Genome-wide association study reveals the genetic basis of brace root angle and diameter in maize

Brace roots are the main organ to support the above-ground part of maize plant. It involves in plant growth and development by water absorption and lodging resistance. The bracing root angle (BRA) and diameter (BRD) are important components of brace root traits. Illuminating the genetic basis of BRA and BRD will contribute the improvement for mechanized harvest and increasing production. A GWAS of BRA and BRD was conducted using an associated panel composed of 508 inbred lines of maize. The broad-sense heritability of BRA and BRD was estimated to be respectively 71% ± 0.19 and 52% ± 0.14. The phenotypic variation of BRA and BRD in the non-stiff stalk subgroup (NSS) and the stiff stalk subgroup (SS) subgroups are significantly higher than that in the tropical/subtropical subgroup (TST) subgroups. In addition, BRA and BRD are significantly positive with plant height (PH), ear length (EL), and kernel number per row (KNPR). GWAS revealed 27 candidate genes within the threshold of p < 1.84 × 10−6 by both MLM and BLINK models. Among them, three genes, GRMZM2G174736, GRMZM2G445169 and GRMZM2G479243 were involved in cell wall function, and GRMZM2G038073 encoded the NAC transcription factor family proteins. These results provide theoretical support for clarifying the genetic basis of brace roots traits.

[1]  K. Gaikwad,et al.  Single trait versus principal component based association analysis for flowering related traits in pigeonpea , 2022, Scientific Reports.

[2]  Z. Cui,et al.  A Genome-Wide Association Study Dissects the Genetic Architecture of the Metaxylem Vessel Number in Maize Brace Roots , 2022, Frontiers in Plant Science.

[3]  Bailin Li,et al.  Identification of genetic loci associated with rough dwarf disease resistance in maize by integrating GWAS and linkage mapping. , 2021, Plant science : an international journal of experimental plant biology.

[4]  Bowen Luo,et al.  Genetic architecture of maize yield traits dissected by QTL mapping and GWAS in maize , 2021, The Crop Journal.

[5]  M. Noman,et al.  Genome-wide association screening and verification of potential genes associated with root architectural traits in maize (Zea mays L.) at multiple seedling stages , 2021, BMC Genomics.

[6]  R. Hasterok,et al.  3,4-Dehydro-L-proline Induces Programmed Cell Death in the Roots of Brachypodium distachyon , 2021, International journal of molecular sciences.

[7]  Erin E. Sparks,et al.  Brace root phenotypes predict root lodging susceptibility and the contribution to anchorage in maize , 2021 .

[8]  Yunbi Xu,et al.  Identification of major QTL for waterlogging tolerance in maize using genome-wide association study and bulked sample analysis , 2021, Journal of Applied Genetics.

[9]  Juan D Salgado Salter,et al.  Proline-rich Extensin-like Receptor Kinases PERK5 and PERK12 are involved in Pollen Tube Growth , 2021, bioRxiv.

[10]  P. Masson,et al.  Gravity Signaling in Flowering Plant Roots , 2020, Plants.

[11]  Erin E. Sparks,et al.  Maize brace roots provide stalk anchorage , 2020, bioRxiv.

[12]  Z. Cui,et al.  Genome-Wide Association Study Dissects the Genetic Architecture of Maize Husk Tightness , 2020, Frontiers in Plant Science.

[13]  Zhixi Tian,et al.  Identification of QTL and genes for pod number in soybean by linkage analysis and genome-wide association studies , 2020, Molecular Breeding.

[14]  Zhiwu Zhang,et al.  Denser Markers and Advanced Statistical Method Identified More Genetic Loci Associated with Husk Traits in Maize , 2020, Scientific Reports.

[15]  Xiupeng Mei,et al.  QTL identification in backcross population for brace-root-related traits in maize , 2020, Euphytica.

[16]  Dayong Li,et al.  NAC transcription factors in plant immunity , 2019, Phytopathology Research.

[17]  F. Mora,et al.  SNP- and Haplotype-Based GWAS of Flowering-Related Traits in Maize with Network-Assisted Gene Prioritization , 2019, Agronomy.

