Machine-learning meta-analysis reveals ethylene as a central component of the molecular core in abiotic stress responses in Arabidopsis

. 2025 May 22 ; 16 (1) : 4778. [epub] 20250522

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, metaanalýza

Perzistentní odkaz   https://www.medvik.cz/link/pmid40404615

Grantová podpora
G032717N Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
G082421N Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
1288923N Fonds Wetenschappelijk Onderzoek (Research Foundation Flanders)
BOF-BAS Universiteit Gent (UGent)

Odkazy

PubMed 40404615
PubMed Central PMC12098884
DOI 10.1038/s41467-025-59542-3
PII: 10.1038/s41467-025-59542-3
Knihovny.cz E-zdroje

Understanding how plants adapt their physiology to overcome severe and often multifactorial stress conditions in nature is vital in light of the climate crisis. This remains a challenge given the complex nature of the underlying molecular mechanisms. To provide a comprehensive picture of stress-mitigation mechanisms, an exhaustive analysis of publicly available stress-related transcriptomic data has been conducted. We combine a meta-analysis with an unsupervised machine-learning algorithm to identify a core of stress-related genes active at 1-6 h and 12-24 h of exposure in Arabidopsis thaliana shoots and roots. To ensure robustness and biological significance of the output, often lacking in meta-analyses, a triple validation is incorporated. We present a 'stress gene core': a set of key genes involved in plant tolerance to ten adverse environmental conditions and ethylene-precursor supplementation rather than individual conditions. Notably, ethylene plays a key regulatory role in this core, influencing gene expression and acting as a critical factor in stress tolerance. Additionally, the analysis provides insights into previously uncharacterized genes, key genes within large families, and gene expression dynamics, which are used to create biologically validated databases that can guide further abiotic stress research. These findings establish a strong framework for advancing multi-stress-resilient crops, paving the way for sustainable agriculture in the face of climate challenges.

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Food and Agriculture Organization of the United Nations.

Pandey, P., Irulappan, V., Bagavathiannan, M. V. & Senthil-Kumar, M. Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. PubMed DOI PMC

Oshunsanya, S. O., Nwosu, N. J. & Li, Y. Abiotic stress in agricultural crops under climatic conditions. In

Savary, S. et al. The global burden of pathogens and pests on major food crops. PubMed DOI

Zhang, H., Zhao, Y. & Zhu, J.-K. Thriving under stress: how plants balance growth and the stress response. PubMed DOI

Zandalinas, S. I. & Mittler, R. Plant responses to multifactorial stress combination. PubMed DOI

Kuromori, T., Fujita, M., Takahashi, F., Yamaguchi-Shinozaki, K. & Shinozaki, K. Inter-tissue and inter-organ signaling in drought stress response and phenotyping of drought tolerance. PubMed DOI PMC

Li, H., Testerink, C. & Zhang, Y. How roots and shoots communicate through stressful times. PubMed DOI

Singh, A. et al. Tissue specific and abiotic stress regulated transcription of histidine kinases in plants is also influenced by diurnal rhythm. PubMed DOI PMC

Choudhury, F. K., Devireddy, A. R., Azad, R. K., Shulaev, V. & Mittler, R. Rapid accumulation of glutathione during light stress in Arabidopsis. PubMed DOI

Moore, M., Vogel, M. O. & Dietz, K. J. The acclimation response to high light is initiated within seconds as indicated by upregulation of PubMed DOI PMC

Kollist, H. et al. Rapid responses to abiotic stress: priming the landscape for the signal transduction network. PubMed DOI

Depaepe, T. et al. At the crossroads of survival and death: the reactive oxygen species–ethylene–sugar triad and the unfolded protein response. PubMed DOI

Depaepe, T. & Van Der Straeten, D. Tools of the ethylene trade: a chemical kit to influence ethylene responses in plants and its use in agriculture. DOI

Chang, K. N. et al. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in PubMed DOI PMC

Anderson, J. P. et al. Antagonistic interaction between abscisic acid and jasmonate–ethylene signaling pathways modulates defense gene expression and disease resistance in PubMed DOI PMC

Van den Broeck, L. et al. From network to phenotype: the dynamic wiring of an PubMed DOI PMC

Hossain, M. A. et al. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. PubMed DOI

Zhang, X., Shen, L., Li, F., Meng, D. & Sheng, J. DOI

Chou, T.-S., Chao, Y.-Y. & Kao, C. H. Involvement of hydrogen peroxide in heat shock- and cadmium-induced expression of ascorbate peroxidase and glutathione reductase in leaves of rice seedlings. PubMed DOI

Hossain, M. A., Mostofa, M. G. & Fujita, M. Cross protection by cold-shock to salinity and drought stress-induced oxidative stress in mustard (

Atkinson, N. J. & Urwin, P. E. The interaction of plant biotic and abiotic stresses: from genes to the field. PubMed DOI

Panahi, B., Frahadian, M., Dums, J. T. & Hejazi, M. A. Integration of cross species RNA-seq meta-analysis and machine-learning models identifies the most important salt stress-responsive pathways in microalga. PubMed DOI PMC

Toro-Domínguez, D. et al. A survey of gene expression meta-analysis: methods and applications. PubMed DOI

Meta-analysis in basic biology.

