Abstract
Various fungal species continue to be one of the most difficult challenges faced by farmers, and hence societies in whole, when it comes to securing plentiful and wholesome food for a rapidly growing human population. Understanding the biology of pathogenic fungi in detail, both at the population and molecular levels, combined with continued emphasis on resistance breeding of important crops, offers the most obvious sustainable solution to this pressing problem. Here we present results of virulence testing and microsatellite analysis on a collection of Icelandic Rynchosporium commune isolates to test whether the previously demonstrated genetic diversity observed translated into functional diversity in the virulence of these isolates. Our results show considerable diversity in the virulence of the Icelandic R. commune samples with each isolate having a unique virulence spectrum on the 15 near-isogenic barley lines used for screening. Our findings have practical implications, showing that even with short continuous barley cultivation and isolation by geographical distance, breeding for Icelandic, and likely other remote or isolated locations, still needs to consider the importance of disease resistance in breeding decisions and variation in local pathotypes. Moreover, our analysis is the first step to focused breeding for disease resistance for Icelandic conditions, an important step in the ongoing Icelandic barley breeding project.
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Introduction
Cultivated barley (Hordeum vulgare ssp. vulgare) is a diploid annual cereal grain of the family Poaceae and the domesticated form of the wild barley H. vulgare ssp. spontaneum (Stein and Muehlbauer 2018). Barley has been adapted to a great range of climates and daylengths and is cultivated from arid areas of North Africa (Bothmer et al. 1991) to sub-arctic areas near the arctic circle (Hilmarsson et al. 2017). Worldwide in 2017 it ranked fourth of cereal crops for area of cultivation and quantity produced, with 47 million hectares yielding 147 million metric tons, compared to 772 million metric tons of wheat (FAOSTAT 2020).
When Iceland was settled in the ninth century CE the settlers likely brought with them barley from Scandinavia and/or the British Isles (Karlsson 2009). Barley cultivation was then practiced in Iceland for several centuries, but eventually decreased drastically or ceased completely. This most likely happened around the turn of the fourteenth century, possibly due to environmental changes or changes in the price of imported barley (Karlsson 2009) although other sources suggest that changes in population density led to the cessation of barley cultivation in Iceland (Júlíusson 2018). It was not until 1923 that barley was successfully grown in Iceland again for several years in a row. Since 1991 barley production in Iceland has increased considerably, with around 5,000 hectares of land yielding up to 16,000 tons per year, an average yield of 3.2 t/ha (Hilmarsson et al. 2017).
Although several pathogenic fungi have been previously described on barley in Iceland (Hallgrímsson and Eyjolfsdottir 2004; Stefansson and Hallsson 2011), only Rhynchosporium commune (syn. R. graminicola, previously R. secalis), the causal agent of barley scald (Zaffarano et al. 2011), has been suggested as a serious pathogen of economic importance, with reports of up to 36% yield loss and 10–20% average yield loss (Hermannsson 2004).
R. commune, a haploid fungus found in all major barley-growing regions of the world, is a serious disease in cool, semi-humid areas especially where leaves remain wet for long periods (Zhang et al. 1992). Scald symptoms appear as irregular shaped lesions, with the green color of the leave turning chlorotic with brown edges, as the infection develops the lesions can eventually merge. Yield losses are reported to range between 10 and 45% (Avrova and Knogge 2012). Studies on R. commune populations, from different countries, have revealed both genetic and pathogenic variation (Jorgensen and Smedegaard-Petersen 1995; McDermott et al. 1989; McDonald 2015; McDonald et al. 1999; Mohd-Assaad et al. 2018; Salamati et al. 2007; Stefansson et al. 2012, 2013, 2014; Tekauz 1991; Williams et al. 2003; Kequan Xi et al. 2002). Methods used have included virulence tests (Araz and Maden 2006; Kequan Xi et al. 2002), ribosomal DNA (Newton et al. 2001), isozymes (Goodwin et al. 1993), and DNA marker analyses (Bouajila et al. 2007; Kiros-Meles et al. 2005; McDonald et al. 1999). Isolates secured from different scald lesions taken from the same plant or even different spores isolated from the same lesion may vary significantly for virulence and molecular markers (Brown 1985; McDonald et al. 1999). This pathogenic diversity means that R. commune populations can potentially change rapidly in response to selection exerted by the introduction of new resistance genes or fungicides (Zhan et al. 2008) and rapidly render them ineffective (Newton et al. 2001; Oxley et al. 2003; Kegnan Xi et al. 2003).
