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Phosphatidic acid (PA) is an important lipid essential for several aspects of plant development and biotic and abiotic stress responses. We previously suggested that submergence induces PA accumulation in Arabidopsis thaliana ; however, the molecular mechanism underlying PA-mediated regulation of submergence-induced hypoxia signaling remains unknown. Here, we showed that in Arabidopsis, loss of the phospholipase D (PLD) proteins PLDα1 and PLDδ leads to hypersensitivity to hypoxia, but increased tolerance to submergence. This enhanced tolerance is likely due to improvement of PA-mediated membrane integrity. PA bound to the mitogen-activated protein kinase 3 (MPK3) and MPK6 in vitro and contributed to hypoxia-induced phosphorylation of MPK3 and MPK6 in vivo. Moreover, mpk3 and mpk6 mutants were more sensitive to hypoxia and submergence stress compared with wild type, and fully suppressed the submergence-tolerant phenotypes of pldα1 and pldδ mutants. MPK3 and MPK6 interacted with and phosphorylated RELATED TO AP2.12, a master transcription factor in the hypoxia signaling pathway, and modulated its activity. In addition, MPK3 and MPK6 formed a regulatory feedback loop with PLDα1 and/or PLDδ to regulate PLD stability and submergence-induced PA production. Thus, our findings demonstrate that PA modulates plant tolerance to submergence via both membrane integrity and MPK3/6-mediated hypoxia signaling in Arabidopsis. [ABSTRACT FROM AUTHOR]

Summary: Brown planthopper (BPH, Nilaparvata lugens), a highly destructive insect pest, poses a serious threat to rice (Oryza sativa) production worldwide. Jasmonates are key phytohormones that regulate plant defences against BPH; however, the molecular link between jasmonates and BPH responses in rice remains largely unknown. Here, we discovered a Poaceae‐specific metabolite, mixed‐linkage β‐1,3;1,4‐d‐glucan (MLG), which contributes to jasmonate‐mediated BPH resistance. MLG levels in rice significantly increased upon BPH attack. Overexpressing OsCslF6, which encodes a glucan synthase that catalyses MLG biosynthesis, significantly enhanced BPH resistance and cell wall thickness in vascular bundles, whereas knockout of OsCslF6 reduced BPH resistance and vascular wall thickness. OsMYC2, a master transcription factor of jasmonate signalling, directly controlled the upregulation of OsCslF6 in response to BPH feeding. The AT‐rich domain of the OsCslF6 promoter varies in rice varieties from different locations and natural variants in this domain were associated with BPH resistance. MLG‐derived oligosaccharides bound to the plasma membrane‐anchored LECTIN RECEPTOR KINASE1 OsLecRK1 and modulated its activity. Thus, our findings suggest that the OsMYC2‐OsCslF6 module regulates pest resistance by modulating MLG production to enhance vascular wall thickness and OsLecRK1‐mediated defence signalling during rice‐BPH interactions. [ABSTRACT FROM AUTHOR]

In plants, submergence from flooding causes hypoxia, which impairs energy production and affects plant growth, productivity, and survival. In Arabidopsis, hypoxia induces nuclear localization of the group VII ethylene‐responsive transcription factor RELATED TO AP2.12 (RAP2.12), following its dissociation from the plasma membrane‐anchored ACYL‐COA BINDING PROTEIN1 (ACBP1) and ACBP2. Here, we show that polyunsaturated linolenoyl‐CoA (18:3‐CoA) regulates RAP2.12 release from the plasma membrane. Submergence caused a significant increase in 18:3‐CoA, but a significant decrease in 18:0‐, 18:1‐, and 18:2‐CoA. Application of 18:3‐CoA promoted nuclear accumulation of the green fluorescent protein (GFP) fusions RAP2.12‐GFP, HYPOXIA‐RESPONSIVE ERF1‐GFP, and RAP2.3‐GFP, and enhanced transcript levels of hypoxia‐responsive genes. Plants with decreased ACBP1 and ACBP2 (acbp1 ACBP2‐RNAi, produced by ACBP2 RNA interference in the acbp1 mutant) had reduced tolerance to hypoxia and impaired 18:3‐CoA‐induced expression of hypoxia‐related genes. In knockout mutants and overexpression lines of LONG‐CHAIN ACYL‐COA SYNTHASE2 (LACS2) and FATTY ACID DESATURASE 3 (FAD3), the acyl‐CoA pool size and 18:3‐CoA levels were closely related to ERF‐VII‐mediated signaling and hypoxia tolerance. These findings demonstrate that polyunsaturation of long‐chain acyl‐CoAs functions as important mechanism in the regulation of plant hypoxia signaling, by modulating ACBP–ERF‐VII dynamics. [ABSTRACT FROM AUTHOR]