Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (21): 4487-4499.doi: 10.3864/j.issn.0578-1752.2021.21.001


Genome-Wide Association Analysis for Yield and Nitrogen Efficiency Related Traits of Wheat at Seedling Stage

ZHANG PengXia1(),ZHOU XiuWen1,LIANG Xue2,GUO Ying1,ZHAO Yan1,LI SiShen1,KONG FanMei1,*()   

  1. 1Shandong Agricultural University/State Key Laboratory of Crop Biology/National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, Tai’an 271018, Shandong;
    2Caoxian Soil Fertilizer Workstation of Shandong Province, Caoxian 274400, Shandong
  • Received:2021-02-07 Accepted:2021-04-14 Online:2021-11-01 Published:2021-11-09
  • Contact: FanMei KONG;


【Objective】 To identify and locate the molecular markers which were stable and significantly correlated to the traits of biomass and N efficiency under different N nutrition levels will help to provide reference for cloning and characterization of the related genes.【Method】A group of 134 wheat varieties (or lines) were used in a two-years (2013 and 2014) hydroponic experiments, in which three treatments applying normal level N, low level N and high level N were set up. Fourteen traits related to biomass and N efficiency were measured, as the respective average values of each treatment in one year and two years. Genome-wide association analysis using 90K SNP molecular markers was carried out for the tested traits by MLM+K+Q mixed linear model. 【Result】 Compared with normal nitrogen treatments, roots, shoots, and plant nitrogen content and nitrogen accumulation were significantly reduced in low nitrogen treatments, while root biomass and root and plant nitrogen efficiency were significantly increased. In high nitrogen treatments, almost all traits are significantly increased. The heritability of all the tested traits were above 40%. According to genome-wide association analysis on the 9 329 SNPs, a total of 838 molecular marker sites were identified associating with 14 traits significantly (P≤0.001). These markers located on 21 chromosomes, among which 435 (51.91%) molecular marker sites were detected in only one environment, 403 and 8 environment stable sites were identified in at least two or three environments, two environmental stable SNP marker sites were identified in at least four environments. The two stable markers (Kukri_c65481_121 and tplb0025f09_1052) were significantly related to total nitrogen use efficiency of plant (TNUE) and root nitrogen use efficiency (RNUE), respectively. Five multi-trait co-location SNP marker sites which simultaneously associated with at least six traits were located on chromosomes 1A, 1B(2), and 2A(2). Furtherly, candidate gene prediction was conducted in the 214 kb genomic region of 5 SNP sites co-located with 6 traits (biomass and N efficiency traits) and 2 SNP sites associated with multiple environments (4 environments). According to the genome annotation and LD attenuation level, a total of 84 candidate genes were determined. Gene function annotations of these genes were performed using the coding protein types of known cloned nitrogen efficiency genes, candidate gene function annotation information and the use of plant comparative genomics resource library protein sequence homology analysis, 3 candidate genes were initially determined. 【Conclusion】 Different N treatments significantly affected the phenotypic traits of biomass, N efficiency and the expression of related QTLs at seedling stage of wheat. Most SNPs were detected in only one N environment, but there were some locations with relatively strong environmental stability. There was a significant correlation between biomass and N efficiency related traits, and they might be partly controlled by the same QTL/gene. The functions of related candidate genes related to N efficiency and biomass of wheat selected in this paper needed to be further verified.

Key words: wheat, GWAS, biomass, nitrogen efficiency

Table 1

Nutrient solution ingredients for wheat seedling growth in control treatment"

大量元素 Macronutrients 浓度 Concentration (mmol·L-1) 微量元素 Trace elements 浓度 Concentration (μmol·L-1)
KH2PO4 0.2 H3BO3 1.0
MgSO4·7H2O 0.5 (NH4)6Mo7O24·4H2O 0.1
KCl 1.8 CuSO4·5H2O 0.5
CaCl2 1.5 ZnSO4·7H2O 1.0
(NH4)2SO4·H2O 1.0 MnSO4·H2O 1.0
Ca(NO3)2·4H2O 1.0 Fe·EDTA 100.0

Table 2

Statistical parameters and heritability between traits related to biomass and nitrogen efficiency at seedling"

