Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

Accession codes

Primary accessions

NCBI Reference Sequence

Referenced accessions

Gene Expression Omnibus

References

  1. Wiesner-Hanks, T. & Nelson, R. Multiple disease resistance in plants. Annu. Rev. Phytopathol. 54, 229–252 (2016).

    Article  CAS  PubMed  Google Scholar 

  2. Miedaner, T. & Korzun, V. Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102, 560–566 (2012).

    Article  PubMed  Google Scholar 

  3. Zwonitzer, J.C. et al. Mapping resistance quantitative trait loci for three foliar diseases in a maize recombinant inbred line population-evidence for multiple disease resistance? Phytopathology 100, 72–79 (2010).

    Article  PubMed  Google Scholar 

  4. Teran, H., Jara, C., Mahuku, G., Beebe, S. & Singh, S.P. Simultaneous selection for resistance to five bacterial, fungal, and viral diseases in three Andean x Middle American inter-gene pool common bean populations. Euphytica 189, 283–292 (2013).

    Article  CAS  Google Scholar 

  5. Wisser, R.J., Sun, Q., Hulbert, S.H., Kresovich, S. & Nelson, R.J. Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169, 2277–2293 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Krattinger, S.G. et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360–1363 (2009).

    Article  CAS  PubMed  Google Scholar 

  7. Moore, J.W. et al. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 47, 1494–1498 (2015).

    Article  CAS  PubMed  Google Scholar 

  8. Fu, J. et al. Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol. 155, 589–602 (2011).

    Article  CAS  PubMed  Google Scholar 

  9. Jamann, T.M., Poland, J.A., Kolkman, J.M., Smith, L.G. & Nelson, R.J. Unraveling genomic complexity at a quantitative disease resistance locus in maize. Genetics 198, 333–344 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wisser, R.J. et al. Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc. Natl. Acad. Sci. USA 108, 7339–7344 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Bent, A.F. & Mackey, D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399–436 (2007).

    Article  CAS  PubMed  Google Scholar 

  12. Coll, N.S., Epple, P. & Dangl, J.L. Programmed cell death in the plant immune system. Cell Death Differ. 18, 1247–1256 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wisser, R.J., Balint-Kurti, P.J. & Nelson, R.J. The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathology 96, 120–129 (2006).

    Article  CAS  PubMed  Google Scholar 

  14. Fu, D. et al. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323, 1357–1360 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fukuoka, S. et al. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325, 998–1001 (2009).

    Article  CAS  PubMed  Google Scholar 

  16. Yang, Q., Balint-Kurti, P. & Xu, M. Quantitative disease resistance: dissection and adoption in maize. Mol. Plant 10, 402–413 (2017).

    Article  CAS  PubMed  Google Scholar 

  17. Pataky, J.K. & Williams, M. Reactions of sweet corn hybrids to prevalent diseases and herbicides. Midwest Vegetable Variety Trial Rep. 115–148 (2011).

  18. Johal, G.S. & Briggs, S.P. Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258, 985–987 (1992).

    Article  CAS  PubMed  Google Scholar 

  19. Collins, N. et al. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11, 1365–1376 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zuo, W. et al. A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47, 151–157 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Broglie, K. et al. Polynucleotides and methods for making plants resistant to fungal pathogens. US patent 20080016595 A1 (2006).

  22. Hurni, S. et al. The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proc. Natl. Acad. Sci. USA 112, 8780–8785 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhao, B. et al. A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. USA 102, 15383–15388 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Liu, Q. et al. An atypical thioredoxin imparts early resistance to Sugarcane mosaic virus in maize. Mol. Plant 10, 483–497 (2017).

    Article  CAS  PubMed  Google Scholar 

  25. Kump, K.L. et al. Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat. Genet. 43, 163–168 (2011).

    Article  CAS  PubMed  Google Scholar 

  26. Poland, J.A., Bradbury, P.J., Buckler, E.S. & Nelson, R.J. Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc. Natl. Acad. Sci. USA 108, 6893–6898 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Benson, J.M., Poland, J.A., Benson, B.M., Stromberg, E.L. & Nelson, R.J. Resistance to gray leaf spot of maize: genetic architecture and mechanisms elucidated through nested association mapping and near-isogenic line analysis. PLoS Genet. 11, e1005045 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Davis, G.L. et al. A maize map standard with sequenced core markers, grass genome reference points and 932 expressed sequence tagged sites (ESTs) in a 1736-locus map. Genetics 152, 1137–1172 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Belcher, A.R. et al. Analysis of quantitative disease resistance to southern leaf blight and of multiple disease resistance in maize, using near-isogenic lines. Theor. Appl. Genet. 124, 433–445 (2012).

    Article  PubMed  Google Scholar 

  30. Lennon, J.R., Krakowsky, M., Goodman, M., Flint-Garcia, S. & Balint-Kurti, P.J. Identification of alleles conferring resistance to gray leaf spot in maize derived from its wild progenitor species teosinte. Crop Sci. 56, 209–218 (2016).

    Article  CAS  Google Scholar 

  31. McMullen, M.D. et al. Genetic properties of the maize nested association mapping population. Science 325, 737–740 (2009).

    Article  CAS  PubMed  Google Scholar 

  32. Bian, Y., Yang, Q., Balint-Kurti, P.J., Wisser, R.J. & Holland, J.B. Limits on the reproducibility of marker associations with southern leaf blight resistance in the maize nested association mapping population. BMC Genomics 15, 1068 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zwonitzer, J.C. et al. Use of selection with recurrent backcrossing and QTL mapping to identify loci contributing to southern leaf blight resistance in a highly resistant maize line. Theor. Appl. Genet. 118, 911–925 (2009).

    Article  PubMed  Google Scholar 

  34. Schnable, P.S. et al. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112–1115 (2009).

    Article  CAS  PubMed  Google Scholar 

  35. Unterseer, S. et al. European Flint reference sequences complement the maize pan-genome. Preprint at http://www.biorxiv.org/content/early/2017/01/27/103747/ (2017).

  36. Lu, F. et al. High-resolution genetic mapping of maize pan-genome sequence anchors. Nat. Commun. 6, 6914 (2015).

    Article  CAS  PubMed  Google Scholar 

  37. Hirsch, C. et al. Draft assembly of elite inbred line PH207 provides insights into genomic and transcriptome diversity in maize. Plant Cell 28, 2700–2714 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Xu, G., Ma, H., Nei, M. & Kong, H. Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc. Natl. Acad. Sci. USA 106, 835–840 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Singh, P. & Zimmerli, L. Lectin receptor kinases in plant innate immunity. Front. Plant Sci. 4, 124 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bukowski, R. et al. Construction of the third generation Zea mays haplotype map. Preprint at http://www.biorxiv.org/content/early/2016/09/16/026963/ (2015).

  41. Settles, A.M. et al. Sequence-indexed mutations in maize using the UniformMu transposon-tagging population. BMC Genomics 8, 116 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Raes, J., Rohde, A., Christensen, J.H., Van de Peer, Y. & Boerjan, W. Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol. 133, 1051–1071 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Vanholme, R. et al. A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24, 3506–3529 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Li, L. et al. The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase. Plant J. 81, 493–504 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Coletta, V.C., Rezende, C.A., da Conceição, F.R., Polikarpov, I. & Guimarães, F.E.G. Mapping the lignin distribution in pretreated sugarcane bagasse by confocal and fluorescence lifetime imaging microscopy. Biotechnol. Biofuels 6, 43 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Rocha, S. et al. Lignification of developing maize (Zea mays L.) endosperm transfer cells and starchy endosperm cells. Front. Plant Sci. 5, 102 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Gao, X. et al. Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin. Mol. Plant Microbe Interact. 20, 922–933 (2007).

    Article  CAS  PubMed  Google Scholar 

  48. Gao, X. et al. Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Mol. Plant Microbe Interact. 21, 98–109 (2008).

    Article  CAS  PubMed  Google Scholar 

  49. Olukolu, B.A. et al. A genome-wide association study of the maize hypersensitive defense response identifies genes that cluster in related pathways. PLoS Genet. 10, e1004562 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wang, G.F. & Balint-Kurti, P.J. Maize homologs of CCoAOMT and HCT, two key enzymes in lignin biosynthesis, form complexes with the NLR Rp1 protein to modulate the defense response. Plant Physiol. 171, 2166–2177 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Govrin, E.M. & Levine, A. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751–757 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Bos, J.I.B. et al. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J. 48, 165–176 (2006).

    Article  CAS  PubMed  Google Scholar 

  53. Gao, Z., Chung, E.H., Eitas, T.K. & Dangl, J.L. Plant intracellular innate immune receptor resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. Proc. Natl. Acad. Sci. USA 108, 7619–7624 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Bubeck, D.M., Goodman, M.M., Beavis, W.D. & Grant, D. Quantitative trait loci controlling resistance to gray leaf spot in maize. Crop Sci. 33, 838–847 (1993).

    Article  Google Scholar 

  55. Bhuiyan, N.H., Selvaraj, G., Wei, Y. & King, J. Role of lignification in plant defense. Plant Signal. Behav. 4, 158–159 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Tonnessen, B.W. et al. Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol. Biol. 87, 273–286 (2015).

    Article  CAS  PubMed  Google Scholar 

  57. Nicholson, R.L. & Hammerschmidt, R. Phenolic compounds and their role in disease resistance. Annu. Rev. Phytopathol. 30, 369–389 (1992).

    Article  CAS  Google Scholar 

  58. Newman, T.C., Ohme-Takagi, M., Taylor, C.B. & Green, P.J. DST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco. Plant Cell 5, 701–714 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Farré, G., Twyman, R.M., Christou, P., Capell, T. & Zhu, C. Knowledge-driven approaches for engineering complex metabolic pathways in plants. Curr. Opin. Biotechnol. 32, 54–60 (2015).

    Article  CAS  PubMed  Google Scholar 

  60. König, S. et al. Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum. New Phytol. 202, 823–837 (2014).

    Article  CAS  PubMed  Google Scholar 

  61. Blount, J.W. et al. Altering expression of cinnamic acid 4-hydroxylase in transgenic plants provides evidence for a feedback loop at the entry point into the phenylpropanoid pathway. Plant Physiol. 122, 107–116 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Borrego, E.J. & Kolomiets, M.V. Synthesis and functions of jasmonates in maize. Plants (Basel) 5, E41 (2016).

    Article  CAS  Google Scholar 

  63. Spoel, S.H., Johnson, J.S. & Dong, X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl. Acad. Sci. USA 104, 18842–18847 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Hirsch, C.N. et al. Insights into the maize pan-genome and pan-transcriptome. Plant Cell 26, 121–135 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. McCarty, D.R. et al. Steady-state transposon mutagenesis in inbred maize. Plant J. 44, 52–61 (2005).

    Article  CAS  PubMed  Google Scholar 

  66. Carson, M.L., Stuber, C.W. & Senior, M.L. Identification and mapping of quantitative trait loci conditioning resistance to southern leaf blight of maize caused by Cochliobolus heterostrophus race O. Phytopathology 94, 862–867 (2004).

    Article  CAS  PubMed  Google Scholar 

  67. Yang, Q., Zhang, D. & Xu, M. A sequential quantitative trait locus fine-mapping strategy using recombinant-derived progeny. J. Integr. Plant Biol. 54, 228–237 (2012).

    Article  PubMed  Google Scholar 

  68. Kang, H.M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348–354 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zhang, Z. et al. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355–360 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Bian, Y. & Holland, J.B. Ensemble learning of QTL models improves prediction of complex traits. G3 (Bethesda) 5, 2073–2084 (2015).

    Article  Google Scholar 

  71. Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465–W469 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Alonso, J.M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657 (2003).

    Article  PubMed  Google Scholar 

  73. Hubert, D.A., He, Y., McNulty, B.C., Tornero, P. & Dangl, J.L. Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. Proc. Natl. Acad. Sci. USA 106, 9556–9563 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Tornero, P. & Dangl, J.L. A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. Plant J. 28, 475–481 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Holt, B.F. III et al. An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev. Cell 2, 807–817 (2002).

    Article  PubMed  Google Scholar 

  76. Mukhtar, M.S. et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596–601 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Winter, D. et al. An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2, e718 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Yang, L. et al. Pseudomonas syringae type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence. Cell Host Microbe 21, 156–168 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Asai, S. et al. Expression profiling during Arabidopsis/downy mildew interaction reveals a highly-expressed effector that attenuates responses to salicylic acid. PLoS Pathog. 10, e1004443 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Strauch, R.C., Svedin, E., Dilkes, B., Chapple, C. & Li, X. Discovery of a novel amino acid racemase through exploration of natural variation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 112, 11726–11731 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Christensen, S.A. et al. The novel monocot-specific 9-lipoxygenase ZmLOX12 is required to mount an effective jasmonate-mediated defense against Fusarium verticillioides in maize. Mol. Plant Microbe Interact. 27, 1263–1276 (2014).

    Article  CAS  PubMed  Google Scholar 

  82. Ludovici, M. et al. Quantitative profiling of oxylipins through comprehensive LC-MS/MS analysis of Fusarium verticillioides and maize kernels. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 31, 2026–2033 (2014).

    Article  CAS  PubMed  Google Scholar 

  83. Pan, X., Welti, R. & Wang, X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat. Protoc. 5, 986–992 (2010).

    Article  CAS  PubMed  Google Scholar 

  84. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949–956 (2003).

    Article  CAS  PubMed  Google Scholar 

  85. Wang, G. et al. Maize homologs of HCT, a key enzyme in lignin biosynthesis, bind the NLR Rp1 proteins to modulate the defense response. Plant Physiol. 171, 2166–2177 (2015).

    Article  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

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.

Ethics declarations

Competing interests

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)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.3919

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing