ENO2 activity is required for the development and reproductive success of plants, and is feedback-repressed by AtMBP-1

Enolases are key glycolytic enzymes that are highly conserved in prokaryotic and eukaryotic organisms, and are among the most abundant cytosolic proteins. In this study we provide evidence that activity of the enolase ENO2 is essential for the growth and development of plants. We show that Arabidopsis plants with compromised ENO2 function, which were generated by mutating the LOS2/ENO2 locus, have severe cellular defects, including reduced cell size and defective cell differentiation with restricted lignification. At the tissue and organ level LOS2/ENO2-deficient plants are characterized by the reduced growth of shoots and roots, altered vascular development and defective secondary growth of stems, impaired floral organogenesis and defective male gametophyte function, resulting in embryo lethality as well as delayed senescence. These phenotypes correlate with reduced lignin and increased salicylic acid contents as well as altered fatty acid and soluble sugar composition. In addition to an enolase the LOS2/ENO2 locus encodes the transcription factor AtMBP-1, and here we reveal that this bifunctionality serves to maintain the homeostasis of ENO2 activity. In summary, we show that in plants enolase function is required for the formation of chorismate-dependent secondary metabolites, and that this activity is feedback-inhibited by AtMBP-1 to enable the normal development and reproductive success of plants. Significance Statement Enolases are key glycolytic enzymes that are highly conserved in prokaryotic and eukaryotic organisms and are among the most abundant cytosolic proteins. In this study we show that function of the enolase LOS2/ENO2 is essential for the growth and development of plants and is feed-back inhibited by the transcription factor AtMB-1 that is alternatively translated from the LOS2 locus.