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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (3): 623-632.doi: 10.3724/SP.J.1006.2024.34091


Genome-wide association analysis and candidate genes predication of leaf characteristics traits in soybean (Glycine max L.)

WANG Qiong1(), ZHU Yu-Xiang1,2, ZHOU Mi-Mi1, ZHANG Wei1, ZHANG Hong-Mei1, CEHN Xin1, CEHN Hua-Tao1,*(), CUI Xiao-Yan1,*()   

  1. 1Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences / Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210014, Jiangsu, China
    2College of Horticulture and Landscape Architecture, Yangzhou University, Yangzhou 225009, Jiangsu, China
  • Received:2023-05-25 Accepted:2023-09-13 Online:2024-03-12 Published:2023-10-07
  • Contact: *E-mail: cht@jaas.ac.cn; E-mail: cxy@jaas.ac.cn
  • Supported by:
    Natural Science Foundation of Jiangsu Province(BK20220740);Jiangsu Seed Industry Revitalizing Project(JBGS[2021]057);Key Research and Development Program of Jiangsu Province(BE2022328);Jiangsu Agricultural Science and Technology Innovation Fund(CX(22)5002)


Leaf shape and vertical distribution of soybean affect canopy structure, photosynthetic efficiency, and yield. The existence of different leaf shapes and sizes on the same plant, which is known as heterophylly, has been observed in many flowering plant species. Yet, the genetic characteristics and genetic basis of heterophylly in soybean remain unknown. In this study, leaf characteristics such as leaf length, leaf width, leaf shape index, and heterophylly index were investigated in 283 soybean germplasm resources for two consecutive years in Nanjing, Jiangsu Province. A total of 181 related loci were detected by genome-wide association study (GWAS), among which 18 loci could be repeatedly detected in two environments or among multiple traits. Using the loci associated with leaf characteristics, we integrated the GWAS approach with the expression profiling data and gene-based association and functional annotation of orthologs in Arabidopsis to identify candidate genes involved in leaf development in soybean. The known soybean leaf shape regulatory gene Ln (Glyma.20G116200) was found upstream of locus Chr20:36152820. In addition, two candidate genes (Glyma.19G192700 and Glyma.19G194100) were identified near the related locus Chr19:45155943 on chromosome 19, homologous genes of growth-regulating factor 4 (GRF4), and LITTLE ZIPPER 3 (ZPR3), respectively. These results lay a solid foundation for expanding our understanding of the genetic mechanism of heterophylly in soybean.

Key words: soybean, leaf characteristics, heterophylly, GWAS, SNP markers

Fig. 1

Schematic representation of the design in the experiment"

Table 1

Statistical analysis of leaf characteristics traits of soybean association panel"

CV (%)
2021 Nanjing
上部叶长 Upper leaf length 7.00 18.00 11.25±1.94 0.17
上部叶宽 Upper leaf width 2.50 9.70 5.66±1.41 0.25
上部叶形 Upper leaf shape 1.36 3.24 2.05±0.42 0.20
下部叶长 Lower leaf length 4.00 12.10 7.44±1.42 0.19
下部叶宽 Lower leaf width 2.80 8.03 4.94±1.00 0.20
下部叶形 Lower leaf shape 1.12 2.14 1.50±0.22 0.15
异形叶指数 Heterophylly leaf index 0.90 2.11 1.36±0.25 0.18
2022 Nanjing
上部叶长 Upper leaf length 6.67 17.23 11.28±1.86 0.16
上部叶宽 Upper leaf width 3.53 11.17 6.13±1.39 0.23
上部叶形 Upper leaf shape 1.38 2.90 1.90±0.32 0.17
下部叶长 Lower leaf length 4.83 15.13 9.24±1.58 0.17
下部叶宽 Lower leaf width 2.90 9.60 5.72±1.29 0.23
下部叶形 Lower leaf shape 1.20 2.91 1.67±0.35 0.21
异形叶指数 Heterophylly leaf index 0.68 1.76 1.16±0.19 0.16

Fig. 2

Distribution of leaf characteristics traits of soybean association panel"

Table 2

Correlation coefficients of leaf characteristics traits"

Correlation coefficient
上部叶长 Upper leaf length 0.41 6.10E-09
上部叶宽 Upper leaf width 0.61 1.02E-19
上部叶形 Upper leaf shape 0.64 6.19E-22
下部叶长 Lower leaf length 0.26 4.24E-04
下部叶宽 Lower leaf width 0.36 9.75E-07
下部叶形 Lower leaf shape 0.59 4.49E-18
异形叶指数 Heterophylly leaf index 0.53 1.73E-13

Fig. 3

Correlation coefficients among leaf characteristics traits in soybean *, **, and *** mean significant correlation at the 0.05, 0.01, and 0.001 probability levels, respectively."

Table 3

GWAS signals of leaf characteristics traits"

5_10.7 Chr05:10705738 5 10705738 7.47E-07 2021下部叶长 Lower leaf length in 2021
5_10.7 Chr05:10705738 5 10705738 1.93E-06 2021下部叶宽 Lower leaf width in 2021
10_50.7 Chr10:50760191 10 50760191 2.01E-06 2021上部叶形 Upper leaf shape in 2021
10_50.7 Chr10:50760191 10 50760191 1.10E-06 2021异形叶指数 Heterophylly index in 2021
13_39.7 Chr13:39721130 13 39721130 1.53E-06 2022上部叶宽 Upper leaf width in 2022
13_39.7 Chr13:39772387 13 39772387 8.95E-06 2021上部叶形 Upper leaf shape in 2021
16_32.2 Chr16:32235624 16 32235624 3.05E-06 2021上部叶长 Upper leaf length in 2021
16_32.2 Chr16:32236735 16 32236735 1.41E-06 2021下部叶长 Lower leaf length in 2021
17_40.9 Chr17:40908625 17 40908625 9.14E-06 2022 上部叶长 Upper leaf length in 2022
17_40.9 Chr17:40908625 17 40908625 2.91E-06 2022下部叶长 Lower leaf length in 2022
19_23.9 Chr19:23901295 19 23901295 2.43E-06 2021上部叶宽 Upper leaf width in 2021
19_23.9 Chr19:23901508 19 23901508 6.92E-06 2022上部叶宽 Upper leaf width in 2022
19_45.1 Chr19:45151266 19 45151266 6.05E-06 2022上部叶形 Upper leaf shape in 2022
19_45.1 Chr19:45155931 19 45155931 9.51E-06 2022上部叶宽 Upper leaf width in 2022
19_45.1 Chr19:45155943 19 45155943 2.45E-07 2021上部叶形 Upper leaf shape in 2021
19_45.1 Chr19:45155943 19 45155943 2.84E-08 2021异形叶指数 Heterophylly index in 2021
20_19.2 Chr20:19295767 20 19295767 8.08E-06 2022上部叶形 Upper leaf shape in 2022
20_19.2 Chr20:19295767 20 19295767 3.39E-06 2022下部叶形 Lower leaf shape in 2022

Fig. S1

Manhattan plots for GWAS of leaf characteristics traits"

Fig. 4

Relative expression pattern of candidate genes Glyma.19G192700"

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