Evaluation of a global spring wheat panel for stripe rust: Resistance loci validation and novel resources identification


Autoři: Ibrahim S. Elbasyoni aff001;  Walid M. El-Orabey aff003;  Sabah Morsy aff001;  P. S. Baenziger aff002;  Zakaria Al Ajlouni aff004;  Ismail Dowikat aff002
Působiště autorů: Crop Science Department, Damanhur University, Damanhur, Egypt aff001;  Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE, United States of America aff002;  Wheat Diseases Res. Department, Plant Pathology Res. Institute, ARC, Giza, Egypt aff003;  Jordan University of Science and Technology, Department of Plant Pathology, Irbid, Jordan aff004
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222755

Souhrn

Stripe rust (incited by Puccinia striiformis f. sp. tritici) is airborne wheat (Triticum aestivum L.) disease with dynamic virulence evolution. Thus, anticipatory and continued screening in hotspot regions is crucial to identify new pathotypes and integrate new resistance resources to prevent potential disease epidemics. A global wheat panel consisting of 882 landraces and 912 improved accessions was evaluated in two locations in Egypt during 2016 and 2017. Five prevalent and aggressive pathotypes of stripe rust were used to inoculate the accessions during the two growing seasons and two locations under field conditions. The objectives were to evaluate the panel for stripe rust resistance at the adult plant stage, identify potentially novel QTLs associated with stripe rust resistance, and validate previously reported stripe rust QTLs under the Egyptian conditions. The results indicated that 42 landraces and 140 improved accessions were resistant to stripe rust. Moreover, 24 SNPs were associated with stripe rust resistance and were within 18 wheat functional genes. Four of these genes were involved in several plant defense mechanisms. The number of favorable alleles, based upon the associated SNPs, was significant and negatively correlated with stripe rust resistance score, i.e., as the number of resistances alleles increased the observed resistance increased. In conclusion, generating new stripe rust phenotypic information on this panel while using the publicly available molecular marker data, contributed to identifying potentially novel QTLs associated with stripe rust and validated 17 of the previously reported QTLs in one of the global hotspots for stripe rust.

Klíčová slova:

Alleles – DNA-binding proteins – Egypt – Genome-wide association studies – Molecular genetics – Quantitative trait loci – Spring – Wheat


Zdroje

1. Yuan FP, Zeng QD, Wu JH, Wang QL, Yang ZJ, Liang BP, et al. QTL mapping and validation of adult plant resistance to stripe rust in chinese wheat landrace humai 15. Front Plant Sci [Internet]. 2018 [cited 2018 Oct 30];9(July):1–13. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30026752

2. Zhang HY, Wang Z, Ren JD, Du ZY, Quan W, Zhang YB, et al. A QTL with Major Effect on Reducing Stripe Rust Severity Detected From a Chinese Wheat Landrace. Plant Dis [Internet]. 2017 Aug 15 [cited 2018 Oct 8];101(8):1533–9. Available from: doi: 10.1094/PDIS-08-16-1131-RE 30678599

3. Dracatos PM, Zhang P, Park RF, McIntosh RA, Wellings CR. Complementary resistance genes in wheat selection ‘Avocet R’ confer resistance to stripe rust. Theor Appl Genet [Internet]. 2016 Jan 3 [cited 2018 Oct 8];129(1):65–76. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26433828 doi: 10.1007/s00122-015-2609-7 26433828

4. Wabila C, Neumann K, Kilian B, Radchuk V, Graner A. A tiered approach to genome-wide association analysis for the adherence of hulls to the caryopsis of barley seeds reveals footprints of selection. BMC Plant Biol [Internet]. 2019 Dec 6 [cited 2019 Apr 12];19(1):95. Available from: doi: 10.1186/s12870-019-1694-1 30841851

5. Dangl JL, Horvath DM, Staskawicz BJ. Pivoting the plant immune system from dissection to deployment [Internet]. Vol. 341, Science. NIH Public Access; 2013 [cited 2018 Oct 8]. p. 746–51. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23950531 doi: 10.1126/science.1236011 23950531

6. Wang L, Zheng D, Zuo S, Chen X, Zhuang H, Huang L, et al. Inheritance and Linkage of Virulence Genes in Chinese Predominant Race CYR32 of the Wheat Stripe Rust Pathogen Puccinia striiformis f. sp. tritici. Front Plant Sci [Internet]. 2018 Feb 8 [cited 2018 Oct 8];9:120. Available from: doi: 10.3389/fpls.2018.00120 29472940

