Genomic Basis Underlying The Metabolome-mediated Drought Adaptation Of Maize

Maize(Zea mays L.)is one of the most important crops and its production is threated by drought.It is of great significance to dissect the genetic architecture and the molecular mechanism for breeding of drought-tolerant maize.However,there is very limited knowledge of plant drought response and drought-tolerance mechanism.Metabolism is a bridge connecting the genetic variance(and/or gene expression)and phenotypes/traits.The complex agronomic traits could be divided into metabolic traits,which could be very helpful for people to dissect the genetic control of these complex traits.However,there is no such metabolic studies of crop drought responses at population level.Here,we performed non-targeted metabolic profiling of 385 maize natural inbred lines grown under well-watered(WW)as well as drought-stressed(DS)conditions.A total of3890 metabolites were detected and 1035 were identified as differentially-produced metabolites in drought.Combing genetic variances and transcriptome profiles of this population,we constructed gene-metabolite networks under WW and DS conditions by using multiple statistical methods such as m GWAS,correlation analysis,network analysis,and e QTL analysis.These results indicated the complex genetic control of maize drought responses.Moreover,we observed that there were more hub g enes(a hub gene:associated/correlated with more than 6 metabolites)detected in networks under DS conditions as compared with the ones under WW conditions,and that the hub genes from DS networks were more explainable and meaningful as regarding to the drought responses.Furthermore,two hub genes detected under DS conditions,Zm Bx12 and Zm GLK44,were selected for deep study in maize drought response.Zm Bx12 encodes an Omethyltransferase,which is an important enzyme in DIMBOA biosynthesis pathway.In the coding region of Zm Bx12,we detected a CACTA transposon insertion that improved DIMBOA accumulation and reduced the drought tolerance.The insertion has been strongly selected during the spreading of maize from the tropic regions to the temperate ones.Zm GLK44 encodes a Golden 2-like transcription factor.Zm GLK44 promoted the expression of TSB2,a tryptophan synthase,which in turn enhanced the production of tryptophan in maize under drought conditions.Zm GLK44 transgenic plants showed higher tryptophan accumulation and increased drought tolerance as compare with its negative siblings,while,there was no significant difference between the positive and negative transgenic plants under WW conditions.Moreover,spraying exogenous tryptophan improved the tolerance of maize with different genotypes to drought,indicating the potential of tryptophan as a chemical regulator in drought response.In conclusion,we utilized untargeted metabolomic data to dissect the genetic control of maize drought tolerance based on a large population,and detected a large amount of potential metabolic and genetic targets for drought-tolerance breeding.Our work also demonstrated that metabolomics is a powerful tool to dissect the genetic control of plant complex traits.