Gibney, E. Could machine learning fuel a reproducibility crisis in science? PubMed DOI

Cortes, C. & Vapnik, V. Support-vector networks. DOI

Winters-Hilt, S. & Merat, S. SVM clustering. PubMed DOI PMC

Krishnaveni, N. & Radha, V. Performance evaluation of clustering-based classification algorithms for detection of online spam reviews. In

Yan, J. & Wang, X. Unsupervised and semi-supervised learning: the next frontier in machine learning for plant systems biology. PubMed DOI

Codjoe, J. M., Miller, K. & Haswell, E. S. Plant cell mechanobiology: greater than the sum of its parts. PubMed DOI PMC

Tenhaken, R. Cell wall remodeling under abiotic stress. PubMed PMC

Ghosh, D. & Xu, J. Abiotic stress responses in plant roots: a proteomics perspective. PubMed DOI PMC

Huang, P.-Y., Catinot, J. & Zimmerli, L. Ethylene response factors in PubMed DOI

Xu, J. & Zhang, S. Regulation of ethylene biosynthesis and signaling by protein kinases and phosphatases. PubMed DOI

Xu, J. et al. Activation of PubMed DOI

Shin, K. et al. Genetic identification of PubMed DOI

Zhu, T. et al. Mitochondrial alternative oxidase-dependent autophagy involved in ethylene-mediated drought tolerance in PubMed DOI PMC

Birkenbihl, R. P., Kracher, B., Roccaro, M. & Somssich, I. E. Induced genome-wide binding of three PubMed DOI PMC

Shi, J., Drummond, B. J., Wang, H., Archibald, R. L. & Habben, J. E. Maize and Arabidopsis ARGOS proteins interact with ethylene receptor signaling complex, supporting a regulatory role for ARGOS in ethylene signal transduction. PubMed DOI PMC

Samalova, M. et al. Hormone-regulated expansins: expression, localization, and cell wall biomechanics in PubMed PMC

Samalova, M., Gahurova, E. & Hejatko, J. Expansin-mediated developmental and adaptive responses: a matter of cell wall biomechanics? PubMed PMC

Xie, Z., Nolan, T. M., Jiang, H. & Yin, Y. PubMed DOI PMC

Nakano, T., Suzuki, K., Fujimura, T. & Shinshi, H. Genome-wide analysis of the ERF gene family in PubMed DOI PMC

Zhang, M. & Zhang, S. Mitogen-activated protein kinase cascades in plant signaling. PubMed DOI

Kvint, K., Nachin, L., Diez, A. & Nyström, T. The bacterial universal stress protein: function and regulation. PubMed DOI

Shaik, R. & Ramakrishna, W. Machine learning approaches distinguish multiple stress conditions using stress-responsive genes and identify candidate genes for broad resistance in rice. PubMed DOI PMC

Ma, C., Xin, M., Feldmann, K. A. & Wang, X. Machine learning-based differential network analysis: a study of stress-responsive transcriptomes in PubMed DOI PMC

English, P. J., Lycett, G. W., Roberts, J. A. & Jackson, M. B. Increased 1-aminocyclopropane-1-carboxylic acid oxidase activity in shoots of flooded tomato plants raises ethylene production to physiologically active levels. PubMed DOI PMC

Depaepe, T., Vanhaelewyn, L. & Van Der Straeten, D. UV-B responses in the spotlight: dynamic photoreceptor interplay and cell-type specificity. PubMed DOI

Xiong, L. & Zhu, J. K. Molecular and genetic aspects of plant responses to osmotic stress. PubMed DOI

Kim, J. S., Kidokoro, S., Yamaguchi-Shinozaki, K. & Shinozaki, K. Regulatory networks in plant responses to drought and cold stress. PubMed DOI PMC

Lewandowska, M. et al. Wounding triggers wax biosynthesis in PubMed DOI PMC

Prasad, A., Sedlářová, M., Balukova, A., Rác, M. & Pospíšil, P. Reactive oxygen species as a response to wounding: imaging in PubMed DOI PMC