The source of the genetic diversity in R. commune has been the subject of several studies leading to suggestions including asexual genetic exchange (Forgan et al. 2007; Newman and Owen 1985), frequency-dependent selection (Goodwin et al. 1993; McDermott et al. 1989), spontaneous mutations and migration (Goodwin et al. 1994; Williams et al. 2003), and sexual reproduction (Linde et al. 2003; McDonald et al. 1999; Salamati et al. 2007). Additional factors influencing genetic diversity in R. commune populations could be a large effective population size (McDermott et al. 1989), gene flow within regions by air-borne ascospores (Zhan et al. 2008), and gene flow between regions by seed trade (Zaffarano et al. 2007). Although a teleomorph has not yet been recognized research has shown gametic equilibrium of alleles within populations (Burdon et al. 1994; Salamati et al. 2007), but the degree of equilibrium can be used as an indirect measure of the significance of genetic exchange and recombination in presumably asexual populations (Chen and McDonald 1996; Linde et al. 2003). Linde et al. (2003) studied the frequency of mating type alleles in R. commune populations from six countries and found equal frequencies in most of the populations, suggesting frequency dependent selection consistent with sexual reproduction. Both mating types were frequently found occupying the same lesions or leaf, providing opportunity for isolates of opposite mating types to reproduce sexually (Linde et al. 2003).
Stefansson et al. (2012) have previously shown that Icelandic R. commune isolates are genetically polymorphic and distinct from populations in Scandinavia, but no virulence tests have been carried out with these Icelandic isolates. The aim of this study was to characterize virulence of Icelandic isolates of R. commune, and compare those results to population structure using microsatellite markers. The virulence tests were carried out on a set of near isogenic barley lines with resistance genes for R. commune, with the aim of informing further resistance breeding efforts in Iceland and beyond.
Materials and methods
Fungal isolates
Infected leaves with visual scald symptoms were collected from six locations in Iceland (Fig. 1 and Table 1) as previously described (Stefansson et al. 2012; Stefansson and Hallsson 2011). Each leaf was placed in a paper bag and dried at room temperature for 2–3 days. Leaves were then sterilized in 70% ethanol for 10 s and in 0.5% NaOCl for 90 s, rinsed twice with distilled water and dried on filter paper. Sterilized leaf segments were placed on wheat germ agar (WGA) plates covered with aluminum foil and kept at room temperature in the dark for seven days. Mycelium from the lesions was transferred onto new WGA plates and kept in the dark at room temperature for another 14 days. Pieces of WGA with R. commune culture were transferred to Eppendorf tubes containing 0.75 mL distilled water, the tubes shaken, and contents poured onto WGA plates. When mycelium growth became visible through a microscope, single spore cultures were picked using a wire inoculation loop, dissolved in water, and spread onto new WGA plates and stored for 14 days in the dark at 18 °C. This yielded 39 single spore R. commune isolates (Table 1) that were then used for both microsatellite analysis and greenhouse trials.
For inoculum preparation, conidia were scraped from the agar with a microscope glass and suspended in 10 mL of distilled water. Conidia were counted using a hemocytometer and the concentration adjusted to 1 × 106 conidia per mL.
For fungal DNA extraction, single spore isolates were transferred on to WGA plates and incubated at 16 °C in the dark for 10 to 14 days. Fungal mycelium and spores were scraped off the plates and total DNA extracted using Microbial DNA isolation Kit (MoBio, cat. No. 12224). Fungal species were identified as described by Stefansson and Hallsson (2011).
