Genetics of Resistance and Pathogenicity in the Maize/Setosphaeria turcica Pathosystem and Implications for Breeding

Northern corn leaf blight (NCLB), the most devastating leaf pathogen in maize (Zea mays L.), is caused by the heterothallic ascomycete Setosphaeria turcica. The pathogen population shows an extremely high genetic diversity in tropical and subtropical regions. Varietal resistance is the most efficient technique to control NCLB. Host resistance can be qualitative based on race-specific Ht genes or quantitative controlled by many genes with small effects. Quantitative resistance is moderately to highly effective and should be more durable combatting all races of the pathogen. Quantitative resistance must, however, be analyzed in many environments (= location × year combinations) to select stable resistances. In the tropical and subtropical environments, quantitative resistance is the preferred option to manage NCLB epidemics. Resistance level can be increased in practical breeding programs by several recurrent selection cycles based on disease severity rating and/or by genomic selection. This review aims to address two important aspects of the NCLB pathosystem: the genetics of the fungus S. turcica and the modes of inheritance of the host plant maize, including successful breeding strategies regarding NCLB resistance. Both drivers of this pathosystem, pathogen, and host, must be taken into account to result in more durable resistance.

[1]  E. Cunningham.  Multi-stage index selection , 2004, Theoretical and Applied Genetics.

[2]  H. Ceballos,et al.  Recurrent selection for resistance to Exserohilum turcicum in eight subtropical maize populations , 1991 .

[3]  J. Kimenju,et al.  Reaction of Some Kenyan Maize Genotypes to Turcicum Leaf Blight Under Greenhouse and Field Conditions , 2007 .

[4]  A. D. Raymundo.  Effect of GeneHtNon the Development of Northern Corn Leaf Blight Epidemics , 1981 .

[5]  R. R. Bergquist.  Physiologic Specialization in Trichometasphaeria turcica f. sp. zeae and T. turcica f. sp. sorghi in Hawaii , 1974 .

[6]  R. Pratt,et al.  Heritability and number of genes controlling partial resistance to Exserohilum turcicum in maize inbred H99 , 2004 .

[7]  J. Shu,et al.  Identification and Validation of miRNAs Associated with the Resistance of Maize (Zea mays L.) to Exserohilum turcicum , 2014, PloS one.

[8]  D. Zaitlin,et al.  Linkage of a second gene for NCLB resistance to molecular markers in maize , 1992 .

[9]  J. M. Perkins,et al.  Disease development and yield losses associated with northern leaf blight on corn. , 1987 .

[10]  Semi-selective culture medium for Exserohilum turcicum isolation from corn seeds , 2014 .

[11]  Z. Wicks,et al.  Mapping Components of Partial Resistance to Northern Leaf Blight of Maize Using Reciprocal Translocations , 1992 .

[12]  M. Cojocaru,et al.  Purification and structural determination of a phytotoxic substance from Exserohilum turcicum , 1995 .

[13]  R. Nelson,et al.  Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize - Setosphaeria turcica pathosystem , 2010, BMC Plant Biology.

[14]  R. Mitchell.  The Relevance of Non-Host-Specific Toxins in the Expression of Virulence by Pathogens , 1984 .

[15]  H. Geiger,et al.  Genes for resistance to northern corn leaf blight in diverse maize populations. , 2000 .

[16]  V. Sangtong,et al.  Marker assisted selection for resistance to Northern Corn Leaf Blight in sweet corn. , 2016 .

[17]  A. J. Ullstrup,et al.  A Comparison of Maize Diseases in Temperate and in Tropical Environments , 1976 .

[18]  G. Esbroeck,et al.  Use of a Maize Advanced Intercross Line for Mapping of QTL for Northern Leaf Blight Resistance and Multiple Disease Resistance , 2010 .

[19]  P. J. Freymark,et al.  Molecular-marker-facilitated investigation of host-plant response to Exserohilum turcicum in maize (Zea mays L.): components of resistance , 1994, Theoretical and Applied Genetics.

[20]  L. Madden,et al.  Reaction of maize cultivars from Uganda to Exserohilum turcicum , 1993 .

[21]  S. Briggs,et al.  Disease lesion mimics of maize: A model for cell death in plants , 1995 .

[22]  M. McMullen,et al.  Genomic organization of disease and insect resistance genes in maize , 1995 .

[23]  Kreangkrai Kirdsiri,et al.  Efficacies of Some Fungicides and Antagonists in Controlling Northern Corn Leaf Blight Disease , 2015 .

