Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (13): 2509-2524.doi: 10.3864/j.issn.0578-1752.2024.13.002

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

Identification of Resistant Germplasms and Mining of Candidate Genes Associated with Resistance to Stalk Rot Caused by Synergistic Infection with Fusarium spp. in Maize

GUI CuiLin(), MA Liang(), WANG YinYing, XIE FuGui, ZHAO CaiHong, WANG WenMiao, LI Xin, WANG Qing(), GAO XiQuan()   

  1. College of Agriculture, Nanjing Agricultural University/State Key Laboratory for Crop Genetics & Germplasm Enhancement and Utilization/Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing 210095
  • Received:2023-07-11 Accepted:2023-11-10 Online:2024-07-09 Published:2024-07-09
  • Contact: WANG Qing, GAO XiQuan

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Abstract:

【Objective】 Maize stalk rot is one of the common and most devastating diseases in major maize production areas in China. Under natural conditions, maize stalk rot is mostly caused by the synergistic infection of various pathogens. The purpose of this study was to screen elite maize germplasms resistant to the synergistic infection with F. graminearum and F. verticillioides. Meanwhile, QTN associated with resistance to the infection by synergistic infection of two Fusarium species and the candidate resistance genes were identified, which will provide gene resources and theoretical reference for molecular breeding of maize variety resistant to synergistic infection of different pathogens.【Method】 Using a maize natural population as experimental materials, the maize stalk rot phenotypes were investigated upon simultaneous infection with F. graminearum and F. verticillioides. Furthermore, GWAS analysis was conducted to identify significant resistance SNP and to predict candidate genes for stalk rot resistance.【Result】 Through the phenotypic analysis of stalk rot caused by synergistic infection under both field and laboratory conditions, it was found that inbred lines from different sources and subgroups showed significant phenotypic variation. More specifically, the field assay results showed that the inbred lines collected from China were more resistant and that from USA were more susceptible to synergistic infection. Moreover, the inbred lines of tropical and subtropical subgroup were more resistant, whereas the inbred lines of Mixed subgroup more susceptible. The seedling assay results under laboratory condition showed that the lines collected from USA were more resistant, whereas that from CIMMYT were more susceptible. The lines of SS subgroup were more resistant, and that of Mixed subgroup were more susceptible. By integrating field and laboratory phenotypic data, 29 and 16 lines with higher levels of resistance to synergistic infection were screened out respectively, and 6 resistant lines were identified under both conditions. Moreover, based on the field phenotype GWAS, 18 QTNs associated with the resistance were identified, and 93 candidate genes associated with stalk rot resistance to synergistic infection were mined. Among these candidate genes, four genes showed haplotype variation, whose expression levels were up-regulated in disease-resistant lines.【Conclusion】 Using the natural population of maize with great diversity in genetic background, 6 resistant lines to the synergistic infection with Fusarium spp. were identified under two conditions, which can be used as potential germplasm resources for maize stalk rot resistance in the future. Four candidate genes that might be involved in the resistance to synergistic infection were identified by GWAS, which will provide genetic resources for the breeding maize varieties with enhanced resistance to stalk rot caused by F. graminearum and F. verticillioides.

Key words: maize stalk rot, Fusarium graminearum, Fusarium verticillioides, synergistic infection, genome wide association study, resistance genes

Fig. 1

Disease index for phenotypes of maize stalk rot caused by synergistic infection of Fusarium spp. A: Disease index in the laboratory; B: Disease index in the field"

Table 1

Classification standard for maize stalk rot"

病级指数
Disease index		 室内
In the laboratory		 田间
In the field		 抗性评价
Resistance evaluation
1 茎秆未见明显菌丝和明显色泽变化
No obvious hyphae and color change were observed on the stem		 发病面积占接种茎节总面积0%—10%
The lesion area accounts for 0%-10% of the total area of inoculated stems		 高抗
Highly resistant (HR)
2 接种部位出现稀疏菌丝，接种部位表面出现褶皱
The hyphae were sparse and the surface of inoculation site was wrinkled		 发病面积占接种茎节总面积10%—20%
The lesion area accounts for 10%-20% of the total area of inoculated stems		 抗
Resistant (R)
3 有明显菌丝，接种部位颜色加深，出现腐烂变软，但茎秆仍可直立
There are obvious hyphae, the color of the inoculation site is deepened, and it decays and softens, but the stem can still stand upright		 发病面积占接种茎节总面积20%—40%
The lesion area accounts for 20%-40% of the total area of inoculated stems		 中抗
Moderately resistant (MR)
4 菌丝扩展，接种部位腐烂变软出现明显水渍状，茎秆不能直立
The hyphae expanded, the inoculation site rotted and softened, and obvious water soak appeared, and the stems could not stand upright		 发病面积占接种茎节总面积40%—60%
The lesion area accounts for 40%-60% of the total area of inoculated stems.		 感
Susceptible (S)
5 菌丝向上向下密集扩展，腐烂部位深褐色，茎秆倒伏
The hyphae spread densely upward and downward, the rotten parts were dark brown, and the stems were lodging		 发病面积占接种茎节总面积60%—100%
The lesion area accounts for 60%-100% of the total area of inoculated stems		 高感
Highly susceptible (HS)

Fig. 2

Phenotypic identification of maize stalk rot caused by synergistic infection with Fusarium spp. in the field A: The distribution of disease index for different inbred lines. B: Histogram of exponential distribution for disease area and fitting curve of normal distribution for different inbred lines in the field upon synergistic infection with Fusarium spp.. C-D: The distribution of resistance in maize germplasms from different sources and subgroups in response to the synergistic infection with Fusarium spp. **: P<0.01, ***: P<0.005. The numbers in the boxplot represent the average of relative lesion area. The same as below"

Table 2

Phenotypic statistics of maize resistance to the synergistic infection of Fusarium spp."

处理
Treatment		 平均值
Mean		 标准差
SD		 最小值
Min		 最大值
Max		 偏度
Skew		 峰度
Kurt		 遗传率
H2		 相关性
Correlation
重复1 Repeat 1 28.61 15.75 5.00 77.50 0.80 0.34 0.45**
重复2 Repeat 2 27.33 16.21 5.00 90.00 0.94 0.88
最佳线性无偏预测BLUP 28.00 8.35 14.49 56.04 0.75 0.31 0.62

Table 3

Statistics of resistance to stalk rot caused by synergistic infection of Fusarium spp."

数量和百分比 Number and percentage 高抗 HR 抗 R 中抗 MR 感 S 高感 HS
重复1数量No. of repeat 1 22 46 97 38 10
重复1百分比Percentage of repeat 1 (%) 10.33 21.60 45.54 17.84 6.49
重复2数量No. of repeat 2 21 63 81 37 8
重复2百分比Percentage of repeat 2 (%) 10.00 30.00 38.57 17.62 3.81

Fig. 3

Phenotypic identification of maize resistance to the synergistic infection of Fusarium spp. in the laboratory A: Distribution of disease index. B: Histogram of exponential distribution of disease index and fitting curve of normal distribution. C-D: Indicate the disease resistance statistics of maize germplasms from different sources at 3 dpi and 5 dpi, respectively. E-F: Represent the disease resistance statistics of different maize germplasms at 3 dpi and 5 dpi, respectively. *: P<0.05, ****: P<0.001. The same as below"

Table 4

Phenotypic statistics of resistance to maize stalk rot caused by synergistic infection with F. graminearum and F. verticillioides in the laboratory"

处理
Treatment		 平均值
Mean		 标准差
SD		 最小值
Min		 最大值
Max		 偏度
Skew		 峰度
Kurt		 遗传率
H2
重复1 Repeat 1 2.95 0.78 1.00 4.33 -0.60 -0.34
重复2 Repeat2 3.25 0.67 1.45 4.67 -0.57 -0.05
重复3 Repeat3 3.37 0.56 1.52 4.31 -0.91 0.83
最佳线性无偏预测BLUP 3.19 0.20 2.69 3.61 -0.37 -0.40 0.43

Table 5

Statistics of resistance to maize stalk rot caused by synergistic infection with F. graminearum and F. verticillioides in the laboratory"

数量和百分比 Number and percentage 高抗HR 抗R 中抗MR 感S 高感HS
重复1数量No. of repeat 1 2 27 64 87 8
重复1百分比Percentage of repeat 1 (%) 1.06 14.36 34.04 46.28 4.26
重复2数量No. of repeat 2 0 10 47 109 22
重复2百分比Percentage of repeat 2 (%) 0.00 5.32 25.00 57.98 11.70
重复3数量No. of repeat 3 0 6 40 126 16
重复3百分比Percentage of repeat 3 (%) 0.00 3.19 21.28 67.02 8.51

Fig. 4

Population structure of maize natural population materials"

Fig. 5

GWAS analysis of resistance to maize stalk rot caused by synergisitic infection with Fusarium spp. in the field A: Repeat 1 Manhattan plot; B: Repeat 1 QQ plot; C: Repeat 2 Manhattan plot; D: Repeat 2 QQ plot; E: BLUP Manhattan plot; F: BLUP QQ plot"

Table 6

Information of resistance-loci and candidate genes for stalk rot caused by synergistic infection in the field"

标记
Marker		 Bin <BOLD>P</BOLD>值
<BOLD>P</BOLD> value		 位置
Position		 基因
Gene		 基因位置开始-结束
Gene start-end		 注释
Annotation
Chr.1.S_37202321 1.03 2.67E-06 3′UTR GRMZM2G408305 37202146-37215962 ARM重复超家族蛋白
ARM repeat superfamily protein
Chr.1.S_35134046 1.03 1.95E-06 外显子Exonic GRMZM2G136513 35132532-35136898 抗病蛋白RPS2
Disease resistance protein RPS2
Chr.1.S_35136660 1.03 8.73E-06 外显子Exonic GRMZM2G136513 35132532-35136898 抗病蛋白RPS2
Disease resistance protein RPS2
Chr.1.S_230178588 1.08 5.64E-06 外显子Exonic GRMZM5G816209 230176955-30178674
Chr.3.S_6095672 3.02 8.22E-06 3′UTR GRMZM2G468479 6088603-6096563 假定的MYB DNA结合域超家族蛋白
Putative MYB DNA-binding domain superfamily protein
Chr.3.S_198540836 3.07 6.03E-06 内含子Intronic AC209455.3_FG009 198539184-198543636
Chr.4.S_226677337 4.09 6.23E-07 上游Upstream GRMZM2G534064 226678246-226678352
Chr.5.S_110733295 5.04 8.23E-06 基因间区Intergenic GRMZM2G052821
GRMZM5G810549		 110462595-110515712
111031219-111031605		 (6-4) DNA 光解酶
(6-4) DNA photolyase
Chr.6.S_16552209 6.01 3.09E-06 基因间区Intergenic GRMZM2G357280
GRMZM2G519047		 16469580-16476098
16592323-16592418‬
Chr.6.S_166899228 6.08 7.19E-07 3′UTR GRMZM2G158998 166897023-166899522 Phox相关结构域
Phox-associated domain
Chr.7.S_13209638 7.01 5.63E-06 3′UTR GRMZM2G150091 13208679-13209853 硫氧还蛋白
Thioredoxin
Chr.7.S_133361933 7.03 4.56E-06 外显子Exonic GRMZM2G103902 133359936-133367491 EMSY-LIKE 4蛋白
Protein EMSY-LIKE 4
Chr.7.S_133367147 7.03 4.56E-06 外显子Exonic GRMZM2G103902 133359936-133367491 EMSY-LIKE 4蛋白
Protein EMSY-LIKE 4
Chr.7.S_133367336 7.03 4.56E-06 外显子Exonic GRMZM2G103902 133359936-133367491 EMSY-LIKE 4蛋白
Protein EMSY-LIKE 4
Chr.7.S_145977576 7.03 3.70E-06 外显子Exonic GRMZM2G146240 145968303-145978114
Chr.7.S_173375841 7.05 5.90E-06 基因间区Intergenic GRMZM2G349655
GRMZM5G867912		 173327041-173328625
173447389-173451235		 钙结合蛋白CAST
Calcium-binding protein CAST
Chr.10.S_10615482 10.02 9.26E-07 外显子Exonic GRMZM2G103662 10613555-10616571 天冬氨酰蛋白酶APCB1
Aspartyl protease APCB1
Chr.10.S_28599638 10.03 7.00E-06 基因间区Intergenic GRMZM2G052606
GRMZM2G121031		 28600793-28603531
28588781-28589630		 次生壁MYB46转录因子Secondary wall MYB46 transcription factor

Fig. 6

Visualization of SNP LD block A: Visualization of SNP LD block in GRMZM136513; B: Visualization of SNP LD block in GRMZM2G103902"

Fig. 7

Haplotype analysis of candidate genes for significant SNP in the field"

Fig. 8

Gene expression of candidate genes with haplotype difference Different letters mean significant difference between samples (P<0.05)"

[1]
GAIKPA D S, MIEDANER T. Genomics-assisted breeding for ear rot resistances and reduced mycotoxin contamination in maize: Methods, advances and prospects. Theoretical and Applied Genetics, 2019, 132(10): 2721-2739.

doi: 10.1007/s00122-019-03412-2 pmid: 31440772
[2]
郭成, 王宝宝, 杨洋, 王春明, 周天旺, 李敏权, 段灿星. 玉米茎腐病研究进展. 植物遗传资源学报, 2019, 20(5): 1118-1128.

doi: 10.13430/j.cnki.jpgr.20181223001
GUO C, WANG B B, YANG Y, WANG C M, ZHOU T M, LI M Q, DUAN C X. Advances in studies of maize stalk rot. Journal of Plant Genetic Resources, 2019, 20(5): 1118-1128. (in Chinese)
[3]
钮笑晓, 李小波, 孙毅, 马海林, 张洁, 刘亚飞, 郝曜山, 崔贵梅. 玉米茎腐(青枯)病研究进展. 华北农学报, 2020, 35(S1): 433-440.

doi: 10.7668/hbnxb.20191448
NIU X X, LI X B, SUN Y, MA H L, ZHANG J, LIU Y F, HAO Y S, CUI G M. Research progress of maize stalk rot disease. Acta Agriculturae Boreali-Sinica, 2020, 35(S1): 433-440. (in Chinese)

doi: 10.7668/hbnxb.20191448
[4]
YU C J, SARAVANAKUMAR K, XIA H, GAO J X, FU K H, SUN J N, DOU K, CHEN J E. Occurrence and virulence of Fusarium spp. associated with stalk rot of maize in North-East China. Physiological and Molecular Plant Pathology, 2017, 98: 1-8.
[5]
JANSE VAN RENSBURG B, MC LAREN N W, SCHOEMAN A, FLETT B C. The effects of cultivar and prophylactic fungicide spray for leaf diseases on colonisation of maize ears by fumonisin producing Fusarium spp. and fumonisin synthesis in South Africa. Crop Protection, 2016, 79: 56-63.
[6]
MA Z Q, XIE Q, LI G Q, JIA H Y, ZHOU J Y, KONG Z X, LI N, YUAN Y. Germplasms, genetics and genomics for better control of disastrous wheat Fusarium head blight. Theoretical and Applied Genetics, 2020, 133(5): 1541-1568.
[7]
LI L N, QU Q, CAO Z Y, GUO Z Y, JIA H, LIU N, WANG Y H, DONG J G. The relationship analysis on corn stalk rot and ear rot according to Fusarium species and fumonisin contamination in kernels. Toxins, 2019, 11(6): 320.
[8]
段灿星, 曹言勇, 董怀玉, 夏玉生, 李红, 胡清玉, 杨知还, 王晓鸣. 玉米种质资源抗腐霉茎腐病和镰孢茎腐病精准鉴定. 中国农业科学, 2022, 55(2): 265-279. doi: 10.3864/j.issn.0578-1752.2022.02.003.
DUAN C X, CAO Y Y, DONG H Y, XIA Y S, LI H, HU Q Y, YANG Z H, WANG X M. Precise characterization of maize germplasm for resistance to Pythium stalk rot and Gibberella stalk rot. Scientia Agricultura Sinica, 2022, 55(2): 265-279. doi: 10.3864/j.issn.0578-1752.2022.02.003. (in Chinese)
[9]
渠清, 李丽娜, 刘俊, 王绍新, 曹志艳, 董金皋. 我国部分常用玉米种质资源对镰孢菌病害的抗性评价. 中国农业科学, 2019, 52(17): 2962-2971. doi: 10.3864/j.issn.0578-1752.2019.17.005.
QU Q, LI L N, LIU J, WANG S X, CAO Z Y, DONG J G. Resistance evaluation of some commonly used maize germplasm resources to Fusarium diseases in China. Scientia Agricultura Sinica, 2019, 52(17): 2962-2971. doi: 10.3864/j.issn.0578-1752.2019.17.005. (in Chinese)
[10]
邹成佳, 崔丽娜, 章振羽, 张小飞, 李荣进, 陈耕, 李晓. 玉米自交系对轮枝镰孢菌穗腐病的抗性评价. 西南农业学报, 2017, 30(6): 1346-1349.
ZOU C J, CUI L N, ZHANG Z Y, ZHANG X F, LI R J, CHEN G, LI X. Evaluation of maize inbred lines for resistance to Fusarium verticillioides ear rot. Southwest China Journal of Agricultural Sciences, 2017, 30(6): 1346-1349. (in Chinese)
[11]
TONG L X, YAN M Z, ZHU M, YANG J, LI Y P, XU M L. ZmCCT haplotype H5 improves yield, stalk-rot resistance, and drought tolerance in maize. Frontiers in Plant Science, 2022, 13: 984527.
[12]
WANG C, YANG Q, WANG W X, LI Y P, GUO Y L, ZHANG D F, MA X N, SONG W, ZHAO J R, XU M L. A transposon-directed epigenetic change in ZmCCT underlies quantitative resistance to Gibberella stalk rot in maize. The New Phytologist, 2017, 215(4): 1503-1515.
[13]
YE J R, ZHONG T, ZHANG D F, MA C Y, WANG L N, YAO L S, ZHANG Q Q, ZHU M, XU M L. The auxin-regulated protein ZmAuxRP1 coordinates the balance between root growth and stalk rot disease resistance in maize. Molecular Plant, 2019, 12(3): 360-373.

doi: S1674-2052(18)30310-1 pmid: 30853061
[14]
ZHANG D F, LIU Y J, GUO Y L, YANG Q, YE J R, CHEN S J, XU M L. Fine-mapping of qRfg2, a QTL for resistance to Gibberella stalk rot in maize. Theoretical and Applied Genetics, 2012, 124(3): 585-596.
[15]
MA C Y, MA X N, YAO L S, LIU Y J, DU F L, YANG X H, XU M L. qRfg3, a novel quantitative resistance locus against Gibberella stalk rot in maize. Theoretical and Applied Genetics, 2017, 130(8): 1723-1734.
[16]
CHEN Q, SONG J, DU W P, XU L Y, JIANG Y, ZHANG J, XIANG X L, YU G R. Identification, mapping, and molecular marker development for Rgsr8.1: A new quantitative trait locus conferring resistance to Gibberella stalk rot in maize (Zea mays L.). Frontiers in Plant Science, 2017, 8: 1355.
[17]
SUN Y L, RUAN X S, WANG Q, ZHOU Y, WANG F, MA L, WANG Z H, GAO X Q. Integrated gene co-expression analysis and metabolites profiling highlight the important role of ZmHIR3 in maize resistance to Gibberella stalk rot. Frontiers in Plant Science, 2021, 12: 664733.
[18]
ZWONITZER J C, COLES N D, KRAKOWSKY M D, ARELLANO C, HOLLAND J B, MCMULLEN M D, PRATT R C, BALINT- KURTI P J. Mapping resistance quantitative trait loci for three foliar diseases in a maize recombinant inbred line population- evidence for multiple disease resistance? Phytopathology, 2010, 100(1): 72-79.
[19]
RASHID Z, SOFI M, HARLAPUR S I, KACHAPUR R M, DAR Z A, SINGH P K, ZAIDI P H, VIVEK B S, NAIR S K. Genome-wide association studies in tropical maize germplasm reveal novel and known genomic regions for resistance to Northern corn leaf blight. Scientific Reports, 2020, 10: 21949.

doi: 10.1038/s41598-020-78928-5 pmid: 33319847
[20]
YANG Q, HE Y J, KABAHUMA M, CHAYA T, KELLY A, BORREGO E, BIAN Y, EL KASMI F, YANG L, TEIXEIRA P, KOLKMAN J, NELSON R, KOLOMIETS M, DANGL J L, WISSER R, CAPLAN J, LI X, LAUTER N, BALINT-KURTI P. A gene encoding maize caffeoyl-CoA O-methyltransferase confers quantitative resistance to multiple pathogens. Nature Genetics, 2017, 49(9): 1364-1372.

doi: 10.1038/ng.3919 pmid: 28740263
[21]
ZUO W L, CHAO Q, ZHANG N, YE J R, TAN G Q, LI B L, XING Y X, ZHANG B Q, LIU H J, FENGLER K A, ZHAO J, ZHAO X R, CHEN Y S, LAI J S, YAN J B, XU M L. A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics, 2015, 47(2): 151-157.

doi: 10.1038/ng.3170 pmid: 25531751
[22]
YANG P, SCHEUERMANN D, KESSEL B, KOLLER T, GREENWOOD J R, HURNI S, HERREN G, ZHOU S H, MARANDE W, WICKER T, KRATTINGER S G, OUZUNOVA M, KELLER B. Alleles of a wall-associated kinase gene account for three of the major northern corn leaf blight resistance loci in maize. The Plant Journal, 2021, 106(2): 526-535.

doi: 10.1111/tpj.15183 pmid: 33533097
[23]
HOLT R D, BONSALL M B. Apparent competition. Apparent competition. Annual Review of Ecology, Evolution, and Systematics, 2017, 48: 447-471.
[24]
ABDULLAH A S, MOFFAT C S, LOPEZ-RUIZ F J, GIBBERD M R, HAMBLIN J, ZERIHUN A. Host-multi-pathogen warfare: pathogen interactions in co-infected plants. Frontiers in Plant Science, 2017, 8: 1806.

doi: 10.3389/fpls.2017.01806 pmid: 29118773
[25]
SUN Y L, RUAN X S, MA L, WANG F, GAO X Q. Rapid screening and evaluation of maize seedling resistance to stalk rot caused by Fusarium spp. Bio-Protocol, 2018, 8(10): e2859.
[26]
苏爱国, 王帅帅, 段赛茹, 张如养, 邢锦丰, 杨扬, 宋伟, 赵久然. 玉米抗禾谷镰孢菌穗粒腐病种质资源鉴定. 植物遗传资源学报, 2021, 22(4): 971-978.

doi: 10.13430/j.cnki.jpgr.20210201004
SU A G, WANG S S, DUAN S R, ZHANG R Y, XING J F, YANG Y, SONG W, ZHAO J R. Identification for ear rot resistance against Fusarium graminearum in maize germplasm. Journal of Plant Genetic Resources, 2021, 22(4): 971-978. (in Chinese)
[27]
LIU H J, LUO X, NIU L Y, XIAO Y J, CHEN L, LIU J, WANG X Q, JIN M L, LI W Q, ZHANG Q H, YANG J B. Distant eQTLs and non-coding sequences play critical roles in regulating gene expression and quantitative trait variation in maize. Molecular Plant, 2017, 10(3): 414-426.

doi: S1674-2052(16)30129-0 pmid: 27381443
[28]
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
[29]
PURCELL S, NEALE B, TODD-BROWN K, THOMAS L, FERREIRA M A R, BENDER D, MALLER J, SKLAR P, DE BAKKER P I W, DALY M J, SHAM P C. PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics, 2007, 81(3): 559-575.
[30]
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
[31]
YANG J, LEE S H, GODDARD M E, VISSCHER P M. GCTA: A tool for genome-wide complex trait analysis. American Journal of Human Genetics, 2011, 88(1): 76-82.

doi: 10.1016/j.ajhg.2010.11.011 pmid: 21167468
[32]
LETUNIC I, BORK P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Research, 2019, 47(W1): W256-W259.

doi: 10.1093/nar/gkz239
[33]
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
[34]
KANG H M, SUL J H, SERVICE S K, ZAITLEN N A, KONG S Y, FREIMER N B, SABATTI C, ESKIN E. Variance component model to account for sample structure in genome-wide association studies. Nature Genetics, 2010, 42(4): 348-354.

doi: 10.1038/ng.548 pmid: 20208533
[35]
WANG K, LI M Y, HAKONARSON H. ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Research, 2010, 38(16): e164.
[36]
DONG S S, HE W M, JI J J, ZHANG C, GUO Y, YANG T L. LDBlockShow: A fast and convenient tool for visualizing linkage disequilibrium and haplotype blocks based on variant call format files. Briefings in Bioinformatics, 2021, 22(4): bbaa227.
[37]
YANG Q, YIN G M, GUO Y L, ZHANG D F, CHEN S J, XU M L. A major QTL for resistance to Gibberella stalk rot in maize. Theoretical and Applied Genetics, 2010, 121(4): 673-687.
[38]
CHEN J F, DING J Q, LI H M, LI Z M, SUN X D, LI J J, WANG R X, DAI X D, DONG H F, SONG W B, CHEN W, XIA Z L, WU J Y. Detection and verification of quantitative trait loci for resistance to Fusarium ear rot in maize. Molecular Breeding, 2012, 30(4): 1649-1656.
[39]
WEN J, SHEN Y Q, XING Y X, WANG Z Y, HAN S P, LI S J, YANG C M, HAO D Y, ZHANG Y. QTL mapping of Fusarium ear rot resistance in maize. Plant Disease, 2021, 105(3): 558-565.
[40]
DEMIRJIAN C, VAILLEAU F, BERTHOMÉ R, ROUX F. Genome- wide association studies in plant pathosystems: Success or failure? Trends in Plant Science, 2023, 28(4): 471-485.
[41]
ZHANG L, PAASCH B C, CHEN J, DAY B, HE S Y. An important role of L-fucose biosynthesis and protein fucosylation genes in Arabidopsis immunity. The New Phytologist, 2019, 222(2): 981-994.
[42]
BENT A F, KUNKEL B N, DAHLBECK D, BROWN K L, SCHMIDT R, GIRAUDAT J, LEUNG J, STASKAWICZ B J. RPS2 of Arabidopsis thaliana : A leucine-rich repeat class of plant disease resistance genes. Science, 1994, 265(5180): 1856-1860.
[43]
LI W, ZHENG X, CHENG R, ZHONG C J, ZHAO J, LIU T H, YI T Y, ZHU Z D, XU J T, MEKSEM K, DAI L Y, LIU S M. Soybean zinc finger protein03 targets two superoxide dismutase1s and confers resistance to Phytophthora sojae. Plant Physiology, 2023, 192(1): 633-647.
[44]
ZHANG J Q, XIA C J, WANG X M, DUAN C X, SUN S L, WU X F, ZHU Z D. Genetic characterization and fine mapping of the novel Phytophthora resistance gene in a Chinese soybean cultivar. Theoretical and Applied Genetics, 2013, 126(6): 1555-1561.
[45]
RUAN X S, MA L, ZHANG Y Y, WANG Q, GAO X Q. Dissection of the complex transcription and metabolism regulation networks associated with maize resistance to Ustilago maydis. Genes, 2021, 12(11): 1789.
[46]
BRASIL J N, CABRAL L M, ELOY N B, PRIMO L M F, BARROSO-NETO I L, GRANGEIRO L P, GONZALEZ N, INZÉ D, FERREIRA P C G, HEMERLY A S. AIP1 is a novel Agenet/Tudor domain protein from Arabidopsis that interacts with regulators of DNA replication, transcription and chromatin remodeling. BMC Plant Biology, 2015, 15(1): 270.
[47]
TSUCHIYA T, EULGEM T. EMSY-like genes are required for full RPP7-mediated race-specific immunity and basal defense in Arabidopsis. Molecular Plant-Microbe Interactions, 2011, 24(12): 1573-1581.
[48]
YOSHIE Y, GOTO K, TAKAI R, IWANO M, TAKAYAMA S, ISOGAI A, CHE F S. Function of the rice gp91phox homologs OsrbohA and OsrbohE genes in ROS-dependent plant immune responses. Plant Biotechnology, 2005, 22(2): 127-135.
[49]
LIU Q Q, LIU H H, GONG Y Q, TAO Y F, JIANG L, ZUO W L, YANG Q, YE J R, LAI J S, WU J Y, LÜBBERSTEDT T, XU M L. An atypical thioredoxin imparts early resistance to sugarcane mosaic virus in maize. Molecular Plant, 2017, 10(3): 483-497.

doi: S1674-2052(17)30041-2 pmid: 28216424
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