Quantitative Disease Resistance: Dissection and Adoption in Maize.

Maize is the world's most produced crop, providing food, feed, and biofuel. Maize production is constantly threatened by the presence of devastating pathogens worldwide. Characterization of the genetic components underlying disease resistance is a major research area in maize which is highly relevant for resistance breeding programs. Quantitative disease resistance (QDR) is the type of resistance most widely used by maize breeders. The past decade has witnessed significant progress in fine-mapping and cloning of genes controlling QDR. The molecular mechanisms underlying QDR remain poorly understood and exploited. In this review we discuss recent advances in maize QDR research and strategy for resistance breeding.

[1]  K. Korus,et al.  First Report of Goss's Bacterial Leaf Blight and Wilt of Corn Caused by Clavibacter michiganensis subsp. nebraskensis in North Dakota. , 2014, Plant disease.

[2]  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.

[3]  F. Katagiri,et al.  Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. , 2010, Current opinion in plant biology.

[4]  A. J. Ullstrup,et al.  Linkage Relationships of a Gene in Corn Determining Susceptibility to a Helminthosporium Leaf Spot 1 , 1947 .

[5]  R. Sharma,et al.  Diseases of maize in South and South-East Asia: Problems and progress , 1993 .

[6]  Martin S. Taylor,et al.  Genome-wide genetic association of complex traits in heterogeneous stock mice , 2006, Nature Genetics.

[7]  Jinsheng Lai,et al.  An Atypical Thioredoxin Imparts Early Resistance to Sugarcane Mosaic Virus in Maize. , 2017, Molecular plant.

[8]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[9]  Roy Johnson.  Durable resistance: definition of, genetic control, and attainment in plant breeding. , 1981 .

[10]  Genlou Sun,et al.  Molecular mapping of QTLs for resistance to Gibberella ear rot, in corn, caused by Fusarium graminearum. , 2005, Genome.

[11]  Jason G. Wallace,et al.  Entering the second century of maize quantitative genetics , 2013, Heredity.

[12]  J. Dubcovsky,et al.  A Kinase-START Gene Confers Temperature-Dependent Resistance to Wheat Stripe Rust , 2009, Science.

[13]  T. Marcel,et al.  Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. , 2015, Annual review of phytopathology.

[14]  Wei Chen,et al.  High-resolution mapping and characterization of qRgls2, a major quantitative trait locus involved in maize resistance to gray leaf spot , 2014, BMC Plant Biology.

[15]  W. Tracy,et al.  Widespread Occurrence of Common Rust, Caused by Puccinia sorghi, on Rp-Resistant Sweet Corn in the Midwestern United States. , 1999, Plant disease.

[16]  H. Piepho,et al.  QTL detection power of multi-parental RIL populations in Arabidopsis thaliana , 2012, Heredity.

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

[18]  P. Goldsbrough,et al.  Heterogeneous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci , 1997, Theoretical and Applied Genetics.

[19]  H. O. Gevers,et al.  Diallel cross analysis of resistance to gray leaf spot in maize , 1994 .

[20]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[21]  J. Pataky,et al.  Reduction in Common Rust Severity Conferred by the Rp1D Gene in Sweet Corn Hybrids Infected by Mixtures of Rp1D-Virulent and Avirulent Puccinia sorghi. , 2007, Plant disease.

[22]  Yan Xu,et al.  Genetic analysis and molecular mapping of two dominant complementary genes determining resistance to sugarcane mosaic virus in maize , 2007, Euphytica.

[23]  B. Cassone,et al.  Maize Lethal Necrosis (MLN), an Emerging Threat to Maize-Based Food Security in Sub-Saharan Africa. , 2015, Phytopathology.

[24]  M. Latif,et al.  Molecular progress on the mapping and cloning of functional genes for blast disease in rice (Oryza sativa L.): current status and future considerations , 2016, Critical reviews in biotechnology.

[25]  N. Ranc,et al.  Usefulness of Multiparental Populations of Maize (Zea mays L.) for Genome-Based Prediction , 2014, Genetics.

[26]  P. J. Maughan,et al.  SNP genotyping using KASPar assays. , 2015, Methods in molecular biology.

[27]  John P. Rathjen,et al.  Plant immunity: towards an integrated view of plant–pathogen interactions , 2010, Nature Reviews Genetics.

[28]  S. Salvi,et al.  To clone or not to clone plant QTLs: present and future challenges. , 2005, Trends in plant science.

[29]  D. K. Willis,et al.  Copy Number Variation of Multiple Genes at Rhg1 Mediates Nematode Resistance in Soybean , 2012, Science.

