAs and epitranscriptomic marks (e.g.

m⁶A)

governing transcript integrity and translation of ECM biosynthetic pathways. These pathways all impinge upon transcription factor–epigenetic modifier complexes (e.g.

NAC/MYB

WRKY–BRAHMA)

with receptor kinases such as WAKs and FERONIA enforcing ECM-derived inputs upon receptor kinase-mediated outputs by changing nuclear chromatin states. Stress-specific strategies such as DNA hypermethylation under drought stress

histone acetylation under salinization stress

and chromatin priming by pathogen or cold stress create both transient defenses and long-term stress memories such that some modifications are passed through multiple generations. Together

these findings make epigenetic regulation out to be a molecular switchboard balancing immediate plasticity with heritable resilience. This integrated conceptual framework not only clarifies knowledge about nuclear but also provides indications for translational potential by breeding climatically resilient crops through specified epigenetic priming and selection.

关键词

Keywords

references

Houston, K., Tucker, M. R., Chowdhury, J., Shirley, N., & Little, A. (2016). The Plant Cell Wall: A Complex and Dynamic Structure As Revealed by the Responses of Genes under Stress Conditions. Frontiers in Plant Science , 7 .

Seifert, G. J., & Blaukopf, C. (2010). Irritable Walls: The Plant Extracellular Matrix and Signaling. Plant Physiology , 153 (2), 467–478.

Zhao, N., Zhou, Z., Cui, S., Zhang, X., Zhu, S., Wang, Y., … Wenjing, L. (2025). Advanced imaging-enabled understa nding of cell wall remodeling mechanisms mediating plant drought stress tolerance. Frontiers in Plant Science , 16 .

Marques, J. P. R., Hoy, J. W., Appezzato-da-Glória, B., Viveros, A. F. G., Vieira, M. L. C., & Baisakh, N. (2018). Sugarcane Cell Wall-Associated Defense Responses to Infection by Sporisorium scitamineum. Frontiers in Plant Science , 9 .

Malinovsky, F. G., Fangel, J. U., & Willats, W. G. T. (2014). The role of the cell wall in plant immunity. Frontiers in Plant Science , 5 .

Miedes, E., Vanholme, R., Boerjan, W., & Molina, A. (2014). The role of the secondary cell wall in plant resistance to pathogens. Frontiers in Plant Science , 5 .

Tenhaken, R. (2015). Cell wall remodeling under abiotic stress. Frontiers in Plant Science , 5 .

Kim, J.-M., Sasaki, T., Ueda, M., Sako, K., & Seki, M. (2015). Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Frontiers in Plant Science , 6 .

Lämke, J., & Bäurle, I. (2017). Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biology , 18 (1).

Ding, Y., Fromm, M., & Avramova, Z. (2012). Multiple exposures to drought "train" transcriptional responses in Arabidopsis. Nature Communications , 3 (1).

Crisp, P. A., Ganguly, D., Eichten, S. R., Borevitz, J. O., & Pogson, B. J. (2016). Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Science Advances , 2 (2), e1501340.

Li, W., Ying-Chung Jimmy Lin, Chen, Y.-L., Zhou, C., Li, S., Nette De Ridder, … Boerjan, W. (2024). Woody plant cell walls: Fundamentals and utilization. Molecular Plant/Molecular plant , 17 (1), 112–140.

Chen, B., Guo, Y., Zhang, X., Wang, L., Cao, L., Zhang, T., … Zhang, Q. (2022). Climate-responsive DNA methylation is involved in the biosynthesis of lignin in birch. Frontiers in plant science , 13 .

Lin, W., Sun, L., Huang, R.-Z., Liang, W., Liu, X., He, H., … Qian, W. (2020). Active DNA demethylation regulates tracheary element differentiation in Arabidopsis . Science Advances , 6 (26).

Kim, J.-M., Sasaki, T., Ueda, M., Sako, K., & Seki, M. (2015). Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Frontiers in Plant Science , 6 .

Shi, L., Cui, X., & Shen, Y. (2024). The roles of histone methylation in the regulation of abiotic stress responses in plants. Plant Stress , 11 , 100303.

Faivre, L., Kinscher, N.-F., Kuhlmann, A. B., Xu, X., Kaufmann, K., & Schubert, D. (2024). Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana. Frontiers in Plant Science , 15 .

Archacki, R., Ruslan Yatusevich, Buszewicz, D., Katarzyna Krzyczmonik, Patryn, J., Roksana Iwanicka-Nowicka, … Szymon Swiezewski. (2016). Arabidopsis SWI/SNF chromatin remodeling complex binds both promoters and terminators to regulate gene expression. Nucleic Acids Research , gkw1273–gkw1273.

Rudy, E., Grabsztunowicz, M., Arasimowicz‐Jelonek, M., Umesh Kumar Tanwar, Maciorowska, J., & Sobieszczuk‐Nowicka, E. (2023). N6-methyladenosine (m6A) RNA modification as a metabolic switch between plant cell survival and death in leaf senescence. Frontiers in Plant Science , 13 .

Chenna Swetha, Basu, D., Kannan Pachamuthu, Varsha Tirumalai, Nair, A., Prasad, M., & Shivaprasad, P. V. (2018). Major Domestication-Related Phenotypes in Indica Rice Are Due to Loss of miRNA-Mediated Laccase Silencing. The Plant Cell , 30 (11), 2649–2662.

Dash, P. K., Gupta, P., Pradhan, S. K., Shasany, A. K., & Rai, R. (2022). Analysis of Homologous Regions of Small RNAs MIR397 and MIR408 Reveals the Conservation of Microsynteny among Rice Crop-Wild Relatives. Cells , 11 (21), 3461.

