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Plant Cell
Plant Cell
plcell
The Plant Cell
1040-4651
1532-298X
Oxford University Press US

38916882
10.1093/plcell/koae188
koae188
In Brief
AcademicSubjects/SCI01270
AcademicSubjects/SCI01280
AcademicSubjects/SCI02286
AcademicSubjects/SCI02287
AcademicSubjects/SCI02288
What doesn’t kill you makes you stronger: Multi-omics analysis of jasmonate responses in rice
https://orcid.org/0000-0003-0235-2985
Sanchez-Muñoz Raul Assistant Features Editor, The Plant Cell, American Society of Plant Biologists
Laboratory of Functional Plant Biology, Department of Biology, Faculty of Sciences, Ghent University, Gent B-9000, Belgium

Author for correspondence: raul.sanchezmunoz@ugent.be
9 2024
25 6 2024
25 6 2024
36 9 33223323
20 6 2024
20 6 2024
17 7 2024
© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.
2024
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pmcGrowing in complex environments involves interspecific interactions, which can be either positive or negative. The presence of species that act as colonizers, pathogens, or even consumers creates evolutionary pressure that drives plants to develop intricate molecular defensive responses. However, growth and defense responses must be perfectly balanced and regulated, as defense responses usually have a negative impact on vegetative growth (Depaepe et al. 2021). Jasmonates (JA) are key players in plant defense responses. JA signaling has been extensively studied, particularly its conjugation with amino acids, especially isoleucine (Ile), and its subsequent sensing by CORONATINE INSENSITIVE 1 (COI1). This process is crucial for targeting and degrading the repressor proteins JASMONATE ZIM-DOMAINS (JAZs), thereby activating the transcription of JA-responsive genes (Chini et al. 2023). Despite these advances, the specific players involved in the downstream effects of JA and its spatiotemporal regulation have not been fully elucidated.

In this issue, Yumeng Chen, Gaochen Jin, and colleagues (Chen et al. 2024) shed light on the different modules involved in JA signaling by performing an exhaustive analysis of rice JA transcriptional alterations in response to biotic stress stimuli. First, the analysis of an RNA-seq time series from different tissues (roots, leaves, and leaf sheaths) revealed the presence of both shared and tissue-specific transcriptional responses when comparing control and treated samples. Among them, roots showed a higher number of differentially expressed genes (DEGs) compared with leaves. Among the tissue-specific genes, those involved in the synthesis of specialized metabolites were highlighted, such as diterpenes in roots and phenylpropanoids in leaf sheaths, which are generally associated with defense responses. The tissue specificity in terms of specialized—or secondary—metabolites was further investigated through an untargeted metabolomic approach, which confirmed the differential accumulation of terpenoids in roots, leaves, and leaf sheaths. Among the shared genes, JA-responsive and JA-biosynthetic genes stood out, validating the biological relevance of this dataset in terms of JA molecular mechanisms.

With these data, a gene coexpression network highlighted the transcription factor MYC2 as a master regulator of JA responses. To validate this observation, a MYC2 ChIP-seq provided empirical evidence of the direct interaction between MYC2 and specific promoter regions. The presence of known targets of MYC2, such as JAZ1, JAZ3, and JAZ8 (Kazan and Manners 2013; Liu et al. 2019), validated the results. Comparing the list of genes found in the ChIP-seq analysis with the previous RNA-seq data revealed that over one-half of the MYC2-regulated genes were either up- or downregulated after treatment with methyl JA, highlighting its key role in the transcriptional alterations after JA signaling. Interestingly, upregulated genes were related to JA responses, while downregulated genes were associated with growth responses and primary metabolism. In addition, to support the role of MYC2 as a master regulator of JA responses, these results showed the direct role of MYC2 in balancing defense and growth responses.

The combination of the MYC2 ChIP-seq and RNA-seq datasets in a gene coexpression network allowed the reconstruction of gene cascades and revealed a series of transcription factors (TFs) that act downstream of MYC2. Some NAC TFs found in the ChIP-seq were upregulated genes in the RNA-seq assay. When a triple knockout mutant for NAC1, NAC3, and NAC4 (nac1nac3nac4) was analyzed, JA-related responses were significantly higher compared with wild-type rice plants, revealing their combined role as negative regulators of JA responses. Concordantly, nac1nac3nac4 plantlets showed resistance to biotic stress exposure but were significantly smaller in size, probably due to the imbalance between defense and growth responses.

The exhaustive analysis and multi-omics perspective adopted in this work aims to provide a holistic picture of the molecular responses to JA in defense mechanisms. Through this analysis, the authors were able to define 3 modules: a tissue-specific module, mainly involved in the synthesis of specialized metabolites; a core-regulatory module, with MYC2 as a master regulator; and a negative feedback module, which limits JA responses to ensure a balance between growth and defense responses (Fig.). These results not only dissect JA responses to fine-tune engineering strategies for developing resilient rice varieties but also provide a valuable dataset that will significantly advance JA research.

Figure. Proposed model for the different sectors involved in JA-mediated defense responses in rice, based on data presented by Chen et al. (2024). Image credit: Raul Sanchez-Muñoz.
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Chini A , MonteI, ZamarrenoAM, Garcia-MinaJM, SolanoR. Evolution of the jasmonate ligands and their biosynthetic pathways. New Phytol. 2023:238 (5 ):2236–2246. 10.1111/nph.18891 36942932
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