Genome-wide association study of maize resistance to Pythium aristosporum stalk rot

Stalk rot, a severe and widespread soil-borne disease in maize, globally reduces yield and quality. Recent documentation reveals that Pythium aristosporum has emerged as one of the dominant causal agents of maize stalk rot. However, a previous study of maize stalk rot disease resistance mechanisms and breeding had mainly focused on other pathogens, neglecting P. aristosporum. To mitigate crop loss, resistance breeding is the most economical and effective strategy against this disease. This study involved characterizing resistance in 295 inbred lines using the drilling inoculation method and genotyping them via sequencing. By combining with population structure, disease resistance phenotype, and genome-wide association study (GWAS), we identified 39 significant single-nucleotide polymorphisms (SNPs) associated with P. aristosporum stalk rot resistance by utilizing six statistical methods. Bioinformatics analysis of these SNPs revealed 69 potential resistance genes, among which Zm00001d051313 was finally evaluated for its roles in host defense response to P. aristosporum infection. Through virus-induced gene silencing (VIGS) verification and physiological index determination, we found that transient silencing of Zm00001d051313 promoted P. aristosporum infection, indicating a positive regulatory role of this gene in maize’s antifungal defense mechanism. Therefore, these findings will help advance our current understanding of the underlying mechanisms of maize defense to Pythium stalk rot.

[1]  Zhendong Zhu,et al.  Integrative transcriptome and proteome analysis reveals maize responses to Fusarium verticillioides infection inside the stalks , 2023, Molecular plant pathology.

[2]  P. Balint-Kurti,et al.  A Leucine Rich Repeat Receptor Kinase Gene Confers Quantitative Susceptibility to Maize Southern Leaf Blight. , 2023, The New phytologist.

[3]  S. Nair,et al.  Identification and validation of a key genomic region on chromosome 6 for resistance to Fusarium stalk rot in tropical maize , 2022, TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik.

[4]  Ruyang Zhang,et al.  RppM, Encoding a Typical CC-NBS-LRR Protein, Confers Resistance to Southern Corn Rust in Maize , 2022, Frontiers in Plant Science.

[5]  Baobao Wang,et al.  Genomic insights into historical improvement of heterotic groups during modern hybrid maize breeding , 2022, Nature Plants.

[6]  C. Zipfel,et al.  Molecular mechanisms of early plant pattern-triggered immune signaling. , 2021, Molecular cell.

[7]  Y. Pei,et al.  Phytophthora sojae leucine-rich repeat receptor-like kinases: diverse and essential roles in development and pathogenicity , 2021, iScience.

[8]  Zhendong Zhu,et al.  First Report of Maize Stalk Rot Caused by Fusarium kyushuense in China. , 2021, Plant disease.

[9]  Xiaohe Yang,et al.  First report of Pythium aristosporum causing corn stalk rot in China. , 2021, Plant disease.

[10]  Yuanxin Yan,et al.  An updated census of the maize TIFY family , 2021, PloS one.

[11]  Shuangshuang Liu,et al.  Combination of Genome-Wide Association Study and QTL Mapping Reveals the Genetic Architecture of Fusarium Stalk Rot in Maize , 2021, Frontiers in Agronomy.

[12]  Guanghui Hu,et al.  Development of an inoculation technique for rapidly evaluating maize inbred lines for resistance to stalk rot caused by Fusarium spp. in the field. , 2020, Plant disease.

[13]  Zhiwu Zhang,et al.  GAPIT Version 3: Boosting Power and Accuracy for Genomic Association and Prediction , 2020, bioRxiv.

[14]  David T. W. Tzeng,et al.  Reconstructing the maize leaf regulatory network using ChIP-seq data of 104 transcription factors , 2020, Nature Communications.

[15]  Yasubumi Sakakibara,et al.  RNA secondary structure prediction using deep learning with thermodynamic integration , 2020, Nature Communications.

[16]  Hang He,et al.  Genome-wide selection and genetic improvement during modern maize breeding , 2020, Nature Genetics.

[17]  V. Ranwez,et al.  Origin and Diversity of Plant Receptor-Like Kinases. , 2020, Annual review of plant biology.

[18]  Jarrett Man,et al.  Structural evolution drives diversification of the large LRR‐RLK gene family , 2020, The New phytologist.

[19]  Mingliang Xu,et al.  Combined genome-wide association study and transcriptome analysis reveal candidate genes for resistance to Fusarium ear rot in maize. , 2020, Journal of integrative plant biology.

[20]  T. Lübberstedt,et al.  Integrating a genome-wide association study with transcriptomic analysis to detect genes controlling grain drying rate in maize (Zea may, L.) , 2019, Theoretical and Applied Genetics.

[21]  A. Ghafoor,et al.  Genome-wide association studies of seven agronomic traits under two sowing conditions in bread wheat , 2019, BMC Plant Biology.

[22]  Zhendong Zhu,et al.  Characterization and Molecular Mapping of Two Novel Genes Resistant to Pythium Stalk Rot in Maize. , 2019, Phytopathology.

[23]  Dongfen Zhang,et al.  The Auxin-Regulated Protein ZmAuxRP1 Coordinates the Balance between Root Growth and Stalk Rot Disease Resistance in Maize. , 2019, Molecular plant.

[24]  Z. Fei,et al.  Genomic analyses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history , 2019, Genome Biology.

[25]  Zhiwu Zhang,et al.  BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions , 2018, GigaScience.

[26]  Junyi Yin,et al.  Genome-Wide Association Studies of Photosynthetic Traits Related to Phosphorus Efficiency in Soybean , 2018, Front. Plant Sci..

[27]  Antônio Teixeira do Amaral Júnior,et al.  Genome wide association study for gray leaf spot resistance in tropical maize core , 2018, PloS one.