[30]  Dongfen Zhang,et al.  A sequential quantitative trait locus fine-mapping strategy using recombinant-derived progeny. , 2012, Journal of integrative plant biology.

[31]  Rui Wang,et al.  Molecular dynamics simulations of interaction between protein-tyrosine phosphatase 1B and a bidentate inhibitor , 2006, Acta Pharmacologica Sinica.

[32]  Yunhua Zhang,et al.  Evaluation of maize inbred lines currently used in Chinese breeding programs for resistance to six foliar diseases , 2014 .

[33]  D. S. St. Clair,et al.  Quantitative disease resistance and quantitative resistance Loci in breeding. , 2010, Annual review of phytopathology.

[34]  D. White,et al.  Compendium of corn diseases , 1999 .

[35]  J. Hawk,et al.  Fitness Evaluation of Rcg1, a Locus that Confers Resistance to Colletotrichum graminicola (Ces.) G.W. Wils. Using Near-Isogenic Maize Hybrids , 2011 .

[36]  Norikuni Saka,et al.  Loss of Function of a Proline-Containing Protein Confers Durable Disease Resistance in Rice , 2009, Science.

[37]  David Mackey,et al.  Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. , 2007, Annual review of phytopathology.

[38]  G. Miller,et al.  First Report of Goss’s Bacterial Wilt and Leaf Blight on Corn Caused by Clavibacter michiganensis subsp. nebraskensis in Missouri , 2016 .

[39]  Frederik Coppens,et al.  Genetic properties of the MAGIC maize population: a new platform for high definition QTL mapping in Zea mays , 2015, Genome Biology.

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

[41]  Baobao Wang,et al.  Combined linkage and association mapping reveals candidates for Scmv1, a major locus involved in resistance to sugarcane mosaic virus (SCMV) in maize , 2013, BMC Plant Biology.

[42]  Jing Zhao,et al.  A maize wall-associated kinase confers quantitative resistance to head smut , 2014, Nature Genetics.

[43]  N. Katis,et al.  First report of Maize rough dwarf virus (MRDV) on maize crops in Greece , 2004 .

[44]  James K. M. Brown.  Durable resistance of crops to disease: a Darwinian perspective. , 2015, Annual review of phytopathology.

[45]  B. Keller,et al.  A Putative ABC Transporter Confers Durable Resistance to Multiple Fungal Pathogens in Wheat , 2009, Science.

[46]  Wei Chen,et al.  QTL mapping of resistance to gray leaf spot in maize , 2012, Theoretical and Applied Genetics.

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

[48]  J. Ellis,et al.  Molecular Characterization of the Maize Rp1-D Rust Resistance Haplotype and Its Mutants , 1999, Plant Cell.

[49]  Weixi Li,et al.  Identification of Pathogenic Fusarium spp. Causing Maize Ear Rot and Potential Mycotoxin Production in China , 2016, Toxins.

[50]  Kevin L. Childs,et al.  Draft Assembly of Elite Inbred Line PH207 Provides Insights into Genomic and Transcriptome Diversity in Maize[OPEN] , 2016, Plant Cell.

[51]  Zhang Chunyu,et al.  Pyramiding resistance genes to northern leaf blight and head smut in maize. , 2012 .

[52]  Tyr Wiesner-Hanks,et al.  Multiple Disease Resistance in Plants. , 2016, Annual review of phytopathology.

[53]  Shaojiang Chen,et al.  A major QTL for resistance to Gibberella stalk rot in maize , 2010, Theoretical and Applied Genetics.

[54]  J. Anderson,et al.  Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight , 2016, Nature Genetics.

[55]  M. Krakowsky,et al.  Identification of Alleles Conferring Resistance to Gray Leaf Spot in Maize Derived from its Wild Progenitor Species Teosinte , 2016 .

[56]  J. Chen,et al.  Genome-wide genetic changes during modern breeding of maize , 2012, Nature Genetics.

[57]  S. Briggs,et al.  Reductase activity encoded by the HM1 disease resistance gene in maize. , 1992, Science.

[58]  R. Doerge.  Multifactorial genetics: Mapping and analysis of quantitative trait loci in experimental populations , 2002, Nature Reviews Genetics.

[59]  J. Patrick,et al.  A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat , 2015, Nature Genetics.

[60]  J. Pataky,et al.  First Report of Puccinia sorghi Virulent on Sweet Corn with the Rp1-D Gene in Florida and Texas. , 2000, Plant disease.

[61]  Construction of high-quality recombination maps with low-coverage genomic sequencing for joint linkage analysis in maize , 2015, BMC Biology.

[62]  K. Abdullah,et al.  The TaqMan method for SNP genotyping. , 2009, Methods in molecular biology.

