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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (2): 304-319.doi: 10.3724/SP.J.1006.2022.13002


Dissecting the genetic architecture of maize kernel size based on genome-wide association study

QU Jian-Zhou1,2(), FENG Wen-Hao1, ZHANG Xing-Hua1,2, XU Shu-Tu1,2,*(), XUE Ji-Quan1,2,*()   

  1. 1Key Laboratory of Biology and Genetic Improvement of Maize in Arid Area of Northwest Region, Ministry of Agriculture and Rural Affairs / College of Agronomy, Northwest A&F University, Yangling 712100, Shaanxi, China;
    2Maize Engineering Technology Research Centre of Shaanxi Province, Yangling 712100, Shaanxi, China
  • Received:2021-01-06 Accepted:2021-04-26 Online:2022-02-12 Published:2021-06-03
  • Contact: XU Shu-Tu,XUE Ji-Quan E-mail:qujz0220@163.com;Shutuxu@nwafu.edu.cn;xjq2934@163.com
  • Supported by:
    This study was supported by the National Key Research and Development Program of China(2018YFD0100203);the Agricultural Research System (Maize).(CARS-02-64)


Kernel size related traits are one of the important compounds of yield, and they are also complex quantitative traits regulated by multiple genes. Mining the key regulatory genes of maize kernel size related traits will help to improve the yield. In this study, 212 excellent maize inbred lines were selected as materials. The kernel length, kernel width, and kernel thickness were measured in 2018 and 2019, respectively, and we performed genome-wide association study (GWAS) based on 73,006 single nucleotide polymorphic (SNP) markers uniformly distributed in maize genome. Based on the FarmCPU algorithm, 47 SNP markers associated with kernel size related traits were detected on 10 chromosomes in maize. Combined with the public dynamic spatio-temporal transcriptional data of kernel development of B73 maize inbred line, 58 candidate genes related to kernel size were detected in the linkage disequilibrium (LD) region marked by significant SNP. The proteins encoded by candidate genes interacted with multiple proteins and participated in and regulated many biological processes closely related to kernel development. These results provide a new reference for understanding the molecular regulation mechanism of maize kernel development, improving kernel size and increasing crop yield.

Key words: maize, kernel size, genome-wide association study, gene expression

Table 1

Basic statistical analysis of maize kernel size related traits in different years"

Correlation coefficient
KL (mm)
2018 10.89 1.04 8.52-13.47 0.10 -0.50 0.19 55.12 1.00 0.09 -0.22**
2019 8.96 0.73 6.39-11.87 0.10 0.77 0.04 1.00 0.31** 0.04
BLUP 9.95 0.42 8.74-11.19 0.05 0.10 0.18 1.00 0.22** 0.03
KW (mm)
2018 7.86 0.87 6.22-9.95 0.09 -0.14 0.33 80.76 0.09 1.00 0.24**
2019 7.45 0.66 6.13-9.32 0.09 -0.13 0.35 0.31** 1.00 0.43**
BLUP 7.62 0.44 6.69-8.99 0.06 -0.09 0.30 0.22** 1.00 0.36**
KT (mm)
2018 4.61 0.45 3.60-5.80 0.09 -0.16 0.40 55.52 -0.22** 0.24** 1.00
2019 4.59 0.47 3.41-5.80 0.10 -0.34 0.37 0.04 0.43** 1.00
BLUP 4.60 0.19 4.10-5.14 0.04 -0.22 0.25 0.03 0.36** 1.00

Fig. 1

Population linkage disequilibrium (LD) and population genetic structure The horizontal axis indicates the pairwise distance of SNPs within the same chromosome, and the vertical axis indicates the parameter r2 of LD. B: plot of the cross-validation error value in the range of K = 1 to 20."

Fig. 2

Distribution of SNPs significantly correlated with kernel length (KL), kernel width (KW), and kernel thickness (KT) Red, blue, and yellow backgrounds represent KL, KW, and KT, respectively. Vertical lines indicate the position on the chromosome of the loci associated with kernel size traits. The scale bar indicates the significance level of the association site; the height of the histogram indicates the frequency of the loci."

