Unraveling the polyamine back-conversion catabolism enigma: the role of AtPAO2 in Arabidopsis resistance to Pseudomonas syringae infection

JASSO ROBLES, FI; ULBRICHOVÁ, M; PIECKENSTAIN, FL; CAVAR ZELIJKOVIK, S; DE DIEGO, N; GONZALEZ, ME; RODRÍGUEZ-KESSLER, M

Oaxaca

Congreso; XX National Plant Biochemistry and Molecular Biology Congress, 3rd Meeting of the Mexico Section of the American Society of Plant Biologists, 13th Mexico-USA Plant Biology Symposium; 2023

Polyamine catabolism, orchestrated by polyamine oxidase enzymes, is crucial in plant defense against pathogen infection. In Arabidopsis, the cellular localization of PAO enzymes (cytoplasm or peroxisomes), the type of catabolism (terminal or back-conversion), and the relation to other signaling pathways through the production of reactive oxygen species make polyamine oxidation relevant to understand plant-pathogen interactions. However, the specific mechanisms and role of polyamine oxidation remain elusive. In this study, we characterized the role of the AtPAO1 and AtPAO2 genes in the Arabidopsis-Pseudomonas syringae pv. tomato DC3000 (Pst) interaction employing PAO single and double mutant lines (Atpao1-1, Atpao2-1 and Atpao1-1x Atpao2-1) and overexpression lines (35S::AtPAO1) by combining high-throughput phenotyping screening, targeted metabolomics, and gene expression analysis. Our results demonstrated that AtPAO1 regulates Arabidopsis resistance by modulating the RBOH (respiratory burst oxidase homolog) activity in the presence or absence of Pst, and that response is influenced by spermine supplementation.Furthermore, we reveal that resistance to Pst relies on the fine tune balance between AtPAOback-conversion and terminal catabolism, which significantly affects the overall AtRBOH activity and the content of various polyamines. Interestingly, we found that peroxisomal polyamine catabolism, mainly through AtPAO2, is the primary regulator of defense agains tPst. Specifically, AtPAO back-conversion facilitates putrescine accumulation, reduction of spermine and conjugated/bound polyamines levels, and increase of specific amino acids, including glutamate, acetylornithine, gamma-aminobutyric acid, beta-alanine, proline, and glycine.These metabolic changes ultimately improve plant resistance. Our study indicates that Pst resistance depends on the plant strategy. Whereas a strong upregulation of terminal catabolism (mainly by cytoplasmic AtPAO1) to produce 1,3-diaminopropane can condition plant resistance, Spm catabolism via back-conversion (by peroxisomal AtPAO2), which conduct to putrescine production, confer resistance.