Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (18): 3642-3654.doi: 10.3864/j.issn.0578-1752.2023.18.012

• HORTICULTURE • Previous Articles     Next Articles

Genome Wide Association Study for Resistance to Citrus Brown Spot Disease

YANG ShengNan(), CHENG Li, TAN YueXia, ZHU YanSong, JIANG Dong()   

  1. Citrus Research Institute of Southwest University, Chongqing 400712
  • Received:2023-02-14 Accepted:2023-05-04 Online:2023-09-16 Published:2023-09-21
  • Contact: JIANG Dong

RichHTML

13

PDF

228

Abstract:

【Objective】The study objective was to explore candidate genes associated with resistance to Alternaria brown spot disease in citrus mandarin, so as to provide the basis for developing suitable molecular markers for further citrus resistance breeding work. 【Method】In summer and autumn of 2022, the young leaves of 136 citrus mandarin accessions were picked and inoculated with the fungus mycelium of Alternaria alternata in the laboratory. The combined results of two experiments were used to obtain the reliable results of 121 citrus mandarins responding to Alternaria brown spot. The phenotypes of 121 citrus mandarins were selected to verify the effectiveness of the CAPS marker developed in a previous study. Then, in order to obtain the candidate SNPs related to Alternaria brown spot resistance, the phenotypes of 121 citrus mandarins and corresponding SNP genotype data from GBS sequencing were analyzed with PCA, GWAS, and Fst methods, respectively. Candidate genes had been selected from the flanking region of 25 kb sequences surrounding the candidate SNPs site, and then they were screened out according to phytozome annotations. The expressions of candidate genes were analyzed after inoculating with the pathogen fungus on leave of Chengtuo hongju and Clementina (Algeria) for 24, 48, and 72 h. 【Result】Among 121 citrus mandarins, 67 varieties such as Clementine and Satsuma were resistant to Alternaria brown spot disease, whereas 54 varieties such as Hong Ju and Ponkan were susceptible. Some varieties resistance to Alternaria brown spot disease could discriminated by CAPS, but its accuracy only accounted for 76.86% in the study. GWAS analysis identified six significant SNPs highly associated with disease resistance, among which SNP1 located in Ciclev10021676 at 24 838 146 bp of chromosome 3 could be used to predicate the resistance of varieties, and their genotype showed a strong correlation with phenotype. Eight significant SNPs highly associated with disease resistance selected by Fst analysis. Finally, five genes of Ciclev10018604, Ciclev10023485, Ciclev10023486, Ciclev10024586 and Ciclev10019874 were screened out. The expression levels of these five genes in Chengtuo Hongju were up-regulated extensively after inoculating leaves with the pathogen fungus, and their expression levels reached the highest 48 hours later. 【Conclusion】Through GWAS, the SNP at 24 838 146 bp on chromosome 3 was found to be the most significant one with high resistance correlation to Alternaria brown spot disease, and the genotype at this location could be effectively used to distinguish the resistant varieties. The candidate genes responding to Alternaria brown spot disease in mandarin were discussed, i.e., Ciclev10019874, Ciclev10018604, Ciclev10023485, Ciclev10024586, and Ciclev10023486.

Key words: citrus mandarin, Alternaria brown spot, molecular marker, genome-wide association study, fixation index

Table 1

Primer of CAPS"

引物名称
Primer name		 序列
Primer sequence		 扩增长度
Length (bp)
SNP08-spare-F AGGATTGTGAGGTGACGCTT 747
SNP08-spare-R GCAACATATCCAAATGCGCC

Table 2

Primers for real-time fluorescence quantification of candidate genes"