[28]  Kenneth L. McNally,et al.  Genomic variation in 3,010 diverse accessions of Asian cultivated rice , 2018, Nature.

[29]  Xiaolan Rao,et al.  An Improved Brome mosaic virus Silencing Vector: Greater Insert Stability and More Extensive VIGS1[OPEN] , 2017, Plant Physiology.

[30]  Dongfen Zhang,et al.  A transposon-directed epigenetic change in ZmCCT underlies quantitative resistance to Gibberella stalk rot in maize. , 2017, The New phytologist.

[31]  J. Gai,et al.  Identification of Major Quantitative Trait Loci for Seed Oil Content in Soybeans by Combining Linkage and Genome-Wide Association Mapping , 2017, Front. Plant Sci..

[32]  Congwei Sun,et al.  Genome‐wide association study for 13 agronomic traits reveals distribution of superior alleles in bread wheat from the Yellow and Huai Valley of China , 2017, Plant biotechnology journal.

[33]  J. Batley,et al.  Genotyping‐by‐sequencing approaches to characterize crop genomes: choosing the right tool for the right application , 2017, Plant biotechnology journal.

[34]  Pradeep K. Singh,et al.  Genomic Selection in the Era of Next Generation Sequencing for Complex Traits in Plant Breeding , 2016, Front. Genet..

[35]  B. Olukolu,et al.  A Genome-Wide Association Study for Partial Resistance to Maize Common Rust. , 2016, Phytopathology.

[36]  Jun Wang,et al.  Analytical and Decision Support Tools for Genomics-Assisted Breeding. , 2016, Trends in plant science.

[37]  Yufeng Wang,et al.  Cellular Tracking and Gene Profiling of Fusarium graminearum during Maize Stalk Rot Disease Development Elucidates Its Strategies in Confronting Phosphorus Limitation in the Host Apoplast , 2016, PLoS pathogens.

[38]  Zhiwu Zhang,et al.  Iterative Usage of Fixed and Random Effect Models for Powerful and Efficient Genome-Wide Association Studies , 2016, PLoS genetics.

[39]  Jianbing Yan,et al.  Genome-Wide Association Implicates Candidate Genes Conferring Resistance to Maize Rough Dwarf Disease in Maize , 2015, PloS one.

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

[41]  H. Hirt,et al.  Signaling mechanisms in pattern-triggered immunity (PTI). , 2015, Molecular plant.

[42]  Zhendong Zhu,et al.  Two genes conferring resistance to Pythium stalk rot in maize inbred line Qi319 , 2015, Molecular Genetics and Genomics.

[43]  Hui Xiang,et al.  Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean , 2015, Nature Biotechnology.

[44]  Edward S. Buckler,et al.  A SUPER Powerful Method for Genome Wide Association Study , 2014, PloS one.

[45]  F. Ali,et al.  Genome Wide Association Studies Using a New Nonparametric Model Reveal the Genetic Architecture of 17 Agronomic Traits in an Enlarged Maize Association Panel , 2014, PLoS genetics.

[46]  C. Zipfel Plant pattern-recognition receptors. , 2014, Trends in immunology.

[47]  A. Furtado,et al.  Protocol: a simple method for extracting next-generation sequencing quality genomic DNA from recalcitrant plant species , 2014, Plant Methods.

[48]  R. S. Nelson,et al.  Maize Elongin C interacts with the viral genome-linked protein, VPg, of Sugarcane mosaic virus and facilitates virus infection , 2014, The New phytologist.

[49]  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.

[50]  Yanyong Cao,et al.  Possible involvement of maize Rop1 in the defence responses of plants to viral infection. , 2012, Molecular plant pathology.

[51]  Bjarni J. Vilhjálmsson,et al.  An efficient multi-locus mixed model approach for genome-wide association studies in structured populations , 2012, Nature Genetics.

[52]  Mark H. Wright,et al.  Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa , 2011, Nature communications.

[53]  Peter J. Bradbury,et al.  Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population , 2011, Nature Genetics.

[54]  P. Visscher,et al.  GCTA: a tool for genome-wide complex trait analysis. , 2011, American journal of human genetics.

[55]  Meng Li,et al.  Genome-wide association studies of 14 agronomic traits in rice landraces , 2010, Nature Genetics.

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

[57]  H. Hakonarson,et al.  ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data , 2010, Nucleic acids research.

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

[59]  In Sun Hwang,et al.  The Pepper 9-Lipoxygenase Gene CaLOX1 Functions in Defense and Cell Death Responses to Microbial Pathogens1[C][W][OA] , 2009, Plant Physiology.

[60]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[61]  E. Buckler,et al.  Genetic association mapping and genome organization of maize. , 2006, Current opinion in biotechnology.

[62]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[63]  S. Chen,et al.  Characterization and mapping of Rpi1, a gene that confers dominant resistance to stalk rot in maize , 2005, Molecular Genetics and Genomics.

[64]  J. Peleman,et al.  Breeding by design. , 2003, Trends in plant science.

[65]  Mark Jung,et al.  SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines , 2002, BMC Genetics.

[66]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[67]  D. Davies,et al.  Early signalling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2. , 2001, The New phytologist.

[68]  R. Tarchini,et al.  Mapping quantitative trait loci (QTLs) for resistance to Gibberella zeae infection in maize , 1993, Molecular and General Genetics MGG.

[69]  J. Ribaut,et al.  Inclusive composite interval mapping (ICIM) for digenic epistasis of quantitative traits in biparental populations , 2007, Theoretical and Applied Genetics.

[70]  L. Shun Study on Inoculated Methods of Corn Stalk Rot , 2001 .

[71]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[72]  D. White,et al.  Inheritance of resistance to anthracnose stalk rot of corn , 1993 .