Wang, X., Wang, D., Xu, W., Kong, L., Ye, X., Zhuang, Q., … Luo, K. (2020). Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis in Arabidopsis inflorescence stem. Nucleic Acids Research , 49 (1), 190–205.

Wang, L., Wang, L., Tan, M., Wang, L., Zhao, W., You, J., … Wang, W. (2023). The pattern of alternative splicing and DNA methylation alteration and their interaction in linseed (Linum usitatissimum L.) response to repeated drought stresses. Biological Research , 56 (1).

Wang, W., Qin, Q., Sun, F., Wang, Y., Xu, D., Li, Z., & Fu, B. (2016). Genome-Wide Differences in DNA Methylation Changes in Two Contrasting Rice Genotypes in Response to Drought Conditions. Frontiers in Plant Science , 7 .

Gan, L., Wei, Z., Yang, Z., Li, F., & Wang, Z. (2021). Updated Mechanisms of GCN5—The Monkey King of the Plant Kingdom in Plant Development and Resistance to Abiotic Stresses. Cells , 10 (5), 979.

Di, Q., Zhou, M., Li, Y., Yan, Y., He, C., Wang, J., … Sun, M. (2024). RESPIRATORY BURST OXIDASE HOMOLOG 5.1 regulates H3K4me3 deposition and transcription after cold priming in cucumber. Plant Physiology , 197 (2).

Zhao, X., Wang, Y., Yuan, B., Zhao, H., Wang, Y., Tan, Z., … Gu, Q. (2024). Temporally-coordinated bivalent histone modifications of BCG1 enable fungal invasion and immune evasion. Nature Communications , 15 (1), 231.

Dowen, R. H., Pelizzola, M., Schmitz, R. J., Lister, R., Dowen, J. M., Nery, J. R., … Ecker, J. R. (2012). Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences , 109 (32), E2183–E2191.

Sánchez, A., Joost, Furci, L., Smith, L., & Ton, J. (2016). The role of DNA (de)methylation in immune responsiveness of Arabidopsis, 88 (3), 361–374.

Adam Jackson Parker, Wilkinson, S. T., & Ton, J. (2021). Epigenetics: a catalyst of plant immunity against pathogens. New Phytologist , 233 (1), 66–83.

Jaskiewicz, M., Conrath, U., & Peterhänsel, C. (2010). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO reports , 12 (1), 50–55.

Yusuf, A., Kota Wakaya, Sakamoto, T., Uemura, T., & Gen‐Ichiro Arimura. (2024). Histone Modification‐Dependent Transcriptional Regulation of Defence Genes in Early Response of Arabidopsis to Spodoptera litura Attack. Plant, Cell & Environment , 48 (5), 3257–3268.

Troyee, A. N., Medrano, M., Müller, C., & Alonso, C. (2022). Variation in DNA methylation and response to short-term herbivory in Thlaspi arvense. Flora , 293 , 152106.

Cazzonelli, C. I., Nisar, N., Roberts, A. C., Murray, K. D., Borevitz, J. O., & Pogson, B. J. (2014). A chromatin modifying enzyme, SDG8, is involved in morphological, gene expression, and epigenetic responses to mechanical stimulation. Frontiers in Plant Science , 5 .

Brenya, E., Pervin, M., Chen, Z., Tissue, D. T., Johnson, S., Braam, J., & Cazzonelli, C. I. (2022). Mechanical stress acclimation in plants: Linking hormones and somatic memory to thigmomorphogenesis. Plant, Cell & Environment , 45 (4), 989–1010.

Ibragić, S., Dahija, S., & Karalija, E. (2025). The Good, the Bad, and the Epigenetic: Stress-Induced Metabolite Regulation and Transgenerational Effects. Epigenomes , 9 (2), 10.

Li, F., Luo, B., Wang, Y., Rao, J., Gao, S., Peng, Q., … Yi, L. (2024). Genome-Wide Methylation Landscape Uncovers the Role of DNA Methylation in Ramie (Boehmeria nivea L.) Bast Fiber Growth. Agronomy , 14 (7), 1467.

Kohorn, B. D., & Kohorn, S. L. (2012). The cell wall-associated kinases, WAKs, as pectin receptors. Frontiers in Plant Science , 3 .

Feng, W., Kita, D., Peaucelle, A., Cartwright, H. N., Doan, V., Duan, Q., … Dinneny, J. R. (2018). The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca2+ Signaling. Current Biology , 28 (5), 666-675.e5.

Hu, Y., Luo, Q., Xu, Y., Miao, Y., Tian, X., & Wang, Q. (2022). Transcriptomic and Epigenomic Assessment Reveals Epigenetic Regulation of WRKY Genes in Response to Magnaporthe oryzae Infection in Rice. Current Genomics , 23 (3), 182–194.

Sun, C., Ali, K., Yan, K., Fiaz, S., Dormatey, R., Bi, Z., & Bai, J. (2021). Exploration of Epigenetics for Improvement of Drought and Other Stress Resistance in Crops: A Review. Plants , 10 (6), 1226.

Van Dooren, T. J. M., Silveira, A. B., Gilbault, E., Jiménez-Gómez, J. M., Martin, A., Bach, L., … Colot, V. (2020). Mild drought in the vegetative stage induces phenotypic, gene expression, and DNA methylation plasticity in Arabidopsis but no transgenerational effects. Journal of Experimental Botany , 71 (12), 3588–3602.

Alert me when the article has been cited

Submit

No data

Related Author

No data

Related Institution

No data

⁰