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Genome-Wide Characterization of Jasmonates Signaling Components Reveals the Essential Role of ZmCOI1a-ZmJAZ15 Action Module in Regulating Maize Immunity to Gibberella Stalk Rot.

ABSTRACT: Gibberella stalk rot (GSR) by Fusarium graminearum causes significant losses of maize production worldwide. Jasmonates (JAs) have been broadly known in regulating defense against pathogens through the homeostasis of active JAs and COI-JAZ-MYC function module. However, the functions of different molecular species of JAs and COI-JAZ-MYC module in maize interactions with Fusarium graminearum and regulation of diverse metabolites remain unknown. In this study, we found that exogenous application of MeJA strongly enhanced resistance to GSR. RNA-seq analysis showed that MeJA activated multiple genes in JA pathways, which prompted us to perform a genome-wide screening of key JA signaling components in maize. Yeast Two-Hybrid, Split-Luciferase, and Pull-down assays revealed that the JA functional and structural mimic coronatine (COR) functions as an essential ligand to trigger the interaction between ZmCOIa and ZmJAZ15. By deploying CRISPR-cas9 knockout and Mutator insertional mutants, we demonstrated that coi1a mutant is more resistant, whereas jaz15 mutant is more susceptible to GSR. Moreover, JA-deficient opr7-5opr8-2 mutant displayed enhanced resistance to GSR compared to wild type. Together, these results provide strong evidence that ZmJAZ15 plays a pivotal role, whereas ZmCOIa and endogenous JA itself might function as susceptibility factors, in maize immunity to GSR.

SUBMITTER: Ma L

PROVIDER: S-EPMC7830991 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Genome-Wide Characterization of Jasmonates Signaling Components Reveals the Essential Role of ZmCOI1a-ZmJAZ15 Action Module in Regulating Maize Immunity to Gibberella Stalk Rot.

Ma Liang L Sun Yali Y Ruan Xinsen X Huang Pei-Cheng PC Wang Shi S Li Shunfa S Zhou Yu Y Wang Fang F Cao Yu Y Wang Qing Q Wang Zhenhua Z Kolomiets Michael V MV Gao Xiquan X

International journal of molecular sciences 20210116 2

Gibberella stalk rot (GSR) by <i>Fusarium graminearum</i> causes significant losses of maize production worldwide. Jasmonates (JAs) have been broadly known in regulating defense against pathogens through the homeostasis of active JAs and COI-JAZ-MYC function module. However, the functions of different molecular species of JAs and COI-JAZ-MYC module in maize interactions with <i>Fusarium graminearum</i> and regulation of diverse metabolites remain unknown. In this study, we found that exogenous a ...[more]

PMID: 33467172

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Project description:One of the most destructive diseases, Gibberella stalk rot (GSR), caused by Fusarium graminearum, reduces maize yields significantly. An induced resistance response is a potent and cost-effective plant defense against pathogen attack. The functional counterpart of JAs, coronatine (COR), has attracted a lot of interest recently due to its ability to control plant growth and stimulate secondary metabolism. Although several studies have focused on COR as a plant immune elicitor to improve plant resistance to pathogens, the effectiveness and underlying mechanisms of the suppressive ability against COR to F. graminearum in maize have been limited. We investigated the potential physiological and molecular mechanisms of COR in modulating maize resistance to F. graminearum. COR treatment strongly enhanced disease resistance and promoted stomatal closure with H2O2 accumulation, and 10 μg/mL was confirmed as the best concentration. COR treatment increased defense-related enzyme activity and decreased the malondialdehyde content with enhanced antioxidant enzyme activity. To identify candidate resistance genes and gain insight into the molecular mechanism of GSR resistance associated with COR, we integrated transcriptomic and metabolomic data to systemically explore the defense mechanisms of COR, and multiple hub genes were pinpointed using weighted gene correlation network analysis (WGCNA). We discovered 6 significant modules containing 10 candidate genes: WRKY transcription factor (LOC100279570), calcium-binding protein (LOC100382070), NBR1-like protein (LOC100275089), amino acid permease (LOC100382244), glutathione S-transferase (LOC541830), HXXXD-type acyl-transferase (LOC100191608), prolin-rich extensin-like receptor protein kinase (LOC100501564), AP2-like ethylene-responsive transcription factor (LOC100384380), basic leucine zipper (LOC100275351), and glycosyltransferase (LOC606486), which are highly correlated with the jasmonic acid-ethylene signaling pathway and antioxidants. In addition, a core set of metabolites, including alpha-linolenic acid metabolism and flavonoids biosynthesis linked to the hub genes, were identified. Taken together, our research revealed differentially expressed key genes and metabolites, as well as co-expression networks, associated with COR treatment of maize stems after F. graminearum infection. In addition, COR-treated maize had higher JA (JA-Ile and Me-JA) levels. We postulated that COR plays a positive role in maize resistance to F. graminearum by regulating antioxidant levels and the JA signaling pathway, and the flavonoid biosynthesis pathway is also involved in the resistance response against GSR.

Dataset Information

Genome-Wide Characterization of Jasmonates Signaling Components Reveals the Essential Role of ZmCOI1a-ZmJAZ15 Action Module in Regulating Maize Immunity to Gibberella Stalk Rot.

Publications

Genome-Wide Characterization of Jasmonates Signaling Components Reveals the Essential Role of ZmCOI1a-ZmJAZ15 Action Module in Regulating Maize Immunity to Gibberella Stalk Rot.

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