Multi-Locus Genome-Wide Association Study Reveals the Genetic Architecture of Stalk Lodging Resistance-Related Traits in Maize

Stalk lodging resistance, which is mainly measured by stem diameter (SD), stalk bending strength (SBS), and rind penetrometer resistance (RPR) in maize, seriously affects the yield and quality of maize (Zea mays L.). To dissect its genetic architecture, in this study multi-locus genome-wide association studies for stalk lodging resistance-related traits were conducted in a population of 257 inbred lines, with tropical, subtropical, and temperate backgrounds, genotyped with 48,193 high-quality single nucleotide polymorphisms. The analyses of phenotypic variations for the above traits in three environments showed high broad-sense heritability (0.679, 0.720, and 0.854, respectively). In total, 423 significant Quantitative Trait Nucleotides (QTNs) were identified by mrMLM, FASTmrEMMA, ISIS EM-BLASSO, and pLARmEB methods to be associated with the above traits. Among these QTNs, 29, 34, and 48 were commonly detected by multiple methods or across multiple environments to be related to SD, SBS, and RPR, respectively. The superior allele analyses in 30 elite lines showed that only eight lines contained more than 50% of the superior alleles, indicating that stalk lodging resistance can be improved by the integration of more superior alleles. Among sixty-three candidate genes of the consistently expressed QTNs, GRMZM5G856734 and GRMZM2G116885, encoding membrane steroid-binding protein 1 and cyclin-dependent kinase inhibitor 1, respectively, possibly inhibit cell elongation and division, which regulates lodging resistance. Our results provide the further understanding of the genetic foundation of maize lodging resistance.

[1]  Zhiwu Zhang,et al.  Mixed linear model approach adapted for genome-wide association studies , 2010, Nature Genetics.

[2]  Tadashi Hirasawa,et al.  New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield , 2010, Nature communications.

[3]  Jianbing Yan,et al.  Genome-Wide Association Studies Identified Three Independent Polymorphisms Associated with α-Tocopherol Content in Maize Kernels , 2012, PloS one.

[4]  Qingfeng Meng,et al.  Effects of EDAH, a novel plant growth regulator, on mechanical strength, stalk vascular bundles and grain yield of summer maize at high densities , 2017 .

[5]  Michael D. McMullen,et al.  Quantitative Trait Locus Analysis of Stalk Strength in Four Maize Populations , 2003, Crop Science.

[6]  Shien Yang Lee,et al.  Preventing lodging in bioenergy crops: a biomechanical analysis of maize stalks suggests a new approach. , 2015, Journal of experimental botany.

[7]  K. Torii,et al.  Autonomy of cell proliferation and developmental programs during Arabidopsis aboveground organ morphogenesis. , 2007, Developmental biology.

[8]  D. Latchman Transcription factors: an overview. , 1997, The international journal of biochemistry & cell biology.

[9]  Xiaohong Yang,et al.  Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize , 2011, Molecular Breeding.

[10]  Jianbing Yan,et al.  Genome-wide association study (GWAS) of resistance to head smut in maize. , 2012, Plant science : an international journal of experimental plant biology.

[11]  R. Sekhon,et al.  Transcriptional and Metabolic Analysis of Senescence Induced by Preventing Pollination in Maize1[W][OA] , 2012, Plant Physiology.

[12]  A. Korte,et al.  The advantages and limitations of trait analysis with GWAS: a review , 2013, Plant Methods.

[13]  L. Gou Bending Mechanical Properties of Stalk and Lodging-Resistance of Maize ( Zea mays L.): Bending Mechanical Properties of Stalk and Lodging-Resistance of Maize ( Zea mays L.) , 2008 .

[14]  Andreas Graner,et al.  Whole genome sequencing-based association study to unravel genetic architecture of cooked grain width and length traits in rice , 2017, Scientific Reports.

[15]  Jin Zhang,et al.  Methodological implementation of mixed linear models in multi-locus genome-wide association studies , 2017, Briefings in bioinformatics.

[16]  B. Adelana Relationship between lodging, morphological characters and yield of tomato cultivars. , 1980 .

[17]  Jeffrey Ross-Ibarra,et al.  Genetic Architecture of Maize Kernel Composition in the Nested Association Mapping and Inbred Association Panels1[W] , 2011, Plant Physiology.

[18]  E. Togawa,et al.  Improvement of lodging resistance with QTLs for stem diameter in rice (Oryza sativa L.) , 2008, Theoretical and Applied Genetics.

[19]  Lisa C. Harper,et al.  The Locus Lookup tool at MaizeGDB: identification of genomic regions in maize by integrating sequence information with physical and genetic maps , 2010, Bioinform..

[20]  Xiaoqing Yu,et al.  Genomic prediction of seedling root length in maize (Zea mays L.). , 2015, The Plant journal : for cell and molecular biology.

[21]  E. Meyerowitz,et al.  The AP2/EREBP family of plant transcription factors. , 1998, Biological chemistry.

[22]  Hu Wei-wei Effects of Planting Densities and Modes on Stem Lodging Resistance of Summer Maize , 2011 .

[23]  H. Xue,et al.  Arabidopsis Membrane Steroid Binding Protein 1 Is Involved in Inhibition of Cell Elongationw⃞ , 2005, The Plant Cell Online.

[24]  G. Hagen,et al.  Auxin Response Factors , 2001, Journal of Plant Growth Regulation.

[25]  W. Ewens Genetics and analysis of quantitative traits , 1999 .

[26]  G. Pan,et al.  Transcription Factors Responding to Pb Stress in Maize , 2017, Genes.

[27]  T. Tesso,et al.  Stalk strength and reaction to infection by Macrophomina phaseolina of brown midrib maize (Zea mays) and sorghum (Sorghum bicolor) , 2011 .

[28]  J. Pritchard,et al.  Documentation for structure software : Version 2 . 3 , 2009 .

[29]  S. U. Remison,et al.  Relationship between lodging, morphological characters and yield of varieties of maize (Zea mays L.) , 1978, The Journal of Agricultural Science.

[30]  Y. Li,et al.  Ectopic expression of a novel OsExtensin‐like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice , 2017, Plant biotechnology journal.

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

[32]  Huijun Guo,et al.  Quantitative trait loci (QTL) of stem strength and related traits in a doubled-haploid population of wheat (Triticum aestivum L.) , 2005, Euphytica.

[33]  David Haussler,et al.  Long-read sequence assembly of the gorilla genome , 2016, Science.

[34]  P. Sharma Mechanics of materials. , 2010, Technology and health care : official journal of the European Society for Engineering and Medicine.

[35]  E. Buckler,et al.  Joint‐linkage mapping and GWAS reveal extensive genetic loci that regulate male inflorescence size in maize , 2016, Plant biotechnology journal.

[36]  Chuanxiao Xie,et al.  Genome-Wide Association Study Identifies Candidate Genes That Affect Plant Height in Chinese Elite Maize (Zea mays L.) Inbred Lines , 2011, PloS one.

[37]  Peter J. Bradbury,et al.  Genome-wide association study of leaf architecture in the maize nested association mapping population , 2011, Nature Genetics.

[38]  Yuan-Li Ni,et al.  Iterative sure independence screening EM-Bayesian LASSO algorithm for multi-locus genome-wide association studies , 2017, PLoS Comput. Biol..

[39]  W. M. Ross,et al.  Exact Confidence Intervals for Heritability on a Progeny Mean Basis1 , 1983 .

[40]  Haixiao Hu,et al.  Identifying quantitative trait loci and determining closely related stalk traits for rind penetrometer resistance in a high-oil maize population , 2012, Theoretical and Applied Genetics.

[41]  T. Perneger What's wrong with Bonferroni adjustments , 1998, BMJ.

[42]  S. Morita,et al.  Countermeasures for heat damage in rice grain quality under climate change , 2016 .

[43]  Haixiao Hu,et al.  QTL mapping of stalk bending strength in a recombinant inbred line maize population , 2013, Theoretical and Applied Genetics.

[44]  Gang Zhao,et al.  Effect of planting density on lodging-related morphology, lodging rate, and yield of tartary buckwheat (Fagopyrum tataricum) , 2016 .

[45]  Quantitative Trait Locus Analysis of Stalk Strength in Four Maize Populations , 2003 .

[46]  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.

[47]  C. L. Tamba,et al.  pLARmEB: integration of least angle regression with empirical Bayes for multilocus genome-wide association studies , 2017, Heredity.

[48]  Bo Huang,et al.  Improving power and accuracy of genome-wide association studies via a multi-locus mixed linear model methodology , 2016, Scientific Reports.

[49]  Xiaohong Yang,et al.  Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels , 2012, Nature Genetics.