Plant material and greenhouse trials
Sixteen barley differential lines, consisting of 15 near-isogenic lines (NILs), each with a different resistance allele against R. commune, and the susceptible check ‘Annabell’, a German two rowed spring barley cultivar (Table 2), were used for virulence tests of 14 R. commune isolates (Goodwin et al. 1990; Patil et al. 2002). Two seeds per genotype were sown together with eight or nine genotypes per pot in two replications. Seeds were sown in nutrient supplemented peat and pots placed in the greenhouse at 18–20 °C during the day and 15 °C during the night with a 16 h/8 h photoperiod, with a relative humidity of 60–80%. Two weeks after sowing, at the 2–3 leaf stage, plants were spray inoculated with a homogenized conidial suspension using 0.4 mL per genotype and 3.2 mL per pot. After inoculation, the pots were kept in closed plastic bags for 48 h, with a relative humidity of 100%. Subsequently the bags were opened and water sprayed three times per week. Leaf symptoms were scored on the second leaf 21 days after inoculation using the 0–4 scale of Jackson and Webster (1976), with 0: no symptoms, 1–2: very small to small lesions within leaf margin, 3: large coalescing lesions, 4: collapse of leaf. Virulence patterns on a susceptible reaction (score ≥ 2.5) were used to group isolates as pathotypes with a method adapted from Tekauz (1991). Dendrograms showing the clustering of both barley varieties and fungal isolates were rendered in ClustVis (Metsalu and Vilo 2015) using Euclidean distance and average linkage.
Rhynchosporium commune microsatellite analysis
Thirty-seven of the 39 R. commune isolates were analyzed with 14 polymorphic microsatellite markers (Linde et al. 2005) as previously described (Stefansson et al. 2012). Due to a low recovery rate for SSR marker Rhyncho_14 in the Icelandic population it was omitted from further analysis. For comparison to the Icelandic isolates, isolates from Norway, Sweden, Finland, and Switzerland were used (for details see Stefansson et al. 2012 and references therein). Genetic distances between both individual isolates and groups were calculated using GenAlEx 6.5 (Peakall and Smouse 2005, 2012) using the ‘Haploid-SSR’ option under “Genetic Distance”. A Principal Coordinates Analysis (PCoA) was then used to visualize the results using the ‘Covariance-Standardized’ option. Two samples used in the virulence testing (SB1 and MO25) failed in microsatellite typing and could therefore not be included in the genetic analysis.
Results
Virulence and population structure of Icelandic R. commune isolates
The susceptibility of the barley genotypes ranged from an average score of 0.1 for genotypes MacKey5 and MacKey10 to an average score of 3.7 for ‘Annabell’. All genotypes were susceptible (max score ≥ 2.5; dotted line in Fig. 1A) to at least one isolate except genotypes ‘MacKey5’, ‘MacKey9’, and ‘MacKey10’. All genotypes were resistant (min score ≤ 2) to at least one isolate except genotypes MacKey13 and ‘Annabell’ (Fig. 1A). Ten genotypes were considered resistant (average score ≤ 2) to the Icelandic R. commune isolates and six genotypes were considered susceptible.
The virulence spectrum of each of the R. commune isolates was unique, however, the average virulence only ranged from 1.2 for the isolate SA12 to 2.1 for the isolate VH12. Each isolate was both completely virulent and non-virulent on genotypes of the differential set. Different virulence patterns on a susceptible reaction (score ≥ 2.5) were used to group isolates as pathotypes resulting in eleven pathotypes, with isolates KO12, MO25 and SB1, and isolates KO24 and VH55 grouping together.
Hierarchical clustering separated R. commune isolates into three groups based on their virulence pattern (Fig. 1A). Group 1 (blue) comprised four isolates from three regions (Hofstaðir, Vindheimar, and Korpa). The second group (green) comprised only a single isolate from Stóra-Ármót (SA23). Group three (red) comprised the remaining nine isolates from three locations. Group three was the least virulent group of isolates with a mean virulence score of 1.6 across all NILs, although the other two groups had only slightly higher average virulence scores of 2.0 (Fig. 1A). Group one was more virulent on lines MacKey4, MacKey6 and MacKey7 (score 2.9) compared to groups two and three with mean scores of 1.5 and 0.2, respectively.
Analysis of genetic and geographical distances between the isolates tested did not reveal a separation between individuals in the three different virulence clusters (Fig. 1B).