Table 2

SNPs of kernel length, kernel width, and kernel thickness in different years"

R2 (%)
Affx-291392839 2018 KL C/T 0.45 2 205,144,469 1.29E-05 0.36
Affx-291410933 2018 KL A/C 0.23 2 191,587,706 1.35E-05 4.52
Affx-291385262 2018 KL C/T 0.40 4 188,701,278 8.25E-06 6.96
Affx-158858862 2018 KL A/G 0.47 7 132,422,651 5.35E-07 20.90
Affx-88989857 2019 KL C/A 0.43 5 172,855,146 1.02E-05 11.64
Affx-291391022 2019 KL T/C 0.41 9 207,693,32 8.33E-06 14.53
Affx-291390553 BLUP KL C/T 0.46 1 14,651,295 6.14E-06 1.24
Affx-291430755 BLUP KL T/G 0.26 1 52,391,689 5.62E-07 13.31
Affx-291442609 BLUP KL G/A 0.37 2 134,763,888 2.39E-06 8.31
Affx-291378135 BLUP KL C/T 0.10 3 210,753,912 2.08E-07 5.97
Affx-291412195 BLUP KL C/T 0.30 3 128,909,025 4.11E-07 16.92
Affx-291417243 BLUP KL G/T 0.20 5 132,317,996 6.14E-10 13.73
Affx-291423518 BLUP KL A/G 0.36 5 10,908,609 2.63E-09 22.90
Affx-159157467 BLUP KL G/A 0.38 9 20,345,047 4.14E-06 12.08
Affx-291421141 2018 KW T/C 0.21 1 244,696,518 6.28E-11 18.69
Affx-291429284 2018 KW C/A 0.45 1 95,971,671 4.07E-08 18.38
Affx-291434526 2018 KW C/T 0.21 3 212,098,697 1.14E-05 0.62
Affx-291383862 2018 KW T/C 0.42 4 229,953,723 3.18E-06 14.42
Affx-291396984 2018 KW T/C 0.44 4 118,709,183 3.67E-06 2.38
Affx-291430867 2018 KW G/A 0.33 4 74,628,134 1.30E-05 11.78
Affx-291433635 2018 KW G/A 0.33 4 186,554,980 7.87E-06 19.65
Affx-291390831 2019 KW A/G 0.23 2 7,631,038 1.63E-07 6.09
Affx-291416165 2019 KW G/A 0.27 2 41,515,971 4.32E-07 1.50
Affx-291388322 2019 KW A/G 0.36 6 94,087,816 5.57E-08 5.08
Affx-291396454 2019 KW G/A 0.07 6 21,380,243 9.41E-07 15.80
Affx-291421141 BLUP KW T/C 0.23 1 244,696,518 4.18E-09 18.51
Affx-291391782 BLUP KW G/A 0.49 2 214,513,500 6.90E-12 18.84
Affx-291386982 BLUP KW G/A 0.38 3 140,660,245 7.62E-10 4.90
Affx-291443225 BLUP KW C/T 0.47 5 1,250,179 5.12E-07 1.73
Affx-291416220 BLUP KW G/A 0.41 6 98,426,114 1.09E-05 1.67
Affx-291424033 2018 KT G/A 0.32 1 279,751,443 1.88E-06 7.04
Affx-291437625 2018 KT C/T 0.23 1 246,781,098 1.58E-06 8.62
Affx-291442339 2018 KT T/G 0.10 1 198,355,431 2.82E-06 13.41
Affx-291423488 2018 KT G/A 0.39 3 117,603,753 5.43E-08 14.05
Affx-123595299 2018 KT T/C 0.46 4 33,851,115 6.28E-08 3.06
Affx-291407692 2018 KT C/T 0.47 4 68,756,350 2.42E-10 7.53
Affx-291421461 2018 KT T/G 0.24 5 190,291,719 7.78E-07 12.80
Affx-291440347 2018 KT T/C 0.27 5 46,983,911 2.69E-07 3.51
Affx-291431852 2018 KT C/T 0.09 8 33,721,488 1.07E-12 11.05
Affx-291393756 2018 KT T/C 0.17 10 144,450,832 2.09E-06 4.11
Affx-291392059 2019 KT A/T 0.47 1 204,796,933 1.16E-05 19.87
Affx-291380154 2019 KT T/C 0.13 2 196,175,692 1.10E-05 19.15
Affx-291409744 BLUP KT A/G 0.37 1 181,908,322 1.49E-06 3.75
Affx-291424033 BLUP KT G/A 0.31 1 279,751,443 1.17E-09 10.20
Affx-291384679 BLUP KT C/A 0.32 3 56,819,365 7.59E-06 8.77
Affx-291424461 BLUP KT T/C 0.39 4 43,693,955 1.31E-06 1.38
Affx-291442826 BLUP KT G/A 0.29 4 38,973,447 2.77E-06 15.91
Affx-291427217 BLUP KT T/C 0.46 5 59,748,660 3.61E-06 6.66
Affx-291432324 BLUP KT A/G 0.08 8 18,220,008 1.22E-07 14.41

