Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity

• Published in: Nature plants Vol. 6; no. 11; pp. 1375 - 1388
• Main Authors: Ding, Yezhang, Weckwerth, Philipp R., Poretsky, Elly, Murphy, Katherine M., Sims, James, Saldivar, Evan, Christensen, Shawn A., Char, Si Nian, Yang, Bing, Tong, Anh-dao, Shen, Zhouxin, Kremling, Karl A., Buckler, Edward S., Kono, Tom, Nelson, David R., Bohlmann, Jörg, Bakker, Matthew G., Vaughan, Martha M., Khalil, Ahmed S., Betsiashvili, Mariam, Dressano, Keini, Köllner, Tobias G., Briggs, Steven P., Zerbe, Philipp, Schmelz, Eric A., Huffaker, Alisa
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.11.2020; Nature Publishing Group
• Subjects: 631/1647/2017; 631/1647/296; 631/1647/320; 631/449/1870; 631/449/2169; Anti-Bacterial Agents - biosynthesis; Antibiotics; Biomedical and Life Sciences; Biosynthesis; Cereal crops; Corn; Disease resistance; Disease Resistance - genetics; Disease Resistance - physiology; Enzymes; Gene Expression Profiling; Genes, Plant - genetics; Genes, Plant - physiology; Immunity, Innate - genetics; Life Sciences; Metabolic Networks and Pathways - genetics; Metabolites; Metabolomics; Multigene Family - genetics; Multigene Family - physiology; Phenotypes; Plant Sciences; Proteomics; Zea mays - genetics; Zea mays - immunology; Zea mays - metabolism; Zea mays - microbiology
• ISSN: 2055-0278; 2055-0278
• DOI: 10.1038/s41477-020-00787-9

Specialized metabolites constitute key layers of immunity that underlie disease resistance in crops; however, challenges in resolving pathways limit our understanding of the functions and applications of these metabolites. In maize ( Zea mays ), the inducible accumulation of acidic terpenoids is increasingly considered to be a defence mechanism that contributes to disease resistance. Here, to understand maize antibiotic biosynthesis, we integrated association mapping, pan-genome multi-omic correlations, enzyme structure–function studies and targeted mutagenesis. We define ten genes in three zealexin ( Zx ) gene clusters that encode four sesquiterpene synthases and six cytochrome P450 proteins that collectively drive the production of diverse antibiotic cocktails. Quadruple mutants in which the ability to produce zealexins (ZXs) is blocked exhibit a broad-spectrum loss of disease resistance. Genetic redundancies ensuring pathway resiliency to single null mutations are combined with enzyme substrate promiscuity, creating a biosynthetic hourglass pathway that uses diverse substrates and in vivo combinatorial chemistry to yield complex antibiotic blends. The elucidated genetic basis of biochemical phenotypes that underlie disease resistance demonstrates a predominant maize defence pathway and informs innovative strategies for transferring chemical immunity between crops. In maize, a comprehensive set of approaches enabled the authors to analyse the biosynthetic pathway of the zealexin group of terpenoids and characterize the role of these antibiotic compounds in disease resistance.