Eleven biosynthetic genes explain the majority of natural variation in carotenoid levels in maize grain

Authors: DIEPENBROCK, CHRISTINE - University Of California, Davis; ILUT, DANIEL - Cornell University; MAGALLANES-LUNDBACK, MARIA - Michigan State University; KANDIANIS, CATHERINE - Cornell University; LIPKA, ALEXANDER - University Of Illinois; Bradbury, Peter; Holland, Jim - Jim; HAMILTON, JOHN - Michigan State University; WOOLDRIDGE, EDMUND - Michigan State University; VAILLANCOURT, BRIEANNE - Michigan State University; GÓNGORA-CASTILLO, ELSA - Michigan State University; WALLACE, JASON - University Of Georgia; CEPELA, JASON - Michigan State University; MATEOS-HERNANDEZ, MARIA - Purdue University; OWENS, BRENDA - Purdue University; TIEDE, TYLER - Purdue University; Buckler, Edward - Ed; ROCHEFORD, TORBERT - Purdue University; BUELL, C ROBIN - Michigan State University; GORE, MICHAEL - Cornell University; DELLAPENNA, DEAN - Michigan State University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/26/2021
Publication Date: 4/1/2021
Citation: Diepenbrock, C.H., Ilut, D.C., Magallanes-Lundback, M., Kandianis, C.B., Lipka, A.E., Bradbury, P., Holland, J.B., Hamilton, J.P., Wooldridge, E., Vaillancourt, B., Góngora-Castillo, E., Wallace, J.G., Cepela, J., Mateos-Hernandez, M., Owens, B.F., Tiede, T., Buckler IV, E.S., Rocheford, T., Buell, C., Gore, M.A., Dellapenna, D. 2021. Eleven biosynthetic genes explain the majority of natural variation in carotenoid levels in maize grain. The Plant Cell. 33(4):882–900. https://doi.org/10.1093/plcell/koab032.
DOI: https://doi.org/10.1093/plcell/koab032

Interpretive Summary: Grain carotenoids, including provitamin A compounds, are important for human health. Breeding strategies relevant to these compounds have thus far focused largely on two genes that strongly affect provitamin A levels. To accelerate breeding efforts in this area and fine-tune multi-nutrient breeding strategies for carotenoid-dense maize, a more comprehensive dissection of the genetic basis of carotenoid traits is needed. We identified 11 genes in the precursor and core carotenoid pathways, and one involved in carotenoid degradation, as contributors to natural variation for one or more carotenoid traits. Together the identified genes explained more than 70% of the genetic contribution to the variation in the carotenoid traits investigated. The results of this study will directly inform breeding efforts for multiple carotenoid traits that are important for improved human nutritional status. Two to five major genes were identified per trait which provide clear breeding targets.

Technical Abstract: Vitamin A deficiency remains prevalent in parts of Asia, Latin America and sub-Saharan Africa where maize is a food staple. Extensive natural variation exists for carotenoids in maize grain; to understand its genetic basis, we conducted a joint linkage and genome-wide association study in the U.S. maize nested association mapping panel. Eleven of the 44 detected quantitative trait loci (QTL) were resolved to individual genes. Six of these were expression QTL (eQTL), showing strong correlations between RNA-seq expression abundances and QTL allelic effect estimates across six stages of grain development. These six eQTL also had the largest percent phenotypic variance explained, and in major part comprised the three to five loci capturing the bulk of genetic variation for each trait. Most of these eQTL had highly correlated QTL allelic effect estimates across multiple traits, suggesting that pleiotropy within this pathway is largely regulated at the expression level. Significant pairwise epistatic interactions were also detected. These findings provide the most comprehensive genome-level understanding of the genetic and molecular control of carotenoids in any plant system, and a roadmap to accelerate breeding for provitamin A and other priority carotenoid traits in maize grain that should be readily extensible to other cereals.