[63]  S. Tragoonrung,et al.  QTL Mapping for Partial Resistance to Southern Corn Rust Using RILs of Tropical Sweet Corn , 2013 .

[64]  Yanjun Kou,et al.  Broad-spectrum and durability: understanding of quantitative disease resistance. , 2010, Current opinion in plant biology.

[65]  R. Nelson,et al.  Characterization and fine-mapping of a resistance locus for northern leaf blight in maize bin 8.06 , 2010, Theoretical and Applied Genetics.

[66]  R. Howard,et al.  First Report of Goss’s Bacterial Wilt and Leaf Blight on Corn Caused by Clavibacter michiganensis subsp. nebraskensis in Alberta, Canada , 2015 .

[67]  K. Korus,et al.  First Report of Goss's Bacterial Wilt and Leaf Blight (Clavibacter michiganensis subsp. nebraskensis) of Corn in Texas. , 2011, Plant disease.

[68]  G. Xia,et al.  From genome to gene: a new epoch for wheat research? , 2015, Trends in plant science.

[69]  Mingliang Xu,et al.  Marker-assisted introgression of qHSR1 to improve maize resistance to head smut , 2012, Molecular breeding.

[70]  S. Hulbert.  Structure and evolution of the rp1 complex conferring rust resistance in maize. , 1997, Annual review of phytopathology.

[71]  B. Thomma,et al.  Of PAMPs and Effectors: The Blurred PTI-ETI Dichotomy[OA] , 2011, Plant Cell.

[72]  Jian Hong,et al.  Characterization of Maize Chlorotic Mottle Virus Associated with Maize Lethal Necrosis Disease in China , 2011 .

[73]  B. S. Dhillon,et al.  Colocalization of QTL for Gibberella Ear Rot Resistance and Low Mycotoxin Contamination in Early European Maize , 2011 .

[74]  K. Cardwell,et al.  Seed transmission of maize downy mildew (Peronosclerospora sorghi) in Nigeria , 2000 .

[75]  R. Nelson,et al.  Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene , 2011, Proceedings of the National Academy of Sciences.

[76]  A. J. Ullstrup.  The Impacts of the Southern Corn Leaf Blight Epidemics of 1970-1971 , 1972 .

[77]  Baobao Wang,et al.  Identification and fine-mapping of a QTL, qMrdd1, that confers recessive resistance to maize rough dwarf disease , 2013, BMC Plant Biology.

[78]  D. Roby,et al.  An Atypical Kinase under Balancing Selection Confers Broad-Spectrum Disease Resistance in Arabidopsis , 2013, PLoS genetics.

[79]  Anne-Katrin Mahlein.  Plant Disease Detection by Imaging Sensors - Parallels and Specific Demands for Precision Agriculture and Plant Phenotyping. , 2016, Plant disease.

[80]  J. Ledeaux,et al.  QTL mapping with near-isogenic lines in maize , 2007, Theoretical and Applied Genetics.

[81]  Werner B. Herppich,et al.  Hyperspectral and Chlorophyll Fluorescence Imaging to Analyse the Impact of Fusarium culmorum on the Photosynthetic Integrity of Infected Wheat Ears , 2011, Sensors.

[82]  D. Charlesworth,et al.  The genetics of inbreeding depression , 2009, Nature Reviews Genetics.

[83]  Shaojiang Chen,et al.  Fine-mapping of qRfg2, a QTL for resistance to Gibberella stalk rot in maize , 2011, Theoretical and Applied Genetics.

[84]  James B. Holland.  MAGIC maize: a new resource for plant genetics , 2015, Genome Biology.

[85]  Jinsheng Lai,et al.  Identification and fine mapping of rhm1 locus for resistance to Southern corn leaf blight in maize. , 2012, Journal of integrative plant biology.

[86]  K. Leonard.  Virulence, Temperature Optima, and Competitive Abilities of Isolines of Races T and O of Bipolaris maydis , 1977 .

[87]  A. Levine,et al.  The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea , 2000, Current Biology.

[88]  Damon L. Smith,et al.  Corn yield loss estimates due to diseases in the United States and Ontario, Canada from 2012 to 2015. , 2016 .

[89]  B. Keller,et al.  Molecular genetics and evolution of disease resistance in cereals. , 2016, The New phytologist.

[90]  A. Melchinger,et al.  High-resolution mapping of loci conferring resistance to sugarcane mosaic virus in maize using RFLP, SSR, and AFLP markers , 1999, Molecular and General Genetics MGG.

[91]  T. Pryor,et al.  Recombination between paralogues at the Rp1 rust resistance locus in maize. , 2001, Genetics.

[92]  Martin Lagat,et al.  Quantitative trait loci (QTLs) for resistance to gray leaf spot and common rust diseases of maize , 2008 .

