Genome-Wide Association Studies on the Kernel Row Number in a Multi-Parent Maize Population
Abstract
:1. Introduction
2. Results
2.1. Phenotypic Analysis of KRN in the Multi-Parent Population
2.2. Structure Analysis of the Multi-Parent Population
2.3. Genome-Wide Association Analysis for KRN
2.4. Detection of Candidate Genes
2.5. Linkage Analysis
2.5.1. Parental Line Variation for KRN
2.5.2. Construction of Linkage Maps
2.5.3. QTL Mapping
2.6. Joint Analysis of GWAS and QTL
2.7. Haplotype Analysis
2.8. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) Enrichment Analysis
3. Discussion
3.1. 18 Co-Located Genes Were Confirmed to Be Associated with KRN
3.2. Key Candidate Genes Linked to KRN Were Identified through GO and KEGG Analysis
3.3. Alternative Reference Genome May Help Identify Candidate Gene
3.4. Key Candidate Genes Associated with KRN
4. Materials and Methods
4.1. Experimental Materials
4.2. Field Experimental Design and Phenotyping
4.3. Phenotypic Data Analysis
4.4. Genotyping
4.5. Structure Analysis
4.6. Genome-Wide Association Analysis
4.7. Haplotype Analysis
4.8. Candidate Gene Screening
4.9. Construction of Genetic Linkage Map
4.10. QTL Mapping Analysis
4.11. GO and KEGG Enrichment Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Environment | Min | Max | AVE | SD | CV(%) | H2 (%) |
---|---|---|---|---|---|---|
19DH | 6.5 | 16.67 | 12.1647 | 1.46912 | 12.07691106 | 76.8 |
19BS | 5.33 | 16.67 | 11.8247 | 1.54526 | 13.06806938 | |
21YS | 6 | 16 | 11.9313 | 1.83939 | 15.41650951 | |
21JH | 8 | 20 | 13.2378 | 1.59104 | 12.01891552 | |
22YS | 9 | 19.5 | 12.7630 | 1.70710 | 13.37538196 |
Gene ID | Env | SNP | Chr | PVE (%) | Function | Expression (FPKM) | |||
---|---|---|---|---|---|---|---|---|---|
Meristem_16–19 | Ear_Primordium (2–4 mm) | Ear_Primordium (6–8 mm) | Female_Spikelet | ||||||
Zm00001d007924 | 21YS | 242858336 | 2 | 17.74 | Cytochrome P450 41 | NA | NA | NA | NA |
Zm00001d007925 | Cyclic nucleotide-gated ion channel 18 | NA | NA | NA | NA | ||||
Zm00001d025694 | 22YS | 126528998 | 10 | 14.88 | Surfeit locus protein 2 [52] | 58.5 | 73.9 | 63 | 35.7 |
Zm00001d025695 | Tetratricopeptide-like helical domain superfamily | 1.0 | 1.2 | 1.4 | 2.2 | ||||
Zm00001d025696 | Cellulase (Glycosyl hydrolase family 5) Protein | 4.1 | 5.0 | 5.1 | 6.0 | ||||
Zm00001d029702 | 21JH | 83163645 | 1 | 21.01 | glutathione S-transferase | NA | NA | NA | NA |
Zm00001d006733 | 21JH | 215468689 | 2 | 14.31 | Transcription factor bHLH85 | NA | NA | NA | NA |
Zm00001d006734 | Zinc finger protein AZF2 | Not reported | |||||||
Zm00001d006735 | Zinc finger protein AZF1 | ||||||||
Zm00001d014435 | 21JH | 46725146 | 5 | 10.57 | D-xylose-proton symporter-like 3 | 58.5 | 49.8 | 46 | 29.3 |
Zm00001d016202 | 21JH | 150393177 | 5 | 10.64 | E3 ubiquitin-protein ligase COP1 | 0.1 | 0.2 | 0.2 | NA |
Zm00001d016203 | Actin-related protein 2/3 complex subunit 3 | 20.3 | 11.9 | 11.6 | 11.1 | ||||
Zm00001d016204 | Putative ubiquitin-like-specific protease 1B | Not reported | |||||||