CV (%)
hB2 (%)
CV (%)
hB2 (%)
SDW (mg)
T1E1 107.95cd 21.40 94.95 地上部氮累积量
SNA (mg/plant)
T1E1 5.00d 12.77 93.53
T2E1 104.08d 23.99 T2E1 5.98c 6.93
T3E1 124.71b 23.51 T3E1 7.64b 10.36
T1E2 112.33c 19.16 T1E2 4.32e 8.64
T2E2 129.49b 22.28 T2E2 7.79b 10.23
T3E2 148.77a 22.62 T3E2 9.68a 4.76
RDW (mg)
T1E1 27.80c 35.87 92.76 根系氮累积量
T1E1 0.99c 22.54 93.49
T2E1 19.50e 21.49 T2E1 0.77d 24.18
T3E1 22.40d 22.99 T3E1 0.98c 24.21
T1E2 50.10a 27.03 T1E2 1.14b 19.78
T2E2 27.60c 22.30 T2E2 1.00c 23.44
T3E2 32.20b 22.89 T3E2 1.27a 23.85
TDW (mg)
T1E1 136.06d 21.00 95.37 植株总氮累积量
TNA (mg/plant)
T1E1 5.97d 26.93 94.31
T2E1 123.08e 21.99 T2E1 6.75c 24.20
T3E1 147.10c 22.81 T3E1 8.62b 25.48
T1E2 162.52b 20.53 T1E2 5.46d 21.53
T2E2 157.18b 21.77 T2E2 8.79b 25.94
T3E2 180.66a 22.03 T3E2 10.95a 23.66
T1E1 0.27b 32.68 89.72 氮累积量根冠比
T1E1 0.20b 37.13 84.25
T2E1 0.19d 16.80 T2E1 0.13c 23.66
T3E1 0.18d 17.48 T3E1 0.13c 26.83
T1E2 0.44a 16.12 T1E2 0.27a 28.16
T2E2 0.22c 13.16 T2E2 0.13c 26.20
T3E2 0.22c 14.00 T3E2 0.13c 27.63
SNC (g·kg-1)
T1E1 46.31d 6.42 86.39 地上部氮利用效率
SNUE (g·g-1kg-1)
T1E1 2.35bc 26.93 94.79
T2E1 57.55c 3.86 T2E1 1.82e 24.20
T3E1 61.21b 3.85 T3E1 2.04d 25.48
T1E2 38.66e 10.41 T1E2 3.00a 21.53
T2E2 59.79b 4.75 T2E2 2.18cd 25.94
T3E2 64.96a 4.47 T3E2 2.29b 23.66
RNC (g·kg-1)
T1E1 35.32c 8.21 85.71 根系氮利用效率
RNUE (g·g-1kg-1)
T1E1 0.80b 27.23 89.44
T2E1 40.48b 8.09 T2E1 0.47c 22.32
T3E1 43.74a 12.5 T3E1 0.51c 18.75
T1E2 22.64d 7.25 T1E2 2.26a 19.18
T2E2 35.51c 10.1 T2E2 0.78b 16.92
T3E2 39.44b 9.37 T3E2 0.81b 17.52
TNC (g·kg-1)
T1E1 44.07d 5.26 23.68 植株总氮利用效率
TNUE (g·g-1kg-1)
T1E1 3.09b 22.66 41.34
T2E1 54.87c 6.12 T2E1 2.25e 24.62
T3E1 58.56b 4.25 T3E1 2.51d 23.62
T1E2 33.75e 5.10 T1E2 4.92a 22.15
T2E2 55.50c 11.20 T2E2 2.84c 21.40
T3E2 60.44a 5.26 T3E2 2.99b 22.11

Fig. 1

Correlation coefficients (r) between traits related to biomass and nitrogen efficiency at seedling SDW: Shoot dry weight; TDW: Total dry weight of plant; RSDW: Root/shoot ratio of biomass; SNC: Shoot nitrogen concentration; RNC: Root nitrogen concentration; TNC: Total nitrogen concentration of plant; SNA: Shoot nitrogen accumulation; RNA: Root nitrogen accumulation; TNA: Total nitrogen accumulation of plant; RSNC: Root/shoot ratio of nitrogen accumulation; SNUE: Shoot nitrogen use efficiency; RNUE: Root nitrogen use efficiency; TNUE: Total nitrogen use efficiency of plant. The same as below"

Fig. 2

Population structure analysis of 134 cultivars based on unlinked SNP markers a: Graphical relationship between K and ΔK for wheat accessions; b: Neighbor-joining tree of 134 wheat accessions; c: Population structure of wheat accessions; The two subgroups identified from the tree are in different colors"

Table 3

SNPs associated with stable sites in multiple environments for traits related to biomass and nitrogen efficiency (P≤0.001)"

