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Recommended allele symbols for leaf rust resistance genes in barley J.D. Franckowiak1, Y. Jin2, and B.J. SteffensonDepartment of Plant Sciences 3 Department of Plant Pathology North Dakota State University, Fargo, ND 58105, USA 2 Plant Science Department South Dakota State University, Brookings, SD 57007, USA. Several additional examples of alleles at the same locus in barley (Hordeum vulgare L.) producing different reactions to a series of Puccinia hordei Otth isolates have been reported recently (Chicaiza et al., 1996; Jin et al., 1996). Because allelism information is important when new resistance genes are utilized, revision of symbols assigned to leaf rust resistance genes is proposed to reflect allelic differences. Symbols for barley genes controlling response to leaf rust were first recommended by Roane and Starling (1967). A series of genes, Pa1 to Pa5, were shown to be at different loci and confer different reactions to race 4 isolate 57-19 of P. anomala Rostr. (Levine and Cherewick, 1952; Roane and Starling, 1967). Based on the report of the Barley Genetics Committee to the Eighth American Barley Research Workers Conference (Ramage, 1972) and the name change for the leaf rust pathogen from P. anomala to P. hordei, Moseman (1972) suggested that the gene symbols be changed to Rph1 to Rph5. Since then, ten additional genes, Rph6 to Rph15, have been demonstrated to be non-allelic to previously identified genes for reaction to P. hordei (Chicaiza et al., 1996; Jin et al., 1996; Jrgensen, 1993). Allele symbols starting with the letter a were added to the Rph symbols by Roane (1976) when Barley Genetic Stock (BGS) descriptions of leaf rust resistance genes were published. If a second cultivar was shown to have an allele at the same locus, the same gene symbol was recommended for both cultivars. Since only one isolate of P. hordei was used in some studies on the genetics of leaf rust resistance, the existence of different Rph genes at the same locus could not be demonstrated in those studies. Henderson (1945), Jin et al. (1996), Roane (1962), and Starling (1956) reported that leaf rust resistance genes in several cultivars are alleles at the Rph2 locus. The inheritance studies indicated that some cultivars with the Rph2 gene have one gene for resistance and others have two. When collections of the pathogen were evaluated, some cultivars with the Rph2 gene reacted differently to the isolates (Moseman and Roane, 1959; Moseman and Greeley, 1965). Unpublished data from the International Barley Disease Nursery, from 1956 to 1971, show a similar pattern of infection response variability over cultivars having the Rph2 gene. Reinhold and Sharp (1982) evaluated isolates of P. hordei from North America, North Africa, and the Middle East on a series of barley cultivars. They demonstrated that several cultivars with the Rph2 gene reacted differently to one or more of the isolates. Based on their results, they suggested that an allelic series exists at the Rph2 locus. Steffenson and Jin (1997), Tan (1977b), Walther and Lehmann (1980), and Yahyaoui and Sharp (1987) reported similar results and noted the variable response of cultivars with a resistance gene at the Rph2 locus to P. hordei isolates. Jin et al. (1996) and Chicaiza et al. (1996) recently reported new alleles at the Rph2 and Rph7 loci, respectively. To avoid confusion, cultivars with different alleles at an Rph locus should have different allele symbols. Barley researchers often use the nomenclature outlined in volume 2 of the Barley Genetics Newsletter (Ramage, 1972) as a guide for new gene symbol recommendations. Utilization of permanent allele symbols is the suggested solution for identifying alleles at the same locus. Based on that proposal, demonstrating that two resistance genes react differently to one or more isolates of P. hordei justifies the assignment of a different allele symbol to each gene. Ramage (1972) recommended that the first gene in the grouping of phenotypically similar genes be assigned the letter a; the second, the letter b; and so on. After z is used, the next Rph gene would be assigned the permanent code letters aa, the next ab, etc. Since leaf rust is an important barley disease in many areas of the world, the same Rph gene could be present in accessions from different regions. This has been demonstrated for the Rph1 and Rph4 loci (Henderson, 1945; Roane, 1962; and Roane and Starling, 1970). They reported that two or more cultivars exhibited the same infection response pattern to several P. hordei isolates. Assigning both locus and allele symbols to an Rph gene requires evidence that 1) the resistance is conferred by a single gene, 2) the gene confers a unique infection response pattern compared to other 'known' genes, and 3) allelism tests with potential alleles are negative and/or the gene maps to a unique location. The last requirement is not necessary prior to assignment of an incomplete gene symbol, or only an allele symbol, to an Rph gene. To aid in understanding the Rph gene symbols, we placed a period between the locus and allele portions of the gene symbol. Based on the symbols recommended by Roane and Starling (1967) and Roane (1976), the first Rph gene is assigned the symbol Rph1.a and is associated with a DNA segment in the cultivar