Zm00001d024390 | 21JH | 68447065 | 10 | 11.15 | Sec14p-like phosphatidylinositol transfer family protein | 3.6 | 8.8 | 9.1 | NA |
Gene | Loc | SNP | Chr | PVE (%) | Function | Expression (FPKM) | |||
---|---|---|---|---|---|---|---|---|---|
Meristem_16–19_Day | Ear_Primordium (2–4 mm) | Ear_Primordium (6–8 mm) | Female_Spikelet | ||||||
Zm00001d022420 | 19DH | 177304649 | 7 | 6.79 | ricin B-like lectins | NA | NA | NA | 61.5 |
Zm00001d022421 | 122.7 | 156 | 124.5 | 464.8 |
Loc | Chr | Start | End | Number of Repeated Genes |
---|---|---|---|---|
sub-pop3/21JH | 4 | 75,627,569 | 151,339,536 | 648 |
sub-pop4/22YS | 4 | 46,403,895 | 172,368,609 | |
sub-pop3/22YS | 4 | 8,043,739 | 18,953,659 | 29 |
sub-pop3/BLUP | 4 | 8,043,739 | 10,683,376 | |
sub-pop4/21JH | 4 | 31,671,021 | 31,671,020 | 0 |
sub-Pop4/21YS | 4 | 31,409,140 | 31,409,140 | |
Total | 677 |
Gene ID | PVE (%) | GWAS-Loc | Start | End | SNP | Chr | QTL-Loc | |
---|---|---|---|---|---|---|---|---|
Zm00001d031666 | 7.02 | 21JH | 198,109,347 | 198,149,347 | 3 | 1 | 312/19DH | |
Zm00001d031667 | ||||||||
Zm00001d031668 | ||||||||
Zm00001d031669 | ||||||||
Zm00001d031709 | 6.14 | 21JH | 199,086,836 | 199,126,836 | 4 | 1 | 312/19DH | |
Zm00001d031713 | 8.41 | 21JH | 199,202,030 | 199,242,030 | 5 | 1 | 312/19DH | |
Zm00001d031715 | ||||||||
Zm00001eb036870 | 6.48 | 21JH | 199,294,176 | 199,334,176 | 6 | 1 | 312/19DH | |
Zm00001eb036890 | 4.73 | 21JH | 199,315,283 | 199,355,283 | 7 | 1 | 312/19DH | |
Zm00001d031648 | ||||||||
Zm00001d031772 | 5.57 | 21JH | 201,335,723 | 201,375,824 | 8 | 1 | 312/19DH | |
Zm00001d050984 | 6.70 | 21JH | 135,263,055 | 135,303,055 | 1 | 4 | 312/21JH | 444/22YS |
Zm00001d050985 | ||||||||
Zm00001d016000 | 8.40 | 21JH | 138,534,600 | 138,574,630 | 2 | 5 | 444/21YS | |
Zm00001d016202 | 10.64 | 21JH | 150,373,177 | 150,413,177 | 1 | 5 | 444/21YS | |
Zm00001d016203 | ||||||||
Zm00001d016204 | ||||||||
Zm00014a012929 | 8.83 | 19DH | 120,35,0778 | 120,390,778 | 1 | 5 | 312/19BS | 444/21YS |
Gene | Chr | Function | Expression (FPKM) | |||
---|---|---|---|---|---|---|
Meristem_16–19 | Ear_Primordium (2–4 mm) | Ear_Primordium (6–8 mm) | Female_Spikelet | |||
Zm00001d031666 | 1 | Probable aldo-keto reductase 2 | 2.1 | 4.3 | 4.5 | 6.2 |
Zm00001d031667 | 1 | Discolored-paralog2 | 13.3 | 12.3 | 15.2 | 7.8 |
Zm00001d031668 | 1 | Ubiquitin thioesterase otubain-like | 8.9 | 5.2 | 6.4 | 7.3 |
Zm00001d031669 | 1 | O-fucosyltransferase family protein | 12.3 | 8.9 | 8.7 | 8.8 |
Zm00001d031709 | 1 | Replication protein A 70 kDa DNA-binding subunit B | NA | NA | NA | NA |
Zm00001d031713 | 1 | CBL-interacting protein kinase 19 | NA | NA | NA | NA |
Zm00001d031715 | 1 | CBL-interacting serine/threonine-protein kinase 9 | NA | 1.3 | 1.8 | NA |
Zm00001eb036870 | 1 | Unknown | Unreported | |||
Zm00001eb036890 | 1 | Protein S-acyltransferase4 | ||||
Zm00001d031648 | 1 | Protein S-acyltransferase4 | 47.5 | 26.6 | 26.2 | 64.8 |
Zm00001d031772 | 1 | Protein NtpR | NA | NA | NA | NA |
Zm00001d050984 | 4 | Rab-proteins geranylgeranyltransferase component A | NA | 0.2 | 0.2 | NA |
