Advertisement

Theoretical and Applied Genetics

, Volume 129, Issue 3, pp 591–602 | Cite as

A remorin gene is implicated in quantitative disease resistance in maize

  • Tiffany M. Jamann
  • Xingyu Luo
  • Laura Morales
  • Judith M. Kolkman
  • Chia-Lin Chung
  • Rebecca J. Nelson
Original Article

Abstract

Key message

Quantitative disease resistance is used by plant breeders to improve host resistance. We demonstrate a role for a maize remorin ( ZmREM6.3 ) in quantitative resistance against northern leaf blight using high-resolution fine mapping, expression analysis, and mutants. This is the first evidence of a role for remorins in plant-fungal interactions.

Abstract

Quantitative disease resistance (QDR) is important for the development of crop cultivars and is particularly useful when loci also confer multiple disease resistance. Despite its widespread use, the underlying mechanisms of QDR remain largely unknown. In this study, we fine-mapped a known quantitative trait locus (QTL) conditioning disease resistance on chromosome 1 of maize. This locus confers resistance to three foliar diseases: northern leaf blight (NLB), caused by the fungus Setosphaeria turcica; Stewart’s wilt, caused by the bacterium Pantoea stewartii; and common rust, caused by the fungus Puccinia sorghi. The Stewart’s wilt QTL was confined to a 5.26-Mb interval, while the rust QTL was reduced to an overlapping 2.56-Mb region. We show tight linkage between the NLB QTL locus and the loci conferring resistance to Stewart’s wilt and common rust. Pleiotropy cannot be excluded for the Stewart’s wilt and the common rust QTL, as they were fine-mapped to overlapping regions. Four positional candidate genes within the 243-kb NLB interval were examined with expression and mutant analysis: a gene with homology to an F-box gene, a remorin gene (ZmREM6.3), a chaperonin gene, and an uncharacterized gene. The F-box gene and ZmREM6.3 were more highly expressed in the resistant line. Transposon tagging mutants were tested for the chaperonin and ZmREM6.3, and the remorin mutant was found to be more susceptible to NLB. The putative F-box is a strong candidate, but mutants were not available to test this gene. Multiple lines of evidence strongly suggest a role for ZmREM6.3 in quantitative disease resistance.

Keywords

Quantitative Trait Locus Diseased Leaf Area Northern Leaf Blight Quantitative Disease Resistance Nest Association Mapping 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank Dr. Peter Balint-Kurti for assisting with the field trial in Clayton, NC. We would also like to acknowledge Drs. Randall Wisser, Jesse Poland, Santiago Mideros, and Peter Balint-Kurti for helpful discussions. We also thank Alyssa Cowles, William Miller, Chris Mancuso, Katharine Constas, and Ariel Fialko for their assistance with field work.

Compliance with ethical standards

Funding

This work was funded by National Science Foundation award 1127076, the McKnight Foundation, the Cornell University Agricultural Experiment Station federal formula funds, Project No. NYC-153418 received from the National Institute of Food and Agriculture (NIFA), United States Department of Agriculture, and Cornell University. Any opinions, findings, conclusions or recommendations expressed in the publication are those of the author(s) and do not necessarily reflect the view of the National Institute of Food and Agriculture (NIFA), of the United States Department of Agriculture (USDA), or of the other funders.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2015_2650_MOESM1_ESM.pdf (80 kb)
Supplementary material 1 (PDF 80 kb)

