Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (5): 801-820.doi: 10.3864/j.issn.0578-1752.2023.05.001

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Genome-Wide Association Studies and Mining for Favorable Loci of Root Traits at Seedling Stage in Wheat

WANG Mai1(), DONG QingFeng1, GAO ShenAo1, LIU DeZheng1, LU Shan1, QIAO PengFang1, CHEN Liang1, HU YinGang1,2()   

  1. 1 College of Agronomy, Northwest A & F University/State Key Laboratory of Crop Stress Biology for Arid Areas, Yangling 712100, Shaanxi
    2 Institute of Water-Saving Agriculture in Arid Areas of China, Yangling 712100, Shaanxi
  • Received:2022-10-06 Accepted:2022-12-13 Online:2023-03-01 Published:2023-03-13

Abstract:

【Objective】Plant roots are critical for water and nutrient acquisition, crop growth and development as well as yield formation. Exploring SNP loci significantly associated with root traits in wheat at seedling stage and mining candidate genes, will lay a foundation for understanding the genetic mechanism of wheat root system architecture and breeding wheat elite varieties with better root architecture.【Method】In this study, 189 diverse wheat cultivars were assembled as an association-mapping panel, five root traits including total root length (TRL), total root area (TRA), total root volume (TRV), average root diameter (ARD) and root dry weight (RDW) were investigated by growing in two culture conditions (Hoagland nutrient solution and pure water), and the experiments were repeated twice. Then, genome-wide association studies (GWAS) were performed for the five root traits with genotypic data derived from Wheat 660K SNP Array. Candidate genes were predicted by sequence alignment, domain analysis, and annotation information. Futhermore, kompetitive allele specific PCR (KASP) markers were developed for root traits. 【Result】The root traits varied greatly among the 189 cultivars, and the roots were thick and short cultured under Hoagland nutrient solution, while slender seminal roots and more lateral roots were observed under pure water. A total of 95 QTLs significantly associated with root traits cultured in two conditions (P<10-3) were identified by genome-wide association studies with four models of BLINK (bayesian-information and linkage-disequilibrium iteratively nested keyway), CMLM (compressed mixed linear model), FarmCPU (fixed and random model circulating probability unification) and MLM (mixed linear model). Among them, 18 QTLs were detected in both culture conditions and distributed on chromosomes of 7A, 1B, 2B, 3B, 7B, 1D, 2D, and 3D, which explained 8.68%-14.07% of phenotypic variation. Of those significant loci, 4 QTLs were similar or consistent with that reported previously, and the rest were novel ones. Haplotype analysis conducted for co-localization QTLs of 10 SNPs revealed significant differences in root traits between the two haplotypes of wheat cultivars. Based on these SNPs, KASP markers XNR7143 and XNR3707 were developed for total root volume and root dry weight, respectively. In addition, 12 candidate genes possibly regulating root development were found by mining the genes within the interval of co-localization significant SNPs. Of them, TraesCS7A02G160600, encoding 3-oxoacyl-[acyl-carrier-protein] synthase, is involved in the synthesis of root fatty acids; TraesCS1B02G401800, encoding syntaxin, plays an important role in plant tropism; TraesCS7B02G417900, encoding aldehyde oxidase, contributes to the synthesis of abscisic acid and regulation of crop root development. 【Conclusion】The root traits of wheat varied significantly among the wheat genotypes. Genome-wide association studies detected 18 significant QTLs linked with root traits simultaneously in two culture conditions, two KASP markers were developed for root traits, and 12 candidate genes related to root development were screened, which might provide reference for understanding the regulation mechanism of wheat root traits and molecular marker-assisted breeding for wheat improvement.

Key words: wheat, root traits, genome-wide association study, co-localization SNPs, KASP (kompetitive allele specific PCR) markers, candidate genes

Table 1

Primer sequences of polymorphic KASP markers"

标记名称 KASP name 引物序列 Primer sequence (5′-3′)
XNR7143 F-P GAAGGTGACCAAGTTCATGCTgtgacatggaggacgctgc
V-P GAAGGTCGGAGTCAACGGATTgtgacatggaggacgctgt
R-P tcgtggagaacatcttgcgt
XNR3707 F-P GAAGGTGACCAAGTTCATGCTtgcatcatagtacataccactgc
V-P GAAGGTCGGAGTCAACGGATTtgcatcatagtacataccactgt
R-P aattggcgacattgggagac

Fig.1

Frequency distribution f root traits in different culture conditions A-E: Hogland culture; F-J: Pure water culture"

Table 2

Descriptive statistics of root traits in different culture conditions"