Zm00001d050985 | 4 | Ultraviolet-B receptor UVR8 | 8.7 | 18.8 | 18.1 | 15.7 |
Zm00001d016000 | 5 | Myb-related protein 3R-1 | 52.3 | 55.5 | 59.3 | 2.6 |
Zm00001d016202 | 5 | E3 ubiquitin-protein ligase COP1 | NA | NA | NA | NA |
Zm00001d016203 | 5 | Actin-related protein 2/3 complex subunit 3 | 20.3 | 11.9 | 11.6 | 11.1 |
Zm00001d016204 | 5 | Putative ubiquitin-like-specific protease 1B | NA | NA | NA | NA |
Zm00014a012929 (mo17) | 5 | Unknown | Unreported |
LOC | Category | GO ID | Description | Gene Ratio | p Value |
---|---|---|---|---|---|
Sub-pop3/21JH and sub-pop4/22YS | BP | GO:0015780 | Nucleotide-sugar transmembrane transport | 2/170 | 0.011210655 |
BP | GO:0090481 | Pyrimidine nucleotide-sugar transmembrane transport | 2/170 | 0.011210655 | |
BP | GO:0006914 | Autophagy | 2/170 | 0.013554188 | |
BP | GO:0061919 | Process utilizing autophagic mechanism | 2/170 | 0.013554188 | |
BP | GO:0006325 | Chromatin organization | 4/170 | 0.020186478 | |
BP | GO:1901264 | Carbohydrate derivative transport | 2/170 | 0.021710384 | |
BP | GO:0015698 | Inorganic anion transport | 3/170 | 0.024541102 | |
BP | GO:0006821 | Chloride transport | 2/170 | 0.034964547 | |
BP | GO:0006497 | Protein lipidation | 2/170 | 0.054807613 | |
BP | GO:0006505 | GPI anchor metabolic process | 2/170 | 0.054807613 | |
CC | GO:0000139 | Golgi membrane | 2/59 | 0.02194791 | |
CC | GO:0098791 | Golgi subcompartment | 2/59 | 0.025312478 | |
CC | GO:0031984 | Organelle subcompartment | 3/59 | 0.0600554 | |
CC | GO:1902494 | Catalytic complex | 7/59 | 0.103515469 | |
CC | GO:0005794 | Golgi apparatus | 2/59 | 0.155306753 | |
CC | GO:0044431 | Golgi apparatus part | 2/59 | 0.155306753 | |
CC | GO:0000151 | Ubiquitin ligase complex | 1/59 | 0.166579053 | |
CC | GO:0030286 | Dynein complex | 1/59 | 0.166579053 | |
CC | GO:0098803 | Respiratory chain complex | 1/59 | 0.166579053 | |
CC | GO:0070461 | SAGA-type complex | 1/59 | 0.181653191 | |
MF | GO:0140103 | Catalytic activity, acting on a glycoprotein | 3/239 | 0.001729669 | |
MF | GO:0005338 | Nucleotide-sugar transmembrane transporter activity | 2/239 | 0.009752157 | |
MF | GO:0015165 | Pyrimidine nucleotide-sugar transmembrane transporter activity | 2/239 | 0.009752157 | |
MF | GO:0033926 | Glycopeptide alpha-N-acetylgalactosaminidase activity | 2/239 | 0.011799431 | |
MF | GO:0015103 | Inorganic anion transmembrane transporter activity | 3/239 | 0.016322483 | |
MF | GO:0008509 | Anion transmembrane transporter activity | 3/239 | 0.023303348 | |
MF | GO:0005244 | Voltage-gated ion channel activity | 2/239 | 0.030592768 | |
MF | GO:0005247 | Voltage-gated chloride channel activity | 2/239 | 0.030592768 | |
MF | GO:0005253 | Anion channel activity | 2/239 | 0.030592768 | |
MF | GO:0005254 | Chloride channel activity | 2/239 | 0.030592768 |
Gene | GWAS-Loc | QTL Loc | Description | GO ID | Category |
---|---|---|---|---|---|
Zm00001d050984 | 21JH | Sub-pop3/21JH and sub-pop4/22YS | intracellular signal transduction | GO:0035556 | BP |
