Abstract
The production of malting barley under dryland and irrigated environments in South Africa (SA) has increased recently, making it the second most important winter crop after wheat. To assess the potential vulnerability of adapted barleys from SA to wheat stem rust (caused by Puccinia graminis f. sp. tritici, Pgt, race PTKST) and rye stem rust (Puccinia graminis f. sp. secalis, Pgs, isolate UVPgs1), 50 accessions were evaluated as seedlings and as adult plants. The same barley germplasm was tested against Pgt and Pgs cultures from the USA that have proven useful for detecting the stem rust resistance genes Rpg1 and the rpg4/Rpg5 complex. The possible presence of these resistance genes was assayed using molecular markers and sequence analysis. Barley accessions exhibited mostly resistant infection types (ITs) to the South African cultures, whilst field data revealed that several of the barley varieties displayed high severities in combination with more compatible host response types to race PTKST. The barley accessions exhibited mostly high ITs to cultures from the USA. None of the seedling IT data was sufficiently distinct to reliably postulate the presence of possible resistance genes. This result was corroborated from the molecular assays for Rpg1 and rpg4/Rpg5. Except for one line that tested heterozygous for the Rpg1 gene, none of the test entries contained this gene or a functional rpg4/Rpg5 complex due to the prevalence of mutations in the rpg4/Rpg5 + carriers. Susceptibility among barley varieties to wheat stem rust race PTKST under field conditions in the present study is of concern.
Similar content being viewed by others
References
Arora D, Gross T, Brueggeman RS (2013) Allele characterization of genes required for rpg4-mediated wheat stem rust resistance identifies Rpg5 as the R gene. Phytopathology 103:1153–1161
Boshoff WHP, Pretorius ZA, Van Niekerk BD, Komen JS (2002) First report of virulence in Puccinia graminis f. sp. tritici to wheat stem rust resistance genes Sr8b and Sr38 in South Africa. Plant Dis 86:922
Boshoff WHP, Bender CM, Pretorius ZA (2019) Reaction of South African rye, triticale and barley forage cultivars to stem and leaf rust. SA J Plant Soil 36:77–82
Brueggeman RS, Druka A, Nirmala J, Cavileer T, Drader T, Rostoks A, Han F, Sun Y, Gill K, Steffenson BJ, Kleinhofs A (2008) The stem rust resistance gene Rpg5 encodes, a novel protein with nucleotide binding site, leucine-rich and protein kinase domains. Proc Natl Acad Sci USA 105:14970–14975
Case AJ, Bhavani S, Macharia G, Pretorius ZA, Coetzee V, Kloppers FJ, Tyagi P, Brown-Guedira G, Steffenson BJ (2018) Mapping adult plant stem rust resistance in barley accessions Hietpas-5 and GAW-79. Theor Appl Genet 131:2245–2266
Crous PW, Phillips AJL, Baxter AP (2000) Phytopathogenic fungi from South Africa. University of Stellenbosch, Department of Plant Pathology Press, Stellenbosch, p 358
Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu Pietro D, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in Molecular Plant Pathology. Mol Plant Pathol 13:414–430
Derevnina L, Fetch T, Singh D, Brueggeman RS, Dong C, Park RF (2014) Analysis of stem rust resistance in Australian barley cultivars. Plant Dis 98:1485–1493
Dill-Macky R, Rees RG, Platz GJ (1991) Inoculum pressure and the development of stem rust epidemics in barley. Aust J Agric Res 42:769–777
Doyle JJ, Doyle J (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus 12:13–15
Dracatos P, Singh D, Fetch T Jr, Park RF (2015) Resistance to Puccinia graminis f. sp. avenae in barley is associated with the Rpg5 gene. Phytopathology 105:490–494