Discussion
The fifteen NILs for differentiating R. commune isolates date back to 1977, when James MacKey started crossing 23 barley donor lines with partly known genes for scald resistance with the cultivar ‘Ingrid’ as a recurrent parent (Bjørnstad et al. 2002; Patil et al. 2002). Patil et al. (2002) screened nine of the 23 NILs along with their recurrent parent and donor lines with two fungal isolates (‘4004’ and ‘2’). Three NILs in this study where resistant (R) against both the isolates used by Patil et al. (2002) and all 14 Icelandic isolates: MacKey5, MacKey9 and MacKey10, which are NILs of the donor lines ‘La Mesita’, ‘Atlas 46’, and ‘Hispont’, respectively. It is interesting to note, that the resistance in these three lines, is based on different resistance genes, namely Rh4 and Rh10 in MacKey5, Rh2 and Rh3 in MacKey9 and an unknown resistance gene in MacKey10 (Table 2). MacKey2 was R against ten Icelandic isolates, moderately resistant (MR) against one, and moderately susceptible (MS) against three, and showed MR against ‘4004’ and R against isolate ‘2’. NILs of ‘Modoc’ exhibited MR and R reactions against isolates ‘4004’ and ‘2’, respectively, with MacKey3, the corresponding line in the present study, R against eight isolates, MR against six isolates, and MS against one isolate. MacKey4 was R and MS to susceptible (S) against 9 and 5 Icelandic isolates, MR against ‘4004’ and MR-MS against ‘2’. MacKey6 was R against isolate ‘4004’ and ten Icelandic isolates and S towards isolate ‘2’ and four Icelandic isolates. NILs of ‘Brier’ and corresponding line MacKey7 were resistant towards ‘4004’ and ten Icelandic isolates, MR towards one Icelandic isolate and MS-S towards isolate ‘2’ and three Icelandic isolates. NILs of ‘Abyssinian’ and respective line MacKey8 were R towards isolate ‘2’ and six Icelandic isolates, MR towards ‘4004’ and seven Icelandic isolates, and MS towards one Icelandic isolate.
Hierarchical clustering grouped the Icelandic R. commune isolates into three groups, with groups 2 and 3 closely connected. Isolates belonging to group 1 were collected at locations in the North (Hofstaðir and Vindheimar) and the West (Korpa). No clear connections between location and pathotype can be seen in such a small sample, with four isolates in group 3 being collected at locations in the Northern, Western, and Southern parts of Iceland. Among the 14 R. commune isolates eleven pathotypes were identified. Isolates KO12 (group 3), MO25 (group 3) and SB1 (group 3) belonged to the same pathotype but were collected at different locations. Korpa (KO12) and Efri-Brúnavellir (SB1) in the western part of Iceland are about 80 km apart. Möðruvellir (MO25) is in the North and about 300 and 350 km from Efri-Brúnavellir and Korpa, respectively. Isolates KO24 and VH55 belonged to the same pathotypes and the same group (group 1). Korpa (KO24) and Vindheimar (VH55) are located about 200 km apart. Compared to the number of isolates, a very high number of pathotypes was detected. It shows that even when isolates were collected from the same regions or even within the same fields (see isolates from Korpa) they show a high variability in their pathogenicity. However, the same pathotypes can also occur at regions located far part from, concurrent with previous studies. For example, Tekauz (1991) tested 111 isolates from five locations in Canada on a set of 14 barley differentials and identified 45 different pathotypes. With ‘CAN 1’, the most common pathotype, found in all five regions. Xi et al. (2002) collected 256 isolates from nine locations in Alberta, Canada, and identified 52 pathotypes, many of which were comprised of only one isolate. RFLP analysis with 265 Australian isolates from five locations revealed 214 distinct genotypes (McDonald et al. 1999). The same study was able to show that R. commune populations are highly variable, and most of the genetic variation is found within fields, which supports the findings in the present study. Considering the low total number of isolates tested here this study should not be considered a final word in the analysis of pathogenicity and diversity of scald in Iceland, rather a first step to better understanding a complex population structure dictated by various genetic and environmental factors, such as sexual reproduction, climate change, fluctuating weather conditions, and flow of genetic