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Transcriptome and oxylipin profiling joint analysis reveals the opposite roles of 9-oxylipins and jasmonic acid in maize resistance to Gibberella stalk rot

ABSTRACT: Gibberella stalk rot (GSR) caused by Fusarium graminearum is one of the devastating diseases causing significant losses to maize production worldwide. Although plant oxylipins have been widely reported as potent signals to activate diverse biotic stress responses, the roles of distinct oxylipin pathway branches initiated by either 9- or 13-lipoxygenases (LOXs) in defense against GSR remain unexplored. In this study, the functional analysis showed that disruption of ZmLOX5, a maize 9-LOX gene, resulted in increased susceptibility to GSR. To identify the key genes and metabolites associated with GSR resistance, we profiled transcriptome and oxylipins in the lox5 mutant and near-isogenic wild type. The results showed that JA biosynthetic pathway genes are highly up-regulated, whereas multiple 9-LOX pathway genes down-regulated in lox5-3 mutant in response to F. graminearum infection. Furthermore, oxylipin profiling of the mutant and corresponding wild type, B73, as well as a more resistant line, W438, uncovered significantly higher contents of JA-isoleucine (JA-Ile) and other jasmonates but relatively lower levels of 9-oxylipins in lox5-3 upon infection. By contrast, resistant line W438 and B73 displayed relatively lower levels of JAs, yet considerable increase of 9-oxylipins. Taken together, these results clearly indicated that the signaling pathways of 9-oxylipins and JAs antagonize each other, and that while ZmLOX5-produced 9-oxylipins contribute to resistance, JAs are likely to function as negative regulator in maize defense against GSR.

ORGANISM(S): Zea mays

PROVIDER: GSE174508 | GEO | 2021/05/17

REPOSITORIES: GEO

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Project description:Plant 9-lipoxygenases (9-LOX) and α-dioxygenases (α-DOX) initiate the synthesis of oxylipins after bacterial infection. Here, the role of these enzymes in plant’s defense was investigated using individual Arabidopsis thaliana lox1 and dox1 mutants and a double lox1 dox1 mutant. Studies with Pseudomonas syringae pv tomato (Pst) revealed the enhanced susceptibility of lox1 to the virulent strain Pst DC3000 and the partial impairment of lox1 and dox1 mutants to activate systemic acquired resistance. Notably, both defects were enhanced in the lox1 dox1 plants as compared with individual mutants. We found that pre-treatment with 9-LOX- and -DOX-generated oxylipins protected plant tissues against bacterial infection. The strongest effect in this respect was exerted by 9-ketooctadecatrienoic acid (9-KOT), which is produced from linolenic acid by 9-LOX. Quantification of 9-KOT revealed its accumulation after bacterial infection. The levels were reduced in lox1 and lox1 dox1 plants but strongly increased in the dox1 mutant due to metabolic interaction of the two pathways. Transcriptional analyses indicated that 9-KOT pre-treatment modifies hormone homeostasis during bacterial infection. The nature of the changes detected suggested that 9-KOT interfers the hormonal changes caused by bacterial effectors. This notion was substantiated by the finding that 9-KOT failed to reduce the growth of PstDC3000hrpA, a mutant compromised in effector secretion, and of the avirulent strain Pst DC3000 avrRpm1. Further support to the action of the 9-LOX- and -DOX-oxylipin pathways as modulators of hormone homeostasis was the observation that lox1 dox1 seedlings are hypersensitive to the growth-inhibitory effect of ABA and showed enhanced activation of ABA-inducible marker genes. Two experiments, Col-0 treated with 9-KOT vs. Col-0 treated with water and Col-0 treated with 9-KOT vs. Col-0 treated with water after treatment with Pst DC3000. Biological replicates: 4 control replicates treated , 4 9-KOT treated replicates; 4 control treated and Pst DC3000 replicates and 4 9-KOT treated and Pst DC3000 replicates

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Transcriptome and oxylipin profiling joint analysis reveals the opposite roles of 9-oxylipins and jasmonic acid in maize resistance to Gibberella stalk rot

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