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

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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>值
-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值
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
[1]
RAY D K, MUELLER N D, WEST P C, FOLEY J A. Yield trends are insufficient to double global crop production by 2050. PLoS ONE, 2013, 8(6): e66428.
[2]
SHARMA I, TYAGI B, SINGH G, VENKATESH K, GUPTA O. Enhancing wheat production-A global perspective. Indian Journal of Agricultural Sciences, 2015, 85(1): 3-13.
[3]
郭海宇. 植物根系图像的特征分析方法研究与实现. 电子科技大学计算机软件与理论, 2013.
GUO H Y. Research and implementation of feature analysis method of plant root images. Computer Software and Theory of University of Electronic Science and Technology, 2013.(in Chinese)
[4]
CHEN X X, DING Q S, BŁASZKIEWICZ Z, SUN J A, SUN Q, HE R Y, LI Y N. Phenotyping for the dynamics of field wheat root system architecture. Scientific Reports, 2017, 7: 37649.

doi: 10.1038/srep37649 pmid: 28079107
[5]
ATKINSON J A, POUND M P, BENNETT M J, WELLS D M. Uncovering the hidden half of plants using new advances in root phenotyping. Current Opinion in Biotechnology, 2019, 55: 1-8.

doi: S0958-1669(18)30052-1 pmid: 30031961
[6]
LI X K, GUO Z L, LV Y, CEN X, DING X P, WU H, LI X H, HUANG J P, XIONG L Z. Genetic control of the root system in rice under normal and drought stress conditions by genome-wide association study. PLoS Genetics, 2017, 13(7): e1006889.
[7]
MACCAFERRI M, EL-FEKI W, NAZEMI G, SALVI S, CANÈ M A, COLALONGO M C, STEFANELLI S, TUBEROSA R. Prioritizing quantitative trait loci for root system architecture in tetraploid wheat. Journal of Experimental Botany, 2016, 67(4): 1161-1178.

doi: 10.1093/jxb/erw039 pmid: 26880749
[8]
XIE Q, FERNANDO K M C, MAYES S, SPARKES D L. Identifying seedling root architectural traits associated with yield and yield components in wheat. Annals of Botany, 2017, 119(7): 1115-1129.

doi: 10.1093/aob/mcx001 pmid: 28200109
[9]
MAN J G, SHI Y, YU Z W, ZHANG Y L. Dry matter production, photosynthesis of flag leaves and water use in winter wheat are affected by supplemental irrigation in the Huang-Huai-Hai plain of China. PLoS ONE, 2015, 10(9): e0137274.
[10]
MA J H, ZHAO D Y, TANG X X, YUAN M, ZHANG D J, XU M Y, DUAN Y Z, REN H Y, ZENG Q D, WU J H, HAN D J, LI T, JIANG L N. Genome-wide association study on root system architecture and identification of candidate genes in wheat (Triticum aestivum L.). International Journal of Molecular Sciences, 2022, 23(3): 1843.

doi: 10.3390/ijms23031843
[11]
陈贵菊, 靳义荣, 刘彩云, 贾德新, 樊庆琦, 刘金栋, 刘鹏. 普通小麦根系建成相关性状的全基因组关联分析. 植物遗传资源学报, 2020, 21(4): 975-983.
CHEN G J, JIN Y R, LIU C Y, JIA D X, FAN Q Q, LIU J D, LIU P. Genome-wide association study of root system architecture related traits in common wheat (Triticum aestivum L.). Journal of Plant Genetic Resources, 2020, 21(4): 975-983.(in Chinese)
[12]
HUANG F, CHEN Z Y, DU D J, GUAN P F, CHAI L L, GUO W L, HU Z R, XIN M M, PENG H R, YAO Y Y, NI Z F. Genome-wide linkage mapping of QTL for root hair length in a Chinese common wheat population. The Crop Journal, 2020, 8(6): 1049-1056.

doi: 10.1016/j.cj.2020.02.007
[13]
KHODAEE S M M, HASHEMI M, MIRLOHI A, MAJIDI M M, SUKUMARAN S, ESMAELZAEH MOGHADDAM M, ABDOLLAHI M. Root characteristics of an elite spring wheat panel under contrasting water treatments and their genome-wide association study. Rhizosphere, 2021, 19: 100413.

