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A gene encoding maize caffeoyl-CoA O-methyltransferase confers quantitative resistance to multiple pathogens

Nature Genetics volume 49, pages 1364–1372 (2017)Cite this article

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Abstract

Alleles that confer multiple disease resistance (MDR) are valuable in crop improvement, although the molecular mechanisms underlying their functions remain largely unknown. A quantitative trait locus, qMdr9.02, associated with resistance to three important foliar maize diseases—southern leaf blight, gray leaf spot and northern leaf blight—has been identified on maize chromosome 9. Through fine-mapping, association analysis, expression analysis, insertional mutagenesis and transgenic validation, we demonstrate that ZmCCoAOMT2, which encodes a caffeoyl-CoA O-methyltransferase associated with the phenylpropanoid pathway and lignin production, is the gene within qMdr9.02 conferring quantitative resistance to both southern leaf blight and gray leaf spot. We suggest that resistance might be caused by allelic variation at the level of both gene expression and amino acid sequence, thus resulting in differences in levels of lignin and other metabolites of the phenylpropanoid pathway and regulation of programmed cell death.

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Figure 1: Phenotype and fine-mapping of qMdr9.02.
Figure 2: Association and expression analyses of candidate genes in the qMdr9.02 region.
Figure 3: Transgenic overexpression of ZmCCoAOMT2.
Figure 4: Evaluation of transposon-insertion lines.
Figure 5: Differential levels of lignin and lignin precursors identified in resistant and susceptible NILs.
Figure 6: Function of ZmCCoAOMT2 in repressing the hypersensitive response (HR) induced by autoactive NLR proteins.

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Gene Expression Omnibus

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Acknowledgements

We thank J. Holland and J. Dunne for help with association analysis and providing the filtered hapmap3 marker set in the qMdr9.02 region in NAM founder lines. We thank W. Boerjan (Ghent University), K. Wang (Iowa State University), D. McCarty (University of Florida), K. Koch (University of Florida) and J. Brumos (North Carolina State University) for providing materials. We thank R. Franks, E. Johannes and S. Sermons for technical assistance. We thank C. Herring, G. Marshall and the staff at Central Crops Research Station for help with field work. We thank C. Saravitz and the staff at the NCSU Phytotron for growth-chamber-trial support. We thank D. Jackson, S. Kamoun, S. Christensen, B. Olukolu and T. Jamann for helpful discussions. We acknowledge the MaizeGDB database (URLs), which was essential to this work. Research was supported by the USDA and United States National Science Foundation grants IOS-1127076 to R.W. and 1444503 to P.B.-K. Purchase of and access to microscopes was made possible by NIH shared instrumentation grant S10 OD016361 and NIH-NIGMS grant P20 GM103446, both to J.C.

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Authors and Affiliations

  1. Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, North Carolina, USA

    Qin Yang, Yijian He, Amy Kelly & Peter Balint-Kurti

  2. Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, USA

    Mercy Kabahuma & Nick Lauter

  3. Department of Plant and Soil Sciences, University of Delaware, Newark, Delaware, USA

    Timothy Chaya, Randall Wisser & Jeffrey Caplan

  4. Department of Plant Pathology and Microbiology, Texas A&M University, College Station, Texas, USA

    Eli Borrego & Michael Kolomiets

  5. Department of Crop Science, North Carolina State University, Raleigh, North Carolina, USA

    Yang Bian

  6. Department of Biology, Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA

    Farid El Kasmi, Li Yang, Paulo Teixeira & Jeffery L Dangl

  7. School of Integrative Plant Science, Cornell University, Ithaca, New York, USA

    Judith Kolkman & Rebecca Nelson

  8. Department of Biological Sciences, University of Delaware, Newark, Delaware, USA

    Jeffrey Caplan

  9. Department of Plant and Microbial Biology, Plants for Human Health Institute, North Carolina State University, Kannapolis, North Carolina, USA

    Xu Li

  10. USDA-ARS Corn Insects and Crop Genetics Research Unit, Ames, Iowa, USA

    Nick Lauter

  11. USDA-ARS Plant Science Research Unit, Raleigh, North Carolina, USA

    Peter Balint-Kurti

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Contributions

Q.Y., initiation of project, experimental design, gene cloning and functional validation, data analyses and writing the manuscript. Y.H., experimental design, HR suppression experiment, bacterial infection assays and writing the manuscript. M.K., generation of transgenic maize lines and seed production. T.C., histological analysis. A.K., participation in genotyping transgenic lines, making Gateway constructs and gene expression analysis. E.B., defense metabolite analysis and discussion. Y.B., candidate region–based association analysis. F.E.K., Hpa-isolate Emwa1 infection assays in Arabidopsis, expression data analysis and manuscript editing. L.Y., Hpa-isolate Noco2 infection assays in Arabidopsis and manuscript editing. P.T., Arabidopsis gene expression analysis based on published data. J.K. and R.N., generating F2:3 families for insertion lines, and conception and planning of the project. M.K., discussion and defense metabolite analysis. J.L.D., Arabidopsis pathology assays and manuscript writing and editing. R.W., conception and planning of the project. J.C., conception and planning of the project, and histological analysis. X.L., metabolite profiles and lignin analysis. N.L., conception and planning of the project, and generation of transgenic lines. P.B.-K., initiation of the project, experimental design, conception and planning of the project, and manuscript writing and editing.

Corresponding authors

Correspondence to Qin Yang or Peter Balint-Kurti.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–15 and Supplementary Tables 1–3 and 6–8 (PDF 2583 kb)

Supplementary Table 4

Variants found in the ZmCCoAOMT2 gene in the 26 NAM founder lines. (XLSX 27 kb)

Supplementary Table 5

qMdr9.02 region based association analysis for SLB in maize NAM population. The r2 value measures the linkage disequilibrium (LD) with the most significant variant with 1 being complete LD. The P-values is −log10(P) of association with SLB resistance. (XLSX 28 kb)

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Yang, Q., He, Y., Kabahuma, M. et al. A gene encoding maize caffeoyl-CoA O-methyltransferase confers quantitative resistance to multiple pathogens. Nat Genet 49, 1364–1372 (2017). https://doi.org/10.1038/ng.3919

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