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Acta Agronomica Sinica ›› 2025, Vol. 51 ›› Issue (8): 2020-2032.doi: 10.3724/SP.J.1006.2025.51020

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

Genome-wide association study of root traits in wheat seedlings and identification of a superior allele at TaSRL-3B

CAI Jin-Shan1(), LI Chao-Nan2, WANG Jing-Yi2, LI Ning1, LIU Yu-Ping2, JING Rui-Lian2, LI Long2,*(), SUN Dai-Zhen1,*()   

  1. 1College of Agriculture, Shanxi Agricultural University, Taigu 030801, Shanxi, China
    2State Key Laboratory of Crop Gene Resources and Breeding / Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
  • Received:2025-02-24 Accepted:2025-06-01 Online:2025-08-12 Published:2025-06-10
  • Contact: *E-mail: sdz64@126.com;E-mail: lilong01@caas.cn
  • Supported by:
    National Key R&D Program of China(2022YFD1200201);China Agriculture Research System of MOF and MARA(CARS-03-5)

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Abstract:

The root system is the primary organ responsible for water and nutrient uptake in wheat, and its morphological characteristics are closely associated with yield and tolerance to abiotic stress. Therefore, identifying genetic loci and favorable alleles that control root morphology is of great importance for wheat improvement. In this study, 277 wheat accessions were evaluated using a gel-chamber-based observation method to characterize eight root morphological traits at the seedling stage, including total root length, root surface area, and root angle. Based on genotyping with the Wheat 660K SNP Array, a genome-wide association study (GWAS) was performed using three models (GLM, MLM, and FarmCPU), leading to the identification of 52 associated loci. Among them, six pleiotropic loci (Loci17, Loci20, Loci22, Loci38, Loci46, and Loci47) were located on chromosomes 3A, 3B, 3D, 5A, 6A, and 6B, respectively. Within Loci20, the candidate gene TaSRL-3B, associated with root morphology, was cloned. This gene has a full-length sequence of 1089 bp, lacks introns, and contains a conserved NAC domain between amino acids 78 and 235. A 20-bp insertion/deletion (InDel717) in the coding region of TaSRL-3B caused a frameshift mutation and showed strong linkage (R2 = 0.84) with the candidate SNP (AX-108758584) in Loci20. Accessions carrying the TaSRL-3BIn allele exhibited significantly greater maximum root length, total root length, and root surface area compared to those with the TaSRL-3BIn. A backcross introgression line population (BC3F5) was developed using Lumai 14 (LM14, carrying TaSRL-3BDel as the recurrent parent and Shaanhe 6 (SH6, carrying TaSRL-3BIn as the donor. A molecular marker based on InDel717 was used to identify five near-isogenic lines (NILs) carrying TaSRL-3BIn from this population. Compared to LM14, these lines showed significant improvements in maximum root length, total root length, root surface area, and root volume, further confirming the role of TaSRL-3B in shaping seedling root morphology. Notably, the frequency of the long-root allele TaSRL-3BIn has declined in modern Chinese cultivars compared to landraces. This study provides valuable insights into the genetic regulation of wheat root traits and supports the genetic improvement of root systems for enhanced wheat performance.

Key words: wheat, seedling, root morphology, genome-wide association analysis, candidate gene

Table 1

Statistic analysis of root traits"

性状
Trait		 变异范围
Range		 均值
Mean		 标准差
SD		 变异系数
CV (%)		 广义遗传力
Broad-sense heritability (%)
最大根长 MRL (cm) 7.59-20.30 16.02 1.56 9.74 83.41
总根长 TRL (cm) 32.88-71.89 51.37 7.85 15.28 79.16
根直径 RD (mm) 0.40-0.57 0.49 0.03 6.12 78.10
根数目 RN 3.11-5.67 4.49 0.55 12.25 74.13
根表面积 RS (cm2) 4.70-11.57 7.85 1.23 15.67 76.32
根体积 RV (cm3) 0.06-0.17 0.09 0.02 22.22 74.05
根鲜重 RFW (g) 0.03-0.11 0.07 0.01 14.29 69.13
根角度 RA (°) 25.90-155.82 108.26 28.29 26.13 77.79