Du Plessis AJ (1933) The history of small-grains culture in South Africa. Ann Univ Stellenbosch 8:1652–1752
Eckstein P, Rossnagel B, Scoles G (2003) Allele-specific markers within the barley stem rust resistance gene (Rpg1). Barley Gen Newsl 33:7–11
Fox SL, Harder DE (1995) Resistance to stem rust in barley and inheritance of resistance to race QCC. Can J Plant Sci 75:781–788
Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Henningsen EC, Matny O, Szinyei T, Figueroa M, Steffenson BJ (2020) Rpg7: A new gene for stem rust resistance from Hordeum vulgare ssp. spontaneum. Phytopathology First Look. https://doi.org/10.1094/PHYTO-08-20-0325-R
Hodson DP (2011) Shifting boundaries: challenges for rust monitoring. Euphytica 179:93–104
Jin Y, Steffenson BJ, Fetch TG (1994a) Sources of resistance to pathotype QCC of Puccinia graminis f. sp. tritici in barley. Crop Sci 34:285–288
Jin Y, Steffenson BJ, Miller JD (1994b) Inheritance of resistance to pathotypes QCC and MCC of Puccinia graminis f. sp. tritici in barley line Q21861 and temperature effects on the expression of resistance. Phytopathology 84:452–455
Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch TG (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92:923–926
Lehmensiek A, Bester-van der Merwe AE, Sutherland MW, Platz G, Kriel WM, Potgieter GF, Prins R (2010) Population structure of South African and Australian Pyrenophora teres isolates. Plant Pathol 59:504–515
Loughman R, Jayasena K, Majewski J (2005) Yield loss and fungicide control of stem rust in wheat. Aust J Agric Res 56:91–96
Luig NH, Watson IA (1972) The role of wild and cultivated grasses in the hybridization of formae speciales of Puccinia graminis. Aust J Biol Sci 25:335–342
McIntosh RA, Wellings CR, Park RF (1995) Wheat rusts: An atlas of resistance genes. CSIRO, Australia
Mirlohi A, Brueggeman R, Drader T, Nirmala J, Steffenson BJ, Kleinhofs A (2008) Allele sequencing of the barley stem rust resistance gene Rpg1 identifies regions relevant to disease resistance. Phytopathology 98:910–918
Mwando KE, Tabu IM, Otaye OD, Njau PN (2012) Effect of stem rust on the quality of selected barley genotypes. ISRN Agron 2012:1–8
Oliveira P, Newcomb M, Szabo LJ, Rouse M, Johnson J, Gale S, Luster DG, Hodson D, Cox JA, Burgin L, Hort M, Gilligan CA, Patpour M, Justesen AF, Hovmøller MS, Getaneh W, Hailu E, Hundie B, Tadesse K, Pumphrey M, Singh RP, Jin Y (2015) Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in southern Ethiopia in 2013-14. Phytopathology 105:917–928
Park RF (2007) Stem rust of wheat in Australia. Aust J Agric Res 58:558–566
Pretorius ZA, Singh RP, Wagoire WW, Payne TT (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84:203
Pretorius ZA, Pakendorf KW, Marais GF, Prins R, Komen JS (2007) Challenges for sustainable control of cereal rust diseases in South Africa. Aust J Agric Res 58:593–601
Pretorius ZA, Bender CM, Visser B, Terefe T (2010) First report of a Puccinia graminis f. sp. tritici race virulent to the Sr24 and Sr31 wheat stem rust resistance genes in South Africa. Plant Dis 94:784
Pretorius ZA, Bender CM, Visser B (2015) The rusts of wild rye in South Africa. SA J Bot 96:94–98
Roelfs AP (1982) Effects of barberry eradication on stem rust in the United States. Plant Dis 66:177–181
Sallam AH, Tyagi P, Brown-Guedira G, Muehlbauer GJ, Hulse A, Steffenson BJ (2017) Genome-wide association mapping of stem rust resistance in Hordeum vulgare subsp. spontaneum. G3:3491–3507
Sharma Poudel R, Al-Hashel AF, Gross T, Gross P, Brueggeman RS (2018) Pyramiding rpg4- and Rpg1-mediated stem rust resistance in barley requires the Rrr1 gene for both to function. Front Plant Sci 9:1789
