Arabidopsis responds to Alternaria alternata volatiles by triggering plastid phosphoglucose isomerase-independent mechanisms

Sánchez-López, Ángela María et al.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.This work was supported by the Comisión Interministerial de Ciencia y Tecnología and Fondo Europeo de Desarrollo Regional, Spain (grant nos. BIO2010–18239 and BIO2013–49125–C2–1–P), by the Government of Navarra (grant no. IIM010491.RI1), by the I-Link0939 project from the Ministerio de Economía y Competitividad, by the Ministry of Education, Youth, and Sports of the Czech Republic (grant no. LO1204 from the National Program of Sustainability), by Palacky University institutional support, by predoctoral fellowships from the Spanish Ministry of Science and Innovation (to A.M.S.-L. and P.G.-G.), and by postdoctoral fellowships from the Public University of Navarra (to M.B. and G.A.).Peer Reviewe