Fig. 1

Correlation matrix of wheat seedling root traits The diagonal displays histograms of individual root traits. The bottom left part of the matrix shows the scatter plots between root traits, red lines indicate linear regressions, the top right part shows the correlation coefficient. * and ** indicate significant correlation at the 0.05 and 0.01 probability levels, respectively. Darker colors represent stronger correlations. Abbreviations are the same as those given in Table 1."

Fig. 2

GWAS of root traits in wheat seedling A-C: manhattan plots of GWAS results for root traits based on the GLM, MLM, and FarmCPU model, respectively. From the innermost to the outermost rings, the GWAS results are shown for maximum root length, total root length, root diameter, root number, root surface area, root volume, root fresh weight and root angle. D: venn diagram of GWAS results for root traits based on different models. E: distribution of associated loci on chromosomes, red indicates pleiotropic loci. GLM: general linear model; MLM: mixed linear model; FarmCPU: fixed and random model circulating probability unification."

Table S1

Significant associated loci for wheat root traits"

关联位点 性状 候选SNP 染色体 位置 P值GLM P值MLM P值FarmCPU
Associated loci Trait Candidate SNP Chromosome Position (bp) -log10 (PGLM) -log10(PMLM) -log10(PFarmCPU)
Loci1 RA AX-94530450 1A 1,174,785 6.36 4.59 6.36
Loci2 TRL AX-94938835 1A 45,797,074 4.80 3.86 6.81
Loci3 RV AX-108830982 1A 49,331,465 4.96 4.20 4.96
Loci4 RD AX-95211457 1A 57,764,436 4.80 2.51 4.80
Loci5 RA AX-110550989 1A 363,636,440 5.10 2.47 5.10
Loci6 RD AX-95151393 1B 94,831,699 4.95 2.73 4.95
Loci7 RA AX-109887764 1B 684,214,070 5.25 4.32 5.25
Loci8 RD AX-94783903 1D 58,760,372 5.67 2.92 5.67
Loci9 RD AX-94763625 1D 62,415,780 4.79 2.54 4.79
Loci10 RA AX-108748925 1D 293,524,586 4.74 2.14 4.74
Loci11 RN AX-108757188 2A 14,946,475 6.45 5.35 6.45
Loci12 RN AX-110058193 2B 27,539,477 4.88 2.66 4.88
Loci13 RN AX-95124238 2D 598,329,680 5.08 4.15 5.08
Loci14 RD AX-111129296 3A 15,334,246 5.06 4.57 5.06
Loci15 RV AX-94413327 3A 33,200,963 5.60 4.43 5.60
Loci16 RN AX-94531407 3A 355,255,702 5.11 3.97 5.11
Loci17 TRL AX-95170863 3A 642,157,356 8.74 4.90 0.07
Loci17 RS AX-95170863 3A 642,157,356 9.02 5.31 0.78
Loci18 RN AX-110919402 3B 272,543,663 5.80 3.26 5.80
Loci19 TRL AX-109991407 3B 627,748,254 7.07 4.73 8.57
