Please wait a minute...
Journal of Integrative Agriculture  2020, Vol. 19 Issue (8): 2035-2043    DOI: 10.1016/S2095-3119(19)62841-8
Special Issue: 植物抗病遗传合辑Plant Disease-resistance Genetics
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide association analysis for stripe rust resistance in spring wheat (Triticum aestivum L.) germplasm
Sher MUHAMMAD1*, Muhammad SAJJAD2*, Sultan Habibullah KHAN3, Muhammad SHAHID1, Muhammad ZUBAIR1, Faisal Saeed AWAN3, Azeem Iqbal KHAN4, Muhammad Salman MUBARAK3, Ayesha TAHIR2, Muhammad UMER2, Rumana KEYANI2, Muhammad Inam AFZAL2, Irfan MANZOOR1, Javed Iqbal WATTOO5, Aziz-ur REHMAN6
1 Department of Bioinformatics and Biotechnology, GC University, Faisalabad 38090, Pakistan
2 Department of Biosciences, COMSATS University Islamabad (CUI), Islamabad 45550, Pakistan
3 Centre of Agricultural Biochemistry and Biotechnology (CABB), University of Agriculture, Faisalabad 38000, Pakistan
4 Department of Plant Breeding and Genetics, University of Agriculture, Faisalabad 38000, Pakistan
5 Department of Biotechnology, Faculty of Life Sciences, University of Central Punjab, Lahore 54000, Pakistan
6 Wheat Research Institute, Ayub Agricultural Research Institute (AARI), Faisalabad 38950, Pakistan
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Stripe rust is a continuous threat to wheat crop all over the world.  It causes considerable yield losses in wheat crop every year.  Continuous deployment of adult plant resistance (APR) genes in newly developing wheat cultivars is the most judicious strategy to combat this disease.  Herein, we dissected the genetics underpinning stripe rust resistance in Pakistani wheat germplasm.  An association panel of 94 spring wheat genotypes was phenotyped for two years to score the infestation of stripe rust on each accession and was scanned with 203 polymorphic SSRs.  Based on D´ measure, linkage disequilibrium (LD) exhibited between loci distant up to 45 cM.  Marker-trait associations (MTAs) were determined using mixed linear model (MLM).  Total 31 quantitative trait loci (QTLs) were observed on all 21 wheat chromosomes.  Twelve QTLs were newly discovered as well as 19 QTLs and 35 previously reported Yr genes were validated in Pakistani wheat germplasm.  The major QTLs were QYr.uaf.2AL and QYr.uaf.3BS (PVE, 11.9%).  Dissection of genes from the newly observed QTLs can provide new APR genes to improve genetic resources for APR resistance in wheat crop.
Keywords:  wheat        Puccinia striiformis        LD        GWAS        MTA        PCoA  
Received: 08 August 2019   Accepted:
Fund: The authors acknowledge Higher Education Commission (HEC), Islamabad, Pakistan for providing for funding (21-179/SRGP/R&D/HEC/2014) and the International Research Support Initiative Program (IRSIP) Scholarship for this research work.
Corresponding Authors:  Correspondence Muhammad Sajjad, Tel: +92-334-6609080, E-mail:; Sultan Habibullah KHAN, Tel: +92-333-9917733, E-mail:   
About author:  * These authors contributed equally to this study.

Cite this article: 

Sher MUHAMMAD, Muhammad SAJJAD, Sultan Habibullah KHAN, Muhammad SHAHID, Muhammad ZUBAIR, Faisal Saeed AWAN, Azeem Iqbal KHAN, Muhammad Salman MUBARAK, Ayesha TAHIR, Muhammad Umer, Rumana KEYANI, Muhammad Inam AFZAL, Irfan MANZOOR, Javed Iqbal WATTOO, Aziz-ur REHMAN. 2020. Genome-wide association analysis for stripe rust resistance in spring wheat (Triticum aestivum L.) germplasm. Journal of Integrative Agriculture, 19(8): 2035-2043.

Ain Q U, Rasheed A, Anwar A, Mahmood T, Imtiaz M, Mahmood T, Xia X, He Z, Quraishi U M. 2015. Genome-wide association for grain yield under rainfed conditions in historical wheat cultivars from Pakistan. Frontier in Plant Sciences, 6, 743.
Arief V N. 2010. Methodology development to integrate phenotypic and genotypic data from a plant breeding program through association analysis with a case study using data from the CIMMYT International Spring Wheat field trials. Ph D thesis, School of Agriculture and Food Sciences, The University of Queensland, Australia.
Bansal U K, Forrest K L, Hayden M J, Miah H, Singh D, Bariana H S. 2011. Characterisation of a new stripe rust resistance gene Yr47 and its genetic association with the leaf rust resistance gene Lr52. Theoretical and Applied Genetics, 122, 1461–1466.
Basnet B R, Singh R P, Ibrahim A M H, Herrera-Foessel S A, Huerta-Espino J, Lan C, Rudd J C. 2014. Characterization of Yr54 and other genes associated with adult plant resistance to yellow rust and leaf rust in common wheat Quaiu 3. Molecular Breeding, 33, 385–399.
Beddow J M, Pardey P G, Chai Y, Hurley T M, Kriticos D J, Braun H J, Park R F, Cuddy W S, Yonow T. 2015. Research investment implications of shifts in the global geography of wheat stripe rust. Nature Plants, 1, 15132.
Borner A, Roder M S, Unger O, Meinel A. 2000.The detection and molecular mapping of a major gene for non-specific adult-plant disease resistance against stripe rust (Puccinia striiformis) in wheat.Theoretical and Applied Genetics, 100, 1095–1099.
Breseghello F, Sorrells M E. 2006. Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics, 172, 1165–1177.
Chao S, Zhang W, Dubcovsky J, Sorrells M. 2007. Evaluation of genetic diversity and genome-wide linkage disequilibrium among U.S wheat (Triticum aestivum L.) germplasm representing different market classes. Crop Science, 47, 1018–1030.
Cheng P, Xu L S, Wang M N, See D R, Chen X M. 2014. Molecular mapping of genes Yr64 and Yr65 for stripe rust resistance in hexaploid derivatives of durum wheat accessions PI 331260 and PI 480016. Theoretical and Applied Genetics, 127, 2267–2277.
Crossa J, Burgueno J, Dreisickacker S, Vargas M, Herrera-Foessel S A, Lillemo M, Singh R P, Trethowan R, Warburton M, Franco J, Reynolds M, Crouch J H, Ortiz R. 2007. Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure. Genetics, 177, 1889–1913.
Dadkhodaie N, Karaoglou H, Wellings C, Park R. 2011. Mapping genes Lr53 and Yr35 on the short arm of chromosome 6B of common wheat with microsatellite markers and studies of their association with Lr36. Theoretical and Applied Genetics, 122, 479–487.
Devlin B, Risch N. 1995. A comparison of linkage disequilibrium measures for fine-scale mapping. Genomics, 29, 311–322.
Doyle J J, Doyle J L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin, 19, 11–15.
Eriksen L, Afshari F, Christiansen M J, McIntosh R A, Jahoor A, Wellings C R. 2004. Yr32 for resistance to stripe (yellow) rust present in the wheat cultivar Carstens V. Theoretical and Applied Genetics, 108, 567–575.
Gulnaz S, Zulkiffal M, Sajjad M, Ahmed J, Musa M, Abdullah M, Ahsan A, Rehman A U. 2019. Identifying Pakistani wheat landraces as genetic resources for yield potential, heat tolerance and rust resistance. International Journal of Agriculture and Biology, 21, 520–526.
Helguera M, Khan I A, Kolmer J, Lijavetzky D, Zhong-qi L, Dubcovsky J. 2003. PCR assays for the Lr37-Yr17-Sr38 cluster of rust resistance genes and their use to develop isogenic hard red spring wheat lines. Crop Science, 43, 1839–1847.
Herrera-Foessel S A, Lagudah E S, Huerta-Espino J, Hayden M J, Bariana H S, Singh D, Singh R P. 2011. New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theoretical and Applied Genetics, 122, 239–249
Herrera-Foessel S A, Singh R P, Lan C X, Huerta-Espina J, Calvo-Salazar V, Bansal U K, Bariana H S, Lagudah E S. 2015. Yr60, a gene conferring moderate resistance to stripe rust in wheat. Plant Disease, 99, 508–511.
Hickey L T, Lawson W, Platz G J, Dieters M, Arief V N, German S, Fletcher S, Park R F, Singh D, Pereyra S, Franckowiak J. 2011. Mapping Rph20: A gene conferring adult plant resistance to Puccinia hordei in barley. Theoretical and Applied Genetics, 123, 55–68.
Lagudah E, Krattinger S, Herrera-Foessel S A, Singh R, Huerta-Espino J, Spielmeyer W, Brown-Guedira G, Selter L, Keller B. 2009. Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theoretical and Applied Genetics, 119, 889–898.
