Arabidopsis Responds to Alternaria alternata Volatiles by Triggering Plastid Phosphoglucose Isomerase-Independent Mechanisms.

Adriana Ricarte-Bermejo, Javier Pozueta-Romero, Edurne Baroja-Fernández, Rosana Navajas, María Carmen Mena, Sergio Ciordia, Karel Doležal, Lukáš Spíchal, Jan F Humplík, Ondřej Novák, Ángela María Sánchez-López, Kinia Ameztoy, Pablo García-Gómez, Goizeder Almagro, Francisco José Muñoz, Jun Li, Marouane Baslam, Nuria De Diego, Abdellatif Bahaji

Journal: Plant physiology 2017;172(3):1989-2001

PMID: 27663407

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Abstract

Volatile compounds (VCs) emitted by phylogenetically diverse microorganisms (including plant pathogens and microbes that do not normally interact mutualistically with plants) promote photosynthesis, growth, and the accumulation of high levels of starch in leaves through cytokinin (CK)-regulated processes. In Arabidopsis (Arabidopsis thaliana) plants not exposed to VCs, plastidic phosphoglucose isomerase (pPGI) acts as an important determinant of photosynthesis and growth, likely as a consequence of its involvement in the synthesis of plastidic CKs in roots. Moreover, this enzyme plays an important role in connecting the Calvin-Benson cycle with the starch biosynthetic pathway in leaves. To elucidate the mechanisms involved in the responses of plants to microbial VCs and to investigate the extent of pPGI involvement, we characterized pPGI-null pgi1-2 Arabidopsis plants cultured in the presence or absence of VCs emitted by Alternaria alternata We found that volatile emissions from this fungal phytopathogen promote growth, photosynthesis, and the accumulation of plastidic CKs in pgi1-2 leaves. Notably, the mesophyll cells of pgi1-2 leaves accumulated exceptionally high levels of starch following VC exposure. Proteomic analyses revealed that VCs promote global changes in the expression of proteins involved in photosynthesis, starch metabolism, and growth that can account for the observed responses in pgi1-2 plants. The overall data show that Arabidopsis plants can respond to VCs emitted by phytopathogenic microorganisms by triggering pPGI-independent mechanisms.

Address: Instituto de Agrobiotecnología, Consejo Superior de Investigaciones Científicas/UPNA/Gobierno de Navarra, 31192 Mutiloabeti, Nafarroa, Spain (A.M.S.-L., A.B., M.B., J.L., F.J.M., G.A., P.G.-G., K.A., A.R.-B., E.B.-F., J.P.-R.).; Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, Olomouc CZ-78371, Czech Republic (N.D.D., J.F.H., L.S., K.D.).; Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, and Institute of Experimental Botany AS CR, Olomouc CZ-78371, Czech Republic (O.N., K.D.); and.; Unidad de Proteómica Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Campus de Cantoblanco, Madrid 28049, Spain (S.C., M.C.M., R.N.).; Instituto de Agrobiotecnología, Consejo Superior de Investigaciones Científicas/UPNA/Gobierno de Navarra, 31192 Mutiloabeti, Nafarroa, Spain (A.M.S.-L., A.B., M.B., J.L., F.J.M., G.A., P.G.-G., K.A., A.R.-B., E.B.-F., J.P.-R.); [email protected].; Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, Olomouc CZ-78371, Czech Republic (N.D.D., J.F.H., L.S., K.D.); [email protected].; Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University, and Institute of Experimental Botany AS CR, Olomouc CZ-78371, Czech Republic (O.N., K.D.); and [email protected].; Unidad de Proteómica Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Campus de Cantoblanco, Madrid 28049, Spain (S.C., M.C.M., R.N.) [email protected].

DOI: 10.1104/pp.16.00945

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MeSH Terms: Alternaria, Arabidopsis, Arabidopsis Proteins, Cell Wall, Cytokinins, Glucose-6-Phosphate Isomerase, Light, Mesophyll Cells, Mutation, Photosynthesis, Plastids, Proteome, Starch, Volatile Organic Compounds