variation from outside of Iceland. Even considering the short-comings of the study presented her the practical implications of our findings are that even with short continuous barley cultivation and isolation by geographical distance, breeding for remote locations, still needs to consider the importance of disease resistance and possible differences in pathotypes in localized breeding projects. Also, here we take the first steps to identify relevant resistance alleles that could be of use under Icelandic conditions, an important step in the ongoing Icelandic barley breeding project. Based on our analysis a good starting point would be to take a closer look at the resistance alleles found in the MacKey 3, MacKey 5, MacKey 9, and MacKey 10 NILs, as they show a broad resistance to all the Icelandic isolates tested here.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Araz A, Maden S (2006) Pathogenic Variation among Isolates of Rhynchosporium secalis from Cultivated Barley Growing in Central Anatolia. Turkey Plant Pathol J 5(2):244–247
Avrova A, Knogge W (2012) Rhynchosporium commune: A persistent threat to barley cultivation. Mol Plant Pathol 13(9):986–997. https://doi.org/10.1111/j.1364-3703.2012.00811.x
Bjørnstad Å, Patil V, Tekauz A, Marøy AG, Skinnes H, Jensen A et al (2002) Resistance to Scald (Rhynchosporium secalis) in Barley (Hordeum vulgare) Studied by Near-Isogenic Lines: I Markers and Differential Isolates. Phytopathology 92(7):710–720. https://doi.org/10.1094/phyto.2002.92.7.710
Bothmer R von, International Board for Plant Genetic Resources N, Baden C, Joergensen RB, Linde-Laursen I (1991) An Ecogeographical study of the genus Hordeum. Systematic and Ecogeographic Studies on Crop Genepools (IBPGR). IBPGR.
Bouajila A, Abang MM, Haouas S, Udupa S, Rezgui S, Baum M, Yahyaoui AH (2007) Genetic diversity of Rhynchosporium secalis in Tunisia as revealed by pathotype, AFLP, and microsatellite analyses. Mycopathologia 163(5):281–294. https://doi.org/10.1007/s11046-007-9012-0
Brown JS (1985) Pathogenic variation among isolates of Rhynchosporium secalis from cultivated barley growing in Victoria. Australia Euphytica 34(1):129–133. https://doi.org/10.1007/BF00022872
Burdon JJ, Abbott D, Brown A, Brown J (1994) Genetic structure of the scald pathogen (Rhynchosporium secalis) in South East Australia: implications for control strategies. Aust J Agric Res 45:1445–1454
Chen RS, McDonald BA (1996) Sexual Reproduction Plays a Major Role in the Genetic Structure of Populations of the Fungus Mycosphaerella Graminicola. Genetics 142(4):1119–1127. https://doi.org/10.1093/genetics/142.4.1119
FAOSTAT (2020) http://www.fao.org/faostat/en/#home. Accessed 31 January 2020
Forgan AH, Knogge W, Anderson PA (2007) Asexual Genetic Exchange in the Barley Pathogen Rhynchosporium secalis. Phytopathology 97(5):650–654. https://doi.org/10.1094/phyto-97-5-0650
Goodwin SB, Allard RW, Webster R (1990) A Nomenclature for Rhynchosporium secalis Pathotypes. Phytopathology. https://doi.org/10.1094/phyto-80-1330
Goodwin SB, Saghai-Maroof M, Allard RW, Webster R (1993) Isozyme variation within and among populations of Rhynchosporium secalis in Europe, Australia and the United States. Mycol Res 97(1):49–58. https://doi.org/10.1016/S0953-7562(09)81112-X
Goodwin SB, Webster R, Allard RW (1994) Evidence for Mutation and Migration as Sources of Genetic Variation in Populations of Rhynchosporium secalis. Phytopathology. https://doi.org/10.1094/phyto-84-1047
Hallgrímsson H, Eyjolfsdottir G (2004) Íslenskt sveppatal. Checklist of Icelandic fungi. 1, Microfungi. The Icelandic Institute Natl History 45
Hermannsson J (2004) Sjúkdómar í byggi (in Icelandic). In Fræðaþing Landbúnaðarins (pp. 178–184). Reykjavik, Iceland: BÍ/LbhÍ
Hilmarsson HS, Göransson M, Lillemo M, Kristjánsdóttir ÞA, Hermannsson J, Hallsson JH (2017) An overview of barley breeding and variety trials in Iceland in 1987–2014. Icelandic Agric Sci 30, 13–28. https://doi.org/10.16886/ias.2017.02
Jackson LF, Webster RK (1976) Race differentiation, distribution, and frequency of Rhynchosporium secalis in California. Phytopathology 66:719–725
Jorgensen H, Smedegaard-Petersen V (1995) Pathogenic variation of Rhynchosporium secalis in Denmark and sources of resistance in barley. Plant Dis 79:297–301
Júlíusson AD (2018) Af hverju strái : saga af byggð, grasi og bændum 1300–1700. (Háskólaútgáfan, Ed.)