Loci20 MRL AX-108758584 3B 658,464,182 8.00 5.16 13.56
Loci20 TRL AX-108758584 3B 658,464,182 10.28 4.78 0.03
Loci20 RS AX-108758584 3B 658,464,182 9.51 5.01 13.92
Loci21 RD AX-108861242 3D 41,269,285 4.80 5.37 4.80
Loci22 MRL AX-95079631 3D 496,787,830 7.37 5.01 0.14
Loci22 TRL AX-95079631 3D 496,787,830 10.33 5.94 9.82
Loci22 RS AX-95079631 3D 496,787,830 8.90 5.65 0.09
Loci23 TRL AX-94519825 3D 504,057,903 8.55 4.98 0.13
Loci24 RN AX-111498171 3D 587,502,221 5.07 3.73 5.07
Loci25 RN AX-109907879 3D 611,193,094 4.77 3.66 4.77
Loci26 RFW AX-110691523 4A 2,981,188 4.83 3.52 4.83
Loci27 RA AX-110721031 4A 601,774,555 4.91 2.99 4.91
Loci28 RA AX-109400915 4A 614,230,276 6.70 4.77 6.70
Loci29 RD AX-110473901 4A 719,247,368 4.83 2.68 4.83
Loci30 RA AX-95229763 4B 14,112,442 4.83 3.02 4.83
Loci31 RA AX-109453026 4B 217,485,661 5.36 2.92 5.36
Loci32 RA AX-111556840 4B 226,194,248 4.88 2.47 4.88
Loci33 RA AX-111593000 4B 237,489,681 5.29 2.66 5.29
Loci34 RA AX-94629126 4B 281,732,587 5.06 3.69 5.06
Loci35 RA AX-109330449 4B 306,933,435 4.80 2.36 4.80
Loci36 RA AX-110103911 4B 361,732,573 4.96 2.57 4.96
Loci37 RV AX-109216467 4D 206,954,832 5.12 4.61 5.12
Loci38 TRL AX-109929811 5A 39,928,718 6.15 4.87 7.16
Loci38 RFW AX-109929811 5A 39,928,718 5.17 4.69 5.17
Loci38 RS AX-109929811 5A 39,928,718 5.77 4.66 11.90
Loci39 RN AX-94790761 5B 15,321,516 4.74 3.88 4.74
Loci40 MRL AX-109840604 5B 604,060,280 4.77 3.46 6.71
Loci41 RA AX-110957626 5B 691,956,913 7.53 6.64 7.53
Loci42 RD AX-110048366 5D 31,117,168 5.04 2.98 5.04
Loci43 RA AX-94486801 5D 553,010,006 5.16 3.70 5.16
Loci44 RD AX-108863773 6A 13,601,639 4.95 3.17 4.95
Loci45 RFW AX-109936313 6A 50,437,525 5.53 4.24 5.53
Loci46 TRL AX-110579044 6A 58,050,390 6.32 3.48 6.99
Loci46 RFW AX-110579044 6A 58,050,390 6.58 4.57 6.58
Loci46 RS AX-110579044 6A 58,050,390 6.93 3.96 9.22
Loci47 MRL AX-95018127 6B 19,999,314 7.67 5.22 0.34
Loci47 TRL AX-95018127 6B 19,999,314 8.97 5.08 0.29
Loci47 RS AX-95018127 6B 19,999,314 7.72 4.83 0.01
Loci48 RV AX-108958707 6B 93,414,710 5.08 4.03 5.08
Loci49 RFW AX-109954348 6B 94,122,920 6.60 4.56 6.60
Loci50 TRL AX-108776159 6B 713,461,853 5.00 2.75 5.56
Loci51 RA AX-109078183 6D 7,469,443 5.18 3.40 5.18
Loci52 RN AX-94519359 7A 538,102,732 4.93 3.59 4.93

Table 2

Pleiotropic associated loci for wheat root traits"

