Abstract
Among wheat diseases, leaf (brown) rust caused by Puccinia triticina Eriks. causes more damage to the crop than any other rust. The pathogen is very dynamic and renders rust-resistant wheat cultivars susceptible by evolving new pathotypes. To counter such threats, developing wheat cultivars using diverse germplasm carrying rust resistance genes effective at different growth stages is required. Forty elite wheat genotypes were selected for characterizing race specific (Lr19/Sr25, Lr24/Sr24) and non-race specific (Lr34/Yr18/Pm38/Sr57, Lr46/Yr29/Pm39) rust resistance genes using Sequence Tagged Site (STS) markers Sr24#12, Gb, csLV34 and SSR marker wmc44. The marker analysis revealed the presence of Lr24/Sr24 genes in 47% of the wheat genotypes, whereas 22.2% possessed Lr24/Sr24 and Lr34/Yr18/Pm38/Sr57 gene combination. Two genotypes G16 and G12 were confirmed to have Lr19/Sr25, Lr24/Sr24, Lr34/Yr18/Pm38/Sr57 and Lr24/Sr24, Lr34/Yr18/Pm38/Sr57, Lr46/Yr29/Pm39 gene combinations, respectively. Genetic diversity analysis based on the dissimilarity indices indicated the presence of huge genetic diversity among the wheat germplasm. The presence of Lr24/Sr24 using Sr24#12 marker was confirmed in HS545, which showed monogenic control of leaf rust resistance against pathotype 77–5 (THTTM). Leaf rust and stem rust resistance present in this set of diverse germplasm could be used as potent donors for durable rust resistance breeding in wheat. The molecular markers utilized in this study would also be useful in pyramiding or transferring the R genes into the rust susceptible agronomically superior wheat germplasm. Genotypes G12 and G19 resistant to rusts and also had significant grain yield superiority over HS490 could be a better choice for their use in rust resistance breeding.
Similar content being viewed by others
Availability of data and material
Available.
Code availability
Not applicable.
References
Bansal U, Hayden MJ, Venkata BP, Khanna R, Saini RG, Bariana HS (2008) Genetic mapping of adult plant leaf rust resistance genes Lr48 and Lr49 in common wheat. Theor Appl Genet 17:307–312
Bariana HS, Brown GN, Bansal UK, Miah H, Standen GE, Lu M (2007) Breeding triple rust resistant wheat cultivars for Australia using conventional and marker assisted selection technologies. Australian J Agric Res 58(6):576. https://doi.org/10.1071/ar07124
Bhardwaj SC (2012) Wheat rust pathotypes in Indian sub-continent then and now. Wheat-Productivity enhancement under changing climate (Eds. Singh SS, Hanchinal RR, Singh G, Sharma RK, Saharan MS, Sharma I). Narosa Publishing House Pvt. Ltd.22, Delhi Medical Association Road, Daryaganj, New Delhi 110002, pp 227–238
Bhardwaj SC, Kumar S, Gangwar OP, Prasad P, Kashyap PL, Khan H, Savadi S, Singh GP, Gupta N, Thakur R (2021) Physiologic specialization and genetic differentiation of Puccinia triticina causing leaf rust of wheat in the Indian subcontinent during 2016–2019. Plant Dis. https://doi.org/10.1094/PDIS-06-20-1382-RE
Bhardwaj SC, Prashar M, Kumar S, Jain SK, Datta D (2005) Lr19 resistance in wheat becomes susceptible to Puccinia triticina in India. Plant Dis 89:1360
Bhardwaj SC, Singh GP, Gangwar OP, Prasad P, Kumar S (2019) Status of Wheat Rust Research and Progress in Rust Management-Indian Context. Agronomy 9(12). https://doi.org/10.3390/agronomy9120892