[24]  M. Carson.  A new gene in maize conferring the "chlorotic halo" reaction to infection by Exserohilum turcicum , 1995 .

[25]  J. Hartman,et al.  Influence of environment and plant maturity on gray leaf spot of corn caused by Cercospora zeae-maydis. , 1982 .

[26]  R. Nelson,et al.  The genetic architecture of disease resistance in maize: a synthesis of published studies. , 2006, Phytopathology.

[27]  G. M. Dunn,et al.  Relationship of Hydroxamic Acid Content in Maize and Resistance to Northern Corn Leaf Blight 1 , 1975 .

[28]  T. Wicker,et al.  The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase , 2015, Proceedings of the National Academy of Sciences.

[29]  B. Vivek,et al.  Validation of consensus quantitative trait loci associated with resistance to multiple foliar pathogens of maize. , 2009, Phytopathology.

[30]  T. Miedaner.  Breeding Strategies for Improving Plant Resistance to Diseases , 2016 .

[31]  Jingao Dong,et al.  Geographic Distribution and Genetic Analysis of Physiological Racesof Setosphaeria turcica in Northern China , 2008 .

[32]  M. Etcheverry,et al.  Selection of potential biological control of Exserohilum turcicum with epiphytic microorganisms from maize. , 2015, Revista Argentina de microbiologia.

[33]  T. Miedaner,et al.  8 Biology, Diversity, and Management of FHB-Causing Fusarium Species in Small-Grain Cereals , 2013 .

[34]  H. Geiger,et al.  Molecular marker analysis of European Setosphaeria turcica populations , 1998, European Journal of Plant Pathology.

[35]  O Appel,et al.  Disease Resistance in Plants , 1915, Nature.

[36]  C. S. Levings,et al.  Molecular basis of disease susceptibility in the Texas cytoplasm of maize , 1992, Plant Molecular Biology.

[37]  M. Carson,et al.  Temporal Variation in Setosphaeria turcica Between 1974 and 1994 and Origin of Races 1, 23, and 23N in the United States. , 2007, Phytopathology.

[38]  M. Pagés,et al.  Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. , 2002, The Plant journal : for cell and molecular biology.

[39]  P. Vasarinsh.  A Histological Study , 2017 .

[40]  J. Brewbaker.  Registration of nine maize populations resistant to tropical diseases. , 2009 .

[41]  A. Melchinger,et al.  Genome-wide association mapping of flowering time and northern corn leaf blight (Setosphaeria turcica) resistance in a vast commercial maize germplasm set , 2012, BMC Plant Biology.

[42]  R. K. Jones,et al.  Characterization of a New Race of Exserohilum turcicum Virulent on Corn with Resistance Gene HtN , 1989 .

[43]  Patrice Koehl,et al.  Plant NBS-LRR proteins: adaptable guards , 2006, Genome Biology.

[44]  Y. Levy,et al.  Differential response of sweet corn cultivars to phytotoxic water-soluble compounds from culture filtrates of Exserohilum turcicum , 1992 .

[45]  G. Johal,et al.  Cell death in maize. , 2000 .

[46]  A. Melchinger,et al.  QTLs for resistance to Setosphaeria turcica in an early maturing Dent×Flint maize population , 1999, Theoretical and Applied Genetics.

[47]  B. Vivek,et al.  Genetic gain and cost efficiency of marker-assisted selection of maize for improved resistance to multiple foliar pathogens , 2012, Molecular Breeding.

[48]  A. J. Ullstrup.  A comparison of monogenic and polygenic resistance to Helminthosporium turcicum in Corn. , 1970 .

[49]  I. Geraldi,et al.  New resistance genes in the Zea mays: exserohilum turcicum pathosystem , 2005 .

[50]  R. Bernardo,et al.  Germplasm Architecture Revealed through Chromosomal Effects for Quantitative Traits in Maize , 2016, The plant genome.

[51]  Jonathan H. Crouch,et al.  Marker-Assisted Selection in Plant Breeding: From Publications to Practice , 2008 .

[52]  M. Carson,et al.  Inheritance of latent period length in maize infected with Exserohilum turcicum , 1995 .

[53]  H. Ceballos,et al.  A Dominant Inhibitor Gene Inhibits the Expression of Ht2 against Exserohilum turcicum Race 2 in Corn Inbred Lines Related to B14 , 1989 .

[54]  Antonio Teixeira do Amaral Júnior,et al.  History of northern corn leaf blight disease in the seventh cycle of recurrent selection of an UENF-14 popcorn population , 2016 .