基因名称
Gene name		 引物名称
Primer name		 序列
Primer sequence
β-Actin F CCCCATCGTTACCGTCCAG
R CGCCTTGCCAGTTGAATATCC
Ciclev10018604 F GGGAGCTTGTGGCACTGTAT
R TCCTTCACCACGCAACTTGA
Ciclev10019874 F GAATCCCTTCTCTCCGGCTG
R GTGGTGGAGTGATGAGGTGG
Ciclev10023485 F GAGTCACCTGACAAGAGAATGC
R ACTTGCAGCAACATCATCCAAG
Ciclev10024586 F GCATAGGCCTTGCCAATGTT
R CGATAATCAACGACACGGGC
Ciclev10023486 F AAACAGCATTCCAAGCGTGC
R AATCCCATCCGCATAGGTCG

Fig. 1

Example diagram of resistance to citrus brown spot disease A: Symptom of Alternaria alternata inoculated young leaves of Da Xianggan in summer; B: Symptom of Alternaria alternata inoculated young leaves of Guiping Zhushaju in summer; C: Symptom of Alternaria alternata inoculated young leaves of Da Xianggan in autumn; D: Symptom of Alternaria alternata inoculated young leaves of Guiping Zhushaju in autumn. The left three leaves of Fig. 1-A and Fig. 1-B were inoculated leaves, and the right three leaves were control leaves; The first 15 leaves in Fig. 1-C and Fig. 1-D were inoculated leaves, and the last 15 leaves were control leaves"

Fig. 2

esistance prediction results of CAPS A: CAPS results of 20 citrus mandarin; 1: 2000DNA marker; the varieties from 2 to 21 lane are as follow: Minneola Tangelo, Tangor 22-53, Yuanhong Xianggan, Clementina (Algeria), Anjiang Hongju, Jinju, Suanganzi, Wilking Mandarin, Apireno, Shagan, Clementina×Bendizao, Tsunonozomi, 1-26, Duong Mandarin, Kiyomi×Minneola, Ortanique, Calamondin, Seedless W. murcott, Seedless Zaoju, Huapi Ju. B: Pie chart of CAPS accuracy"

Fig. 3

Results of PCA, GWAS and Fst A: Principal component analysis of 121 citrus mandarins; B: Manhattan plot of GWAS for displaying SNPs related to resistance to Alternaria brown spot; C: QQ plot of GWAS for resistance to Alternaria brown spot; D: Manhattan plot of Fst for displaying SNPs related to resistance to Alternaria brown spot"

Table 3

The information of 14 SNPs from GWAS analysis and Fst analysis"

来源
Source		 编号
Code		 染色体
Chromosome		 位置
Location (bp)		 P值/Fst值
P value/ Fst value
GWAS筛选 Screening of GWAS SNP1 3 24838146 7.742227
GWAS筛选 Screening of GWAS SNP2 3 29033460 6.01147
GWAS筛选 Screening of GWAS SNP3 2 9623685 5.404526
GWAS筛选 Screening of GWAS SNP4 3 10912656 4.899702
GWAS筛选 Screening of GWAS SNP5 3 29379604 4.524974
GWAS筛选 Screening of GWAS SNP6 3 29379461 4.504927
Fst筛选 Screening of Fst SNP7 5 9384031 0.427099
Fst筛选 Screening of Fst SNP8 3 21846432 0.407686
Fst筛选 Screening of Fst SNP9 3 30824581 0.402405
Fst筛选 Screening of Fst SNP10 2 32716438 0.400017
Fst筛选 Screening of Fst SNP11 3 11889486 0.395677
Fst筛选 Screening of Fst SNP12 3 30230610 0.391282
Fst筛选 Screening of Fst SNP13 3 30132014 0.381140
Fst筛选 Screening of Fst SNP14 3 33601151 0.380600

Table 4

The information of 6 SNPs genotype from GWAS analysis"

