Arabidopsis plants lacking plastid phosphoglucose isomerase respond to microbial volatiles through GLUCOSE-6-P/PHOSPHATE TRANSLOCATOR2 action

Abstract

Recent studies have shown that PGI1 is an important determinant of photosynthesis, growth and starch production, likely as a consequence of its involvement in the synthesis of plastidial isoprenoid compounds such as hormones and photosynthetic pigments (Bahaji et al. 2015; Bahaji et al. 2018). We have shown that volatile compounds (VCs) emitted by microbes promote growth, photosynthesis, and accumulation of cytokinins (CK) and starch (Sánchez-Lopez et al. 2016a). This response was PGI1-independent, as fungal VCs exposed PGI1 null pgi1-2 plants grew faster and accumulated exceedingly higher levels of starch and CKs than plants not exposed to VCs (Sánchez-López et al. 2016b). The most up-regulated gene in leaves of fungal VCs exposed plants was At1g61800, encoding the plastidial GPT2 glucose-6-phosphate (G6P)/phosphate translocator. Whether the response of pgi1-2 to fungal VCs could be due to the GPT2-mediated transport of cytosolic G6P into the chloroplast was investigated by characterizing pgi1-2/gpt2-2 PGI1- and GPT2-null double mutants cultured in the presence or absence of VCs emitted by the fungal phytopathogen Alternaria alternata. We found that photosynthesis, active CKs content, growth and leaf starch content in pgi1-2/gpt2-2 plants exposed to fungal VCs were lower than in VCs exposed WT, gpt2-2 and pgi1-2 plants. Proteomic analyses revealed that fungal VCs strongly up-regulate the expression of proteins involved in photosynthesis in WT, gpt2-2 and pgi1-2 plants, but in much lower extent in pgi1-2/gpt2-2 plants. The overall data show that the combined action of PGI1 and GTP2 is an important determinant of the plant´s response to microbial VCs. The possible involvement of these functions in the production of growth- and foliar metabolism-regulating isoprenoid hormones in heterotrophic organs is discussed.