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Downregulation of polyphenol oxidase in potato tubers redirects phenylpropanoid metabolism enhancing chlorogenate content and late blight resistance

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Abstract

Land plants synthesize phenolic compounds involved in plant defense against invading pathogens through the phenylpropanoid pathway. Although not considered as part of the phenylpropanoid pathway, plant polyphenol oxidases (PPOs) are enzymes that catalyze cresolase and catecholase reactions on several phenolic compounds. Here, transgenic potato (Solanum tuberosum) tubers with downregulated PPO genes (-PPO) were challenged with the oomycete pathogen Phytophthora infestans to investigate the interactions between PPO, phenylpropanoid metabolism, and disease resistance. We found that pathogen invasiveness was reduced in -PPO lines, while microscopic evidences suggested that the mechanism underlying the defense response involved the participation of phenolic compounds. Detailed metabolite-profiling analyses demonstrated that the concentration of metabolites related to the phenylpropanoid pathway and chlorogenate in particular was largely altered in PPO-downregulated tubers. Silencing of PPO caused a shift in metabolism from phenylpropanoid precursors to downstream phenylpropanoid products. The presented results suggest that downregulation of PPO redirects the phenylpropanoid metabolism leading to the accumulation of defensive phenolic compounds in the plant cells, consequently enhancing resistance to the pathogen. These results emphasize the importance of components acting in parallel to canonical metabolic pathway constituents in influencing plant metabolism and reveal new scenarios for modulating the levels of phenolics in crops.

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Acknowledgments

We thank A. Andreu and F. Mauch for kindly providing the P. infestans and P. infestans-GFP strains, respectively. We thank C. Cvitanich and E. Orlowska for valuable experimental advice, and also M. A. Phillips, M. E. Segretin, and D. Caparrós-Ruiz for their critical analysis of the manuscript. This work was funded by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad de Buenos Aires (UBA), and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Argentina. Additional support was received from Coimbra Group and Wood-Whelan research fellowships from the International Union of Biochemistry and Molecular Biology (IUBMB).

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Authors and Affiliations

  1. Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, 08034, Barcelona, Spain

    Briardo Llorente

  2. Instituto de Investigaciones en Ingeniería Genética y Biología Molecular Dr. Hector N. Torres (INGEBI), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), C1428ADN, Buenos Aires, Argentina

    Briardo Llorente, Mirtha M. Flawiá, Guillermo D. Alonso & Fernando Bravo-Almonacid

  3. Instituto de Biotecnología, Instituto Nacional de Tecnología Agrícola, B1712WAA, Castelar, Argentina

    Mariana G. López & Fernando Carrari

  4. Departamento de Bioquímica Clínica, Facultad de Ciencias Químicas, CIBICI-CONICET, Universidad Nacional de Córdoba, X5000HUA, Córdoba, Argentina

    Ramón Asís & Romina D. Di Paola Naranjo

  5. Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EGA, Buenos Aires, Argentina

    Mirtha M. Flawiá & Guillermo D. Alonso

  6. Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, B1876BXD, Bernal, Argentina

    Fernando Bravo-Almonacid

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  1. Briardo Llorente
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  2. Mariana G. López
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Llorente, B., López, M.G., Carrari, F. et al. Downregulation of polyphenol oxidase in potato tubers redirects phenylpropanoid metabolism enhancing chlorogenate content and late blight resistance. Mol Breeding 34, 2049–2063 (2014). https://doi.org/10.1007/s11032-014-0162-8

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