SNP编号
SNP code		 基因型
genotype		 感病资源数量
Number of susceptible varieties		 抗病资源数量
Number of resistant varieties		 感病资源占比
The proportion of susceptible varieties (%)		 抗病资源占比
The proportion of resistant varieties (%)
SNP1 G/G 13 0 100 0
G/A 45 14 76 24
A/A 7 39 15 85
SNP2 C/C 13 0 100 0
C/T 37 11 77 23
T/T 14 42 25 75
SNP3 C/C 33 4 89 11
C/A 28 16 64 36
A/A 5 33 13 87
SNP4 G/G 13 0 100 0
G/T 36 10 78 22
T/T 16 43 27 73
SNP5 A/A 19 1 5 95
A/T 24 21 47 53
T/T 37 13 74 26
SNP6 C/C 12 0 100 0
C/T 35 11 76 24
T/T 15 42 26 74

Table 5

Functional annotation of five candidate genes"

基因
Gene		 注释
Annotation		 连锁SNP编号
Chain SNP code
Ciclev10019874 丝氨酸/苏氨酸-蛋白激酶wag1
Serine/threonine-protein kinase wag1		 SNP2
Ciclev10023485 非特异性丝氨酸/苏氨酸蛋白激酶；苏氨酸特异性蛋白激酶
Non-specific serine/threonine protein kinase; Threonine-specific protein kinase		 SNP14
Ciclev10018604 蛋白激酶结构域；富含亮氨酸重复序列N端结构域（LRRNT_2）；富含亮氨酸重复序列（LRR_8）
Protein kinase domain; Leucine rich repeat N-terminal domain (LRRNT_2); Leucine rich repeat (LRR_8)		 SNP2
Ciclev10024586 富含亮氨酸重复序列（LRR_1）；富含亮氨酸重复序列N端结构域（LRRNT_2）
Leucine Rich Repeat (LRR_1); Leucine rich repeat N-terminal domain (LRRNT_2)		 SNP14
Ciclev10023486 富含亮氨酸重复序列的蛋白
Leucine-rich repeat-containing protein		 SNP8

Fig. 4

Analysis of relative expression levels of five candidate genes *, ** and *** indicate significant difference at 0.05, 0.01 and 0.001 level, respectively. CTHJ-24, CTHJ-48 and CTHJ-72 represent Chengtuo Hongju after inoculating with Alternaria alternata 24, 48 and 72 h, respectively. XKLMD-24, XKLMD-48, and XKLMD-72 represent Clementina (Algeria) after inoculating with Alternaria alternata 24, 48 and 72 h, respectively"

[1]
GAI Y P, MA H J, CHEN Y N, LI L, CAO Y Z, WANG M S, SUN X P, JIAO C, RIELY B K, LI H Y. Chromosome-scale genome sequence of Alternaria alternata causing Alternaria brown spot of Citrus. Molecular Plant-Microbe Interactions, 2021, 34(7): 726-732.

doi: 10.1094/MPMI-10-20-0278-SC
[2]
LLORENS E, FERNÁNDEZ-CRESPO E, VICEDO B, LAPEÑA L, GARCÍA-AGUSTÍN P. Enhancement of the citrus immune system provides effective resistance against Alternaria brown spot disease. Journal of Plant Physiology, 2013, 170(2): 146-154.

doi: 10.1016/j.jplph.2012.09.018
[3]
陈昌胜, 黄峰, 程兰, 冯春刚, 黄涛江, 李红叶. 红橘褐斑病病原鉴定. 植物病理学报, 2011, 41(5): 449-455.
CHEN C S, HUANG F, CHENG L, FENG C G, HUANG T J, LI H Y. Identification of the pathogenic fungus causing brown spot on tangerine (Citrus reticulata CV. Hongjv. Acta Phytopathologica Sinica, 2011, 41(5): 449-455. (in Chinese)
[4]
张玉洁, 杨续旺, 张志信, 李红超, 田洪, 张铁. 柑橘褐斑病的病原分离和药物筛选. 北方园艺, 2010(14): 169-171.
ZHANG Y J, YANG X W, ZHANG Z X, LI H C, TIAN H, ZHANG T. Isolation of Citrus black patch pathogen and comparison of the sensitivities to eleven kind fungicides. Northern Horticulture, 2010(14): 169-171. (in Chinese)
[5]
REIS R F, DE ALMEIDA T F, STUCHI E S, DE GOES A. Susceptibility of citrus species to Alternaria alternata, the causal agent of the Alternaria brown spot. Scientia Horticulturae, 2007, 113(4): 336-342.