[93]  John Doebley,et al.  Maize association population: a high-resolution platform for quantitative trait locus dissection. , 2005, The Plant journal : for cell and molecular biology.

[94]  R. Nelson,et al.  Shades of gray: the world of quantitative disease resistance. , 2009, Trends in plant science.

[95]  V. Walbot.  Maize genome in motion , 2008, Genome Biology.

[96]  Construction of the third generation Zea mays haplotype map , 2015 .

[97]  Mingliang Xu,et al.  The genetic and molecular basis of plant resistance to pathogens. , 2013, Journal of genetics and genomics = Yi chuan xue bao.

[98]  M. McMullen,et al.  Genetic Properties of the Maize Nested Association Mapping Population , 2009, Science.

[99]  J. Pataky,et al.  Puccinia sorghi in Sinaloa, Mexico Virulent on Corn with the Rp1-D Gene. , 2000, Plant disease.

[100]  Thomas Meitinger,et al.  A powerful tool for genome analysis in maize: development and evaluation of the high density 600 k SNP genotyping array , 2014, BMC Genomics.

[101]  M. Zhang,et al.  The resistance to banded leaf and sheath blight in maize of 282 inbred lines , 2013 .

[102]  M. McMullen,et al.  Genetic Design and Statistical Power of Nested Association Mapping in Maize , 2008, Genetics.

[103]  Christian Bauckhage,et al.  Metro Maps of Plant Disease Dynamics—Automated Mining of Differences Using Hyperspectral Images , 2015, PloS one.

[104]  J. Holland,et al.  Yield Effects of Two Southern Leaf Blight Resistance Loci in Maize Hybrids , 2014 .

[105]  A. Iyer-Pascuzzi,et al.  Mechanisms of quantitative disease resistance in plants. , 2016, Seminars in cell & developmental biology.

[106]  T. Isakeit,et al.  Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. , 2009, Molecular plant-microbe interactions : MPMI.

[107]  Darren P Martin,et al.  Maize streak virus: an old and complex 'emerging' pathogen. , 2010, Molecular plant pathology.

[108]  D. quito-avila,et al.  Occurrence of maize lethal necrosis in Ecuador: a disease without boundaries? , 2016, European Journal of Plant Pathology.

[109]  G. Payne,et al.  QTL Mapping for Fusarium Ear Rot and Fumonisin Contamination Resistance in Two Maize Populations , 2006 .

[110]  Xun Xu,et al.  Comparative population genomics of maize domestication and improvement , 2012, Nature Genetics.

[111]  K. Wise,et al.  First Report of Goss's Bacterial Wilt and Leaf Blight on Corn Caused by Clavibacter michiganensis subsp. nebraskensis in Indiana. , 2009, Plant disease.

[112]  Chuanxiao Xie,et al.  Identification of a major quantitative trait locus for resistance to maize rough dwarf virus in a Chinese maize inbred line X178 using a linkage map based on 514 gene-derived single nucleotide polymorphisms , 2011, Molecular Breeding.

[113]  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.

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

[115]  V. Rhoades,et al.  The Location of a Gene for Disease Resistance in Maize. , 1935, Proceedings of the National Academy of Sciences of the United States of America.

[116]  Y. Xing,et al.  Analysis of sugarcane mosaic virus resistance in maize in an isogenic dihybrid crossing scheme and implications for breeding potyvirus-resistant maize hybrids. , 2006, Genome.

[117]  Xiaojun Wu,et al.  Fine mapping of RppP25, a southern rust resistance gene in maize. , 2013, Journal of integrative plant biology.

[118]  Jian Wang,et al.  Genome-wide patterns of genetic variation among elite maize inbred lines , 2010, Nature Genetics.

[119]  A. Paterson,et al.  Generation-means analysis and quantitative trait locus mapping of anthracnose stalk rot genes in maize , 1994, Theoretical and Applied Genetics.

[120]  Jing Zhao,et al.  Identification and fine-mapping of a major QTL conferring resistance against head smut in maize , 2008, Theoretical and Applied Genetics.

[121]  X.-D. Xu,et al.  First Report of Gray Leaf Spot of Maize Caused by Cercospora zeina in China. , 2013, Plant disease.

[122]  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.

[123]  S. Chander,et al.  QTL mapping of resistance to Fusarium ear rot using a RIL population in maize , 2008, Molecular Breeding.

[124]  D. Malvick,et al.  Goss's Bacterial Blight and Wilt of Corn Caused by Clavibacter michiganensis subsp. nebraskensis Occurs in Minnesota. , 2010, Plant disease.

[125]  R. Nielsen.  Corn Disease Management , 1993 .