References

  1. Adipala E, Lipps P, Madden L (1993) Occurrence of Exserohilum turcicum on maize in Uganda. Plant Dis 77:202CrossRefGoogle Scholar
  2. Bozkurt T, Richardson A, Dagdas Y, Mongrand S, Kamoun S et al (2014) The plant membrane-associated REM1.3 remorin accumulates in discrete perihaustorial domains and enhances susceptibility to Phytophthora infestans. Plant Physiol 165:1005–1018PubMedCentralCrossRefPubMedGoogle Scholar
  3. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890CrossRefPubMedGoogle Scholar
  4. Canaran P, Buckler ES, Glaubitz JC, Stein L, Sun Q et al (2008) Panzea: an update on new content and features. Nucl Acids Res 36:D1041–D1043PubMedCentralCrossRefPubMedGoogle Scholar
  5. Chia JM, Song C, Bradbury PJ, Costich D, de Leon N et al (2012) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44:803–807CrossRefPubMedGoogle Scholar
  6. Chisholm ST, Dahlbeck D, Krishnamurthy N, Day B, Sjolander K et al (2005) Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc Natl Acad Sci 102:2087–2092PubMedCentralCrossRefPubMedGoogle Scholar
  7. Chung CL, Jamann T, Longfellow J, Nelson R (2010a) Characterization and fine-mapping of a resistance locus for northern leaf blight in maize bin 8.06. Theor Appl Genet 121:205–227CrossRefPubMedGoogle Scholar
  8. Chung CL, Longfellow JM, Walsh EK, Kerdieh Z, Van Esbroeck G et al (2010b) Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize–Setosphaeria turcica pathosystem. BMC Plant Biol 10:103PubMedCentralCrossRefPubMedGoogle Scholar
  9. Cook DE, Lee TG, Guo X, Melito S, Wang K et al (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338(6111):1206–1209CrossRefPubMedGoogle Scholar
  10. De Boeck P, Bakker M, Zwitser R, Nivard M, Hofman A et al (2011) The estimation of item response models with the lmer function from the lme4 package in R. J Stat Softw 39:1–28CrossRefGoogle Scholar
  11. den Boer E, Zhang NW, Pelgrom K, Visser RG, Niks RE et al (2013) Fine mapping quantitative resistances to downy mildew in lettuce revealed multiple sub-QTLs with plant stage dependent effects reducing or even promoting the infection. Theor Appl Genet 126:2995–3007CrossRefGoogle Scholar
  12. Doyle JJ, Dickson EE (1987) Preservation of plant samples for DNA restriction endonuclease analysis. Taxon 36(4):715–722CrossRefGoogle Scholar
  13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797PubMedCentralCrossRefPubMedGoogle Scholar
  14. Esker P, Nutter F (2002) Assessing the risk of Stewart’s disease of corn through improved knowledge of the role of the corn flea beetle vector. Phytopathology 92:668–670CrossRefPubMedGoogle Scholar
  15. Felsenstein J (1989) PHYLIP—phylogeny inference package (version 3.2). Cladistics 5:164–166Google Scholar
  16. Fininsa C, Yuen J (2001) Association of maize rust and leaf blight epidemics with cropping systems in Hararghe highlands, eastern Ethiopia. Crop Prot 20:669–678CrossRefGoogle Scholar
  17. Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM et al (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064CrossRefPubMedGoogle Scholar
  18. Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L et al (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323:1357–1360PubMedCentralCrossRefPubMedGoogle Scholar
  19. Fukuoka S, Saka N, Koga H, Ono K, Shimizu T et al (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001CrossRefPubMedGoogle Scholar
  20. Gore M, Chia J, Elshire R, Sun Q, Ersoz E et al (2009) A first-generation haplotype map of maize. Science 326:1115CrossRefPubMedGoogle Scholar
  21. Groth JV, Zeyen RJ, Davis DW, Christ BJ (1983) Yield and quality losses caused by common rust (Puccinia sorghi Schw.) in sweet corn (Zea mays) hybrids. Crop Protection 2(1):105–111CrossRefGoogle Scholar
  22. Huerta-Cepas J, Dopazo J, Gabaldón T (2010) ETE: a python environment for tree exploration. BMC Bioinformatics 1(1):24CrossRefGoogle Scholar