Karlsson G (2009) Handbók í íslenskri miðaldasögu: Lífsbjörg íslendinga frá 10. öld til 16. aldar, 1st edn. University of Iceland Press, Reykjavík, Iceland
Kiros-Meles A, Udupa S, Abang MM, Abu-Blan H, Baum M, Ceccarelli S, Yahyaoui AH (2005) Amplified fragment length polymorphism among Rhynchosporium secalis isolates collected from a single barley field in Syria. Ann Appl Biol 146(3):389–394. https://doi.org/10.1111/j.1744-7348.2005.040139.x
Linde CC, Zala M, Ceccarelli S, McDonald BA (2003) Further evidence for sexual reproduction in Rhynchosporium secalis based on distribution and frequency of mating-type alleles. Fungal Genet Biol 40(2):115–125. https://doi.org/10.1016/S1087-1845(03)00110-5
Linde CC, Zala M, McDonald BA (2005) Isolation and characterization of microsatellite loci from the barley scald pathogen Rhynchosporium Secalis. Mole Ecol Notes 5(3):546–548. https://doi.org/10.1111/j.1471-8286.2005.00983.x
McDermott JM, McDonald BA, Allard RW, Webster R (1989) Genetic variability for pathogenicity, isozyme, ribosomal DNA and colony color variants in populations of Rhynchosporium secalis. Genetics 122(3):561–565
McDonald BA (2015) How can research on pathogen population biology suggest disease management strategies? The example of barley scald (Rhynchosporium commune). Plant Pathol 64(5):1005–1013. https://doi.org/10.1111/ppa.12415
McDonald BA, Zhan J, Burdon JJ (1999) Genetic Structure of Rhynchosporium secalis in Australia. Phytopathology 89(8):639–645. https://doi.org/10.1094/phyto.1999.89.8.639
Metsalu T, Vilo J (2015) ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res 43(W1):W566–W570. https://doi.org/10.1093/nar/gkv468
Mohd-Assaad N, McDonald BA, Croll D (2018) Genome-wide detection of genes under positive selection in worldwide populations of the barley scald pathogen. Genome Biol Evol 10(5):1315–1332. https://doi.org/10.1093/gbe/evy087
Newman PL, Owen H (1985) Evidence of asexual recombination in Rhynchosporium secalis. Plant Pathol 34(3):338–340. https://doi.org/10.1111/j.1365-3059.1985.tb01370.x
Newton AC, Searle J, Guy DC, Hackett CA, Cooke DEL (2001) Variability in pathotype, aggressiveness, RAPD profile, and rDNA ITS1 sequences of UK isolates of Rhynchosporium secalis. J Plant Dis Prot 108(5):446–458
Oxley S, Cooke L, Black L, Huner A, Mercer P (2003)Project Report 315 Management of Rhynchosporium in different barley varieties and cropping systems London
Patil V, Bjørnstad Å, Magnus H, Mac Key J (2002) Resistance to scald (Rhynchosporium secalis) in barley (Hordeum vulgare L.). II Diallel Analysis of near-Isogenic Lines. Hereditas 137:186–197
Peakall R, Smouse PE (2005) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research--an update. Bioinformatics (Oxford, England), 28(19), 2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Salamati S, Zhan J, Burdon JJ, McDonald BA (2007) The Genetic Structure of Field Populations of Rhynchosporium secalis from Three Continents Suggests Moderate Gene Flow and Regular Recombination. Phytopathology 90(8):901–908. https://doi.org/10.1094/phyto.2000.90.8.901
Stefansson TS, Hallsson JH (2011) Analysis of the species diversity of leaf pathogens in Icelandic barley fields. Icel Agric Sci 24:13–23