[55]  M. Carson.  Response of a Maize Synthetic to Selection for Components of Partial Resistance to Exserohilum turcicum. , 2006, Plant disease.

[56]  Oryza sativa protein phosphatase 1a (OsPP1a) involved in salt stress tolerance in transgenic rice , 2016, Molecular Breeding.

[57]  N. Mallikarjuna,et al.  Turcicum leaf blight—sustainable management of a re-emerging maize disease , 2017 .

[58]  B. D. Kohorn,et al.  The cell wall-associated kinases, WAKs, as pectin receptors , 2012, Front. Plant Sci..

[59]  R. Nelson,et al.  Targeted discovery of quantitative trait loci for resistance to northern leaf blight and other diseases of maize , 2011, Theoretical and Applied Genetics.

[60]  Identification of RAPD and SCAR markers linked to northern leaf blight resistance in waxy corn (Zea mays var. ceratina) , 2008, Euphytica.

[61]  O. Martin,et al.  A Large Maize (Zea mays L.) SNP Genotyping Array: Development and Germplasm Genotyping, and Genetic Mapping to Compare with the B73 Reference Genome , 2011, PloS one.

[62]  G. M. Dunn,et al.  Role of cyclic hydroxamic acids in monogenic resistance of maize to Helminthosporium turcicum , 1971 .

[63]  H. Geiger,et al.  Dynamic gene action at QTLs for resistance to Setosphaeria turcica in maize , 1999, Theoretical and Applied Genetics.

[64]  A. Hooker,et al.  Measuring the relationship between northern corn leaf blight and yield losses , 1981 .

[65]  C. Magorokosho,et al.  Genome-wide association mapping reveals novel sources of resistance to northern corn leaf blight in maize , 2015, BMC Plant Biology.

[66]  Xiaolan Zhang,et al.  Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize , 2014 .

[67]  R. A. Fullerton,et al.  Northern leaf blight of maize in New Zealand: relationship of Drechslera turcica airspora to factors influencing sporulation, conidium development, and chlamydospore formation. , 1977 .

[68]  V. Walbot,et al.  Disease Lesion Mimic Mutations , 1983 .

[69]  Peter Jeschke,et al.  Pivoting the Plant Immune System from Dissection to Deployment , 2013 .

[70]  R. Bernardo.  Molecular Markers and Selection for Complex Traits in Plants: Learning from the Last 20 Years , 2008 .

[71]  S. Leath,et al.  Effects of the Ht, Ht2, and/or Ht3 genes in three maize inbreds on quantitative resistance to Exserohilum turcicum race 2 , 1986 .

[72]  H. Geiger,et al.  Genetic Structure of Setosphaeria turcica Populations in Tropical and Temperate Climates. , 1998, Phytopathology.

[73]  Y. Levy,et al.  Epidemiology of Northern leaf blight on sweet corn , 1992, Phytoparasitica.

[74]  Z. Cao,et al.  MAP kinase gene STK1 is required for hyphal, conidial, and appressorial development, toxin biosynthesis, pathogenicity, and hypertonic stress response in the plant pathogenic fungus Setosphaeria turcica , 2016 .

[75]  Albrecht E. Melchinger,et al.  Genomic Prediction of Northern Corn Leaf Blight Resistance in Maize with Combined or Separated Training Sets for Heterotic Groups , 2013, G3: Genes | Genomes | Genetics.

[76]  M. Lee,et al.  Interval mapping of genes for quantitative resistance of maize to Setosphaeria turcica, cause of northern leaf blight, in a tropical environment , 1996, Molecular Breeding.

[77]  H. H. Flor.  The Complementary Genic Systems in Flax and Flax Rust , 1956 .

[78]  J. Juvik,et al.  Quantitative Trait Loci in Sweet Corn Associated with Partial Resistance to Stewart's Wilt, Northern Corn Leaf Blight, and Common Rust. , 2001, Phytopathology.

[79]  R. Nelson,et al.  Unraveling Genomic Complexity at a Quantitative Disease Resistance Locus in Maize , 2014, Genetics.

[80]  R. Nelson,et al.  A remorin gene is implicated in quantitative disease resistance in maize , 2016, Theoretical and Applied Genetics.

[81]  M. Rostás.  The effects of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one on two species of Spodoptera and the growth of Setosphaeria turcica in vitro , 2007, Journal of Pest Science.

[82]  S. Bentolila,et al.  Identification of an RFLP marker tightly linked to theHt1 gene in maize , 1991, Theoretical and Applied Genetics.