培养条件
Environment
性状
Traits
变异范围
Range
均值
Mean
标准差
SD
变异系数
CV (%)
霍格兰营养液
HL
根系总长度TRL (cm) 8.42—141.54 43.73 23.57 52.69
根系总表面积TRA (cm2) 2.09—33.15 12.53 6.47 51.62
根系总体积TRV (cm3) 0.03—1.37 0.41 0.27 66.38
根系平均直径ARD (mm) 0.43—1.40 0.95 0.21 22.13
根系干重RDW (g) 0.0010—0.0180 0.0061 0.0025 40.31
去离子水
PW
根系总长度TRL (cm) 49.45—348.24 211.01 51.68 24.49
根系总表面积TRA (cm2) 10.20—39.22 25.27 5.62 22.26
根系总体积TRV (cm3) 0.13—0.61 0.32 0.08 25.52
根系平均直径ARD (mm) 0.33—1.09 0.4304 0.07 15.43
根系干重RDW (g) 0.0088—0.0244 0.0171 0.0030 17.76

Table 3

Variance analysis and broad-sense heritability of root traits in wheat"

性状
Traits
基因型 Genotype 处理 Treatment 基因型×处理 Genotype×Treatment 广义遗传力(H2
Broad-sense
heritability (%)
F <BOLD>P</BOLD> <BOLD>F</BOLD> <BOLD>P</BOLD> <BOLD>F</BOLD> <BOLD>P</BOLD>
根系总长度 TRL (cm) 7.35 4.79E-79*** 10443.99 5.35E-45*** 6.74 3.99E-72*** 62.40
根系总表面积 TRA (cm2) 6.19 1.47E-65*** 2328.39 1.61E-220*** 5.26 4.72E-54*** 64.24
根系总体积 TRV (cm3) 4.55 9.65E-45*** 83.44 7.64E-19*** 4.15 2.06E-39*** 62.88
根系平均直径 ARD (mm) 5.14 1.59E-52*** 5089.04 3.69E-56*** 5.07 1.35E-51*** 60.41
根系干重 RDW (g) 24.51 5.27E-221*** 33559.75 4.19E-40*** 18.23 2.19E-183*** 65.30

Fig. 2

Correlation coefficients between root traits under different culture conditions A: Hogland culture; B: Pure water culture. *, ** and *** represent significance of difference at P<0.05, P<0.01 and P<0.001, respectively. The same as below"

Fig. 3

Distribution of SNPs on each chromosome of bread wheat"

Table 4

The number and polymorphism of SNP markers on each chromosome of wheat"

染色体
Chromosome
标记数目
No. of markers
长度
Length (Mb)
标记密度
Density of markers
遗传多样性
Genetic diversity
多态信息含量
PIC
1A 19003 594.10 0.03 0.3251 0.2642
1B 16540 689.99 0.04 0.3851 0.3036
1D 7935 495.45 0.06 0.3349 0.2713
2A 22510 780.80 0.03 0.3567 0.2892
2B 19755 801.26 0.04 0.3651 0.2906
2D 7174 651.85 0.09 0.3689 0.2930
3A 12754 750.84 0.06 0.3687 0.2927
3B 36612 830.83 0.02 0.3518 0.2870
3D 4883 615.55 0.13 0.3463 0.2802
4A 12345 744.59 0.06 0.3522 0.2836
4B 10959 673.62 0.06 0.3449 0.2799
4D 2408 509.86 0.21 0.3654 0.2900
5A 17658 709.77 0.04 0.3912 0.3083
5B 26618 713.15 0.03 0.3743 0.2972
5D 5628 566.08 0.10 0.3430 0.2747
6A 12934 618.08 0.05 0.3799 0.3004
6B 17890 720.99 0.04 0.3635 0.2911
6D 4997 473.59 0.09 0.3378 0.2728
7A 18490 736.71 0.04 0.3287 0.2639
7B 12260 750.62 0.06 0.3776 0.2985
7D 6758 638.69 0.09 0.3359 0.2706
A基因组A genome 115694 4934.89 0.04 0.3575 0.2860
B基因组B genome 140634 5180.46 0.04 0.3660 0.2926
D基因组D genome 39783 3951.07 0.10 0.3475 0.2789
总计Total 296111 14066.42 0.05 0.3570 0.2858

Fig. 4

Population structure and linkage disequilibrium analysis of 189 wheat varieties (cultivars) A: CV error of subpopulation; B: Population structure; C: Principal component analysis of 189 wheat varieties (cultivars); D: Linkage disequilibrium attenuation distance of subgenomes and the whole genome"

Fig.5

Circular Manhattan plots and QQ plots of root traits in different culture conditions A-E: Hogland culture; F-J: Pure water culture; Manhattan plots: The BLINK, CMLM, FarmCPU and MLM models of root traits from the inner to outer were respectively showed"