关联位点 性状 候选SNP 染色体 位置 P值GLM P值MLM P值FarmCPU
Associated loci Trait Candidate SNP Chromosome Position (bp) -log10(PGLM) -log10(PMLM) -log10(PFarmCPU)
Loci17 TRL AX-95170863 3A 642,157,356 8.74 4.90 0.07
Loci17 RS AX-95170863 3A 642,157,356 9.02 5.31 0.78
Loci20 MRL AX-108758584 3B 658,464,182 8.00 5.16 13.56
Loci20 TRL AX-108758584 3B 658,464,182 10.28 4.78 0.03
Loci20 RS AX-108758584 3B 658,464,182 9.51 5.01 13.92
Loci22 MRL AX-95079631 3D 496,787,830 7.37 5.01 0.14
Loci22 TRL AX-95079631 3D 496,787,830 10.33 5.94 9.82
Loci22 RS AX-95079631 3D 496,787,830 8.90 5.65 0.09
Loci38 TRL AX-109929811 5A 39,928,718 6.15 4.87 7.16
Loci38 RFW AX-109929811 5A 39,928,718 5.17 4.69 5.17
Loci38 RS AX-109929811 5A 39,928,718 5.77 4.66 11.90
Loci46 TRL AX-110579044 6A 58,050,390 6.32 3.48 6.99
Loci46 RFW AX-110579044 6A 58,050,390 6.58 4.57 6.58
Loci46 RS AX-110579044 6A 58,050,390 6.93 3.96 9.22
Loci47 MRL AX-95018127 6B 19,999,314 7.67 5.22 0.34
Loci47 TRL AX-95018127 6B 19,999,314 8.97 5.08 0.29
Loci47 RS AX-95018127 6B 19,999,314 7.72 4.83 0.01

Table 3

Annotation of genes in Loci20"

基因号 Gene ID 物理位置 Physical position (bp) 功能注释 Gene annotation
TraesCS3B02G421100 Chr.3B: 658,058,978-658,060,408 多巴双加氧酶 4,5-DOPA dioxygenase extradiol
TraesCS3B02G421200 Chr.3B: 658,062,268-658,065,391 外二醇双加氧酶 Extradiol dioxygenase
TraesCS3B02G421300 Chr.3B: 658,462,627-658,463,973 含NAC结构域蛋白 NAC domain containing protein
TraesCS3B02G421400 Chr.3B: 658,486,988-658,488,416 邻氨基苯甲酸 O-甲基转移酶1 Anthranilate O-methyltransferase 1
TraesCS3B02G421500 Chr.3B: 658,489,846-658,491,612 邻氨基苯甲酸 O-甲基转移酶1 Anthranilate O-methyltransferase 1
TraesCS3B02G421600 Chr.3B: 658,494,276-658,498,604 转录起始因子TFIID 亚基9 TFIID subunit 9

Fig. 3

Association of TaSRL-3B allelic variation with cSNP and root phenotype A: analysis of allelic variation of TaSRL-3B gene and its association with root traits (MLM model). Red, yellow, and blue dots represent the results of association analysis between TaSRL-3B gene alleles and maximum root length (MRL), root surface area (RS) and total root length (TRL), respectively. B: linkage disequilibrium analysis of TaSRL-3B gene alleles and cSNP. C-E: differences of root traits between wheat accessions with In717 and Del717. ** indicates significant correlation at the 0.01 probability level. Abbreviations are the same as those given in Table 1. cSNP: coding region single nucleotide polymorphism; In: insertion; Del: deletion."

Fig. 4

Creation and root phenotypic analysis of near-isogenic lines of LM14 A: genotyping of LM14 and SH6 identified by molecular marker STSTaSRL-3B. B: the creation process of near-isogenic lines of LM14. C: photograph of the seedling roots of LM14 and its near-isogenic lines, scale bar is 2 cm. D-G: comparison of root traits of LM14 and its near-isogenic lines at seedling stage. Letters above the bars indicate significant differences among groups; different lowercase letters denote significance at the α = 0.05 level. LM14: Lumai 14; SH6: Shaanhe 6."

Fig. 5

Frequency distribution of TaSRL-3B alleles in 10 wheat production zones across China A: distribution of TaSRL-3B alleles in landraces. B: distribution of TaSRL-3B alleles in modern varieties. I: northern winter wheat zone; II: Huang-huai river valleys facultative wheat zone; III: middle and low Yangtze valleys autumn-sown spring wheat zone; IV: southwestern autumn-sown spring wheat zone; V: southern autumn-sown spring wheat zone; VI: northeastern spring wheat zone; VII: northern spring wheat zone; VIII: northwestern spring wheat zone; IX: Qinghai-tibetan plateau spring-winter wheat zone; X: xinjiang winter-spring wheat zone."

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