Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot

Sun, Yali; Ruan, Xinsen; Wang, Qing; Zhou, Yu; Wang, Fang; Ma, Liang; Wang, Zhenhua; Gao, Xiaoge

doi:10.3389/fpls.2021.664733

Cited by 14 publications

(9 citation statements)

References 78 publications

(96 reference statements)

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“…To identify oxylipins that may explain decreased resistance of zmlox5-3 mutant, we performed oxylipin quantification in the mutant and B73 at different time points upon infection with F. graminearum . To hone-in a subset of oxylipins associated with GSR resistance, we included the GSR resistant inbred line W438 (Sun et al, 2021 ) in the panel subjected to oxylipin profiling. The principal component analysis showed a clear trend of separation between control and infected samples for all three lines.…”

Section: Resultsmentioning

confidence: 99%

Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot

et al. 2021

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Gibberella stalk rot caused by Fusarium graminearum is one of the devastating diseases of maize that causes significant yield losses worldwide. The molecular mechanisms regulating defense against this pathogen remain poorly understood. According to recent studies, a major oxylipin hormone produced by 13-lipoxygenases (LOX) namely jasmonic acid (JA) has been associated with maize susceptibility to GSR. However, the specific roles of numerous 9-LOX-derived oxylipins in defense against Gibberella stalk rot (GSR) remain unexplained. In this study, we have shown that disruption of a 9-LOX gene, ZmLOX5, resulted in increased susceptibility to GSR, indicating its role in defense. To understand how ZmLOX5 regulates GSR resistance, we conducted transcriptome and oxylipin profiling using a zmlox5-3 mutant and near-isogenic wild type B73, upon infection with F. graminearum. The results showed that JA biosynthetic pathway genes were highly up-regulated, whereas multiple 9-LOX pathway genes were down-regulated in the infected zmlox5-3 mutant. Furthermore, oxylipin profiling of the mutant revealed significantly higher contents of several jasmonates but relatively lower levels of 9-oxylipins in zmlox5-3 upon infection. In contrast, B73 and W438, a more resistant inbred line, displayed relatively lower levels of JAs, but a considerable increase of 9-oxylipins. These results suggest antagonistic interaction between 9-oxylipins and JAs, wherein 9-oxylipins contribute to resistance while JAs facilitate susceptibility to F. graminearum.

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Section: Resultsmentioning

confidence: 99%

Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot

et al. 2021

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“…In addition, it has been established that ZmWRKY83 is a crucial transcription factor for plant disease resistance [41]. Moreover, using integrated gene co-expression analysis and metabolite profiling, it was discovered that ZmHIR3 likely contributes to disease resistance to GSR, probably through the transcriptional regulation of key genes, functional metabolites, and the control of cell death [42].…”

Section: Discussionmentioning

confidence: 99%

Coronatine-Induced Maize Defense against Gibberella Stalk Rot by Activating Antioxidants and Phytohormone Signaling

Liu,

Sui,

et al. 2023

JoF

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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.

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“…In rice, the NH1/OsNPR1 paralog can enhance disease resistance and hypersensitivity and participate in cell death [ 76 ]. In maize, ZmHIR3 is a hypersensitive response-related gene that increases resistance to Gibberella stalk rot [ 77 ]. We found that hypersensitive and apoptotic processes are likely involved in the response to RBSDV infections in maize.…”

Section: Discussionmentioning

confidence: 99%

Genome-Wide Profiling of Alternative Splicing and Gene Fusion during Rice Black-Streaked Dwarf Virus Stress in Maize (Zea mays L.)

Zhou

Zhang

et al. 2022

Genes

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Rice black-streaked dwarf virus (RBSDV) causes maize rough dwarf disease (MRDD), which is a viral disease that significantly affects maize yields worldwide. Plants tolerate stress through transcriptional reprogramming at the alternative splicing (AS), transcriptional, and fusion gene (FG) levels. However, it is unclear whether and how AS and FG interfere with transcriptional reprogramming in MRDD. In this study, we performed global profiling of AS and FG on maize response to RBSDV and compared it with transcriptional changes. There are approximately 1.43 to 2.25 AS events per gene in maize infected with RBSDV. GRMZM2G438622 was only detected in four AS modes (A3SS, A5SS, RI, and SE), whereas GRMZM2G059392 showed downregulated expression and four AS events. A total of 106 and 176 FGs were detected at two time points, respectively, including six differentially expressed genes and five differentially spliced genes. The gene GRMZM2G076798 was the only FG that occurred at two time points and was involved in two FG events. Among these, 104 GOs were enriched, indicating that nodulin-, disease resistance-, and chloroplastic-related genes respond to RBSDV stress in maize. These results provide new insights into the mechanisms underlying post-transcriptional and transcriptional regulation of maize response to RBSDV stress.

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Integrated Gene Co-expression Analysis and Metabolites Profiling Highlight the Important Role of ZmHIR3 in Maize Resistance to Gibberella Stalk Rot

Cited by 14 publications

References 78 publications

Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot

Transcriptome and Oxylipin Profiling Joint Analysis Reveals Opposite Roles of 9-Oxylipins and Jasmonic Acid in Maize Resistance to Gibberella Stalk Rot

Coronatine-Induced Maize Defense against Gibberella Stalk Rot by Activating Antioxidants and Phytohormone Signaling

Genome-Wide Profiling of Alternative Splicing and Gene Fusion during Rice Black-Streaked Dwarf Virus Stress in Maize (Zea mays L.)

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