Caldwell RM (1968) Breeding for general and/or specific plant disease resistance. p 263–272. In: KW Finlay and KW Shephard (Eds) Proceedings of the 3rd International Wheat Genetic Symposium, Australian Acedemy of Sciences, Canberra, Australia
Charpe A, Koul S, Gupta SK, Singh A, Pallavi JK, Prabhu KV (2012) Marker assisted gene pyramiding of leaf rust resistance genes Lr9, Lr24 and Lr28 in a bread wheat cultivar HD2329. J Wheat Res 4(1):20–28
Czajowski G, Strzambicka A, Karska K (2011) Virulence in population of Puccinia triticina, the casual agent of wheat and triticale leaf rust in Poland in 2008–2010. Bull Plant Breed ACCLIM Inst 260(261):145–153
Dyck PL (1987) The association of a gene for leaf rust resistance with the chromosome 7D suppressor of stem rust resistance in common wheat. Genome 29:467–469
Dyck PL (1991) Genetics of adult plant leaf rust resistance in Chinese Spring and Sturdy wheat. Crop Sci 31(2):309–311
Ejaz M, Iqbal M, Shahzad A, Atiq-ur-Rehman AI, Ali GM (2012) Genetic variation for markers linked to stem rust resistance genes in Pakistani wheat varieties. Crop Sci 52:2638–2648. https://doi.org/10.2135/cropsci2012.01.0040
Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN (2014) The past, present and future of breeding rust resistant wheat. Front Plant Sci 5:641. https://doi.org/10.3389/fpls.2014.00641
German SE, Kolmer JA (1992) Effect of Gene Lr34 in the Enhancement of Resistance to Leaf Rust of Wheat. Theor Appl Genet 84:97–105
Huerta-Espino J, Singh R, Crespo-Herrera LA, Vilasenor-Mir HE, Rodriguez-Garcia MF, Dreisigacker S, Baroenas-Santana D, Lagudah E (2020) Adult plant slow rusting genes confer high levels of resistance to rusts in bread wheat cultivars from Mexico. Front Plant Sci 11:827. https://doi.org/10.3389/fpls.2020.00824
Huerta-Espino J, Singh RP, German S, McCallum BD, Park RF, Chen WQ, Bhardwaj SC, Goyeau H (2011) Global status of wheat leaf rust caused by Puccinia triticina. Euphytica 179:143–160. https://doi.org/10.1007/S10681-011-0361-x
Kolmer JA, Chen X, Jin Y (2008b) Diseases which challenge global wheat production the wheat rusts. In: BF Carver, Editor Wheat: Science and trade. Wiley-Stemwell, Ames, IA
Kolmer JA, Singh RP, Garvin DF, Viccars L, William HM, Huerta-Espino J, Ogbonnaya FC, Raman H, Orford S, Bariana HS, Lagudah HS (2008a) Analysis of the Lr34/Yr18 rust resistance region in wheat germplasm. Crop Sci 48:1841–1852
Kumar S, Bhardwaj SC, Gangwar OP, Sharma A, Qureshi N, Kumaran VV, Khan H, Prasad P, Miah H, Singh GP, Sharma K, Verma H, Forrest KL, Trethowan RM, Bariana H, Bansal UK (2021) Lr80: A new and widely effective source of leaf rust resistance of wheat for enhancing diversity of resistance among modern cultivars. Theor Appl Genet. https://doi.org/10.1007/s00122-020-03735-5
Lagudah ES, Mc Fadden H, Singh RP, Huerta-Espino J, Bariana HS, Spielmeyer W (2006) Molecular genetic characterization of the Lr34/Yr18 slow rusting resistance gene region in wheat. Theor Appl Genet 114:21–30
Lillemo M, Asalf B, Singh RP, Huerta-Espino J, Chen XM, He ZH, et al (2008) The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theor Appl Genet 116.https://doi.org/10.1007/s00122-008-0743-1
Lillemo M, Joshi AK, Prasad R, Chand R, Singh RP (2013) QTL for spot blotch resistance in bread wheat line Saar co-locate to the biotrophic disease resistance loci Lr34 and Lr46. Theor Appl Genet 126(3):711–719