doi: 10.1016/j.scienta.2007.04.005
[6]
SOLEL Z, KIMCHI M. Susceptibility and resistance of Citrus genotypes to Alternaria alternata pv. citri. Journal of Phytopathology, 1997, 145(8/9): 389-391.

doi: 10.1111/jph.1997.145.issue-8-9
[7]
符雨诗, 罗君琴, 徐建国, 李红叶. 不同柑橘品种对链格孢褐斑病的感病性离体评价. 浙江农业学报, 2016, 28(1): 84-89.
FU Y S, LUO J Q, XU J G, LI H Y. In vitro susceptibility evaluation of citrus cultivars to Alternaria alternata pv.citri. Acta Agriculturae Zhejiangensis, 2016, 28(1): 84-89. (in Chinese)
[8]
DALKILIC Z, TIMMER L W, GMITTER F G. Linkage of an Alternaria disease resistance gene in mandarin hybrids with RAPD fragments. Journal of the American Society for Horticultural Science, 2005, 130(2): 191-195.

doi: 10.21273/JASHS.130.2.191
[9]
CUENCA J, ALEZA P, VICENT A, BRUNEL D, OLLITRAULT P, NAVARRO L. Genetically based location from triploid populations and gene ontology of a 3.3-mb genome region linked to Alternaria brown spot resistance in citrus reveal clusters of resistance genes. PLoS ONE, 2013, 8(10): e76755.

doi: 10.1371/journal.pone.0076755
[10]
CUENCA J, ALEZA P, GARCIA-LOR A, OLLITRAULT P, NAVARRO L. Fine mapping for identification of Citrus Alternaria brown spot candidate resistance genes and development of new SNP markers for marker-assisted selection. Frontiers in Plant Science, 2016, 7: 1948.
[11]
ARLOTTA C, CIACCIULLI A, STRANO M C, CAFARO V, SALONIA F, CARUSO P, LICCIARDELLO C, RUSSO G, SMITH M W, CUENCA J, ALEZA P, CARUSO M. Disease resistant Citrus breeding using newly developed high resolution melting and CAPS protocols for Alternaria brown spot marker assisted selection. Agronomy, 2020, 10(9): 1368.

doi: 10.3390/agronomy10091368
[12]
唐科志, 周常勇. 红橘响应褐斑病菌侵染的转录组学分析. 中国农业科学, 2020, 53(22): 4584-4600. doi: 10.3864/j.issn.0578-1752.2020.22.006.

doi: 10.3864/j.issn.0578-1752.2020.22.006
TANG K Z, ZHOU C Y. Transcriptome analysis of Citrus reticulata blanco, cv.Hongjv infected with Alternaria alternata tangerine pathotype. Scientia Agricultura Sinica, 2020, 53(22): 4584-4600. doi: 10.3864/j.issn.0578-1752.2020.22.006. (in Chinese)

doi: 10.3864/j.issn.0578-1752.2020.22.006
[13]
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.

doi: 10.1016/j.tplants.2022.11.006
[14]
LI Y L, RUPERAO P, BATLEY J, EDWARDS D, DAVIDSON J, HOBSON K, SUTTON T. Genome analysis identified novel candidate genes for Ascochyta blight resistance in chickpea using whole genome re-sequencing data. Frontiers in Plant Science, 2017, 8: 359.
[15]
刘荣萍, 胡军华, 姚廷山, 王雪莲, 左佩佩, 王延杰, 李鸿筠. 柑橘褐斑病室内快速评价方法的研究. 果树学报, 2013, 30(5): 889-892.
LIU R P, HU J H, YAO T S, WANG X L, ZUO P P, WANG Y J, LI H Y. A rapid laboratory evaluation method of citrus brown spot caused by Alternaria alternate. Journal of Fruit Science, 2013, 30(5): 889-892. (in Chinese)
[16]
王小柯, 江东, 孙珍珠. 利用GBS技术研究240份宽皮柑橘的系统演化. 中国农业科学, 2017, 50(9): 1666-1673. doi: 10.3864/j.issn.0578-1752.2017.09.012.

doi: 10.3864/j.issn.0578-1752.2017.09.012
WANG X K, JIANG D, SUN Z Z. Study on phylogeny of 240 mandarin accessions with genotyping-by-sequencing technology. Scientia Agricultura Sinica, 2017, 50(9): 1666-1673. doi: 10.3864/j.issn.0578-1752.2017.09.012. (in Chinese)

doi: 10.3864/j.issn.0578-1752.2017.09.012
[17]
WRIGHT S. The genetical structure of populations. Annals of Eugenics, 1951, 15(4): 323-354.

doi: 10.1111/j.1469-1809.1949.tb02451.x pmid: 24540312
[18]
PEEVER T L, OLSEN L, IBAÑEZ A, TIMMER L W. Genetic differentiation and host specificity among populations of Alternaria spp.causing brown spot of grapefruit and tangerine × grapefruit hybrids in Florida. Phytopathology, 2000, 90(4): 407-414.

doi: 10.1094/PHYTO.2000.90.4.407
[19]
BHATTARAI G, SHI A N, MOU B Q, CORRELL J C. Resequencing worldwide spinach germplasm for identification of field resistance QTLs to downy mildew and assessment of genomic selection methods. Horticulture Research, 2022, 9: uhac205.

doi: 10.1093/hr/uhac205
[20]
ALAVILLI H, LEE J J, YOU C R, POLI Y, KIM H J, JAIN A, SONG K. GWAS reveals a novel candidate gene CmoAP2/ERF in Pumpkin (Cucurbita moschata) involved in resistance to powdery mildew. International Journal of Molecular Sciences, 2022, 23(12): 6524.

doi: 10.3390/ijms23126524
[21]
PHUKE R M, HE X Y, JULIANA P, KABIR M R, ROY K K, MARZA F, ROY C, SINGH G P, CHAWADE A, JOSHI A K, SINGH P K. Identification of genomic regions and sources for wheat blast resistance through GWAS in Indian wheat genotypes. Genes, 2022, 13(4): 596.

doi: 10.3390/genes13040596
[22]
TERAKAMI S, ADACHI Y, IKETANI H, SATO Y, SAWAMURA Y, TAKADA N, NISHITANI C, YAMAMOTO T. Genetic mapping of genes for susceptibility to black spot disease in Japanese pears. Genome, 2007, 50(8): 735-741.

pmid: 17893733
[23]
MORIYA S, TERAKAMI S, OKADA K, SHIMIZU T, ADACHI Y, KATAYOSE Y, FUJISAWA H, WU J, KANAMORI H, YAMAMOTO T, ABE K. Identification of candidate genes responsible for the susceptibility of apple (Malus × domestica Borkh.) to Alternaria blotch. BMC Plant Biology, 2019, 19(1): 1-13.

doi: 10.1186/s12870-018-1600-2
[24]
DALIO R J D, MAGALHÃES D M, RODRIGUES C M, ARENA G D, OLIVEIRA T S, SOUZA-NETO R R, PICCHI S C, MARTINS P M M, SANTOS P J C, MAXIMO H J, PACHECO I S, DE SOUZA A A, MACHADO M A. PAMPs, PRRs, effectors and R-genes associated with citrus-pathogen interactions. Annals of Botany, 2017, 119(5): 749-774.

doi: 10.1093/aob/mcw238 pmid: 28065920
[25]
KOURELIS J, VAN DER HOORN R A L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. The Plant Cell, 2018, 30(2): 285-299.

doi: 10.1105/tpc.17.00579 pmid: 29382771
[26]
WANG J, TAN S J, ZHANG L, LI P, TIAN D C. Co-variation among major classes of LRR-encoding genes in two pairs of plant species. Journal of Molecular Evolution, 2011, 72(5/6): 498-509.

doi: 10.1007/s00239-011-9448-1
[27]
SCHWESSINGER B, ZIPFEL C. News from the frontline: recent insights into PAMP-triggered immunity in plants. Current Opinion in Plant Biology, 2008, 11(4): 389-395.

doi: 10.1016/j.pbi.2008.06.001 pmid: 18602859
[28]
CHAPARRO-GARCIA A, WILKINSON R C, GIMENEZ-IBANEZ S, FINDLAY K, COFFEY M D, ZIPFEL C, RATHJEN J P, KAMOUN S, SCHORNACK S. The receptor-like kinase SERK3/ BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS ONE, 2011, 6(1): e16608.

doi: 10.1371/journal.pone.0016608
[29]
DANNA C H, MILLET Y A, KOLLER T, HAN S W, BENT A F, RONALD P C, AUSUBEL F M. The Arabidopsis flagellin receptor FLS 2 mediates the perception of Xanthomonas Ax21 secreted peptides. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(22): 9286-9291.
[30]
TAKAI R, ISOGAI A, TAKAYAMA S, CHE F S. Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Molecular Plant-Microbe Interactions, 2008, 21(12): 1635-1642.

doi: 10.1094/MPMI-21-12-1635 pmid: 18986259
[31]
ENCISO-RODRÍGUEZ F E, GONZÁLEZ C, RODRÍGUEZ E A, LÓPEZ C E, LANDSMAN D, BARRERO L S, MARIÑO-RAMÍREZ L. Identification of immunity related genes to study the Physalis peruviana: Fusarium oxysporum pathosystem. PLoS ONE, 2013, 8(7): e68500.

doi: 10.1371/journal.pone.0068500
[32]
LI J Y, WANG X D, ZHANG L R, MENG Q F, ZHANG N, YANG W X, LIU D Q. A wheat NBS-LRR gene TaRGA19 participates in Lr19-mediated resistance to Puccinia triticina. Plant Physiology and Biochemistry, 2017, 119: 1-8.

doi: 10.1016/j.plaphy.2017.08.009
[33]
LV L L, LIU Y S, BAI S H, TURAKULOV K S, DONG C H, ZHANG Y G. A TIR-NBS-LRR gene MdTNL1 regulates resistance to Glomerella leaf spot in apple. International Journal of Molecular Sciences, 2022, 23(11): 6323.

doi: 10.3390/ijms23116323
[34]
GAO Y L, WANG B W, XU Z L, LI M Y, SONG Z B, LI W Z, LI Y P. Tobacco serine/threonine protein kinase gene NrSTK enhances black shank resistance. Genetics and Molecular Research, 2015, 14(4): 16415-16424.

doi: 10.4238/2015.December.9.11 pmid: 26662438
[35]
马璐琳, 段青, 杜文文, 张艺萍, 崔光芬, 贾文杰, 吴学尉, 王祥宁, 王继华. 泸定百合丝氨酸/苏氨酸蛋白激酶基因(LsS/TK)的克隆与表达分析. 分子植物育种, 2020, 18(18): 5925-5932.
MA L L, DUAN Q, DU W W, ZHANG Y P, CUI G F, JIA W J, WU X W, WANG X N, WANG J H. Cloning and expression analysis of a serine/threonine protein kinase gene (LsS/TK) in Lilium sargentiae. Molecular Plant Breeding, 2020, 18(18): 5925-5932. (in Chinese)
[36]
BRUEGGEMAN R, DRADER T, KLEINHOFS A. The barley serine/threonine kinase gene Rpg1 providing resistance to stem rust belongs to a gene family with five other members encoding kinase domains. Theoretical and Applied Genetics, 2006, 113(6): 1147-1158.

doi: 10.1007/s00122-006-0374-3 pmid: 16896706
[37]
CHAKRABORTY S, NGUYEN B, WASTI S D, XU G Z. Plant leucine-rich repeat receptor kinase (LRR-RK): Structure, ligand perception, and activation mechanism. Molecules, 2019, 24(17): 3081.

doi: 10.3390/molecules24173081
[38]
CHEN T S. Identification and characterization of the LRR repeats in plant LRR-RLKs. BMC Molecular and Cell Biology, 2021, 22(1): 9.

doi: 10.1186/s12860-021-00344-y pmid: 33509084
[39]
MATSUSHIMA N, MIYASHITA H. Leucine-rich repeat (LRR) domains containing intervening motifs in plants. Biomolecules, 2012, 2(2): 288-311.

doi: 10.3390/biom2020288 pmid: 24970139
[40]
DÍAZ L, DEL RÍO J A, PÉREZ-GILABERT M, ORTUÑO A. Involvement of an extracellular fungus laccase in the flavonoid metabolism in Citrus fruits inoculated with Alternaria alternata. Plant Physiology and Biochemistry, 2015, 89: 11-17.

doi: 10.1016/j.plaphy.2015.02.006
[41]
ORTUÑO A, NEMSA I, ALVAREZ N, LACASA A, PORRAS I, GARCIA LIDÓN A, DEL RÍO J A. Correlation of ethylene synthesis in Citrus fruits and their susceptibility to Alternaria alternata pv. citri. Physiological and Molecular Plant Pathology, 2008, 72(4/5/6): 162-166.