signal transduction | GO:0007165 | BP | |||
signaling | GO:0023052 | BP | |||
small GTPase mediated signal transduction | GO:0007264 | BP | |||
cell communication | GO:0007154 | BP | |||
nucleoside-triphosphatase regulator activity | GO:0060589 | MF | |||
GTPase regulator activity | GO:0030695 | MF | |||
GDP-dissociation inhibitor activity | GO:0005092 | MF | |||
enzyme regulator activity | GO:0030234 | MF | |||
molecular function regulator | GO:0098772 | MF |
Loc | KEGGID | Description | Bg Ratio | p Value |
---|---|---|---|---|
Sub-Pop3/21JH and sub-pop4/22YS | zma00650 | Butanoate metabolism | 30/5493 | 0.010066583 |
zma00902 | Monoterpenoid biosynthesis | 12/5493 | 0.013495559 | |
zma00770 | Pantothenate and CoA biosynthesis | 40/5493 | 0.021995592 | |
zma00020 | Citrate cycle (TCA cycle) | 72/5493 | 0.022923456 | |
zma00290 | Valine, leucine and isoleucine biosynthesis | 22/5493 | 0.042859117 | |
zma00563 | Glycosylphosphatidylinositol (GPI)-anchor biosynthesis | 24/5493 | 0.050229291 | |
zma04712 | Circadian rhythm—plant | 58/5493 | 0.056694817 | |
zma01210 | 2-Oxocarboxylic acid metabolism | 61/5493 | 0.064061405 | |
zma01200 | Carbon metabolism | 290/5493 | 0.070207933 | |
zma01040 | Biosynthesis of unsaturated fatty acids | 29/5493 | 0.070421369 | |
Sub-pop3/22YS and sub-pop4/BLUP | zma00062 | Fatty acid elongation | 40/5493 | 0.028819143 |
zma00053 | Ascorbate and aldarate metabolism | 60/5493 | 0.042992849 | |
zma00040 | Pentose and glucuronate interconversions | 77/5493 | 0.054918027 | |
zma01250 | Biosynthesis of nucleotide sugars | 105/5493 | 0.074316114 | |
zma00480 | Glutathione metabolism | 111/5493 | 0.07843369 | |
zma00520 | Amino sugar and nucleotide sugar metabolism | 160/5493 | 0.111548551 | |
zma04626 | Plant-pathogen interaction | 228/5493 | 0.156015338 | |
zma01240 | Biosynthesis of cofactors | 265/5493 | 0.179497585 |
Parental Lines | Pedigree | Heterotic Group | Ecotype |
---|---|---|---|
Ye107 | From US hybrid DeKalb XL8 | Reid | Temperate |
CML312 | S89500-F2-2-2-1-1-B | Non-Reid | Tropical |
CML444 | P43-C9-1-1-1-1-1 | Non-Reid | Tropical |
YML46 | Selected from Suwan1 | Suwan | Tropical |
YML32 | Selected from Suwan1 | Suwan | Tropical |
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Wang, Y.; Ran, F.; Yin, X.; Jiang, F.; Bi, Y.; Shaw, R.K.; Fan, X. Genome-Wide Association Studies on the Kernel Row Number in a Multi-Parent Maize Population. Int. J. Mol. Sci. 2024, 25, 3377. https://doi.org/10.3390/ijms25063377
Wang Y, Ran F, Yin X, Jiang F, Bi Y, Shaw RK, Fan X. Genome-Wide Association Studies on the Kernel Row Number in a Multi-Parent Maize Population. International Journal of Molecular Sciences. 2024; 25(6):3377. https://doi.org/10.3390/ijms25063377
Chicago/Turabian StyleWang, Yizhu, Fengyun Ran, Xingfu Yin, Fuyan Jiang, Yaqi Bi, Ranjan K. Shaw, and Xingming Fan. 2024. "Genome-Wide Association Studies on the Kernel Row Number in a Multi-Parent Maize Population" International Journal of Molecular Sciences 25, no. 6: 3377. https://doi.org/10.3390/ijms25063377