  23. Jamann T, Poland J, Kolkman K, Smith L, Nelson R (2014) Unraveling genomic complexity at a quantitative disease resistance locus in maize. Genetics 198(1):333–344PubMedCentralCrossRefPubMedGoogle Scholar
  24. Jennings P, Ullstrup A (1957) A histological study of three Helminthosporium leaf blights of corn. Phytopathology 47:707–714Google Scholar
  25. Johnson EB, Haggard JE, St Clair DA (2012) Fractionation, stability, and isolate-specificity of QTL for resistance to Phytophthora infestans in cultivated tomato (Solanum lycopersicum). G3 Genes Genomes Genet 2:1145–1159Google Scholar
  26. Khan A, Ries S, Pataky J (1996) Transmission of Erwinia stewartii through seed of resistant and susceptible field and sweet corn. Plant Dis 80:398–403CrossRefGoogle Scholar
  27. Kim HS, Delaney TP (2002) Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance. Plant Cell 14:1469–1482PubMedCentralCrossRefPubMedGoogle Scholar
  28. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J et al (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363CrossRefPubMedGoogle Scholar
  29. Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR et al (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43:163–168CrossRefPubMedGoogle Scholar
  30. Lefebvre B, Timmers T, Mbengue M, Moreau S, Herve C et al (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci 107:2343–2348PubMedCentralCrossRefPubMedGoogle Scholar
  31. Leonard K, Levy Y, Smith D (1989) Proposed nomenclature for pathogenic races of Exserohilum turcicum on corn. Plant Dis 73:776–777Google Scholar
  32. Levy Y, Pataky J (1992) Epidemiology of northern leaf blight on sweet corn. Phytoparasitica 20:53–66CrossRefGoogle Scholar
  33. Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH et al (2009) A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol 149:286–296PubMedCentralCrossRefPubMedGoogle Scholar
  34. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H et al (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740CrossRefPubMedGoogle Scholar
  35. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J et al (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601PubMedCentralCrossRefPubMedGoogle Scholar
  36. Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A et al (2014) The genome portal of the department of energy joint genome institute: 2014 updates. Nucl Acids Res 42:D26–D31PubMedCentralCrossRefPubMedGoogle Scholar
  37. Nurmberg PL, Knox KA, Yun BW, Morris PC, Shafiei R et al (2007) The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response. Proc Natl Acad Sci 104:18795–18800PubMedCentralCrossRefPubMedGoogle Scholar
  38. Perkins JM (1987) Disease development and yield losses associated with northern leaf blight on corn. Plant Dis 71:940CrossRefGoogle Scholar
  39. Perraki A, Binaghi M, Mecchia M, Gronnier J, German-Retana S et al (2014) StRemorin1.3 hampers Potato virus X TGBp1 ability to increase plasmodesmata permeability, but does not interfere with its silencing suppressor activity. FEBS Lett 588:1699–1705CrossRefPubMedGoogle Scholar
  40. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29CrossRefPubMedGoogle Scholar
  41. Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Natl Acad Sci 108:6893–6898PubMedCentralCrossRefPubMedGoogle Scholar
  42. R Core Development Team (2013) R: a language and environment for statistical computing. ViennaGoogle Scholar
  43. Raffaele S, Mongrand S, Gamas P, Niebel A, Ott T (2007) Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol 145:593–600PubMedCentralCrossRefPubMedGoogle Scholar
  44. Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S et al (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21:1541–1555PubMedCentralCrossRefPubMedGoogle Scholar