Table 3

Candidate genes and their annotations of KL, KW, and KT in maize"

Affx-291430755 GRMZM2G033570 KL 1 52,391,689 ETHYLENE-INSENSITIVE3-like 1 protein M1
Affx-291410933 GRMZM2G014313 KL 2 191,587,706 Protein pob M2
Affx-291410933 GRMZM2G007885 KL 2 191,587,706 Myosin heavy chain-related protein M3
Affx-291410933 GRMZM2G150319 KL 2 191,587,706 O-fucosyltransferase family protein M4
Affx-291392839 GRMZM5G821439 KL 2 205,144,469 Chitin-inducible gibberellin-responsive protein 1 M5
Affx-291392839 GRMZM2G046011 KL 2 205,144,469 60S ribosomal protein L38 M6
Affx-291392839 GRMZM2G163233 KL 2 205,144,469 Male sterile 32 M7
Affx-291412195 GRMZM2G122443 KL 3 128,909,025 OS-9-like protein M8
Affx-291412195 GRMZM2G122481 KL 3 128,909,025 Cytochrome c oxidase subunit 5C M9
Affx-291412195 GRMZM2G138077 KL 3 128,909,025 Uncharacterized protein
Affx-291378135 AC230013.2_FG007 KL 3 210,753,912 60S ribosomal protein L18a
Affx-291378135 GRMZM2G150631 KL 3 210,753,912 Transducin/WD40 repeat-like superfamily protein M10
Affx-88989857 GRMZM2G119517 KL 5 172,855,146 ACT domain-containing protein ACR3 M11
Affx-291423518 GRMZM2G145854 KL 5 10,908,609 NADH-ubiquinone oxidoreductase subunit M12
Affx-291423518 GRMZM2G569855 KL 5 10,908,609 Threonine dehydratase 1 biosynthetic M13
Affx-291423518 GRMZM2G109383 KL 5 10,908,609 Phosphoglucomutase 2 M14
Affx-291391022 GRMZM5G829544 KL 9 20,769,332 Fatty acyl-ACP thioesterase 2 M15
Affx-291391022 GRMZM2G147399 KL 9 20,769,332 Early nodulin 93 M16
Affx-291391022 GRMZM2G131421 KL 9 20,769,332 Early nodulin 93 M17
Affx-291391022 GRMZM2G404897 KL 9 20,769,332 Zinc finger protein M18
Affx-159157467 GRMZM2G173693 KL 9 20,345,047 Pre-mRNA-splicing factor 38B-like M19
Affx-291416165 GRMZM2G325131 KW 2 41,515,971 Anthranilate synthase homolog 1 M20
Affx-291391782 GRMZM2G049347 KW 2 214,513,500 Synaptotagmin-5 M21
Affx-291434526 GRMZM2G152686 KW 3 212,098,697 Pyruvate kinase M22
Affx-291434526 GRMZM2G070360 KW 3 212,098,697 V-type proton ATPase subunit E-like M23
Affx-291430867 GRMZM2G117755 KW 4 74,628,134 Hypersensitive-induced response protein 2 M24
Affx-291383862 GRMZM2G162992 KW 4 229,953,723 KH domain-containing protein M25
Affx-291443225 GRMZM2G034326 KW 5 1,250,179 DNA-directed RNA polymerases II, IV, and V subunit 8B M26
Affx-291443225 GRMZM2G069916 KW 5 1,250,179 LUC7 related protein M27
Affx-291443225 GRMZM2G138676 KW 5 1,250,179 Shaggy-related protein kinase kappa M28
Affx-291396454 GRMZM2G060856 KW 6 21,380,243 Membrane protein M29
Affx-291442339 GRMZM2G318475 KT 1 198,355,431 Eukaryotic translation initiation factor 6 M30
Affx-291442339 GRMZM2G017110 KT 1 198,355,431 Glutamate decarboxylase M31
Affx-291437625 GRMZM2G012119 KT 1 246,781,098 Post-illumination chlorophyll fluorescence increase M32
Affx-291437625 GRMZM2G013600 KT 1 246,781,098 DNA-directed RNA polymerases I, II, and III polypeptide M33
Affx-291437625 GRMZM2G146819 KT 1 246,781,098 Uncharacterized protein M34
Affx-291437625 GRMZM2G146818 KT 1 246,781,098 40S ribosomal protein
Affx-291437625 GRMZM2G146589 KT 1 246,781,098 Lysine-tRNA ligase M35
Affx-291437625 GRMZM2G146486 KT 1 246,781,098 P-loop containing nucleoside triphosphate hydrolase Superfamily protein M36
Affx-291437625 GRMZM2G034417 KT 1 246,781,098 Inositol-phosphate phosphatase M37
Affx-291424033 GRMZM2G047456 KT 1 279,751,443 Peroxidase 35 M38
Affx-291424033 GRMZM2G307252 KT 1 279,751,443 SecY protein transport family protein M39
Affx-291392059 GRMZM2G357804 KT 1 204,796,933 UDP-N-acetylglucosamine-peptide N-acetylglucosaminyltransferase SPINDLY M40
Affx-291392059 GRMZM2G057608 KT 1 204,796,933 40S ribosomal protein S25-1 M41
Affx-291392059 GRMZM2G167548 KT 1 204,796,933 Multiple myeloma tumor-associated protein 2 M42
Affx-291392059 GRMZM2G167836 KT 1 204,796,933 Vesicle-associated membrane protein 727 M43
Affx-291380154 GRMZM2G073942 KT 2 196,175,692 Uncharacterized protein
Affx-291423488 GRMZM2G138268 KT 3 117,603,753 Auxin-responsive protein IAA 10 M44
Affx-123595299 GRMZM2G139550 KT 4 33,851,115 Aldolase superfamily protein M45
Affx-123595299 GRMZM5G870572 KT 4 33,851,115 BSD domain containing protein M46
Affx-291442826 GRMZM2G064807 KT 4 38,973,447 Pentatricopeptide repeat-containing protein M47
Affx-291442826 GRMZM2G158153 KT 4 38,973,447 KH domain-containing protein M48
Affx-291421461 GRMZM2G004847 KT 5 190,291,719 Pectin lyase-like superfamily protein M49
Affx-291427217 GRMZM2G102447 KT 5 59,748,660 WAS/WASL-interacting protein family member 1-like M50
Affx-291431852 GRMZM2G180990 KT 8 33,721,488 Ligatin M51
Affx-291432324 GRMZM2G107696 KT 8 18,220,008 Ubiquitin carboxyl-terminal hydrolase M52
Affx-291432324 GRMZM2G107639 KT 8 18,220,008 Transaminase M53
Affx-291393756 GRMZM2G086030 KT 10 144,450,832 Tetratricopeptide repeat (TPR)-like superfamily protein M54