[83]  F. Qiu,et al.  Mapping of HtNB, a gene conferring non-lesion resistance before heading to Exserohilum turcicum (Pass.), in a maize inbred line derived from the Indonesian variety Bramadi. , 2012, Genetics and molecular research : GMR.

[84]  W. Mengesha.  Genetic diversity, stability, and combining ability of maize genotypes for grain yield and resistance to NCLB in the mid-altitude sub-humid agro ecologies of Ethiopia. , 2013 .

[85]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[86]  Shi-Hong Zhang,et al.  Efficacy assessment of antifungal metabolites from Chaetomium globosum No.05, a new biocontrol agent, against Setosphaeria turcica , 2013 .

[87]  M Frey,et al.  Analysis of a chemical plant defense mechanism in grasses. , 1997, Science.

[88]  M. Carson,et al.  Spatial Diversity of Setosphaeria turcica Sampled from the Eastern United States. , 2004, Phytopathology.

[89]  S. Prathuangwong,et al.  Sexual Reproduction of Setosphaeria turcica in Natural Corn Fields in Thailand , 2014 .

[90]  R. Frankham.  Introduction to quantitative genetics (4th edn): by Douglas S. Falconer and Trudy F.C. Mackay Longman, 1996. £24.99 pbk (xv and 464 pages) ISBN 0582 24302 5 , 1996 .

[91]  G. Tusiime,et al.  Response to two cycles of S1 recurrent selection for turcicum leave blight in anopen pollinated maize variety population (Longe 5) , 2015 .

[92]  A. Hooker.  A Second Major Gene Locus in Corn for Chlorotic-Lesion Resistance to Helminthosporium turicum 1 , 1977 .

[93]  H. Geiger,et al.  Genetics of quantitative resistance to fungal diseases , 1989 .

[94]  Y. Levy.  Differential Effect of Light on Spore Germination ofExserohilum turcicumon Corn Leaves and Corn Leaf Impressions , 1983 .

[95]  ScienceOpen Admin.  Genomic Prediction , 2019 .

[96]  P. Sirithunya,et al.  Study of the host range of Northern Corn Leaf Blight disease and effect of Exserohilum turcicum toxin on sweet corn. , 2015 .

[97]  J. M. Al-Khayri,et al.  Advances in Plant Breeding Strategies: Agronomic, Abiotic and Biotic Stress Traits , 2016, Springer International Publishing.

[98]  Y. Levy,et al.  Involvement of a phytotoxic peptide in the development of the Northern leaf blight of corn , 1996, European journal of plant pathology.

[99]  H. Geiger,et al.  QTL for Resistance to Setosphaeria turcica in Tropical African Maize , 1999 .

[100]  Jianbing Yan,et al.  Mapping of QTL conferring resistance to northern corn leaf blight using high-density SNPs in maize , 2015, Molecular Breeding.

[101]  H. Welz,et al.  Generation means and combining ability analysis of resistance to Setosphaeria turcica in African maize , 1997 .

[102]  V. Walbot,et al.  Disease lesion mimics in maize. I. Effect of genetic background, temperature, developmental age, and wounding on necrotic spot formation with Les1. , 1982, Developmental biology.

[103]  M. Sachs,et al.  Protein Synthesis in Maize during Anaerobic and Heat Stress. , 1992, Plant physiology.

[104]  Chris Haley,et al.  Efficiency of marker assisted selection , 1997 .

[105]  Shizhong Xu,et al.  Efficiency of multistage marker-assisted selection in the improvement of multiple quantitative traits , 1998, Heredity.

[106]  R. Bernardo,et al.  Genomewide Association Mapping of Flowering Time, Kernel Composition, and Disease Resistance in Historical Minnesota Maize Inbreds , 2013 .

[107]  D. Sumner,et al.  Effects of Reduced Tillage and Multiple Cropping on Plant Diseases , 1981 .

[108]  Jean-Luc Jannink,et al.  Genomic selection in plant breeding: from theory to practice. , 2010, Briefings in functional genomics.

[109]  J. Pataky.  Stewart's Wilt of Corn , 2003 .

[110]  A. Fourie,et al.  Field evaluation of maize inbred lines for resistance to Exserohilum turcicum , 2011 .

[111]  A. Macone,et al.  A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides , 2010, Proceedings of the National Academy of Sciences.

[112]  R. Lande,et al.  Efficiency of marker-assisted selection in the improvement of quantitative traits. , 1990, Genetics.

[113]  B. McDonald,et al.  Pathogen population genetics, evolutionary potential, and durable resistance. , 2002, Annual review of phytopathology.