Stefansson TS, McDonald B, Willi Y (2013) Local adaptation and evolutionary potential along a temperature gradient in the fungal pathogen Rhynchosporium commune. Evol Appl 6(3):524–534. https://doi.org/10.1111/eva.12039
Stefansson TS, Serenius M, Hallsson J (2012) The genetic diversity of Icelandic populations of two barley leaf pathogens, Rhynchosporium commune and Pyrenophora teres. Eur J Plant Pathol 134(1):167–180. https://doi.org/10.1007/s10658-012-9974-8
Stefansson TS, Willi Y, Croll D, McDonald BA (2014) An assay for quantitative virulence in Rhynchosporium commune reveals an association between effector genotype and virulence. Plant Pathol 63(2):405–414. https://doi.org/10.1111/ppa.12111
Stein N, Muehlbauer FJ (2018) Compendium of Plant Genomes The Barley Genome. (N. Stein and F. J. Muehlbauer, Eds.)Compendium of Plant Genomes: The Barley Genome. Springer. 167/3/869
Tekauz A (1991) Pathogenic variation in Rhynchosporium secalis on barley in Canada. Can J Plant Path 13(4):298–304 https://doi.org/10.1080/07060669109500915
Williams K, Donnellan S, Smyl C, Scott L, Wallwork H (2003) Molecular variation in Rhynchosporium secalis isolates obtained from hotspots. Australas Plant Pathol 32(2):257–262. https://doi.org/10.1071/AP03008
Xi K, Turkington TK, Meadus J, Helm JH, Tewari J (2003) Dynamics of Rhynchosporium secalis pathotypes in relation to barley cultivar resistance. Mycol Res 107(12):1485–1492. https://doi.org/10.1017/S0953756203008748
Xi K, Turkington TK, Helm JH, Bos C (2002) Pathogenic variation of Rhynchosporium secalis in Alberta. Can J Plant Path 24(2):176–183 https://doi.org/10.1080/07060660309506993
Zaffarano PL, McDonald BA, Linde CC (2011) Two new species of Rhynchosporium. Mycologia 103(1):195–202. https://doi.org/10.3852/10-119
Zaffarano PL, McDonald BA, Zala M, Linde CC (2007) Global Hierarchical Gene Diversity Analysis Suggests the Fertile Crescent Is Not the Center of Origin of the Barley Scald Pathogen Rhynchosporium secalis. Phytopathology 96(9):941–950. https://doi.org/10.1094/phyto-96-0941
Zhan J, Fitt BDL, Pinnschmidt HO, Oxley S, Newton AC (2008) Resistance, epidemiology and sustainable management of Rhynchosporium secalis populations on barley. Plant Pathol 57(1):1–14. https://doi.org/10.1111/j.1365-3059.2007.01691.x
Zhang Q, Webster R, Crandall B, Jackson L, Saghai-Maroof M (1992) Race composition and pathogenicity associations of Rhynchosporium secalis in California. Phytopathology 82:798–803
Acknowledgements
The authors would like to thank farmers around Iceland for assistance with sample collection. We would also like to thank the Icelandic Agricultural Productivity Fund for funding.
Funding
Open access funding provided by Swedish University of Agricultural Sciences. The project was partly funded by the Icelandic Agricultural Productivity Fund.
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Novakazi, F., Göransson, M., Stefánsson, T.S. et al. Virulence of Rhynchosporium commune isolates collected in Iceland. J Plant Pathol 103, 935–942 (2021). https://doi.org/10.1007/s42161-021-00888-0
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DOI: https://doi.org/10.1007/s42161-021-00888-0