7. Safavi SA, Afshari F, Yazdansepas A. Effective and ineffective resistance genes to wheat yellow rust during six years monitoring in Ardabil. Arch Phytopathol Plant Prot [Internet]. 2013 Apr [cited 2018 Oct 8];46(7):774–80. Available from: http://www.tandfonline.com/doi/abs/10.1080/03235408.2012.752142

8. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science (80-) [Internet]. 2009 Mar 6 [cited 2018 Oct 8];323(5919):1360–3. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19229000 doi: 10.1126/science.1166453 19229000

9. Dong Z, Hegarty JM, Zhang J, Zhang W, Chao S, Chen X, et al. Validation and characterization of a QTL for adult plant resistance to stripe rust on wheat chromosome arm 6BS (Yr78). Theor Appl Genet [Internet]. 2017 Oct [cited 2018 Oct 30];130(10):2127–37. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28725946 doi: 10.1007/s00122-017-2946-9 28725946

10. Elad Y, Pertot I. Climate Change Impacts on Plant Pathogens and Plant Diseases. J Crop Improv [Internet]. 2014 Jan 2 [cited 2018 Oct 30];28(1):99–139. Available from: http://www.tandfonline.com/doi/abs/10.1080/15427528.2014.865412

11. Nanda S, Chand SK, Mandal P, Tripathy P, Joshi RK. Identification of novel source of resistance and differential response of allium genotypes to purple blotch pathogen, Alternaria porri (Ellis) Ciferri. Plant Pathol J [Internet]. 2016 Dec [cited 2018 Oct 30];32(6):519–27. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27904458 doi: 10.5423/PPJ.OA.02.2016.0034 27904458

12. Bux H, Ashraf M, Husain F, Rattu AUR, Fayaz M. Characterization of wheat germplasm for stripe rust (Puccini striiformis f. Sp. Tritici) resistance. Aust J Crop Sci [Internet]. 2012 [cited 2017 Jun 10];6(1):116–20. Available from: http://www.cropj.com/bux_6_1_2012_116_120.pdf

13. Kumar S, Archak S, Tyagi RK, Kumar J, Vikas VK, Jacob SR, et al. Evaluation of 19,460 wheat accessions conserved in the indian national genebank to identify new sources of resistance to rust and spot blotch diseases. Bai G, editor. One PLoS [Internet]. 2016 Dec 12 [cited 2017 Jun 10];11(12):e0167702. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27942031 doi: 10.1371/journal.pone.0167702 27942031

14. Cobb JN, DeClerck G, Greenberg A, Clark R, McCouch S. Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype–phenotype relationships and its relevance to crop improvement. Theor Appl Genet [Internet]. 2013 Apr 8 [cited 2017 Jun 29];126(4):867–87. Available from: doi: 10.1007/s00122-013-2066-0 23471459

15. Maccaferri M, Zhang J, Bulli P, Abate Z, Chao S, Cantu D, et al. A Genome-Wide Association Study of Resistance to Stripe Rust (Puccinia striiformis f. sp. tritici) in a Worldwide Collection of Hexaploid Spring Wheat (Triticum aestivum L.). G3: Genes|Genomes|Genetics [Internet]. 2015 Mar 20 [cited 2018 Oct 18];5(3):449–65. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25609748 doi: 10.1534/g3.114.014563 25609748

16. Muleta KT, Bulli P, Rynearson S, Chen X, Pumphrey M. Loci associated with resistance to stripe rust (Puccinia striiformis f. sp.Tritici) in a core collection of spring wheat (Triticum aestivum). Zhang A, editor. PLoS One [Internet]. 2017 Jun 7 [cited 2018 Oct 30];12(6):e0179087. Available from: doi: 10.1371/journal.pone.0179087 28591221

17. Kertho A, Mamidi S, Bonman JM, McClean PE, Acevedo M. Genome-wide association mapping for resistance to leaf and stripe rust in winter-habit hexaploid wheat landraces. PLoS One [Internet]. 2015 [cited 2018 Oct 18];10(6):e0129580. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26076040 doi: 10.1371/journal.pone.0129580 26076040

18. Friedmann M, Asfaw A, Anglin N, Becerra L, Bhattacharjee R, Brown A, et al. Genomics-Assisted Breeding in the CGIAR Research Program on Roots, Tubers and Bananas (RTB). Agriculture [Internet]. 2018;8(7):89. Available from: http://www.mdpi.com/2077-0472/8/7/89

19. Shahin A., Abu AAA, Shahin SI. Virulence and Diversity of Wheat Stripe Rust Pathogen in Egypt. J Am Sci. 2015;11(6):7–8.

