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Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity

Nature Plants volume 6, pages 1375–1388 (2020)Cite this article

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Abstract

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.

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Fig. 1: A genetically variable cluster of four maize TPSs ensures the production of ZX precursors.
Fig. 2: Zx gene cluster II contains three 71Z-family cytochrome (CYP) P450s that catalyse the production of A- and D-series ZXs.
Fig. 3: Association mapping reveals that Zx gene cluster III contains three CYP81A-family P450s.
Fig. 4: Enzyme coexpression defines the role of Zx gene cluster III in antibiotic biosynthesis.
Fig. 5: ZX-pathway activation occurs during the large-scale reprograming of fungal-induced defences.
Fig. 6: The maize ZX pathway is a biosynthetic hourglass with genetic redundancy and enzyme promiscuity that ensures the production of protective antibiotic cocktails.

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Data availability

Publicly available datasets used in the study include the National Center for Biotechnology Information (NCBI) Sequence Read Archive project ID SRP115041 and the MaizeGDB BLAST database (https://maizegdb.org/popcorn/main/index.php). Raw read sequences have been deposited at the NCBI Gene Expression Omnibus under accession numbers GSE138961 and GSE138962. Raw sequence data from the root microbiome are available at NCBI BioProject under accession number PRJNA580260. Raw proteomic mass spectra have been deposited at the Mass Spectrometry Interactive Virtual Environment repository (ftp://massive.ucsd.edu/MSV000084285). Maize-related germplasm used in this research have been previously described27,39,43,44,45,72,73 and can be obtained from US Department of Agriculture Germplasm Resources Information Network (https://www.ars-grin.gov) and the Maize Genetics Cooperation Stock Center (http://maizecoop.cropsci.uiuc.edu). Where possible, gene identifiers used throughout the manuscript were in reference to B73 RefGen_v4 (https://www.maizegdb.org/genome/assembly/Zm-B73-REFERENCE-GRAMENE-4.0), which was used as a foundation for the study. All data are available from the corresponding author on request.

Code availability

For the gene-duplication date estimations, scripts to perform translations, alignments and backtranslations as well as data files and BEAST control files have been deposited at GitHub (https://github.com/TomJKono/Zealexin_Dating).

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Acknowledgements

We thank A. Steinbrenner, J. Chan, K. O’Leary, M. Broemmer, H. Riggleman, S. Reyes and S. Delgado for help with planting, treatments and sampling (UCSD); L. Smith (UCSD) for shared UCSD Biology Field Station management; B. Hamberger (Michigan State University) for the ElHMGR gene. This work was partially supported by the USDA-ARS National Programs for Food Safety and Plant Genetic Resources, Genomics and Genetic Improvement (to M.M.V., M.G.B. and S.A.C.). Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. Research was supported by grants from the National Science Foundation, Division of Integrative Organismal Systems (NSF-IOS) (grant no. 1936492 to B.Y. and grant no. 1546899 to S.P.B.), USDA NIFA AFRI (grant no. 2018-67013-28125 to A.H. and E.S.) for sesquiterpenoids, NSF Plant-Biotic Interactions Program (grant no. 1758976 to E.S. and P.Z.) for diterpenoids, NSF Faculty Early Career Development Program (grant no. 1943591 to A.H.), the DOE Joint Genome Institute Community Science Program (JGI-CSP) (grant nos. CSP 2568 (to P.Z., J.B., E.S. and A.H.) and CSP 503420 (to A.H. and E.S.)) and fellowships provided by the NSF Graduate Research Fellowship Program (to K.M.M.), the U.C. Davis Innovation Institute for Food and Health (IIFH) Fellowship Program (to K.M.M. and P.Z.), the USDA NIFA Predoctoral Fellowship Program (award no. 2019-67011-29544, to K.M.M.) and a Fulbright Research Grant (E0581299, to M.B.).

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Author notes

  1. These authors contributed equally: Yezhang Ding, Philipp R. Weckwerth.

Authors and Affiliations

  1. Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, CA, USA

    Yezhang Ding, Philipp R. Weckwerth, Elly Poretsky, Evan Saldivar, Anh-dao Tong, Zhouxin Shen, Ahmed S. Khalil, Mariam Betsiashvili, Keini Dressano, Steven P. Briggs, Eric A. Schmelz & Alisa Huffaker

  2. Department of Plant Biology, University of California Davis, Davis, CA, USA

    Katherine M. Murphy & Philipp Zerbe

  3. ETH Zurich, Institute of Agricultural Sciences, Zurich, Switzerland

    James Sims

  4. Chemistry Research Unit, Center for Medical, Agricultural and Veterinary Entomology, Department of Agriculture, Agricultural Research Service, Gainesville, FL, USA

    Shawn A. Christensen

  5. Division of Plant Sciences, Bond Life Sciences Center, University of Missouri, Columbia, MO, USA

    Si Nian Char & Bing Yang

  6. Donald Danforth Plant Science Center, St Louis, MO, USA

    Bing Yang

  7. Department of Plant Breeding and Genetics, Cornell University, Ithaca, NY, USA

    Karl A. Kremling & Edward S. Buckler

  8. Robert W. Holley Center for Agriculture and Health, Ithaca, US Department of Agriculture, Agricultural Research Service, New York, NY, USA

    Edward S. Buckler

  9. Minnesota Supercomputing Institute, University of Minnesota, Minneapolis, MN, USA

    Tom Kono

  10. University of Tennessee Health Science Center, Memphis, TN, USA

    David R. Nelson

  11. Michael Smith Laboratories, University of British Columbia, Vancouver, British Columbia, Canada

    Jörg Bohlmann

  12. National Center for Agricultural Utilization Research, US Department of Agriculture, Agricultural Research Service, Peoria, IL, USA

    Matthew G. Bakker & Martha M. Vaughan

  13. Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada

    Matthew G. Bakker

  14. Max Planck Institute for Chemical Ecology, Jena, Germany

    Tobias G. Köllner

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Contributions

Y.D., P.R.W., E.P., P.Z., J.S., J.B., K.D., E.A.S. and A.H. designed the experiments and analysed the data. Y.D., E.P., S.A.C., T.G.K., P.Z., K.A.K. and E.S.B. designed, performed and analysed the transcriptome data. Y.D., E.S., A.S.K., K.M.M., P.Z., A.H. and E.A.S. performed MS experiments and MS-related metabolite data analysis. Y.D., E.S., K.M.M., P.Z., E.A.S. and A.H. performed and analysed the enzyme coexpression data. Z.S., A.-D.T. and S.P.B. analysed the combined proteome and transcriptome dataset. T.K. calculated estimates of gene evolution dates. D.R.N. assigned subfamily names for P450 proteins. M.M.V. and M.G.B. generated and analysed the root microbiome data. B.Y., S.N.C. and P.R.W. designed gRNA constructs and generated the zx1 zx2 zx3 and zx1 zx2 zx3 zx4 maize mutants. J.S. and M.B. performed metabolite purifications and analysed the NMR data. Y.D. and P.R.W. performed the in vitro and in vivo antibiotic resistance assays. Y.D., P.R.W., E.P., P.Z., E.A.S. and A.H. wrote the manuscript with input from all of the authors.

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Correspondence to Alisa Huffaker.

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Ding, Y., Weckwerth, P.R., Poretsky, E. et al. Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity. Nat. Plants 6, 1375–1388 (2020). https://doi.org/10.1038/s41477-020-00787-9

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