Table 5

Significant SNPs detected simultaneously in two culture conditions"

显著性标记
SNP
关联性状
Related traits
染色体
Chromosome
位置
Position (Mb)
<BOLD>P</BOLD>
-log10(<BOLD>P</BOLD>)
贡献率
R2 (%)
AX-109555941 TRL 1B 689.00 4.63 14.07
AX-108888527 TRL 2D 556.05 4.12 11.73
TRA 4.11 10.64
AX-94581300 TRL 3D 239.36 3.56 10.83
AX-108889829 TRL 2B 85.25 4.15 11.52
AX-111514405 TRL 2B 81.55 3.57 9.33
AX-109029863 RDW 3B 416.69 4.13 11.18
TRA 4.28 11.11
AX-108924279 RDW 2B 57.67 3.36 9.02
AX-110371944 RDW 2B 57.68 3.43 9.01
AX-110455550 RDW 2B 57.67 3.43 9.01
AX-110567747 RDW 2B 57.78 3.36 8.68
AX-109933707 RDW 2B 57.68 3.49 9.09
AX-108792070 TRA 7A 638.24 3.79 11.19
TRV 3.70 11.13
AX-110097055 TRA 7A 638.52 3.79 11.19
TRV 3.70 11.13
AX-110497143 TRV 7A 116.76 4.28 11.19
AX-110491393 TRV 1B 632.00 5.11 13.93
AX-111564445 TRV 3B 757.93 4.10 10.60
AX-94823257 TRV 1D 460.79 4.14 10.75
AX-110122975 TRV 7B 686.14 3.54 9.82

Fig. 6

Haplotype of SNPs in the stable region at 57.144-57.960 Mb on chromosome 2B A: LD heat map on 57.144-57.960 Mb of chromosome 2B; B: Two haplotypes with different alleles; C: Phenotypic effects of different haplotypes"

Fig. 7

Haplotype analysis of significant SNP loci in root traits of wheat at seedling stage"

Table 6

Annotations of candidate genes for root traits"

候选基因 Candidate genes 物理位置 Position (bp) 功能注释 Gene annotations
TraesCS7A02G160600 Chr.7A:116650020—116654196 3-氧酰基-酰基载体蛋白质合成酶 3-oxoacyl-[acyl-carrier-protein] synthase
TraesCS1B02G401800 Chr.1B:631998104—632003904 突触融合蛋白 Syntaxin
TraesCS2B02G097600 Chr.2B:57672647—57676616 黄条转运蛋白12 Yellow stripe-like transporter 12
TraesCS2B02G097800 Chr.2B:57679415—57682721 MLO蛋白 MLO-like protein
TraesCS2B02G097900 Chr.2B:57778375—57781675 MLO蛋白 MLO-like protein
TraesCS2B02G117900 Chr.2B:81755546—81758516 WUSCHEL相关同源框蛋白 WUSCHEL-related homeobox
TraesCS2B02G119200 Chr.2B:85320654—85325523 三磷酸腺苷双磷酸酶 Apyrase-like protein
TraesCS3B02G516000 Chr.3B:757920799—757926024 转录起始因子TFIID亚基9 Transcription initiation factor TFIID subunit 9
TraesCS7B02G417900 Chr.7B:686141549—686157029 醛脱氢酶 Aldehyde oxidase
TraesCS1D02G388600 Chr.1D:460789199 - 460794120 解毒蛋白 Detoxification protein
TraesCS2D02G445500 Chr.2D:556053437—556059076 E3泛素蛋白连接酶RNF14 E3 ubiquitin-protein ligase RNF14
TraesCS3D02G201400 Chr.3D:239349590—239362410 分子伴侣 danJ Chaperone protein dnaJ

Fig. 8

Expression heatmap of candidate genes for root traits Red indicates high expression of the gene at a certain tissue, while pink and white indicate low expression of the gene at a certain tissue"

Fig. 9

Genotyping of KASP markers in natural population Red indicates that the bases are homozygous for TT genotypes; blue indicates that the bases are homozygous for CC genotypes; Black represent NTC (no template control); Pink indicates that the genotypes could not be separated clearly"

Table 7

Phenotypic verification of XNR7143 and XNR3707 in natural population"

性状
Traits
标记
Marker
<BOLD>KASP</BOLD>标记
<BOLD>KASP </BOLD>marker
基因型
Genotype
数量
Number
均值
Mean
P
P value
根系总体积
TRV (cm3)
AX-110497143 XNR7143 CC 165 0.4000 2×10-6**
TT 6 0.9300
根系干重
RDW (g)
AX-109933707 XNR3707 CC 94 0.0162 0.001**
TT 77 0.0180
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