It is known that volatile emissions from some beneficial rhizosphere microorganisms promote plant growth. Here we show that volatile compounds (VCs) emitted by phylogenetically diverse rhizosphere and non-rhizhosphere bacteria and fungi (including plant pathogens and microbes that do not normally interact mutualistically with plants) promote growth and flowering of various plant species, including crops. In Arabidopsis plants exposed to VCs emitted by the phytopathogen Alternaria alternata, changes included enhancement of photosynthesis and accumulation of high levels of cytokinins (CKs) and sugars. Evidence obtained using transgenic Arabidopsis plants with altered CK status show that CKs play essential roles in this phenomenon, because growth and flowering responses to the VCs were reduced in mutants with CK-deficiency (35S:AtCKX1) or low receptor sensitivity (ahk2/3). Further, we demonstrate that the plant responses to fungal VCs are light-dependent. Transcriptomic analyses of Arabidopsis leaves exposed to A. alternata VCs revealed changes in the expression of light- and CK-responsive genes involved in photosynthesis, growth and flowering. Notably, many genes differentially expressed in plants treated with fungal VCs were also differentially expressed in plants exposed to VCs emitted by the plant growth promoting rhizobacterium Bacillus subtilis GB03, suggesting that plants react to microbial VCs through highly conserved regulatory mechanisms.

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

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 Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University and Institute of Experimental Botany ASCR Olomouc CZ 78371 Czech Republic

Instituto de Agrobiotecnología Iruñako etorbidea 123 31192 Mutiloabeti Nafarroa Spain

Instituto de Agrobiotecnología Iruñako etorbidea 123 31192 Mutiloabeti Nafarroa Spain College of Agronomy and Plant Protection Qingdao Agricultural University 266109 Qingdao China

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University and Institute of Experimental Botany ASCR Olomouc CZ 78371 Czech Republic

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