Soko T, Bender CM, Prins R, Pretorius ZA (2018) Yield loss associated with different levels of stem rust resistance in bread wheat. Plant Dis 102:2531–2538
Solanki S, Richards J, Ameen G, Wang X, Khan A, Ali H, Stangel A, Tamang P, Gross T, Gross P, Fetch TG, Brueggeman RS (2019) Characterization of genes required for both Rpg1 and rpg4-mediated wheat stem rust resistance in barley. BMC Genom 20:495
Steffenson BJ (1992) Analysis of durable resistance to stem rust in barley. Euphytica 63:153–167
Steffenson BJ, Wilcoxson RD, Roelfs AP (1985) Resistance of barley to Puccinia graminis f. sp. tritici and Puccinia graminis f. sp. secalis. Phytopathology 75:1108–1111
Steffenson BJ, Jin Y, Brueggeman RS, Kleinhofs A, Sun Y (2009) Resistance to stem rust race TTKSK maps to the rpg4/Rpg5 complex of chromosome 5H of barley. Phytopathology 99:1135–1141
Steffenson BJ, Solanki S, Brueggeman RS (2016) Landraces from mountainous regions of Switzerland are sources of important genes for stem rust resistance in barley. Alpine Bot 126:23–33
Steffenson BJ, Case AJ, Pretorius ZA, Coetzee V, Kloppers FJ, Zhou H, Chai Y, Wanyera R, Macharia G, Bhavani S, Grando S (2017) Vulnerability of barley to African pathotypes of Puccinia graminis f. sp. tritici and sources of resistance. Phytopathology 107:950–962
Sun Y, Steffenson BJ (1997) Effect of incubation time and temperature on the phenotypic expression of rpg4 to Puccinia graminis f. sp. tritici in barley. Can J Plant Pathol 19:25–29
Sun Y, Steffenson BJ (2005) Reaction of barley seedlings with different stem rust resistance genes to Puccinia graminis f. sp. tritici and Puccinia graminis f. sp. secalis. Can J Plant Pathol 27:80–89
Sun Y, Steffenson BJ, Jin Y (1996) Genetics of resistance to Puccinia graminis f. sp. secalis in barley line Q21861. Phytopathology 86:1299–1302
Terefe T, Pretorius ZA, Visser B, Boshoff WHP (2019) First Report of Puccinia graminis f. sp. tritici race PTKSK, a variant of wheat stem rust race Ug99 in South Africa. Plant Dis 103:1421
Van Niekerk BD, Pretorius ZA, Boshoff WHP (2001) Occurrence and pathogenicity of Puccinia hordei on barley in South Africa. Plant Dis 85:713–717
Verwoerd L (1931) Die fisiologiese vorms van Puccinia graminis Pers. wat in Suid-Afrika voorkom. SA J Sci 28:274–279
Wang X, Richards J, Gross T, Druka A, Kleinhofs A, Steffenson BJ, Acevedo M, Brueggeman RS (2013) The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene and an actin depolymerisation factor. Mol Plant Micr Int 26:407–418
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421
Acknowledgements
We thank the South African Winter Cereal Trust (WCT/B/2013/01), National Research Foundation (NRF: UID85943, UID96099), and the Lieberman-Okinow Endowment at the University of Minnesota for financial support. The NRF is also thanked for funding the equipment based at the Central Analytical Facilities of Stellenbosch University (UID65258). The South African Barley Breeding Institute is thanked for access to the barley cultivars and advanced breeding lines used in this study. Debbie Snyman, Lizaan Rademeyer, Corneli de Klerk, Kelly Breeds (CenGen), Matthew Martin, Tamas Szinyei (University of Minnesota), Dr Rikus Kloppers, Vicky Coetzee and Ash Babooram (Corteva Agriscience™) are thanked for assistance throughout the study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Prins, R., Steffenson, B.J., Case, A.J. et al. Assessments and perspectives on stem rust resistance in South African malting barley. Australasian Plant Pathol. 49, 679–690 (2020). https://doi.org/10.1007/s13313-020-00744-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13313-020-00744-2