doi: 10.1016/j.rhisph.2021.100413
[14]
杨青青, 唐家琪, 张昌泉, 高继平, 刘巧泉. KASP标记技术在主要农作物中的应用及展望. 生物技术通报, 2022, 38(4): 58-71.

doi: 10.13560/j.cnki.biotech.bull.1985.2021-1378
YANG Q Q, TANG J Q, ZHANG C Q, GAO J P, LIU Q Q. Application and prospect of KASP marker technology in main crops. Biotechnology Bulletin, 2022, 38(4): 58-71.(in Chinese)
[15]
DELANNAY X, MCLAREN G, RIBAUT J M. Fostering molecular breeding in developing countries. Molecular Breeding, 2012, 29(4): 857-873.

doi: 10.1007/s11032-011-9611-9
[16]
KUMAR S, BANKS T W, CLOUTIER S. SNP discovery through next-generation sequencing and its applications. International Journal of Plant Genomics, 2012, 2012: 831460.
[17]
QURESHI N, BARIANA H S, ZHANG P, MCINTOSH R, BANSAL U K, WONG D, HAYDEN M J, DUBCOVSKY J, SHANKAR M. Genetic relationship of stripe rust resistance genes Yr34 and Yr48 in wheat and identification of linked KASP markers. Plant Disease, 2018, 102(2): 413-420.

doi: 10.1094/PDIS-08-17-1144-RE
[18]
FANG T L, LEI L, LI G Q, POWERS C, HUNGER R M, CARVER B F, YAN L L. Development and deployment of KASP markers for multiple alleles of Lr34 in wheat. Theoretical and Applied Genetics, 2020, 133(7): 2183-2195.

doi: 10.1007/s00122-020-03589-x
[19]
REHMAN S U, ALI SHER M, SADDIQUE M A B, ALI Z, KHAN M A, MAO X G, IRSHAD A, SAJJAD M, IKRAM R M, NAEEM M, JING R L. Development and exploitation of KASP assays for genes underpinning drought tolerance among wheat cultivars from Pakistan. Frontiers in Genetics, 2021, 12: 684702.

doi: 10.3389/fgene.2021.684702
[20]
王志伟, 乔祥梅, 王志龙, 杨金华, 程加省, 程耿, 于亚雄. 云南小麦品种(系)抗逆性相关基因的KASP标记检测. 西南农业学报, 2020, 33(8): 1601-1607.
WANG Z W, QIAO X M, WANG Z L, YANG J H, CHENG J S, CHENG G, YU Y X. Identification of genes associated with stress resistance in Yunnan wheat cultivars (lines) by KASP assays. Southwest China Journal of Agricultural Sciences, 2020, 33(8): 1601-1607.(in Chinese)
[21]
BRADBURY P J, ZHANG Z W, KROON D E, CASSTEVENS T M, RAMDOSS Y, BUCKLER E S. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 2007, 23(19): 2633-2635.

doi: 10.1093/bioinformatics/btm308 pmid: 17586829
[22]
YIN L L, ZHANG H H, TANG Z S, XU J Y, YIN D, ZHANG Z W, YUAN X H, ZHU M J, ZHAO S H, LI X Y, LIU X L. rMVP: A memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. Genomics, Proteomics & Bioinformatics, 2021, 19(4): 619-628.
[23]
LIU K J, MUSE S V. PowerMarker: An integrated analysis environment for genetic marker analysis. Bioinformatics, 2005, 21(9): 2128-2129.

doi: 10.1093/bioinformatics/bti282 pmid: 15705655
[24]
ALEXANDER D H, NOVEMBRE J, LANGE K. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 2009, 19(9): 1655-1664.

doi: 10.1101/gr.094052.109 pmid: 19648217
[25]
ZHANG C, DONG S S, XU J Y, HE W M, YANG T L. PopLDdecay: A fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics, 2019, 35(10): 1786-1788.

doi: 10.1093/bioinformatics/bty875 pmid: 30321304
[26]
YU S Z, WU J H, WANG M, SHI W M, XIA G M, JIA J Z, KANG Z S, HAN D J. Haplotype variations in QTL for salt tolerance in Chinese wheat accessions identified by marker-based and pedigree- based kinship analyses. The Crop Journal, 2020, 8(6): 1011-1024.

