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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (11): 2691-2705.doi: 10.3724/SP.J.1006.2022.23019

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Genome-wide association study of leaf angle traits and mining of elite alleles from the major loci in maize

QIN Wen-Xuan1(), BAO Jian-Xi1(), WANG Yan-Bo1, MA Ya-Jie1, LONG Yan1, LI Jin-Ping2, DONG Zhen-Ying1,2,*(), WAN Xiang-Yuan1,2,*()   

  1. 1Zhongzhi International Institute of Agricultural Biosciences, Shunde Graduate School, School of Chemistry and Biological Engineering, Research Center of Biology and Agriculture, University of Science and Technology Beijing (USTB), Beijing 100083, China
    2Beijing Engineering Laboratory of Main Crop Bio-Tech Breeding, Beijing International Science and Technology Cooperation Base of Bio-Tech Breeding, Beijing Solidwill Sci-Tech Co. Ltd., Beijing 100192, China
  • Received:2022-02-27 Accepted:2022-05-05 Online:2022-11-12 Published:2022-05-24
  • Contact: DONG Zhen-Ying,WAN Xiang-Yuan E-mail:qwx18649323612@163.com;bjx1232003@126.com;zydong@ustb.edu.cn;wanxiangyuan@ustb.edu.cn
  • Supported by:
    The National Key Research and Development Program of China(2021YFD1200700)

Abstract:

Leaf angle (LA) is one of the important components of the canopy structure in maize, which can directly affect the distribution of light and CO2 in the canopy and the light capture efficiency of the population, thus affecting the yield of maize. In order to analysis the genetic basis of maize LA traits, an association panel including 854 maize inbred lines was used to analyze the first (ULA1), second (ULA2), and third (ULA3) upper leaf angle of ears in five environments, and then 2795 single nucleotide polymorphic (SNP) markers distributed on 10 chromosomes of maize genome were used for genome-wide association analysis (GWAS) of LA traits based on FarmCPU (fixed and random model circulating probability unification) model. Eighty-one significant SNP associations were identified, among which 26, 27, and 28 significant SNPs associated with ULA1, ULA2, and ULA3, and phenotypic variation explained (PVE) for each SNP was 0.03%-9.68%, 0.06%-9.30%, and 0.01%-8.23%, respectively. We further identified 17 heigh-confidence SNPs repeatedly detected for specific trait, among which three loci were firstly reported in this study, 14 loci located within the intervals that had been previously mapped, and nine SNPs were associated with more than one LA trait. Seven SNPs with PVE > 5% were classified as major SNPs, and thus nine germplasms combining the seven elite alleles with small LAs were isolated. Through searching the candidate regions of the 17 high-confidence SNPs, a total of 131 candidate genes were predicated, and a key gene DRL1 known to regulate LA of maize that located 70 kb downstream of PZE-101039301 on chromosome 1 was also identified as one of candidate genes. In summary, the genetic loci and candidate genes identified by this study will be useful for revealing the genetic mechanism of maize LA traits, and provide clues for cloning LA correlated genes. The identified elite alleles and germplasm resources can be used to increase maize yield by molecular marker-assisted selection of LA traits.

Key words: maize, leaf angle, genome-wide association study, candidate gene, elite allele

Fig. S1

Frequency distribution of LA traits in maize ULA1, ULA2, and ULA3 represent the first, second, and third upper leaf angle of ear, respectively; 19BJ, 20BJ, and 21BJ represent Beijing in 2019, 2020, and 2021, respectively; 20ZC and 21ZC represent Zhucheng in 2020 and 2021, respectively."

