Horizontally acquired CSP genes contribute to wheat adaptation and improvement

Abstract

Although horizontal gene transfer (HGT) often facilitates environmental adaptation of recipient organisms, whether and how they might affect crop evolution and domestication is unclear. Here we show that three genes encoding cold-shock proteins (CSPs) were transferred from bacteria to Triticeae, a tribe of the grass family that includes several major staple crops such as wheat, barley and rye. The acquired CSP genes in wheat (TaCSPs) are functionally conserved in their bacterial homologues by encoding a nucleic acid-binding protein. Experimental evidence indicates that TaCSP genes positively regulate drought response and improve photosynthetic efficiency under water-deficient conditions by directly targeting a type 1 metallothionein gene to increase reactive oxygen species scavenging, which in turn contributed to the geographic expansion of wheat. We identified an elite CSP haplotype in Aegilops tauschii, introduction of which to wheat significantly increased drought tolerance, photosynthetic efficiency and grain yields. These findings not only provide major insights into the role of HGT in crop adaptation and domestication, but also demonstrate that novel microbial genes introduced through HGT offer a stable and naturally optimized resource for transgenic crop breeding and improvement.