20. Ali S, Rodriguez-Algaba J, Thach T, Sørensen CK, Hansen JG, Lassen P, et al. Yellow Rust Epidemics Worldwide Were Caused by Pathogen Races from Divergent Genetic Lineages. Front Plant Sci [Internet]. 2017 [cited 2018 Oct 31];8:1057. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28676811 doi: 10.3389/fpls.2017.01057 28676811

21. Miedaner T, Rapp M, Flath K, Longin CFH, Würschum T. Genetic architecture of yellow and stem rust resistance in a durum wheat diversity panel. Euphytica [Internet]. 2019 Apr 13 [cited 2019 Jul 2];215(4):71. Available from: http://link.springer.com/10.1007/s10681-019-2394-5

22. Mert Z, Nazari K, Karagöz E, Akan K, Öztürk İ, Tülek A. First Incursion of the Warrior Race of Wheat Stripe Rust (Puccinia striiformis f. sp. tritici) to Turkey in 2014. Plant Dis [Internet]. 2015 Feb [cited 2019 Jul 2];100(2):528–528. Available from: http://apsjournals.apsnet.org/doi/10.1094/PDIS-07-15-0827-PDN

23. McIntosh R, Mu J, Han D, Kang Z. Wheat stripe rust resistance gene Yr24/Yr26: A retrospective review [Internet]. Vol. 6, Crop Journal. Elsevier; 2018 [cited 2019 Apr 11]. p. 321–9. Available from: https://www.sciencedirect.com/science/article/pii/S2214514118300242

24. Giesbrecht FG, Gumpertz ML. Planning, Construction, and Statistical Analysis of Comparative Experiments (Google eBook) [Internet]. John Wiley & Sons; 2011 [cited 2013 Aug 18]. 693 p. Available from: http://books.google.com/books?id=GOJjLW13N0QC&pgis=1

25. Shahin S, El-Orabey W. Relationship between Partial Resistance and Inheritance of Adult Plant Resistance Gene Lr 46 of Leaf Rust in Six Bread Wheat Varieties. Adv Crop Sci Technol [Internet]. 2014 [cited 2017 Jun 17];03(01):1511–7. Available from: http://dx.doi.org/10.4172/2329-8863.1000161

26. Roelfs a.P., Singh RP, Saari. Rust Diseases of Wheat: Concepts and methods of disease management. [Internet]. Rust Diseases of Wheat: Concepts and methods of disease management. CIMMYT; 1992 [cited 2019 Aug 16]. 81 p. Available from: http://agris.fao.org/agris-search/search.do?recordID=QY9200317

27. Pauli D, Muehlbauer GJ, Smith KP, Cooper B, Hole D, Obert DE, et al. Association Mapping of Agronomic QTLs in U.S. Spring Barley Breeding Germplasm. Plant Genome [Internet]. 2014;7(3):0. Available from: https://www.crops.org/publications/tpg/abstracts/7/3/plantgenome2013.11.0037

28. Breiman L. Random forests. Mach Learn [Internet]. 2001 [cited 2017 Oct 10];45(1):5–32. Available from: http://link.springer.com/10.1023/A:1010933404324

29. Stekhoven DJ, Bühlmann P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics [Internet]. 2012 Jan 1 [cited 2014 Jan 9];28(1):112–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22039212 doi: 10.1093/bioinformatics/btr597 22039212

30. Cavanagh CCR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, et al. Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc Natl Acad Sci U S A [Internet]. 2013 May 14 [cited 2013 May 1];110(20):8057–62. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23630259 doi: 10.1073/pnas.1217133110 23630259

31. Federer WT, King F. Variations on Split Plot and Split Block Experiment Designs. Variations on Split Plot and Split Block Experiment Designs. John Wiley & Sons: New York, NY, USA; 2006. 1–270 p.

32. Steel RGD, Torrie JH. Principles and Procedures of Statistics: A Biometrical Approach. 2nd Ed. McGraw-Hill Publishing Co., New York. 1980;

33. TUKEY JW. Comparing individual means in the analysis of variance. Biometrics [Internet]. 1949 Jun [cited 2019 Sep 25];5(2):99–114. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18151955 18151955

34. Xanthopoulos P, Pardalos PM, Trafalis TB. Linear Discriminant Analysis. In: A Statistical Approach to Neural Networks for Pattern Recognition [Internet]. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2013 [cited 2018 Oct 30]. p. 27–33. Available from: http://doi.wiley.com/10.1002/9780470148150.ch3

35. Chan AW, Hamblin MT, Jannink J-L, Albers CA, Banks E, DePristo MA, et al. Evaluating Imputation Algorithms for Low-Depth Genotyping-By-Sequencing (GBS) Data. Feltus FA, editor. One PLoS [Internet]. 2016 Aug 18 [cited 2017 Jun 9];11(8):e0160733. Available from: doi: 10.1371/journal.pone.0160733 27537694

36. Gao X, Starmer J. Human population structure detection via multilocus genotype clustering. BMC Genet [Internet]. 2007 Jun 25 [cited 2018 Jul 24];8(1):34. Available from: http://bmcgenet.biomedcentral.com/articles/10.1186/1471-2156-8-34

37. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. 2017.

38. Smith JSC, Chin ECL, Shu H, Smith OS, Wall SJ, Senior ML, et al. An evaluation of the utility of SSR loci as molecular markers in maize (Zea mays L.): Comparisons with data from RFLPS and pedigree. Theor Appl Genet [Internet]. 1997 Jul 28 [cited 2018 Jun 30];95(1–2):163–73. Available from: http://link.springer.com/10.1007/s001220050544

39. Tang Y, Liu X, Wang J, Li M, Wang Q, Tian F, et al. GAPIT Version 2: An Enhanced Integrated Tool for Genomic Association and Prediction. Plant Genome [Internet]. 2016 [cited 2018 Oct 30];9(2):0. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27898829

40. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A [Internet]. 2003 Aug 5 [cited 2017 Aug 9];100(16):9440–5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12883005 doi: 10.1073/pnas.1530509100 12883005

41. Borrill P, Harrington SA, Uauy C. Applying the latest advances in genomics and phenomics for trait discovery in polyploid wheat. Plant J [Internet]. 2019 Jan [cited 2019 Jul 2];97(1):56–72. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30407665 doi: 10.1111/tpj.14150 30407665

42. Chen WQ, Wu LR, Liu TG, Xu SC, Jin SL, Peng YL, et al. Race Dynamics, Diversity, and Virulence Evolution in Puccinia striiformis f. sp. tritici, the Causal Agent of Wheat Stripe Rust in China from 2003 to 2007. Plant Dis. 2009;93(11):1093–101. doi: 10.1094/PDIS-93-11-1093 30754577

43. Bahri B, Shah SJA, Hussain S, Leconte M, Enjalbert J, de Vallavieille-Pope C. Genetic diversity of the wheat yellow rust population in Pakistan and its relationship with host resistance. Plant Pathol [Internet]. 2011 Aug [cited 2018 Oct 31];60(4):649–60. Available from: http://doi.wiley.com/10.1111/j.1365-3059.2010.02420.x

44. Ali S, Gladieux P, Leconte M, Gautier A, Justesen AF, Hovmøller MS, et al. Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen Puccinia striiformis f.sp. tritici. McDonald BA, editor. PLoS Pathog [Internet]. 2014 Jan 23 [cited 2018 Oct 31];10(1):e1003903. Available from: doi: 10.1371/journal.ppat.1003903 24465211

45. Bryant RRM, McGrann GRD, Mitchell AR, Schoonbeek HJ, Boyd LA, Uauy C, et al. A change in temperature modulates defence to yellow (stripe) rust in wheat line UC1041 independently of resistance gene Yr36. BMC Plant Biol [Internet]. 2014 Jan 8 [cited 2018 Oct 31];14(1):10. Available from: http://bmcplantbiol.biomedcentral.com/articles/10.1186/1471-2229-14-10

46. Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN. The past, present and future of breeding rust resistant wheat. Front Plant Sci [Internet]. 2014 [cited 2018 Nov 1];5:641. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25505474 doi: 10.3389/fpls.2014.00641 25505474

47. Tsilo TJ, Kolmer JA, Anderson JA. Molecular mapping and improvement of leaf rust resistance in wheat breeding lines. Phytopathology [Internet]. 2014 [cited 2017 Jul 4];104(8):865–70. Available from: doi: 10.1094/PHYTO-10-13-0276-R 24521485

48. Weinig C, Schmitt J. Environmental Effects on the Expression of Quantitative Trait Loci and Implications for Phenotypic Evolution. Bioscience [Internet]. 2004 Jul 1 [cited 2018 Nov 1];54(7):627. Available from: https://academic.oup.com/bioscience/article/54/7/627-635/223523