Liu S, Yu LX, Singh RP, Jin Y, Sorrells ME, Anderson JA (2010) Diagnostic and co-dominant PCR markers for wheat stem rust resistance genes Sr25 and Sr26. Theor Appl Genet 120:691–697
Mago R, Bariana HS, Dundas LS, Speilmeyer W, Lawrence GJ, Pryor AJ, Ellis JG (2005) Development of PCR markers for the selection of wheat stem rust resistance genes Sr24 and Sr26 in diverse wheat germplasm. Theor Appl Genet 111:496–504. https://doi.org/10.1007/s00122-005-2039-z
Martinez F, Niks RE, Singh RP, Rubiales D (2001) Characterization of Lr46, a gene conferring partial resistance to wheat leaf rust. Hereditas 135:111–114
McIntosh RA, Bariana HS, Park RF, Wellings CR (2001) Aspects of wheat rust research in Australia. Euphytica 119:115–120
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: an atlas of resistance genes. CSIRO, Australia
McIntosh RA, Dubcovsky J, Rogers WJ, Morris C, Xia XC (2017) Catalogue of Gene Symbols for Wheat. Supplement. In: KOMUGI–Integrated Wheat Science Database at http://shigen.nig.ac.jp/wheat/komugi/genes/macgene/supplement2017.pdf
Mishra AN, Prakasha TL, Kaushal K, Dubey VG (2014) Validation of Lr24 in some released bread wheat varieties and its implications in leaf rust resistance breeding and deployment in Central India. Indian Phytopathol 67(1):102–103
Mishra AN, Tiwari KN, Singh VK, Sivasamy M, Pal D, Bhardwaj SC, Gangwar OP, Prakasha TL, Solanki KS, Phuke RM, Sai Prasad SV, Mishra CN, Sawashe SG, Narute TK (2021) Insights into the rust resistance base of common wheat (Triticum aestivum L.) in India. Indian Phytopathol 74:537–548
Monneveux P, Reynolds MP, Gonzalez Aguilar J, Singh RP (2003) Effects of the 7DL.7Ag translocation from Lophopyrum elongatum on wheat yield and related morpho-physiological traits under different environments. Plant Breed 122:379–384
Nayar SK, Bhardwaj SC, Prashar M (1999) Characterization of Lr34 and Sr2 in Indian wheat (Triticum aestivum) germplasm. Indian J Agric Sci 69:718–721
Pal D, Bhardwaj SC, Sharma P, Sharma D, Khan H, Harikrishna BHP, Jha SK, Patial M, Chauhan D, Kumari S, Prabhu KV (2020) Molecular marker aided selection for developing rust resistant genotypes by pyramiding Lr19/Sr25 and Yr15 in wheat. Australas Plant Pathol 49:631–640. https://doi.org/10.1007/s13313-020-00739-0
Panse VG, Sukhatme PV (1995) Statistical methods for agricultural workers. ICAR, New Delhi, pp 1–359
Parlevliet J (1975) Partial resistance of barley to leaf rust, Puccinia hordei. I. Effect of cultivar and development stage on latent period. Euphytica 24(1):21–27
Paterson AH, Tanksley SD, Sorrells ME (1991) DNA markers in Plant Improvement. Adv Agron 46:39–90
Perrier X, Jacquemoud-Collet JP (2006) DARwin software: http://darwin.cirad.fr/darwin
Pretorius ZA, Rijkenberg FHJ, Wilcoxson RD (1988) Effects of growth stage, leaf position and temperature on adult-plant resistance of wheat infected by Puccinia recondita f. sp. tritici. Plant Pathol 37:36–44
Pretorius ZA, Singh RP, Wagoire WW, Payne TS (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis. f. sp. tritici in Uganda. Plant Dis 84:203
Prins R, Groenewaid JZ, Marais GF, Snape JW, Koebner RMD (2001) AFLP and STS tagging of Lr19, a gene conferring resistance to leaf rust in wheat. Theor Appl Genet 103:618–624
