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Background  Drought threatens the food supply of the world population. Dissecting the dynamic responses of plants to drought will be beneficial for breeding drought-tolerant crops, as the genetic controls of these responses remain largely unknown.    Results  Here we develop a high-throughput multiple optical phenotyping system to noninvasively phenotype 368 maize genotypes with or without drought stress over a course of 98 days, and collected multiple optical images, including color camera scanning, hyperspectral imaging, and X-ray computed tomography images. We develop high-throughput analysis pipelines to extract image-based traits (i-traits). Of these i-traits, 10,080 were effective and heritable indicators of maize external and internal drought responses. An i-trait-based genome-wide association study reveals 4322 significant locus-trait associations, representing 1529 quantitative trait loci (QTLs) and 2318 candidate genes, many that co-localize with previously reported maize drought responsive QTLs. Expression QTL (eQTL) analysis uncovers many local and distant regulatory variants that control the expression of the candidate genes. We use genetic mutation analysis to validate two new genes,  ZmcPGM2  and  ZmFAB1A , which regulate i-traits and drought tolerance. Moreover, the value of the candidate genes as drought-tolerant genetic markers is revealed by genome selection analysis, and 15 i-traits are identified as potential markers for maize drought tolerance breeding.    Conclusion  Our study demonstrates that combining high-throughput multiple optical phenotyping and GWAS is a novel and effective approach to dissect the genetic architecture of complex traits and clone drought-tolerance associated genes.    Supplementary Information  The online version contains supplementary material available at 10.1186/s13059-021-02377-0.

Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance