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

Nature Genetics

Volumn 49, Issue 9, 2017, Pages 1364-1372

  Yang, Qin ^a   He, Yijian ^b   Kabahuma, Mercy ^c   Chaya, Timothy ^a   Kelly, Amy ^d   Borrego, Eli ^a   Bian, Yang ^e   El Kasmi, Farid ^e   Yang, Li ^e   Teixeira, Paulo ^e   Kolkman, Judith ^f   Nelson, Rebecca ^f   Kolomiets, Michael ^d   Dangl, Jeffery L ^e   Wisser, Randall ^c   Caplan, Jeffrey ^c   Li, Xu ^a   Lauter, Nick ^b,g   Balint Kurti, Peter ^a,h  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

^d TEXAS A AND M UNIVERSITY   (United States)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

^f Cornell University ^*  (United States)

^g AGRICULTURAL RESEARCH SERVICE   (United States)

^h NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAFFEOYL COENZYME A O METHYLTRANSFERASE; COENZYME A; LIGNIN; LIPOXYGENASE; METHYLTRANSFERASE; UNCLASSIFIED DRUG; CAFFEOYL-COA O-METHYLTRANSFERASE; PHENYLPROPIONIC ACID DERIVATIVE;

AMINO ACID SEQUENCE; ARTICLE; CHROMOSOME 9; GENE EXPRESSION; GENE MAPPING; GENETIC ASSOCIATION; GENETIC RESISTANCE; MAIZE; MUTAGENESIS; NONHUMAN; PLANT DISEASE; PLANT GENE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT LOCUS; APOPTOSIS; CHROMOSOMAL MAPPING; DISEASE RESISTANCE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PLANT LEAF; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC PLANT;

APOPTOSIS; CHROMOSOME MAPPING; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LIGNIN; METHYLTRANSFERASES; MICROSCOPY, FLUORESCENCE; MUTATION; PHENYLPROPIONATES; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; QUANTITATIVE TRAIT LOCI; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ZEA MAYS;

EID: 85028725827     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3919     Document Type: Article

References (85)

1. Wiesner-Hanks, T. & Nelson, R. Multiple disease resistance in plants. Annu. Rev. Phytopathol. 54, 229-252 (2016).
2. Miedaner, T. & Korzun, V. Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102, 560-566 (2012).
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).
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).
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).
6. Krattinger, S.G. et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360-1363 (2009).
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).
8. Fu, J. et al. Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiol. 155, 589-602 (2011).
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).
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).
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).
12. Coll, N.S., Epple, P. & Dangl, J.L. Programmed cell death in the plant immune system. Cell Death Differ. 18, 1247-1256 (2011).
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).
14. Fu, D. et al. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323, 1357-1360 (2009).
15. Fukuoka, S. et al. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325, 998-1001 (2009).
16. Yang, Q., Balint-Kurti, P. & Xu, M. Quantitative disease resistance: dissection and adoption in maize. Mol. Plant 10, 402-413 (2017).
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).
19. Collins, N. et al. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11, 1365-1376 (1999).
20. Zuo, W. et al. A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47, 151-157 (2015).
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).
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).
24. Liu, Q. et al. An atypical thioredoxin imparts early resistance to Sugarcane mosaic virus in maize. Mol. Plant 10, 483-497 (2017).
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).
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).
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).
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).
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).
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).
31. McMullen, M.D. et al. Genetic properties of the maize nested association mapping population. Science 325, 737-740 (2009).
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).
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).
34. Schnable, P.S. et al. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115 (2009).
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).
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).
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).
39. Singh, P. & Zimmerli, L. Lectin receptor kinases in plant innate immunity. Front. Plant Sci. 4, 124 (2013).
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).
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).
43. Vanholme, R. et al. A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24, 3506-3529 (2012).
44. Li, L. et al. The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase. Plant J. 81, 493-504 (2015).
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).
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).
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).
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).
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).
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).
51. Govrin, E.M. & Levine, A. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751-757 (2000).
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).
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).
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).
55. Bhuiyan, N.H., Selvaraj, G., Wei, Y. & King, J. Role of lignification in plant defense. Plant Signal. Behav. 4, 158-159 (2009).
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).
57. Nicholson, R.L. & Hammerschmidt, R. Phenolic compounds and their role in disease resistance. Annu. Rev. Phytopathol. 30, 369-389 (1992).
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).
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).
60. König, S. et al. Soluble phenylpropanoids are involved in the defense response of Arabidopsis against Verticillium longisporum. New Phytol. 202, 823-837 (2014).
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).
62. Borrego, E.J. & Kolomiets, M.V. Synthesis and functions of jasmonates in maize. Plants (Basel) 5, E41 (2016).
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).
64. Hirsch, C.N. et al. Insights into the maize pan-genome and pan-transcriptome. Plant Cell 26, 121-135 (2014).
65. McCarty, D.R. et al. Steady-state transposon mutagenesis in inbred maize. Plant J. 44, 52-61 (2005).
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).
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).
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).
69. Zhang, Z. et al. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355-360 (2010).
70. Bian, Y. & Holland, J.B. Ensemble learning of QTL models improves prediction of complex traits. G3 (Bethesda) 5, 2073-2084 (2015).
71. Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469 (2008).
72. Alonso, J.M. et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657 (2003).
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).
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).
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).
76. Mukhtar, M.S. et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596-601 (2011).
77. Winter, D. et al. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One 2, e718 (2007).
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).
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).
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).
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).
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).
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).
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).
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).