Lan C, Singh R P, Huerta-Espino J, Calvo-Salazar V, Herrera-Foessel S A. 2014. QTL characterization of resistance to leaf rust and stripe rust in the spring wheat line Francolin-1. Molecular Breeding, 34, 789–803.
Li Q, Chen X M, Wang M N, Jing J X. 2011. Yr45, a new wheat gene for stripe rust resistance on the long arm of chromosome 3D. Theoretical and Applied Genetics, 122, 189–197.
Lin F, Chen X M. 2007. Genetics and molecular mapping of genes for race-specific all-stage resistance and non-race-specific high-temperature adult-plant resistance to stripe rust in spring wheat cultivar Alpowa. Theoretical and Applied Genetics, 114, 1277–1287.
Liu C, Yang Z J, Li G R, Zeng Z X, Zhang Y, Zhou J P, Liu Z H, Ren Z L. 2008. Isolation of a new repetitive DNA sequence from Secale africanum enables targeting of Secale chromatin in wheat background. Euphytica, 159, 249–258.
Liu W, Maccaferri M, Chen X, Laghetti G, Pignone D, Pumphrey M, Tuberosa R. 2017. Genome-wide association mapping reveals a rich genetic architecture of stripe rust resistance loci in emmer wheat (Triticum turgidum ssp. dicoccum). Theoretical and Applied Genetics,130, 2249–2270.
Lowe I, Jankuloski L, Chao S M, Chen X M, See D, Dubcovsky J. 2011. Mapping and validation of QTL which confer partial resistance to broadly virulent post-2000 North American races of stripe rust in hexaploid wheat. Theoretical and Applied Genetics, 123, 143–157.
Luo X Y. 2009. Residues from pesticides and countermeasures.Chinese Agricultural Science Bulletin, 18, 344–347. (in Chinease)
Maccaferri M, Ricci A, Salvi S, Milner S G, Noli E, Martelli P L, Casadio R, Akhunov E, Scalabrin S, Vendramin V. 2015. A high-density, SNP based consensus map of tetraploid wheat as a bridge to integrate durum and bread wheat genomics and breeding. Plant Biotechnology Journal, 13, 648–663.
Maccaferri M, Sanguineti M C, Mantovani P, Demontis A, Massi A, Ammar K, Kolmer J A, Czembor J H, Ezrati S, Tuberosa R. 2010. Association mapping of leaf rust response in durum wheat. Molecular Breeding, 26, 189–228.
Maccaferri M, Sanguineti M C, Noli E, Tuberosa R. 2005. Population structure and long-range linkage disequilibrium in a durum wheat elite collection. Molecular Breeding, 15, 271–290.
Muhammad S, Ahmad A, Awan F S, Khan A I, Qasim M, Rehman A, Javed M A, Manzoor I, Sajjad M. 2018. Genome wide association analysis for leaf rust resistance in spring wheat (Triticum aestivum) germplasm. International Journal of Agriculture and Biology, 20, 2387–2394.
Mulki M A, Jighly A, Ye G, Emebiri L C, Moody D, Ansari O, Ogbonnaya F C. 2013. Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat. Molecular Breeding, 31, 299–311.
Murphy L R, Santra D, Kidwell K, Yan G, Chen X, Campbell K G. 2009. Linkage maps of wheat stripe rust resistance genes Yr5 and Yr15 for use in marker-assisted selection. Crop Science, 49, 1786–1790.
Nsabiyera V, Bariana H S, Qureshi N, Wong D, Hayden M J, Bansal U K. 2018. Characterization and mapping of adult plant stripe rust resistance in wheat accession Aus27284. Theoretical and Applied Genetics, 131, 1–9.
Peterson R F, Campbell A B, Hannah A E. 1948. A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Canadian Journal of Research, 26, 496–500.
Qi A Y, Zhang P P, Zhou Y, Yao Z J, Li Z F, Liu D Q, 2016.Mapping of QTL conferring leaf rust resistance in Chinese wheat lines W014204 and Fuyu 3 at adult plant stage. Journal of Integrative Agriculture, 15, 18–28.
Randhawa M, Bansal U K, Valárik M, Klocová B, Dole?el J, Bariana H. 2014. Molecular mapping of stripe rust resistance gene Yr51 in chromosome 4AL of wheat. Theoretical and Applied Genetics, 127, 317–324.
Rehman A, Sajjad M, Khan S H, Ahmad N. 2013. Prospects of wheat breeding for durable resistance against brown, yellow and black rust fungi. International Journal of Agriculture and Biology, 15, 1209?1220.
Reif J C, Gowda M, Maurer H P, Longin C F H, Korzun V, Ebmeyer E, Bothe R, Pietsch C, Würschum T. 2011. Association mapping for quality traits in soft winter wheat.Theoretical and Applied Genetics, 122, 961–970.
Ren R S, Wang M N, Chen X M, Zhang Z J. 2012. Characterization and molecular mapping of Yr52 for high-temperature adult-plant resistance to stripe rust in spring wheat germplasm PI 183527. Theoretical and Applied Genetics, 125, 847–857.
Rosewarne G M, Singh R P, Huerta-Espino J, Herrera-Foessel S A, Forrest K L, Hayden M J, Rebetzke G J. 2013. Analysis of leaf and stripe rust severities reveals pathotype changes and multiple minor QTLs associated with resistance in an Avocet×Pastor wheat population. Theoretical and Applied Genetics, 124, 1283–1294.
Sajjad M, Khan S H, Ahmad M Q, Rasheed A, Mujeeb-Kazi A, Khan I A. 2014. Association mapping identifies QTLS on wheat chromosome 3A for yield related traits. Cereal Reseach Communications, 42, 177–188.
Sajjad M, Khan S H, Kazi A M. 2012. Low down on association mapping in hexaploid wheat (Triticum aestivum L.). Journal of Crop Science and Biotechnology, 15, 147–158.
Sajjad M, Khan S H, Shahzad M. 2018. Patterns of allelic diversity in spring wheat populations by SSR markers. Cytology and Genetics, 52, 155–160.
Shahzad M, Khan S H, Khan A S, Sajjad M, Rehman A, Khan A I. 2016. Identification of QTLs on chromosome 1B for grain quality traits in bread wheat (Triticum aestivum L.). Cytology and Genetics, 50, 89–95.
Singh R, Datta D, Priyamvada, Singh S, Tiwari R. 2009. A diagnostic PCR based assay for stripe rust resistance gene Yr10 in wheat. Acta Phytopathologica et Entomologica Hungarica, 44, 11–18.
Somers D J, Banks T, DePauw R, Fox S, Clarke J, Pozniak C, McCartney C. 2007. Genome-wide linkage disequilibrium analysis in bread wheat and durum wheat. Genome, 50, 557?567.
Somers D J, Isaac P, Edwards K. 2004. A high density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 109, 1105–1114.
Suenaga K, Singh R P, Huerta-Espino J, William H M. 2003. Microsatellite markers for genes Lr34/Yr18 and other quantitative trait loci for leaf rust and stripe rust resistance in bread wheat. Phytopathology, 93, 881–890.
Tommasini L, Schnurbusch T, Fossati D, Mascher F, Keller B. 2007. Association mapping of Stagonospora nodorum blotch resistance in modern European winter wheat varieties.Theoretical and Applied Genetics, 115, 697–708.
Uauy C, Brevis J C, Chen X, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J. 2005. High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theoretical and Applied Genetics, 112, 97.
Yu L X, Lorenz A, Rutkoski J, Singh R P, Bhavani S, Huerta-Espino J, Sorrells M E. 2011. Association mapping and gene-gene interaction for stem rust resistance in CIMMYT spring wheat germplasm. Theoretical and Applied Genetics, 123, 1257–1268.
Zhao Y, Wang H, Chen W, Li Y. 2014. Genetic structure, linkage disequilibrium and association mapping of verticillium wilt resistance in elite cotton (Gossypium hirsutum L.) germplasm population. PLoS ONE, 9, e86308.
Zheng J, Yan Z, Zhao L, Li S, Zhang Z, Garry R, Yang W, Pu Z. 2014. Molecular mapping of a stripe rust resistance gene in wheat line 51. Journal of Genetics, 93, 443–450.
Zhou X L, Han D J, Gou H L, Wang Q L, Zeng Q D, Yuan F P, Zhan G M, Huang L L, Kang Z S. 2014. Molecular mapping of a stripe rust resistance gene in wheat cultivar Wuhan 2. Euphytica, 196, 251–259.
[1] CHU Jin-peng, GUO Xin-hu, ZHENG Fei-na, ZHANG Xiu, DAI Xing-long, HE Ming-rong. Effect of delayed sowing on grain number, grain weight, and protein concentration of wheat grains at specific positions within spikes[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2359-2369.
[2] FAN Ting-lu, LI Shang-zhong, ZHAO Gang, WANG Shu-ying, ZHANG Jian-jun, WANG Lei, DANG Yi, CHENG Wan-li. Response of dryland crops to climate change and drought-resistant and water-suitable planting technology: A case of spring maize[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2067-2079.
[3] WU Xian-xin, ZANG Chao-qun, ZHANG Ya-zhao, XU Yi-wei, WANG Shu, LI Tian-ya, GAO Li.

Characterization of wheat monogenic lines with known Sr genes and wheat cultivars for resistance to three new races of Puccinia graminis f. sp. tritici in China [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1740-1749.

[4] ZHANG Chong, WANG Dan-dan, ZHAO Yong-jian, XIAO Yu-lin, CHEN Huan-xuan, LIU He-pu, FENG Li-yuan, YU Chang-hao, JU Xiao-tang. Significant reduction of ammonia emissions while increasing crop yields using the 4R nutrient stewardship in an intensive cropping system[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1883-1895.
[5] DU Xiang-bei, XI Min, WEI Zhi, CHEN Xiao-fei, WU Wen-ge, KONG Ling-cong. Raised bed planting promotes grain number per spike in wheat grown after rice by improving spike differentiation and enhancing photosynthetic capacity[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1631-1644.
[6] ZHANG Zhen-zhen, CHENG Shuang, FAN Peng, ZHOU Nian-bing, XING Zhi-peng, HU Ya-jie, XU Fang-fu, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Effects of sowing date and ecological points on yield and the temperature and radiation resources of semi-winter wheat[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1366-1380.
[7] LI Jiao-jiao, ZHAO Li, LÜ Bo-ya, FU Yu, ZHANG Shu-fa, LIU Shu-hui, YANG Qun-hui, WU Jun, LI Jia-chuang, CHEN Xin-hong. Development and characterization of a novel common wheat–Mexico Rye T1DL·1RS translocation line with stripe rust and powdery mildew resistance[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1291-1307.
[8] ZHAO Xiao-dong, QIN Xiao-rui, LI Ting-liang, CAO Han-bing, XIE Ying-he. Effects of planting patterns plastic film mulching on soil temperature, moisture, functional bacteria and yield of winter wheat in the Loess Plateau of China[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1560-1573.
[9] DONG Xiu-chun, QIAN Tai-feng, CHU Jin-peng, ZHANG Xiu, LIU Yun-jing, DAI Xing-long, HE Ming-rong. Late sowing enhances lodging resistance of wheat plants by improving the biosynthesis and accumulation of lignin and cellulose[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1351-1365.
[10] JIANG Yun, WANG De-li, HAO Ming, ZHANG Jie, LIU Deng-cai.

Development and characterization of wheat–Aegilops kotschyi 1Uk(1A) substitution line with positive dough quality parameters [J]. >Journal of Integrative Agriculture, 2023, 22(4): 999-1008.

[11] Sunusi Amin ABUBAKAR, Abdoul Kader Mounkaila HAMANI, WANG Guang-shuai, LIU Hao, Faisal MEHMOOD, Abubakar Sadiq ABDULLAHI, GAO Yang, DUAN Ai-wang. Growth and nitrogen productivity of drip-irrigated winter wheat under different nitrogen fertigation strategies in the North China Plain[J]. >Journal of Integrative Agriculture, 2023, 22(3): 908-922.
[12] TU Ke-ling, YIN Yu-lin, YANG Li-ming, WANG Jian-hua, SUN Qun. Discrimination of individual seed viability by using the oxygen consumption technique and headspace-gas chromatography-ion mobility spectrometry[J]. >Journal of Integrative Agriculture, 2023, 22(3): 727-737.
[13] TIAN Jin-yu, LI Shao-ping, CHENG Shuang, LIU Qiu-yuan, ZHOU Lei, TAO Yu, XING Zhi-peng, HU Ya-jie, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Increasing the appropriate seedling density for higher yield in dry direct-seeded rice sown by a multifunctional seeder after wheat-straw return[J]. >Journal of Integrative Agriculture, 2023, 22(2): 400-416.
[14] HU Wen-jing, FU Lu-ping, GAO De-rong, LI Dong-sheng, LIAO Sen, LU Cheng-bin. Marker-assisted selection to pyramid Fusarium head blight resistance loci Fhb1 and Fhb2 in a high-quality soft wheat cultivar Yangmai 15[J]. >Journal of Integrative Agriculture, 2023, 22(2): 360-370.
[15] Zaid CHACHAR, Siffat Ullah KHAN, ZHANG Xue-huan, LENG Peng-fei, ZONG Na, ZHAO Jun. Characterization of transgenic wheat lines expressing maize ABP7 involved in kernel development[J]. >Journal of Integrative Agriculture, 2023, 22(2): 389-399.
No Suggested Reading articles found!