Table 1

Statistical analysis of different LA traits in maize"

性状
Trait
环境
Environment
均值
Mean (°)
标准差
Standard
deviation
方差
Variance
偏度
Skewness
峰度
Kurtosis
变异系数
Variation
coefficient (%)
变异范围
Rang of
variations (°)
遗传力
h2 (%)
穗上第1叶夹角
ULA1
19BJ 23.79 8.741 76.40 1.13 3.18 36.74 5.60-97.85 88.8
20BJ 16.93 8.673 75.22 1.10 3.37 51.23 0.05-83.85
20ZC 17.00 8.333 69.44 0.97 3.43 49.02 0.10-80.10
21BJ 18.21 8.453 71.46 0.75 1.21 46.43 0.25-59.80
21ZC 19.08 8.177 66.86 0.71 1.02 42.85 0.05-62.30
穗上第2叶夹角
ULA2
19BJ 21.40 8.881 78.87 1.25 3.59 41.49 5.50-96.85 90.4
20BJ 15.23 8.646 74.75 1.21 3.42 56.78 0.05-82.93
20ZC 16.57 8.997 80.94 1.04 2.86 54.29 0.00-81.90
21BJ 16.65 8.972 80.50 1.07 2.48 53.87 0.00-81.10
21ZC 15.55 8.030 64.48 0.97 1.76 51.63 0.05-55.30
穗上第3叶夹角
ULA3
19BJ 20.98 9.502 90.29 1.35 3.40 45.29 5.30-90.75 90.7
20BJ 14.41 9.057 82.03 1.29 3.80 62.86 0.00-81.65
20ZC 15.93 9.972 99.44 1.30 4.44 62.62 0.00-97.90
21BJ 16.64 9.686 93.81 1.42 5.57 58.22 0.05-107.95
21ZC 14.61 8.591 73.80 1.49 4.73 58.80 0.00-76.85

Fig. 1

Correlation analysis of LA traits A, B, and C indicate correlation analysis of ULA1, ULA2, and ULA3 traits in different environments, respectively; D indicates correlation analysis of different LA traits. Abbreviations are the same as those given in Table 1."

Fig. S2

Phylogenetic analysis of the association population G1 to G11 represent group one to group eleven."

Fig. 2

Manhattan-plots and QQ plots for GWAS of LA traits in maize A, C, and E indicate the Manhattan plot of ULA1, ULA2, and ULA3, respectively; B, D, and F indicate the QQ plot of ULA1, ULA2, and ULA3, respectively. BLUP represents best linear unbiased prediction. Other abbreviations are the same as those given in Table 1."

Table S1

Summary of the significant SNPs associated with different LA traits"

性状
Trait
标记名称
Marker name
染色体
Chromosome
位置
Position (bp)
P
P-value
表型变异率
PVE (%)
环境/BLUP
Environment/BLUP
ULA1 PZB02058.1 1 28,614,062 2.11E-06 3.67 BLUP
PZE-101063113 1 46,668,336 1.34E-05 5.28 21ZC
PZE-101073494 1 56,920,858 5.31E-06 2.65 21BJ
PZE-101256077 1 305,013,865 5.41E-08 2.58 20BJ/21BJ/BLUP
PZE-102000560 2 837,383 1.57E-09 0.84 20BJ/BLUP
SYN2580a 2 31,809,511 3.22E-06 1.54 21BJ
PZE-102079155 2 63,417,366 1.96E-06 3.64 21ZC
PZE-102142045 2 194,956,148 1.23E-06 7.09 19BJ
PZE-103016432 3 8,535,602 1.41E-10 4.61 19BJ
PZE-103049573 3 53,869,130 3.25E-06 7.18 BLUP
PZE-104023748 4 28,367,320 3.04E-07 6.31 20BJ/BLUP
PZE-104062792 4 127,297,691 8.02E-06 0.11 21BJ
SYN11091 4 172,531,224 1.83E-07 1.26 19BJ/20ZC/BLUP
PZE-104119909 4 201,188,940 6.31E-07 5.57 19BJ
PZE-104123484 4 204,948,076 5.48E-06 4.44 20ZC
PZE-104144719 4 238,721,563 2.85E-06 1.13 21ZC
PZE-105039536 5 25,111,571 3.56E-06 6.80 20BJ/21BJ/BLUP
SYN23915 6 121,768,114 1.84E-06 0.97 20BJ
PZE-107010573 7 7,544,684 3.53E-06 0.17 20BJ/20ZC
PZE-107010578c 7 7,546,222 5.29E-06 0.10 19BJ
PZE-107060629 7 119,797,398 2.65E-06 0.10 20BJ
PZE-108002532 8 2,930,186 8.55E-06 0.03 20ZC
PZE-108052985 8 96,363,878 8.70E-09 1.37 20BJ/20ZC
PZE-109031124 9 37,396,449 5.35E-06 0.17 19BJ/21BJ/BLUP
PZE-109086476 9 137,669,212 4.74E-06 9.68 19BJ/20BJ/20ZC/21ZC/BLUP
SYN23715 10 126,322,856 1.61E-05 3.48 20ZC/21ZC
ULA2 PZE-101039301 1 26,700,206 1.24E-07 4.30 21BJ/BLUP
PZE-101075097 1 59,163,811 1.13E-06 2.99 21BJ
PZE-101256077 1 305,013,865 1.48E-05 2.52 21BJ
PZE-102006385 2 3408,488 1.00E-05 3.67 20BJ
SYN2580a 2 31,809,511 1.46E-07 1.97 21BJ
PZE-102079155 2 63,417,366 3.66E-07 4.21 20ZC/21ZC
PZE-102142045 2 194,956,148 1.33E-05 7.65 19BJ/20BJ
PZE-102191957b 2 241,700,492 7.97E-07 0.06 21ZC
PZE-103016432 3 8,535,602 1.07E-05 5.65 19BJ/20BJ/20ZC/21ZC/BLUP
PZE-104023748 4 28,367,320 5.63E-07 6.90 19BJ/20ZC
PZE-104068824 4 140,064,999 1.35E-05 0.93 19BJ
SYN11091 4 172,531,224 3.58E-06 0.54 19BJ/21BJ
PZE-104123484 4 204,948,076 2.90E-07 6.49 20BJ/20ZC
PZE-104126415 4 208,894,785 8.65E-06 7.13 21ZC
PZE-105042765 5 31,030,693 4.17E-06 1.03 19BJ
PZE-107010573 7 7,544,684 4.73E-06 0.10 19BJ/20BJ
PZE-107010578c 7 7,546,222 8.28E-06 0.11 20ZC
PZE-108052985 8 96,363,878 2.60E-07 1.45 20ZC/21BJ/BLUP
PZE-108091532 8 153,166,307 1.08E-06 6.11 20ZC
PZE-109031124 9 37,396,449 1.16E-09 0.41 19BJ/20BJ/21BJ/BLUP
PZE-109038841 9 72,089,497 1.13E-05 2.47 20ZC
PZE-109041138 9 65,843,923 4.94E-06 0.96 21ZC
PZE-109042223 9 62,588,395 7.38E-06 3.05 21ZC
PZE-109086476 9 137,669,212 6.54E-06 9.30 20BJ/20ZC/21BJ/21ZC
PZE-110036140d 10 68,224,892 2.21E-07 0.22 19BJ
PZE-110064304 10 121,007,535 1.12E-08 0.11 21ZC
SYN15051e 10 125,014,193 1.62E-07 2.19 21ZC
ULA3 PZE-101039301 1 26,700,206 4.81E-07 4.15 21BJ
PZE-101061168 1 45,273,264 7.12E-06 3.98 21BJ/BLUP
PZE-101101518 1 101,087,313 6.86E-07 2.71 21BJ
PZE-101256077 1 305,013,865 3.19E-06 3.34 21ZC
PZE-102079155 2 63,417,366 2.87E-06 3.80 21BJ/21ZC
PZE-102191957b 2 241,700,492 1.47E-05 0.01 21ZC
PZE-103016432 3 8,535,602 2.96E-07 7.46 19BJ/20BJ/20ZC/21ZC/BLUP
PZE-103087199 3 145,604,315 9.49E-06 7.82 21BJ
PZE-103118170 3 179,372,004 1.52E-05 4.25 21ZC
PZE-104023748 4 28,367,320 1.36E-06 5.13 21BJ
SYN11091 4 172,531,224 4.11E-06 0.35 21BJ
PZE-105042690 5 30,864,455 5.59E-07 2.52 21BJ
PZE-105077135 5 88,521,036 3.23E-06 5.73 20BJ
PZE-105157980 5 211,658,642 1.69E-05 5.00 21BJ
ZM013489-0395 5 217,943,859 5.55E-06 0.15 19BJ
PZE-106000325 6 713,929 7.45E-06 0.17 21BJ
PZE-106036880 6 87,796,537 1.97E-06 0.02 19BJ
PZE-107010573 7 7,544,684 4.02E-06 0.13 20BJ/21ZC/BLUP
PZE-107047280 7 99,863,965 2.07E-07 0.03 21BJ
SYN15862 8 2,200,273 1.58E-07 0.01 20BJ
PZE-108052985 8 96,363,878 1.11E-05 1.09 20BJ
PZE-108091532 8 153,166,307 1.15E-07 7.13 20ZC/21BJ/BLUP
PZE-109031124 9 37,396,449 7.79E-06 0.72 19BJ/20BJ/21BJ
PZE-109039325 9 70,992,241 4.68E-06 5.15 21BJ
PZE-109086476 9 137,669,212 5.43E-06 8.23 BLUP
PZE-110036140d 10 68,224,892 1.23E-05 0.18 19BJ
SYN15051e 10 125,014,193 4.40E-07 2.21 21ZC
SYN23715 10 126,322,856 6.89E-06 4.11 21BJ/BLUP

Table 2

Significant SNPs were repeatedly detected and the candidate genes for LA traits."

Fig. 3

Genetic effect of the major SNPs associated with LA traits *** and **** indicate significance difference at P < 0.001 and P < 0.0001, respectively. Abbreviations are the same as those given in Table 1."

Table 3

LA phenotypes of maize elite germplasms in different environments"

自交系
Inbred line
ULA1 (°) ULA2 (°) ULA3 (°)
19BJ 20BJ 20ZC 21BJ 21ZC 19BJ 20BJ 20ZC 21BJ 21ZC 19BJ 20BJ 20ZC 21BJ 21ZC
B241 14.43 6.35 6.65 7.54 7.18 9.40 2.09 5.55 4.46 5.27 10.57 4.35 5.16 5.24 6.71
B292 9.48 4.57 2.56 5.70 5.41 8.78 1.66 1.62 5.65 3.26 8.57 3.33 2.34 2.68 2.87
B630 13.15 3.57 2.73 5.97 7.51 9.61 6.08 6.38 5.61 4.52 10.46 2.24 3.99 7.17 5.07
B631 14.71 4.22 6.16 10.17 9.38 11.63 4.00 6.60 4.46 4.58 9.86 2.47 2.81 4.95 5.51
B634 12.65 4.47 4.86 5.56 10.35 10.43 2.77 5.71 5.08 3.76 10.37 1.63 2.80 4.21 2.97
B635 9.68 2.15 2.71 6.08 4.60 7.84 4.12 5.31 4.83 5.93 7.80 2.81 2.82 6.36 5.51
B638 11.15 2.20 3.40 2.58 9.48 7.42 2.76 4.96 5.17 4.10 7.10 1.92 2.53 2.20 4.60
B640 13.85 5.00 4.97 4.72 11.23 11.55 4.12 6.52 6.96 5.20 10.52 3.74 2.46 5.66 4.60
B709 12.20 6.46 6.04 9.26 9.18 11.38 4.68 6.76 2.88 5.11 10.02 3.94 4.35 6.08 4.97
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