Lee, S. & Park, C. M. Regulation of reactive oxygen species generation under drought conditions in PubMed DOI PMC

Sato, H., Mizoi, J., Shinozaki, K. & Yamaguchi-Shinozaki, K. Complex plant responses to drought and heat stress under climate change. PubMed DOI

Jahed, K. R., Saini, A. K. & Sherif, S. M. Coping with the cold: unveiling cryoprotectants, molecular signaling pathways, and strategies for cold stress resilience. PubMed DOI PMC

Taji, T. et al. Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in PubMed DOI

Tan, W.-J. et al. PubMed DOI PMC

Baez, L. A., Tichá, T. & Hamann, T. Cell wall integrity regulation across plant species. PubMed DOI PMC

Lamers, J., van der Meer, T. & Testerink, C. How plants sense and respond to stressful environments. PubMed DOI PMC

Kudla, J. et al. Advances and current challenges in calcium signaling. PubMed DOI

Wang, C., Teng, Y., Zhu, S., Zhang, L. & Liu, X. NaCl- and cold-induced stress activate different Ca DOI

Corso, M., Doccula, F. G., de Melo, J. R. F., Costa, A. & Verbruggen, N. Endoplasmic reticulum-localized CCX2 is required for osmotolerance by regulating ER and cytosolic Ca dynamics. PubMed DOI PMC

Li, Z. et al. CCX1, a putative cation/Ca PubMed DOI

Dodd, A. N., Kudla, J. & Sanders, D. The language of calcium signaling. PubMed DOI

Zhu, X. et al. Calmodulin-like protein CML24 interacts with CAMTA2 and WRKY46 to regulate ALMT1-dependent Al resistance in PubMed DOI

Menke, F. L. H., van Pelt, J. A., Pieterse, C. M. J. & Klessig, D. F. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in PubMed DOI PMC

Shi, Y. et al. Ethylene signaling negatively regulates freezing tolerance by repressing expression of PubMed DOI PMC

Hartman, S. et al. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. PubMed DOI PMC

Vaseva, I. I. et al. Ethylene signaling in salt-stressed PubMed DOI

Zhang, X. et al. MAMP-elicited changes in amino acid transport activity contribute to restricting bacterial growth. PubMed DOI PMC

Batista-Silva, W. et al. The role of amino acid metabolism during abiotic stress release. PubMed DOI

Chen, Y. & Zhang, J. Multiple functions and regulatory networks of PubMed

De Paepe, A., Vuylsteke, M., Van Hummelen, P., Zabeau, M. & Van Der Straeten, D. Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in PubMed

Kilian, J. et al. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. PubMed DOI

Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. PubMed DOI PMC

Kauffmann, A., Gentleman, R. & Huber, W. arrayQualityMetrics—a bioconductor package for quality assessment of microarray data. PubMed DOI PMC

Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. DOI

Gower, J. C. A general coefficient of similarity and some of its properties. DOI

Galili, T. dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. PubMed DOI PMC

Yoon, S., Baik, B., Park, T. & Nam, D. Powerful PubMed DOI PMC

Sharifi, S. et al. Integration of machine learning and meta-analysis identifies the transcriptomic bio-signature of mastitis disease in cattle. PubMed DOI PMC

Roman, I., Santana, R., Mendiburu, A. & Lozano, J. A. In-depth analysis of SVM kernel learning and its components. DOI

Lameski, P., Zdravevski, E., Mingov, R. & Kulakov, A. SVM parameter tuning with grid search and its impact on reduction of model over-fitting. In: Yao, Y., Hu, Q., Yu, H., Grzymala-Busse, J.W. (eds)

Luesse, D. R., Wilson, M. E. & Haswell, E. S. RNA sequencing analysis of the msl2msl3, crl, and ggps1 mutants indicates that diverse sources of plastid dysfunction do not alter leaf morphology through a common signaling pathway. PubMed DOI PMC

Bedre, R. & Mandadi, K. GenFam: a web application and database for gene family-based classification and functional enrichment analysis. PubMed DOI PMC

Szklarczyk, D. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. PubMed DOI PMC

Grant, C. E., Bailey, T. L. & Noble, W. S. FIMO: scanning for occurrences of a given motif. PubMed DOI PMC

Vanderstraeten, L., Sanchez-Muñoz, R., Depaepe, T., Auwelaert, F. & Van Der Straeten, D. Mix-and-match: an improved, fast and accessible protocol for hypocotyl micrografting of PubMed DOI PMC

De Vylder, J., Vandenbussche, F., Hu, Y., Philips, W. & Van Der Straeten, D. Rosette tracker: an open source image analysis tool for automatic quantification of genotype effects. PubMed DOI PMC

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