Genetic elucidation of complex biochemical traits in crop innate immunity

Authors: DING, YEZHANG - University Of California, San Diego; WECKWERTH, PHILIPP - University Of California, San Diego; PORETSKY, ELLY - University Of California, San Diego; MURPHY, KATHERINE - University Of California, Davis; SIMS, JAMES - Eth Zurich; SALDIVAR, EVAN - University Of California, San Diego; Christensen, Shawn; YANG, BING - University Of Missouri; CHAR, SI NIAN - University Of Missouri; TONG, ANH-DAO - University Of California, San Diego; SHEN, ZHOUXIN - University Of California, San Diego; KREMLING, KARL - Cornell University; BUCKLER, EDWARD - Cornell University; KONO, TOM - University Of Minnesota; NELSON, DAVID - University Of Tennessee; BOHLMAN, JORG - University Of British Columbia; Bakker, Matthew; Vaughan, Martha; KHALIL, AHMED - University Of California, San Diego; BETSIASHVILI, MARIAM - University Of California, San Diego; BRIGGS, STEVEN - University Of California, San Diego; ZERBE, PHILIPP - University Of California, Davis; SCHMELZ, ERIC - University Of California, San Diego; HUFFAKER, ALISA - University Of California, San Diego

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 8/14/2020
Publication Date: 3/5/2021
Citation: Ding, Y., Weckwerth, P., Poretsky, E., Murphy, K.M., Sims, J., Saldivar, E., Christensen, S.A., Yang, B., Char, S., Tong, A., Shen, Z., Kremling, K.A., Buckler, E.S., Kono, T., Nelson, D.R., Bohlman, J., Bakker, M.G., Vaughan, M.M., Khalil, A.S., Betsiashvili, M., Briggs, S.P., Zerbe, P., Schmelz, E.A., Huffaker, A. 2021. Genetic elucidation of complex biochemical traits in crop innate immunity. bioRxiv. https://doi.org/10.1101/2020.03.04.977355.
DOI: https://doi.org/10.1101/2020.03.04.977355

Interpretive Summary: Losses in corn production due to microbial pathogens can result in billions of dollars in lost revenue annually. Despite these great economic losses, only a limited amount of research has demonstrated how corn can defend itself against pathogens using innate antibiotics. Scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL in collaboration with researchers at the University of California at San Diego have identified several new corn-produced compounds that exhibit antibiotic activity. These compounds are termed zealexins (Zx). In our study, genetic testing demonstrated that the antibiotic compounds and the genes that produce them play a significant role in disease resistance. Knowledge from these analyses will contribute to breeding practices that can incorporate these antibiotics into maize for greater disease protection, thus to alleviate large economic losses resulting from microbial-based threats to corn production.

Technical Abstract: Specialized metabolites provide key layers of innate immunity underlying crop resistance; however, challenges in resolving pathways limit the understanding of functions and applications. To understand maize (Zea mays) terpenoid antibiotics underlying disease resistance we integrated large-scale omic correlations, association mapping, enzyme-structure function studies and targeted mutagenesis. Three zealexin (Zx) gene clusters comprised of four sesquiterpene synthases (Zx1-4) and six cytochrome P450s (CYP) in the CYP71Z (Zx5-7) and CYP81A (Zx8-10) families drive the production of diverse antibiotic cocktails. Gene duplications, ensuring pathway resiliency to single null mutations, are combined with enzyme substrate-promiscuity to create a biosynthetic hourglass pathway utilizing diverse substrates to yield complex combinatorial mixtures. Zx pathway activation mediating pathogen resistance occurs during a dramatic reorganization of 50% of the measurable proteome and suppression of constitutive defense pathways. The elucidated genetic basis of complex biochemical phenotypes mediating disease resistance informs innovative strategies for transferring durable chemical immunity between crops.