P 贡献率
RNUE T1E1, T3AV, T3E2 RAC875_c29540_391 1A 8290703 9.95E-04 1.39E-05 11.05—18.34
根系干重RDW T2E1, T3AV, T3E2 BobWhite_c9881_1312 1B 10256166 3.58E-04 3.49E-04 10.09—10.13
根系氮利用效率RNUE T2AV, T2E1, T3E1 BobWhite_c9881_1312 1B 10256166 7.45E-04 3.75E-05 9.04—13.69
地上部氮含量SNC T1E1, T3AV, T3E2 GENE-0427_442 1B 5688119 5.79E-04 8.62E-05 9.35—12.35
植株总干重TDW T1E1, T3AV, T3E2 GENE-0427_442 1B 5688119 6.54E-04 1.88E-04 9.17—11.11
植株总氮含量TNC T1E1, T3AV, T3E2 GENE-0427_442 1B 5688119 6.25E-04 1.08E-04 9.23—11.98
地上部氮含量SNC T2AV, T2E1, T1E2 wsnp_RFL_Contig3060_2967139 2A 9928033 8.05E-04 1.87E-04 11.41—13.91
植株总氮含量TNC T2AV, T2E1, T1E2 wsnp_RFL_Contig3060_2967139 2A 9928033 2.95E-04 2.05E-04 12.57—13.74
植株总氮利用效率TNUE T2AV, T2E1, T1AV, T1E2 Kukri_c65481_121 3B 13483435 7.19E-04 2.08E-04 9.09—11.40
根系氮利用效率RNUE T1AV, T1E1, T3AV, T3E2 tplb0025f09_1052 4B 1591267 7.25E-04 1.32E-09 11.49—36.09
地上部干重SDW T2E2, T1AV, T1E1 wsnp_Ku_c1765_3452586 6A 14086572 6.09E-04 1.39E-04 9.07—11.58
生物量根冠比RSDW T2AV, T2E2, T3E2 BS00022498_51 7B 6251008 5.32E-04 3.25E-04 12.01—12.85

Table 4

The sites which simultaneously located six seedling traits"

标记和染色体 Marker and Chr. 性状 Trait 分析环境 Analysis environment 贡献率 R2 (%)
地上部干重SDW T1E1 12.63
植株总干重TDW T1E1 11.31
地上部氮含量SNC T1E1 11.73
植株总氮含量TNC T1E1 11.76
地上部氮利用效率SNUE T1E1 12.42
植株总氮利用效率TNUE T1E1 11.80
地上部干重SDW T1E1, T3E2 8.93—11.37
植株总干重TDW T1E1 8.60
地上部氮含量SNC T1E1 9.80
植株总氮含量TNC T1E1 8.87
地上部氮利用效率SNUE T1E1, T3E2 10.11—10.75
植株总氮利用效率TNUE T3E2 9.01
地上部干重SDW T1E1, T3E2 10.86—11.65
植株总干重TDW T1E1, T3AV, T3E2 9.17—11.11
地上部氮含量SNC T1E1, T3AV, T3E2 9.35—12.35
植株总氮含量TNC T1E1, T3AV, T3E2 9.23—11.98
地上部氮利用效率SNUE T3E2 10.44
植株总氮利用效率TNUE T3AV, T3E2 9.65—11.33
地上部干重SDW T1E1, T3E2 9.49—11.83
植株总干重TDW T1E1, T3E2 8.82—8.97
地上部氮含量SNC T1E1, T3E2 8.92—9.96
植株总氮含量TNC T1E1, T3E2 8.72—9.30
地上部氮利用效率SNUE T1E1, T3E2 10.82—11.02
植株总氮利用效率TNUE T1E1, T3E2 9.19—9.81
地上部干重SDW T2AV, T2E1 13.39—13.77
植株总干重TDW T2AV, T2E1 12.85—13.57
地上部氮含量SNC T2AV, T2E1, T1E2 13.25—13.91
植株总氮含量TNC T2AV, T2E1, T1E2 13.33—13.74
地上部氮利用效率SNUE T2AV, T2E1 12.99—13.69
植株总氮利用效率TNUE T2AV, T2E1 12.04—12.73

Fig. 3

Haplotype analysis of SNP markers a: Haplotype analysis of BS00065737_51, IACX16577 and GENE-0427_442; b: Haplotype analysis of snp_RFL_Contig3060_2967139. *, **, ***represent significant at the 0.05, 0.01, 0.001 probability levels, respectively"

Table 5

Candidate gene prediction"

Position (Mb)
Gene annotation or coding protein
1B TraesCS1B02G058300 183.39 BS00065737_51 无性的MADS盒子转录因子
Agamous MADS-box transcription factor
2A TraesCS2A02G122000 332.13 wsnp_RFL_Contig3060_2967139 与膜相关的30 kD蛋白
Membrane-associated 30 kD protein
4B TraesCS4B02G007100 46.43 tplb0025f09_1052 含R3h结构域的蛋白质
R3h domain containing protein
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