Evolution of a novel and adaptive floral scent in wild tobacco

Guo H, Lackus ND, Köllner TG, Li R, Bing J, Wang Y, Baldwin IT, Xu S

Abstract

Many plants emit diverse floral scents that mediate plant-environment interactions and attain reproductive success. However, how plants evolve biosynthesis of novel and adaptive floral volatiles remains unclear. Here, we show that in the wild tobacco, Nicotiana attenuata, a dominant species-specific floral volatile (benzyl acetone, BA) that attracts pollinators and deters florivore is synthesized by phenylalanine ammonia-lyase 4 (NaPAL4), isoflavone reductase 3 (NaIFR3), and chalcone synthase 3 (NaCHAL3). Transient expression of NaFIR3 alone in N. attenuata leaves is sufficient and necessary for ectopic foliar BA emissions, and co-expressing NaIFR3 with NaPAL4 and NaCHAL3 increased the BA emission levels. Independent changes in transcription of NaPAL4 and NaCHAL3 contributed to intraspecific variations of floral BA emission. However, among species, the gain of expression in NaIFR3 resulted in the biosynthesis of BA that was only found in N. attenuata. This study suggests that novel metabolic pathways associated with adaptation can arise via re-configurations of gene expression.