doi: 10.1016/j.pmpp.2008.08.003
[1] TAN LiZhi, ZHAO YiQiang. Principle, Optimization and Application of Mixed Models in Genome- Wide Association Study [J]. Scientia Agricultura Sinica, 2023, 56(9): 1617-1632.
[2] WANG Mai, DONG QingFeng, GAO ShenAo, LIU DeZheng, LU Shan, QIAO PengFang, CHEN Liang, HU YinGang. Genome-Wide Association Studies and Mining for Favorable Loci of Root Traits at Seedling Stage in Wheat [J]. Scientia Agricultura Sinica, 2023, 56(5): 801-820.
[3] YANG MingLu, ZHANG HaiLiang, LUO HanPeng, HUANG XiXia, ZHANG HanLin, ZHANG ShiShi, WANG Yan, LIU Lin, GUO Gang, WANG YaChun. Estimation of Genetic Parameters and Genome-Wide Association Study of Heat Indicators in Holstein Cattle Based on Collar-Mounted Device [J]. Scientia Agricultura Sinica, 2023, 56(5): 995-1006.
[4] WANG JiangHao, WANG LiWei, ZHANG DongMin, GUO Rui, ZHANG QuanGuo, LI XingHua, WEI JianFeng, SONG Wei, WANG BaoQiang, LI RongGai. Molecular Marker Assisted Identification and Application of Maize Germplasms for Maize Rough Dwarf Disease Resistance [J]. Scientia Agricultura Sinica, 2023, 56(10): 1838-1847.
[5] WANG MengRui, LIU ShuMei, HOU LiXia, WANG ShiHui, LÜ HongJun, SU XiaoMei. Development of Artificial Inoculation Methodology for Evaluation of Resistance to Fusarium Crown and Root Rot and Screening of Resistance Sources in Tomato [J]. Scientia Agricultura Sinica, 2022, 55(4): 707-718.
[6] ZHAO ChunFang,ZHAO QingYong,LÜ YuanDa,CHEN Tao,YAO Shu,ZHAO Ling,ZHOU LiHui,LIANG WenHua,ZHU Zhen,WANG CaiLin,ZHANG YaDong. Screening of Core Markers and Construction of DNA Fingerprints of Semi-Waxy Japonica Rice Varieties [J]. Scientia Agricultura Sinica, 2022, 55(23): 4567-4582.
[7] BaoHua CHU,FuGuo CAO,NingNing BIAN,Qian QIAN,ZhongXing LI,XueWei LI,ZeYuan LIU,FengWang MA,QingMei GUAN. Resistant Evaluation of 84 Apple Cultivars to Alternaria alternata f. sp. mali and Genome-Wide Association Analysis [J]. Scientia Agricultura Sinica, 2022, 55(18): 3613-3628.
[8] LinHan ZOU,XinYing ZHOU,ZeYuan ZHANG,Rui YU,Meng YUAN,XiaoPeng SONG,JunTao JIAN,ChuanLiang ZHANG,DeJun HAN,QuanHao SONG. QTL Mapping of Thousand-Grain-Weight and Its Related Traits in Zhou 8425B × Xiaoyan 81 Population and Haplotype Analysis [J]. Scientia Agricultura Sinica, 2022, 55(18): 3473-3483.
[9] CHANG LiGuo,HE KunHui,LIU JianChao. Mining of Genetic Locus of Maize Stay-Green Related Traits Under Multi-Environments [J]. Scientia Agricultura Sinica, 2022, 55(16): 3071-3081.
[10] DUAN YaRu,GAO MeiLing,GUO Yu,LIANG XiaoXue,LIU XiuJie,XU HongGuo,LIU JiXiu,GAO Yue,LUAN Feishi. Map-Based Cloning and Molecular Marker Development of Watermelon Fruit Shape Gene [J]. Scientia Agricultura Sinica, 2022, 55(14): 2812-2824.
[11] FANG TaoHong,ZHANG Min,MA ChunHua,ZHENG XiaoChen,TAN WenJing,TIAN Ran,YAN Qiong,ZHOU XinLi,LI Xin,YANG SuiZhuang,HUANG KeBing,WANG JianFeng,HAN DeJun,WANG XiaoJie,KANG ZhenSheng. Application of Yr52 Gene in Wheat Improvement for Stripe Rust Resistance [J]. Scientia Agricultura Sinica, 2022, 55(11): 2077-2091.
[12] PeiPei ZHU,YiJia LUO,Wen XIANG,MingLei ZHANG,JianXia ZHANG. Rescue and Molecular Marker Assisted-Selection of the Cold-Resistant Seedless Grape Hybrid Embryo [J]. Scientia Agricultura Sinica, 2021, 54(6): 1218-1228.
[13] XI Ling, WANG YuQi, YANG Xiu, ZHU Wei, CHEN GuoYue, WANG Yi, QIN Peng, ZHOU YongHong, KANG HouYang. Evaluation of Resistance to Stripe Rust and Molecular Detection of Resistance Gene(s) in 243 Common Wheat Landraces from the Yunnan Province [J]. Scientia Agricultura Sinica, 2021, 54(4): 684-695.
[14] CHEN DouDou, GUAN LiPing, HE LiangLiang, SONG YinHua, ZHANG Peng, LIU SanJun. Commonality Identification of Molecular Markers Linked to Seedless Genes in Grape [J]. Scientia Agricultura Sinica, 2021, 54(22): 4880-4893.
[15] WANG JiQing,REN Yi,SHI XiaoLei,WANG LiLi,ZHANG XinZhong,SULITAN· GuZhaLiAYi,XIE Lei,GENG HongWei. Genome-Wide Association Analysis of Superoxide Dismutase (SOD) Activity in Wheat Grain [J]. Scientia Agricultura Sinica, 2021, 54(11): 2249-2260.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd