Glucose-6-P/phosphate translocator2 mediates the phosphoglucose-isomerase1-independent response to microbial volatiles.

Samuel Gámez-Arcas, Francisco José Muñoz, Adriana Ricarte-Bermejo, Ángela María Sánchez-López, Marouane Baslam, Edurne Baroja-Fernández, Abdellatif Bahaji, Goizeder Almagro, Nuria De Diego, Karel Doležal, Ondřej Novák, Jesús Leal-López, Rafael Jorge León Morcillo, Araceli G Castillo, Javier Pozueta-Romero

Journal: Plant physiology 2022;190(4):2137-2154

PMID: 36111879

Abstract

In Arabidopsis (Arabidopsis thaliana), the plastidial isoform of phosphoglucose isomerase (PGI1) mediates photosynthesis, metabolism, and development, probably due to its involvement in the synthesis of isoprenoid-derived signals in vascular tissues. Microbial volatile compounds (VCs) with molecular masses of <45 Da promote photosynthesis, growth, and starch overaccumulation in leaves through PGI1-independent mechanisms. Exposure to these compounds in leaves enhances the levels of GLUCOSE-6-PHOSPHATE/PHOSPHATE TRANSLOCATOR2 (GPT2) transcripts. We hypothesized that the PGI1-independent response to microbial volatile emissions involves GPT2 action. To test this hypothesis, we characterized the responses of wild-type (WT), GPT2-null gpt2-1, PGI1-null pgi1-2, and pgi1-2gpt2-1 plants to small fungal VCs. In addition, we characterized the responses of pgi1-2gpt2-1 plants expressing GPT2 under the control of a vascular tissue- and root tip-specific promoter to small fungal VCs. Fungal VCs promoted increases in growth, starch content, and photosynthesis in WT and gpt2-1 plants. These changes were substantially weaker in VC-exposed pgi1-2gpt2-1 plants but reverted to WT levels with vascular and root tip-specific GPT2 expression. Proteomic analyses did not detect enhanced levels of GPT2 protein in VC-exposed leaves and showed that knocking out GPT2 reduced the expression of photosynthesis-related proteins in pgi1-2 plants. Histochemical analyses of GUS activity in plants expressing GPT2-GUS under the control of the GPT2 promoter showed that GPT2 is mainly expressed in root tips and vascular tissues around hydathodes. Overall, the data indicated that the PGI1-independent response to microbial VCs involves resetting of the photosynthesis-related proteome in leaves through long-distance GPT2 action.

© The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists.

Address: Instituto de Agrobiotecnología (IdAB), CSIC-Gobierno de Navarra, Iruñako etorbidea 123, 31192 Mutiloabeti, Nafarroa, Spain.; Laboratory of Biochemistry, Faculty of Agriculture, Niigata University, Niigata 950-2181, Japan.; Centre of Region Haná for Biotechnological and Agricultural Research, Czech Advanced Technology and Research Institute, Olomouc, Czech Republic.; Department of Chemical Biology, Faculty of Science, Palacký University, Olomouc CZ-78371, Czech Republic.; Laboratory of Growth Regulators, Faculty of Science of Palacký University and Institute of Experimental Botany of the Czech Academy of Sciences, Olomouc CZ-78371, Czech Republic.; Institute for Mediterranean and Subtropical Horticulture "La Mayora" (IHSM), CSIC-UMA, 29010 Málaga, Spain.
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