Fig. 3

Dynamic expression patterns of candidate genes related to maize kernel length The scale bar indicates normalized gene expression levels."

Fig. 4

Dynamic expression patterns of candidate genes related to maize kernel width The scale bar indicates normalized gene expression levels."

Fig. 5

Dynamic expression patterns of candidate genes related to maize kernel thickness The scale bar indicates normalized gene expression levels."

Fig. 6

Protein-protein interaction networks of 54 highly expressed candidate genes The node indicates the proteins, and the line indicates the interaction between proteins. Red color indicates candidate gene encoded proteins, and the interactive proteins in different networks are distinguished by different colors."

Fig. 7

Functional enrichment analysis of protein-protein interaction networks for candidate genes Circle size indicates the number of genes, the normalized Q-value indicates the significance of enrichment. The biological process of significant protein enrichment in M6, M8, M24, M26, M29, M33, M39, M41, M47, and M51 is in Fig. A; the biological process of significant protein enrichment in M11, M18, M31, M36, M49, and M53 is in Fig. B."

Fig. S1

Population genetic structure analysis Population structure based on k = 15, the length of the different color segments represents the proportion of an ancestor in the individual genome."

Fig. S2

Manhattan plot of genome-wide association study A-C: KL, KW, and KT of 2018; D-F: KL, KW and KT of 2019; G-I: BLUP value of KL, KW, and KT for 2 years. Black horizontal line indicates the genome-wide significance threshold."

Fig. S3

Quantitle-quantitle plot of genome-wide association study A-C: KL, KW, and KT of 2018; D-F: KL, KW and KT of 2019; G-I: BLUP value of KL, KW, and KT for 2 years. The horizontal axis shows normalized expected P-values, and the vertical axis shows normalized observed P-values."

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