Randhawa MS, Bains NS, Sohu VS, Chhuneja P, Trethowan RM, Bariana HS, Bansal U (2019) Molecular marker assisted transfer of stripe rust and stem rust resistance genes into four wheat cultivars. Agronomy 9:497. https://doi.org/10.3390/agronomy9090497
Rattu AR, Ahmad I, Fayyaz M, Akhtar MA, Ulhaque I, Zakri M, Afzal SN (2009) Virulence analysis of Puccinia triticina cause of leaf rust of wheat. Pak J Bot 41:1957–1964
Rautela A, Dwivedi M (2018) Wheat stem rust race Ug99: A shifting enemy. Int J Curr Microbiol Appl Sci 7(1):1262–1266
Roelfs AP (1988) Resistance to leaf and stem rusts in wheat. In: Breeding strategies for resistance to the rusts of wheat (Eds Simmonds NW and Raja Ram), CIMMYT, Mexico. pp 10–25
Roelfs AP, Singh RP, Saari EE (1992) Rust diseases of wheat: concepts and methods of disease management. Mexico CIMMYT
Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5:69–76
Samborski DJ (1985) Wheat leaf rust. The Cereal Rusts, pp 39–59. Roelfs AP and Bushnell WR (Eds). Academic Press, New York
Sawhney RN, Nayar SK, Sharma JB, Bedi R (1989) Mechanism of durable resistance: a new approach. Theoret Appl Genet 78:229–232
Sawhney RN, Sharma DN (1990) Identification of sources for rust resistance and for durability to leaf rust in common wheat. SABRAO J 22:51–55
Singh RP (1992) Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Phytopathol 82:835–838
Singh RP (1993) Genetic association of gene Bdv1 for tolerance to Barley Yellow Dwarf Virus with genes Lr34 and Yr18 for adult plant resistance to rusts in bread wheat. Plant Dis 77:1103–1106
Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P (2008) Will stem rust destroy the world’s wheat crop? Advances in Agron 98:271–309
Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Ann Rev Phytopathol 49:465–481
Singh RP, Hong Ma, Huerta J (1994) Rust diseases of wheat, pp 19–33, In: Special Report No. 24. Guide to the CIMMYT wheat crop protection sub-program (Eds: Saari EE and Hettel GP)
Singh RP, Mujeeb-Kazi A, Huerta Espino J (1998) Lr46: A gene conferring slow rusting resistance to leaf rust in wheat. Phytopathol 88:890–894
Skowronska R, Tomkowiak A, Nawracala J, Kwiatek MT (2020) Molecular identification of slow rusting resistance Lr46/Yr29 gene locus in selected triticale (x Triticosecale Wittmack) cultivars. J Appl Genet 61:359–366
Soengas P, Velasco P, Padilla G, Ordas CME (2006) Genetic Relationships Among Brassica napus Crops Based on SSR Markers. Hort Sci 41(5):1195–1199
Somers DJ, Isaac P, Edwards K (2004) A high- density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114
Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust co-segregate at a locus on the short arm of chromosome 7D of wheat. Theor Appl Genet 111:731–735
Stakman EC, Steward DM, Loegering WQ (1962) Identification of physiologic races of Puccinia graminis var. tritici. USDA-ARS Bull. E-167, Washington DC, USDA eds, 1962, pp 53
Tomar SMS, Menon MK (2001) Genes for disease resistance in wheat. pp152. Indian Agricultural Research Institute, New Delhi
Tomar SMS, Singh SK, Sivasamy M, Vinod, (2014) Wheat rusts in India: Resistance breeding and gene deployment – A review. Indian J Genet 74:129–156
Tomkowiak A, Skowronska R, Kwiatek M, Spychala J, Weight D, Kurasiak-Popowska D, Niemann J, Mikolajczyk S, Nawracala J, Kowalczewski P, Khan K (2021) Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR. Open Life Sci 16:172–183
