Multiple genes recruited from hormone pathways partition maize diterpenoid defences

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 - University Of California, San Diego; WANG, QIANG - Sichuan Agricultural University; JI, LEXIANG - University Of Georgia; SCHMITZ, ROBERT - University Of Georgia; KREMLING, KARL - Cornell University; Buckler, Edward - Ed; SHEN, ZHOUXIAN - 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, San Diego; HUGHES, CHAMBERS - University Of San Diego; 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: 9/16/2019
Citation: Ding, Y., Murphy, K., Poretsky, E., Mafu, S., Yang, B., Char, S., Christensen, S.A., Saldivar, E., Wu, M., Wang, Q., Ji, L., Schmitz, R., Kremling, K., Buckler IV, E.S., Shen, Z., Briggs, S., Bohlmann, J., Sher, A., Castro-Falcon, G., Hughes, C., Huffaker, A., Zerbe, P., Schmelz, E. 2019. Multiple genes recruited from hormone pathways partition maize diterpenoid defences. Nature Plants. https://doi.org/10.1038/s41477-019-0509-6.
DOI: https://doi.org/10.1038/s41477-019-0509-6

Interpretive Summary: Duplication and divergence of primary pathway genes underlie the evolution of plant specialized metabolism; however, mechanisms partitioning parallel hormone and defence pathways are often speculative. For example, the primary pathway intermediate ent-kaurene is essential for gibberellin biosynthesis and is also a proposed precursor for maize antibiotics. By integrating transcriptional coregulation patterns, genome-wide association studies, combinatorial enzyme assays, proteomics and targeted mutant analyses, 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 new 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 the circuitous biosynthesis of ent-kaurene-related antibiotics without the production of growth hormone precursors during defence.

Technical Abstract: Maize is frequently attacked by a wide range of fungi including Fusarium that produces a stalk rot. However, maize also naturally produces a wide range of chemical compounds to fight off these fungi. Through a combination of genetics, genomics, and biochemistry, this study identified four new genes and a whole new network of how these genes work together to produce a variety of chemical defenses. Although related chemicals are also important for plant growth, this study determined how the pathways are separated. This study lays the groundwork for understanding how this natural chemistry could be eventually designed to provide a more effective defense of maize and other crops from fungi.