Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity

Authors: DING, YEZHANG - University Of California, San Diego; MURPHY, KATHERINE - University Of California, Davis; PORETSKY, ELLY - University Of California, San Diego; MAFU, SIBONGILE - University Of California, Davis; YANG, BING - Iowa State University; CHAR, SI NIAN - Iowa State University; Christensen, Shawn; SALDIVAR, EVAN - University Of California, San Diego; WU, MENGXI - Sichuan Agricultural University; WANG, QIANG - Sichuan Agricultural University; JI, LEXIANG - University Of Georgia; SCHMITZ, ROBERT - University Of Georgia; KREMLING, KARL - Cornell University; BUCKLER, EDWARD - Cornell University; SHEN, ZHOUXIN - University Of California, San Diego; BRIGGS, STEVEN - University Of California, San Diego; BOHLMANN, JORG - University Of British Columbia; SHER, ANDREW - University Of California, San Diego; CASTRO-FALCON, GABRIEL - University Of California; HUGHES, CHAMBERS - University Of California; HUFFAKER, ALISA - University Of California, San Diego; ZERBE, PHILIPP - University Of California, Davis; SCHMELZ, ERIC - University Of California, San Diego

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/26/2019
Publication Date: 10/26/2020
Citation: Ding, Y.; Murphy, K.M.; Poretsky, E.; Mafu, S.; Yang, B.; Char, S.; Christensen, S.A.; Saldivar, E.; Wu, M.; Wang, Q.; Ji, L.; Schmitz, R.J.; Kremling, K.A.; Buckler, E.S.; Shen, Z.; Briggs, S.P.; Bohlmann, J.; Sher, A.; Castro-Falcon, G.; Hughes, C.C.; Huffaker, A.; Zerbe, P.; Schmelz, E.A. 2020. Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity. Nature Plants. 6(11):1375-1388. https://doi.org/10.1038/s41477-020-00787-9.
DOI: https://doi.org/10.1038/s41477-020-00787-9

Interpretive Summary: Corn production losses due to biological threats such as microbial pathogens result in billions of dollars in lost revenue annually. Despite these economic losses, little is known about how corn plants can defend themselves against these threats. Scientists at the USDA-ARS Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL in collaboration with researchers at the University of California at San Diego have identified a means by which corn plants defend themselves against fungal pathogens by discovering new antibiotic molecules, termed kauralexins (KAs), and the genes responsible for their production. KAs are produced by the plant in response to fungal contamination as a means to kill the fungus. Interestingly, the production of KAs comes from the same source that makes gibberellins, plant hormones responsible for growth and development. Collectively, these findings help researchers understand that sources responsible for growth and development can evolve to produce antibiotics for defense against microbes. A more detailed future elucidation of all the specific genes involved in the production of KAs may contribute to molecular breeding practices that will make corn plants more resistant to biological threats like pathogens, thus alleviating large economic losses that corn growers experience because of these threats.

Technical Abstract: Duplication and divergence of primary pathway genes underlies the evolutionary expansion of plant specialized metabolism; however, mechanisms partitioning parallel hormone and defense pathways often remain speculative. For example, the primary pathway precursor ent-kaurene is both required for gibberellin biosynthesis and a proposed intermediate for maize antibiotics. By integrating transcriptional co-regulation patterns, Genome Wide Association Mapping Studies, combinatorial enzyme assays, proteomics and targeted mutant analysis, we show that maize kauralexin biosynthesis proceeds via the positional isomer ent-isokaurene formed by a diterpene synthase pair recruited from gibberellin metabolism. The oxygenation and subsequent desaturation of ent-isokaurene by three promiscuous Cytochrome P450s and a novel steroid 5a reductase indirectly yields predominant ent-kaurene-associated antibiotics required for Fusarium stalk rot resistance. The divergence and differential expression of pathway branches derived from multiple duplicated hormone-metabolic genes minimizes dysregulation of primary metabolism via circuitous biosynthesis of ent-kaurene-related antibiotics that avoids the production of growth hormone precursors during defense.