Van der Plank JE (1963) Plant diseases: epidemics and control. Academic Press, New York, p 349
William M, Singh RP, Huerta-Espino J, Ortiz Islas S, Hoisington D (2003) Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in Wheat. Phytopathol 93(2):153–159
Yadav PS, Mishra VK, Arun B, Chand R, Vishwakarma MK, Vasistha NK, Mishra AN, Kalappanavar IK, Joshi AK (2015) Enhanced resistance in wheat against stem rust achieved by marker assisted backcrossing involving three independent Sr genes. Curr Plant Biolol l2:25–33
Yang E-N, Rosewarne GM, Herrera-Foessel SA, Huerta-Espino J, Tang Z-X, Sun C-F et al (2013) QTL analysis of the spring wheat Chapio identifies stable stripe rust resistance despite inter-continental genotype x environment interactions. Theor Appl Genet 126(7):1721–1732. https://doi.org/10.1007/s00122-013-2087-8
Yu LX, Liu S, Anderson JA, Singh RP, Jin Y, Dubcovsky J, Brown-Guidera G, Bhavani S, Morgounov A, He Z, Huerta-Espino J, Sorrells ME (2010) Haplotype diversity of stem rust resistance loci in uncharacterized wheat lines. Mol Breed 26:667–680
Zhang W, Chen S, Abate Z, Nirmala J, Rouse MN, Dubcovsky J (2017) Identification and characterization of Sr13, a tetraploid wheat gene that confers resistance to the Ug99 stem rust race group. Proc Natl Acad Sci USA 114(45):E9483–E9492. https://doi.org/10.1073/pnas.1706277114
Acknowledgements
The authors are grateful to the Director, ICAR- IARI, New Delhi for generous support for conducting this study.
Funding
Indian Council of Agriculture Research (ICAR), New Delhi.
Author information
Authors and Affiliations
Contributions
DP conceived the research idea; SCB did the host pathogen interaction tests; SK, Harikrishna and SKVP did molecular work; NBD carryout diversity analysis; MP helped in data recording; DP and SCB wrote the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent of participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest/Competing interests
The authors declare no conflict of interest.
Supplementary information
Below is the link to the electronic supplementary material.
13313_2022_850_MOESM2_ESM.pptx
Supplementary file2 (PPTX 23218 KB) Fig.S1. Lane M-100bp ladder, 1-36:genotypes; G16, G19, G22, G36 showing amplification of Gb marker for Sr25/Lr19;Lr19 (+ check); AL (– check). Fig. S2. Lane M-100bp ladder, 1-36: genotypes; G1, G2, G3,G4, G5, G6, G8, G9, G10, G11, G12, G16, G17, G20, G21, G24, G34 showingamplification of Sr24#12 marker for Sr24/Lr24; Lr24(+check); AL (– check). Fig. S3. Lane M-100bp ladder, 1-36: genotypes; G1, G3, G4, G6, G7, G8, G9, G10, G11,G12, G16, G32, G33, G34 showing amplification of marker csLV34 for Lr34;Lr34 (+ check); AL (– check). Fig.S4. Lane M-100bp ladder,1-36: genotypes; G2, G10, G12, G15, G19, G21, G29, G30, G31 showingamplification of marker wmc44-1BL for Lr46/Yr29; Lr46(+ check); AL (– check)
Rights and permissions
About this article
Cite this article
Pal, D., Kumar, S., Bhardwaj, S.C. et al. Molecular marker aided characterization of race specific and non-race specific rust resistance genes in elite wheat (Triticum spp.) germplasm. Australasian Plant Pathol. 51, 261–272 (2022). https://doi.org/10.1007/s13313-022-00850-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13313-022-00850-3