49. Visscher PM, Hill WG, Wray NR. Heritability in the genomics era—Concepts and misconceptions. Nat Rev Genet. 2008;9(4):255–66. doi: 10.1038/nrg2322 18319743

50. Lopes MS, El-Basyoni I, Baenziger PS, Singh S, Royo C, Ozbek K, et al. Exploiting genetic diversity from landraces in wheat breeding for adaptation to climate change. J Exp Bot [Internet]. 2015 Jun 1 [cited 2018 Nov 1];66(12):3477–86. Available from: doi: 10.1093/jxb/erv122 25821073

51. Li Q, Guo J, Chao K, Yang J, Yue W, Ma D, et al. High-Density Mapping of an Adult-Plant Stripe Rust Resistance Gene YrBai in Wheat Landrace Baidatou Using the Whole Genome DArTseq and SNP Analysis. Front Plant Sci [Internet]. 2018 Aug 2 [cited 2019 Apr 12];9:1120. Available from: doi: 10.3389/fpls.2018.01120 30116253

52. Lombardi M, Materne M, Cogan NOI, Rodda M, Daetwyler HD, Slater AT, et al. Assessment of genetic variation within a global collection of lentil (Lens culinaris Medik.) cultivars and landraces using SNP markers. BMC Genet [Internet]. 2014 Dec 24 [cited 2018 Oct 31];15(1):150. Available from: http://bmcgenet.biomedcentral.com/articles/10.1186/s12863-014-0150-3

53. Basnet BR, Singh RP, Ibrahim AMH, Herrera-Foessel SA, Huerta-Espino J, Lan C, et al. Characterization of Yr54 and other genes associated with adult plant resistance to yellow rust and leaf rust in common wheat Quaiu 3. Mol Breed [Internet]. 2014 Feb 20 [cited 2018 Oct 29];33(2):385–99. Available from: http://link.springer.com/10.1007/s11032-013-9957-2

54. Elbasyoni I, Morsy S, Ramamurthy R, Nassar A. Identification of Genomic Regions Contributing to Protein Accumulation in Wheat under Well-Watered and Water Deficit Growth Conditions. Plants [Internet]. 2018;7(3):56. Available from: http://www.mdpi.com/2223-7747/7/3/56

55. Liu W, Maccaferri M, Rynearson S, Letta T, Zegeye H, Tuberosa R, et al. Novel Sources of Stripe Rust Resistance Identified by Genome-Wide Association Mapping in Ethiopian Durum Wheat (Triticum turgidum ssp. durum). Front Plant Sci [Internet]. 2017 [cited 2018 Oct 29];8:774. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28553306 doi: 10.3389/fpls.2017.00774 28553306

56. Naruoka Y, Ando K, Bulli P, Muleta KT, Rynearson S, Pumphrey MO. Identification and validation of SNP markers linked to the stripe rust resistance gene Yr5 in wheat. Crop Sci [Internet]. 2016 Aug 7 [cited 2018 Oct 30];56(6):3055–65. Available from: https://dl.sciencesocieties.org/publications/cs/abstracts/56/6/3055

57. Goff KE, Ramonell KM. The Role and Regulation of Receptor-Like Kinases in Plant Defense. Gene Regul Syst Bio [Internet]. 2007 Sep 26 [cited 2018 Oct 18];1:117762500700100. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19936086

58. Hsieh M-H, Goodman HM. Molecular Characterization of a Novel Gene Family Encoding ACT Domain Repeat Proteins in Arabidopsis. PLANT Physiol [Internet]. 2002 Dec [cited 2018 Oct 30];130(4):1797–806. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12481063 doi: 10.1104/pp.007484 12481063

59. Zhong C, Sun S, Yao L, Ding J, Duan C, Zhu Z. Fine Mapping and Identification of a Novel Phytophthora Root Rot Resistance Locus RpsZS18 on Chromosome 2 in Soybean. Front Plant Sci [Internet]. 2018 [cited 2018 Oct 30];9:44. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29441079 doi: 10.3389/fpls.2018.00044 29441079

60. Li J, Ding G, Chen P, Zhang H, Huang X, Zang Y, et al. Regulation of ubiquitin-like with plant homeodomain and RING finger domain 1 (UHRF1) protein stability by heat shock protein 90 chaperone machinery. J Biol Chem [Internet]. 2016 Sep 16 [cited 2018 Oct 30];291(38):20125–35. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27489107 doi: 10.1074/jbc.M116.727214 27489107


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