[18]  Chenwu Xu,et al.  Integrating GWAS and Gene Expression Analysis Identifies Candidate Genes for Root Morphology Traits in Maize at the Seedling Stage , 2019, Genes.

[19]  Erin E. Sparks,et al.  Field‐based mechanical phenotyping of cereal crops to assess lodging resistance , 2019, Applications in plant sciences.

[20]  T. Zhao,et al.  Utilization of Interspecific High-Density Genetic Map of RIL Population for the QTL Detection and Candidate Gene Mining for 100-Seed Weight in Soybean , 2019, Front. Plant Sci..

[21]  D. Jordan,et al.  Large‐scale GWAS in sorghum reveals common genetic control of grain size among cereals , 2019, bioRxiv.

[22]  Gengyun Zhang,et al.  QTL fine-mapping of soybean (Glycine max L.) leaf type associated traits in two RILs populations , 2019, BMC Genomics.

[23]  Yu Li,et al.  Meta-QTL analysis and identification of candidate genes related to root traits in maize , 2018, Euphytica.

[24]  Haiqiu Yu,et al.  Identification of maize brace-root quantitative trait loci in a recombinant inbred line population , 2018, Euphytica.

[25]  J. Eisen,et al.  Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota , 2018, PLoS biology.

[26]  Yan He,et al.  Linkage mapping combined with association analysis reveals QTL and candidate genes for three husk traits in maize , 2018, Theoretical and Applied Genetics.

[27]  C. Marcon,et al.  Proteomics of Maize Root Development , 2018, Front. Plant Sci..

[28]  Jianming Yu,et al.  The genetic architecture of nodal root number in maize , 2018, The Plant journal : for cell and molecular biology.

[29]  Yao Zhou,et al.  BLINK: A Package for Next Level of Genome Wide Association Studies with Both Individuals and Markers in Millions , 2017, bioRxiv.

[30]  Qi Sun,et al.  Characterization and expression analysis of a novel RING-HC gene, ZmRHCP1, involved in brace root development and abiotic stress responses in maize , 2017 .

[31]  R. Mägi,et al.  Trans-ethnic meta-regression of genome-wide association studies accounting for ancestry increases power for discovery and improves fine-mapping resolution , 2017, Human molecular genetics.

[32]  P. Visscher,et al.  10 Years of GWAS Discovery: Biology, Function, and Translation. , 2017, American journal of human genetics.

[33]  Yu-Han H. Hsu,et al.  Discovery and fine-mapping of adiposity loci using high density imputation of genome-wide association studies in individuals of African ancestry: African Ancestry Anthropometry Genetics Consortium , 2017, PLoS genetics.

[34]  Yan He,et al.  Genome-wide association study (GWAS) reveals the genetic architecture of four husk traits in maize , 2016, BMC Genomics.

[35]  S. Sharma,et al.  BRACE: A Method for High Throughput Maize Phenotyping of Root Traits for Short‐Season Drought Tolerance , 2016 .

[36]  A. Travers,et al.  Glycosylation of a Fasciclin-Like Arabinogalactan-Protein (SOS5) Mediates Root Growth and Seed Mucilage Adherence via a Cell Wall Receptor-Like Kinase (FEI1/FEI2) Pathway in Arabidopsis , 2016, PloS one.

[37]  L. Tran,et al.  A transposable element in a NAC gene is associated with drought tolerance in maize seedlings , 2015, Nature Communications.

[38]  Dengfeng Zhang,et al.  Identification of 7 stress-related NAC transcription factor members in maize (Zea mays L.) and characterization of the expression pattern of these genes. , 2015, Biochemical and biophysical research communications.

[39]  S. Gallego,et al.  Early response of wheat seminal roots growing under copper excess. , 2015, Plant physiology and biochemistry : PPB.

[40]  A. Mort,et al.  Identification of the Abundant Hydroxyproline-Rich Glycoproteins in the Root Walls of Wild-Type Arabidopsis, an ext3 Mutant Line, and Its Phenotypic Revertant , 2015, Plants.

[41]  Carson C Chow,et al.  Second-generation PLINK: rising to the challenge of larger and richer datasets , 2014, GigaScience.

[42]  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.

[43]  Yuhong Tang,et al.  Self-rescue of an EXTENSIN mutant reveals alternative gene expression programs and candidate proteins for new cell wall assembly in Arabidopsis. , 2013, The Plant journal : for cell and molecular biology.

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

[45]  F. Song,et al.  Effect of Planting Density on Root Lodging Resistance and Its Relationship to Nodal Root Growth Characteristics in Maize (Zea mays L.) , 2012 .

[46]  L. Ku,et al.  QTL mapping and epistasis analysis of brace root traits in maize , 2012, Molecular Breeding.

[47]  E. Lander,et al.  The mystery of missing heritability: Genetic interactions create phantom heritability , 2012, Proceedings of the National Academy of Sciences.

[48]  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.

[49]  P. Holm,et al.  Characterization of barley (Hordeum vulgare L.) NAC transcription factors suggests conserved functions compared to both monocots and dicots , 2011, BMC Research Notes.

[50]  Youhuang Bai,et al.  Root hair-specific expansins modulate root hair elongation in rice. , 2011, The Plant journal : for cell and molecular biology.

[51]  M. King,et al.  Genetic Heterogeneity in Human Disease , 2010, Cell.

[52]  Christine Fong,et al.  GWAS Analyzer: integrating genotype, phenotype and public annotation data for genome-wide association study analysis , 2010, Bioinform..

[53]  J. Hirschhorn Genomewide association studies--illuminating biologic pathways. , 2009, The New England journal of medicine.

[54]  M. Daly,et al.  Genetic Mapping in Human Disease , 2008, Science.

[55]  T. Baskin,et al.  Two Leucine-Rich Repeat Receptor Kinases Mediate Signaling, Linking Cell Wall Biosynthesis and ACC Synthase in Arabidopsis[W] , 2008, The Plant Cell Online.

[56]  W. G. Hill,et al.  Heritability in the genomics era — concepts and misconceptions , 2008, Nature Reviews Genetics.

[57]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[58]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[59]  Roberto Tuberosa,et al.  Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize , 2007, Proceedings of the National Academy of Sciences.

[60]  Jean Yee Hwa Yang,et al.  A multi-array multi-SNP genotyping algorithm for Affymetrix SNP microarrays , 2007, Bioinform..

[61]  I. Szarejko,et al.  Molecular Cloning and Characterization of β-Expansin Gene Related to Root Hair Formation in Barley1 , 2006, Plant Physiology.

[62]  J. Veyrieras,et al.  Maize Adaptation to Temperate Climate: Relationship Between Population Structure and Polymorphism in the Dwarf8 Gene , 2006, Genetics.

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

[64]  S. Chen,et al.  AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. , 2005, The Plant journal : for cell and molecular biology.

[65]  B. Keller,et al.  The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. , 2001, Genes & development.

[66]  N. Chua,et al.  Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. , 2000, Genes & development.

[67]  Daniel J. Cosgrove,et al.  Loosening of plant cell walls by expansins , 2000, Nature.

[68]  Choi,et al.  Expression of a Soybean Hydroxyproline-Rich Glycoprotein Gene Is Correlated with Maturation of Roots , 1998, Plant physiology.

[69]  Z. Ye,et al.  Tissue-Specific Expression of Cell Wall Proteins in Developing Soybean Tissues. , 1991, The Plant cell.

[70]  C. Lamb,et al.  Specific expression of a novel cell wall hydroxyproline-rich glycoprotein gene in lateral root initiation. , 1989, Genes & development.

[71]  Xiupeng Mei,et al.  QTL Identification for Brace‐Root Traits of Maize in Different Generations and Environments , 2017 .

[72]  S. Asseng,et al.  Adaptation of grain legumes to climate change: a review , 2011, Agronomy for Sustainable Development.

[73]  Tanya M. Teslovich,et al.  LocusZoom: regional visualization of genome-wide association scan results , 2010, Bioinform..

[74]  Frank Hochholdinger,et al.  The Maize Root System: Morphology, Anatomy, and Genetics , 2009 .

[75]  Yi Lee,et al.  Expansins in Plant Development , 2008 .

[76]  M. Canny,et al.  The branch roots of Zea , 1994 .