Natural variations of ZmSRO1d modulate the trade-off between drought resistance and yield by affecting ZmRBOHC-mediated stomatal ROS production in maize

While crop yields have historically increased, drought resistance has become a major concern in the context of global climate change. The trade-off between crop yield and drought resistance is a common phenomenon; however, the underlying molecular modulators remain undetermined. Through genome-wide association study, we revealed that three non-synonymous variants in a drought-resistant allele of ZmSRO1d-R resulted in plasma membrane localization and enhanced mono-ADP-ribosyltransferase activity of ZmSRO1d toward ZmRBOHC, which increased reactive oxygen species (ROS) levels in guard cells and promoted stomatal closure. ZmSRO1d-R enhanced plant drought resilience and protected grain yields under drought conditions, but it led to yield drag under favorable conditions. In contrast, loss-of-function mutants of ZmRBOHC showed remarkably increased yields under well-watered conditions, whereas they showed compromised drought resistance. Interestingly, by analyzing 189 teosinte accessions, we found that the ZmSRO1d-R allele was present in teosinte but was selected against during maize domestication and modern breeding. Collectively, our work suggests that the allele frequency reduction of ZmSRO1d-R in breeding programs may have compromised maize drought resistance while increased yields. Therefore, introduction of the ZmSRO1d-R allele into modern maize cultivars would contribute to food security under drought stress caused by global climate change. This study identifies that ZmSRO1d-R, a natural variation of ZmSRO1d, could enhance maize drought resistance through activating ZmRBOHC and promoting ROS production in guard cells. However, it causes yield penalty under normal conditions. Knocking-out ZmRBOHC reduces ROS levels in guard cells and compromises drought resistance but increases the yield. Further analyses indicate that ZmSRO1d-R has been selected-against during maize domestication and modern breeding programs.