doi: 10.1016/j.cj.2020.03.007
[27]
CHEN C J, CHEN H, ZHANG Y, THOMAS H R, FRANK M H, HE Y H, XIA R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 2020, 13(8): 1194-1202.

doi: S1674-2052(20)30187-8 pmid: 32585190
[28]
HAO C Y, WANG L F, GE H M, DONG Y C, ZHANG X Y. Genetic diversity and linkage disequilibrium in Chinese bread wheat (Triticum aestivum L.) revealed by SSR markers. PLoS ONE, 2011, 6(2): e17279.

doi: 10.1371/journal.pone.0017279
[29]
PFLUGFELDER D, KOCHS J, KOLLER R, JAHNKE S, MOHL C, PARIYAR S, FASSBENDER H, NAGEL K A, WATT M, VAN DUSSCHOTEN D. The root system architecture of wheat establishing in soil is associated with varying elongation rates of seminal roots: Quantification using 4D magnetic resonance imaging. Journal of Experimental Botany, 2022, 73(7): 2050-2060.

doi: 10.1093/jxb/erab551
[30]
FAN Y, MIGUEZ-MACHO G, JOBBÁGY E G, JACKSON R B, OTERO-CASAL C. Hydrologic regulation of plant rooting depth. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(40): 10572-10577.
[31]
MA S C, XU B C, LI F M, LIU W Z, HUANG Z B. Effects of root pruning on competitive ability and water use efficiency in winter wheat. Field Crops Research, 2008, 105(1/2): 56-63.

doi: 10.1016/j.fcr.2007.07.005
[32]
陈德扬. 植物营养元素功能及缺乏和过剩症状(一). 农家之友, 2000(10): 13.
CHEN D Y. Function of plant nutrient elements and symptoms deficiency and excess(Ⅰ). Farmer's Home, 2000(10): 13.(in Chinese)
[33]
王博华, 任毅, 时晓磊, 王继庆, 谢磊, 加娜尔·拜合提, 耿洪伟. 干旱胁迫下小麦苗期根系性状的全基因组关联分析. 植物遗传资源学报, 2022, 23(4): 1111-1123.
WANG B H, REN Y, SHI X L, WANG J Q, XIE L, JIANAER B H T, GENG H W. Genome-wide association analysis of seedling root traits in wheat under drought stress. Journal of Plant Genetic Resources, 2022, 23(4): 1111-1123.(in Chinese)
[34]
XU F D, CHEN S L, YANG X W, ZHOU S M, CHEN X, LI J, ZHAN K H, HE D X. Genome-wide association study on seminal and nodal roots of wheat under different growth environments. Frontiers in Plant Science, 2021, 11: 602399.

doi: 10.3389/fpls.2020.602399
[35]
LIU W B, NI J, SHAH F A, YE K Q, HU H, WANG Q J, WANG D D, YAO Y Y, HUANG S W, HOU J Y, LIU C H, WU L F. Genome-wide identification, characterization and expression pattern analysis of APYRASE family members in response to abiotic and biotic stresses in wheat. PeerJ, 2019, 7: e7622.

doi: 10.7717/peerj.7622
[36]
ABBADI A, BRUMMEL M, SCHÜTT B S, SLABAUGH M B, SCHUCH R, SPENER F. Reaction mechanism of recombinant 3-oxoacyl-(acyl-carrier-protein) synthase III from Cuphea wrightii embryo, a fatty acid synthase type II condensing enzyme. The Biochemical Journal, 2000, 345(Pt1): 153-160.

doi: 10.1042/bj3450153
[37]
DING W N, LIN L, ZHANG B T, XIANG X B, WU J, PAN Z C, ZHU S H. OsKASI, a β-ketoacyl-[acyl carrier protein] synthase I, is involved in root development in rice (Oryza sativa L.). Planta, 2015, 242(1): 203-213.

doi: 10.1007/s00425-015-2296-2
[38]
鲍永美, 王州飞, 张红生. 植物SNARE蛋白的结构与功能. 植物学通报, 2005, 22(6): 715-722.
BAO Y M, WANG Z F, ZHANG H S. Structure and function of SNAREs in plant. Chinese Bulletin of Botany, 2005, 22(6): 715-722.(in Chinese)
[39]
张孝廉, 张吉顺, 雷波, 余婧, 赵德刚. 植物MLO蛋白研究进展. 植物生理学报, 2018, 54(7): 1159-1171.
ZHANG X L, ZHANG J S, LEI B, YU J, ZHAO D G. Research progress of MLO proteins in plants. Plant Physiology Journal, 2018, 54(7): 1159-1171.(in Chinese)
[40]
LI Z, LIU D, XIA Y, LI Z L, JING D D, DU J J, NIU N, MA S C, WANG J W, SONG Y L, YANG Z Q, ZHANG G S. Identification of the WUSCHEL-related homeobox (WOX) gene family, and interaction and functional analysis of TaWOX9 and TaWUS in wheat. International Journal of Molecular Sciences, 2020, 21(5): 1581.

doi: 10.3390/ijms21051581
[41]
ZHAO Y, HU Y F, DAI M Q, HUANG L M, ZHOU D X. The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. The Plant Cell, 2009, 21(3): 736-748.

doi: 10.1105/tpc.108.061655
[42]
刘文博. 小麦APYRASE家族成员鉴定及功能研究[D]. 合肥: 中国科学技术大学, 2019.
LIU W B. Identification and characterization of wheat APYRASE gene family members[D]. Hefei: University of Science and Technology of China, 2019.(in Chinese)
[43]
YUO T, TOYOTA M, ICHII M, TAKETA S. Molecular cloning of a root hairless gene rth1 in rice. Breeding Science, 2009, 59(1): 13-20.

doi: 10.1270/jsbbs.59.13
[44]
ZAREPOUR M, SIMON K, WILCH M, NIELÄNDER U, KOSHIBA T, SEO M, LINDEL T, BITTNER F. Identification of superoxide production by Arabidopsis thaliana aldehyde oxidases AAO1 and AAO3. Plant Molecular Biology, 2012, 80(6): 659-671.

doi: 10.1007/s11103-012-9975-1
[45]
黄守程, 叶梅荣, 刘爱荣, 张远兵. DnaJ-like蛋白在植物胁迫应答中的作用及机制研究进展. 长江大学学报(自科版), 2015, 12(9): 57-62.
HUANG S C, YE M R, LIU A R, ZHANG Y B. Research progress on the role and mechanism of DnaJ-like protein in plant stress response. Journal of Yangtze University (Natural Science Edition), 2015, 12(9): 57-62.(in Chinese)
[46]
CHANG C C, SILVA B B I, HUANG H Y, TSAI C Y, FLORES R J D, TAYO L L, TYAN Y C, TSAI M A, CATULIN G E M, CHUANG K P, YANG J L. Development and validation of KASP assays for the genotyping of racing performance-associated single nucleotide polymorphisms in pigeons. Genes, 2021, 12(9): 1383.

doi: 10.3390/genes12091383
[47]
AYALEW H, TSANG P W, CHU C G, WANG J Z, LIU S Y, CHEN C F, MA X F. Comparison of TaqMan, KASP and rhAmp SNP genotyping platforms in hexaploid wheat. PLoS ONE, 2019, 14(5): e0217222.
[48]
LANDOULSI Z, BENROMDHAN S, BEN DJEBARA M, DAMAK M, DALLALI H, KEFI R, ABDELHAK S, GARGOURI-BERRECHID A, MHIRI C, GOUIDER R. Using KASP technique to screen LRRK2 G2019S mutation in a large Tunisian cohort. BMC Medical Genetics, 2017, 18(1): 70.

doi: 10.1186/s12881-017-0432-5
[49]
HIREMATH P J, KUMAR A, PENMETSA R V, FARMER A, SCHLUETER J A, CHAMARTHI S K, WHALEY A M, CARRASQUILLA-GARCIA N, GAUR P M, UPADHYAYA H D, KAVI KISHOR P B, SHAH T M, COOK D R, VARSHNEY R K. Large-scale development of cost-effective SNP marker assays for diversity assessment and genetic mapping in chickpea and comparative mapping in legumes. Plant Biotechnology Journal, 2012, 10(6): 716-732.

doi: 10.1111/j.1467-7652.2012.00710.x pmid: 22703242
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