  45. Raymundo AD (1981) Measuring the relationship between northern corn leaf blight and yield losses. Plant Dis 65:325CrossRefGoogle Scholar
  46. Roper MC (2011) Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn. Mol Plant Pathol 12:628–637CrossRefPubMedGoogle Scholar
  47. Schaefer CM, Bernardo R (2013) Genomewide association mapping of flowering time, kernel composition, and disease resistance in historical Minnesota maize inbreds. Crop Sci 53:2518–2529CrossRefGoogle Scholar
  48. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefPubMedGoogle Scholar
  49. Settles AM, Latshaw S, McCarty DR (2004) Molecular analysis of high-copy insertion sites in maize. Nucl Acids Res 32:e54PubMedCentralCrossRefPubMedGoogle Scholar
  50. St Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268CrossRefPubMedGoogle Scholar
  51. Suparyono, Pataky JK (1989) Influence of host resistance and growth stage at the time of inouclaiton on Stewart’s wilt and Goss’s wilt development and sweet corn hybrid yield. Plant Dis 73:339–345CrossRefGoogle Scholar
  52. Szalma SJ, Hostert BM, Ledeaux JR, Stuber CW, Holland JB (2007) QTL mapping with near-isogenic lines in maize. Theor Appl Genet 114:1211–1228CrossRefPubMedGoogle Scholar
  53. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M et al (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465:632–636PubMedCentralCrossRefPubMedGoogle Scholar
  54. Tóth K, Stratil TF, Madsen EB, Ye J, Popp C et al (2012) Functional domain analysis of the remorin protein LjSYMREM1 in Lotus japonicus. PLoS One 7(1):e30817PubMedCentralCrossRefPubMedGoogle Scholar
  55. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC et al (2012) Primer3—new capabilities and interfaces. Nucl Acids Res 40:e115PubMedCentralCrossRefPubMedGoogle Scholar
  56. Van Inghelandt D, Melchinger AE, Martinant JP, Stich B (2012) Genome-wide association mapping of flowering time and northern corn leaf blight (Setosphaeria turcica) resistance in a vast commercial maize germplasm set. BMC Plant Biol 12:56PubMedCentralCrossRefPubMedGoogle Scholar
  57. Wallace JG, Larson SJ, Buckler ES (2014a) Association mapping across numerous traits reveals patterns of functional variation in maize. PLoS Genet 10:e1004845PubMedCentralCrossRefPubMedGoogle Scholar
  58. Wallace JG, Bradbury PJ, Zhang N, Gibon Y, Stitt M et al (2014b) Entering the second century of maize quantitative genetics. Heredity 112:30–38PubMedCentralCrossRefPubMedGoogle Scholar
  59. Wilcoxson R, Atif A, Skovmand B (1974) Slow rusting of wheat varieties in the field correlated with stem rust (Puccinia graminis tritici) severity on detached leaves in the greenhouse. Plant Dis Rep 58:1085–1087Google Scholar
  60. Wisser RJ, Sun Q, Hulbert SH, Kresovich S, Nelson RJ (2005) Identification and characterization of regions of the rice genome associated with broad-spectrum, quantitative disease resistance. Genetics 169(4):2277–2293PubMedCentralCrossRefPubMedGoogle Scholar
  61. Wisser RJ, Balint-Kurti PJ, Nelson RJ (2006) The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathology 96:120–129CrossRefPubMedGoogle Scholar
  62. Wisser RJ, Kolkman JM, Patzoldt ME, Holland JB, Yu J et al (2011) Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc Natl Acad Sci 108:7339–7344PubMedCentralCrossRefPubMedGoogle Scholar
  63. Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Tiffany M. Jamann
    • 1
    • 2
  • Xingyu Luo
    • 1
    • 3
  • Laura Morales
    • 1
  • Judith M. Kolkman
    • 1
  • Chia-Lin Chung
    • 1
    • 4
  • Rebecca J. Nelson
    • 1
  1. 1.School of Integrative Plant Science, Cornell UniversityIthacaUSA
  2. 2.Department of Crop SciencesUniversity of IllinoisUrbanaUSA
  3. 3.Department of Plant PathologyUniversity of Wisconsin-MadisonMadisonUSA
  4. 4.Department of Plant Pathology and MicrobiologyNational Taiwan UniversityTaipeiTaiwan

Personalised recommendations