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Phenolic acid-induced phase separation and translation inhibition mediate plant interspecific competition

ABSTRACT: Phenolic acids (PAs) secreted by donor plants suppress the growth of their susceptible plant neighbours. However, how structurally diverse ensembles of PAs are perceived by plants to mediate interspecific competition remains a mystery. Here, we show that a plant stress granule (SG) marker, RNA-BINDING PROTEIN 47B (RBP47B), is a sensor of PAs in Arabidopsis. PAs including salicylic acid (SA), 4-hydroxybenzoic acid, protocatechuic acid, etc. directly bind RBP47B, promote its phase separation and trigger SG formation accompanied by global translation inhibition. SA-induced global translation inhibition depends on RBP47 family members. RBP47s regulate the proteome rather than the absolute quantity of SG. The rbp47 quadruple mutant shows a reduced sensitivity to the inhibitory effect of the PA mixture as well as to that of PA-rich rice when tested in a co-culturing ecosystem. Our study discovers RBP47B as the long sought-after PA sensor and unveils PA-induced SG formation and translation inhibition as one of the PA perception mechanisms.

INSTRUMENT(S): Orbitrap Fusion Lumos

ORGANISM(S): Arabidopsis Thaliana (mouse-ear Cress)

TISSUE(S): Root

SUBMITTER: Zhouli Xie

LAB HEAD: Wei Wang

PROVIDER: PXD043123 | Pride | 2023-08-29

REPOSITORIES: Pride

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Project description:Introduction: Usually whole plant or whole leaf extracts are analyzed to study the chemical ecology of insect-plant interactions. For herbivore species the contact with the leaf surface enables them to estimate the quality of the plant. The relationship between the leaf-surface and leaf-tissue secondary metabolites (SMs) could offer important new insights in insect-plant interactions mediated by SMs. Pyrrolizidine alkaloids (PAs), typical defense chemicals in Jacobaea species, are repellent for generalist herbivores but are attractive to specialists.</br> Objectives: Explore whether the PAs on the leaf surface are a reliable representation of the PAs in the leaf tissue in PA-containing plants.</br> Method: The concentration of individual PAs present on the leaf surface and in the corresponding leaf tissue from 37 genotypes (one plant from each genotype) of an F2 generation of a cross between Jacobaea vulgaris and Jacobaea aquatica was measured by high performance liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS). PAs were removed from the leaf surface by extraction with a slightly acidic aqueous solution.</br> Results: The total amount of PAs present on the surface of the leaves was only 0.015% (range: 0.001-0.163%) of the total amount present in the leaf tissue. Most PAs present in the leaf tissue were also found on the surface, except for jaconine, dehydrojaconine, dehydrojacoline and usaramine N-oxide. Positive correlations between leaf-surface and leaf-tissue concentrations were found for most of the jacobine-like and otosenine-like PAs, but correlations for total PA, senecionine- and erucifoline-like PAs were not significant.</br> Conclusion: These results indicate that PA variation on the leaf surface only partially reflects the PA variation in the leaf tissue. Because most herbivores are affected in a different manner by individual PAs, this result means that the leaf surface does not give a reliable estimate of plant quality to herbivores.

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Phenolic acid-induced phase separation and translation inhibition mediate plant interspecific competition

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