Oderbrucker. The second Rph gene would be Rph2.b, but choosing the type cultivar for the Rph2 locus was a problem. Since Peruvian was the key cultivar in the allelism tests conducted by Starling (1956) and has only one Rph gene, we recommend that the gene symbol Rph2.b be assigned to the Rph gene in this cultivar. Allele symbols a and b in the Rph series of genes will be associated always with the genes from Oderbrucker and Peruvian, respectively. Since Batna and Peruvian have been demonstrated to react differently to some isolates of P. hordei (Moseman and Roane, 1959), the allele symbol b should not be used for both cultivars. The next available allele symbol in the Rph series is j; thus, the gene symbol Rph2.j is suggested for the Rph gene in Batna (Table 1). These procedures were used to recommend new gene symbols for the Rph2 alleles in Weider, Juliaca, Kwan, and Chilean D (Table 1). A list of Rph genes, which are different from each other based on literature reports, has been assembled and permanent allele symbols are allocated to Rph genes from specific cultivars (Table 1). Naming alleles at the Rph2 locus is problem because several cultivars, which were reported to have an Rph2 allele, have a second gene for response to P. hordei (Roane, 1962; Roane and Starling, 1967; Starling, 1956; Zloten, 1952). Since the Rph2 allele in these cultivars has not been isolated in a single line, its response pattern to P. hordei isolates has not been determined. Because original cultivars confer resistance to only a limited number of P. hordei isolates and may not be reevaluated in the future, Rph2 gene symbols are suggested for only five of the previously identified cultivars in this group, Quinn, Bolivia, Ricardo, Reka 1, and Ariana (Table 1). The different geographical origins of these cultivars (Table 2) and the large number of alleles at the Rph2 locus indicate that different Rph2 alleles may exist in these cultivars. If one of these Rph2 alleles is proven to be identical to another named Rph2 allele, its gene symbol would be available for reassignment to another Rph2 allele within this group of two gene cultivars. Jin and Steffenson (1994) and Jin et al. (1995) identified accessions of cultivated and wild barley (H. vulgare subsp. spontaneum) that showed a resistant reaction to isolates of P. hordei that are virulent to all previously reported sources of Rph genes. Several of the accessions possess only one leaf rust resistance gene, and that gene confers a different resistance pattern than any other previously reported Rph gene. Based on these studies, new gene symbols could be assigned to a few genes. However, a complete symbol for the Rph gene in PI 235186 could not be assigned because allelism tests were not completed. Thus, the incomplete gene symbol Rph.v is suggested (Table 1). Yahyaoui et al. (1988) collected land races of barley in Tunisia and demonstrated that three cultivars have Rph genes that differ from those previously identified. Manisterski and Anikster (1995) identified two Rph genes in H. vulgare subsp. spontaneum, which confer resistance to P. hordei isolates virulent on all cultivars having named Rph genes. If resistance is shown to be controlled by only one gene or if a line containing a single gene is developed, the new Rph gene in each of these accessions or its derived line could be assigned an incomplete gene symbol starting with Rph.ae. Table 1. Recommended locus and allele symbols for genes conferring resistance to Puccinia hordei in barley (Hordeum vulgare) and information on seed sources and references. Recom. gene symbol Rph1.a Rph2.b Rph3.c Rph4.d Rph5.e + Rph2.q+ Rph5.e Rph6.f + Rph2.r+ Rph7.g Cultivar or pedigree Oderbrucker Peruvian Estate Gold (Gull) Quinn Magnif 102 Bolivia Cebada Capa USDA-ARS References accession number CIho 940 CIho 935 PI 57700 CIho 1145 PI 39401 CIho 13806 PI 36360 PI 53911 Henderson, 1945; Waterhouse, 1948 Levine and Cherewick, 1952; Starling, 1956; Steffenson and Jin, 1997 Henderson, 1945; Roane and Starling, 1967 Moseman and Reid, 1961; Roane, 1962 Roane and Starling, 1967; Starling, 1956 Frecha, 1970; Yahyaoui and Sharp, 1987 Henderson, 1945; Roane and Starling, 1967; Starling, 1956 Johnson, 1968; Nover and Lehmann, 1974; Parlevliet, 1976; Starling, 1956

Rph8.h Rph9.i Rph2.j Rph2.k Rph2.l Rph2.m Rph2.n Rph10.o Rph11.p Rph2.s+ Rph2.t+ Rph2.u+ Rph.v Rph3.w Rph13.x Rph2.y Rph12.z Rph3.aa Rph14.ab Rph7.ac Rph15.ad
Egypt 4 Hor 2596 Batna Weider (No. 22) Juliaca Kwan Chilean D Clipper BC8 Clipper BC67 Ricardo Reka 1 Ariana Beni Olid Bowman*4/PI 466324 Berac*3/HS2986 HJ198*3/HS2310 Triumph PC249A PI 531901-1 Bowman*4/Tu 17 Bowman*4/PI 355447
CIho 6481 CIho 1243 CIho 3391 PI 39398 PI 39151 PI 39367 PI 48136 T39-3 T38-26 PI 45492 CIho 5051 CIho 14081 PI 235186 PI 466324 PI 531849 PI 531841 PI 268180 PI 584765 PI 584760 Tu 17a PI 355447
Levine and Cherewick, 1952; Tan, 1977a Clifford and Udeogalanya, 1976; Tan, 1977a Reinhold and Sharp, 1982; Starling, 1956; Steffenson and Jin, 1997 Henderson, 1945; Sharp and Reinhold, 1982; Watson and Butler, 1947; Steffenson and Jin, 1997 Levine and Cherewick, 1952; Starling, 1956 Henderson, 1945; Zloten, 1952; Steffenson and Jin, 1997 Levine and Cherewick, 1952; Tan, 1977b Feuerstein et al., 1990 Feuerstein et al., 1990 Henderson, 1945; Moseman and Roane, 1959; Zloten, 1952 Levine and Cherewick, 1952; Starling, 1956; Moseman and Greeley, 1965 Sharp and Reinhold, 1982; Zloten, 1952 Jin and Steffenson, 1994 Jin and Steffenson, 1994; Chiciaza et al., 1996 Jin and Steffenson, 1994; Jin et al., 1996 Jin et al., 1995; Jin et al. 1996 Walther, 1987; Jin et al., 1993 Jin (unpublished). Jin et al., 1996 Chicaiza et al., 1996 Chicaiza et al., 1996
Tentative allele symbols are recommended for the Rph2 allele in these cultivars even though their Rph2 allele has not been studied in lines with only one Rph gene.
Table 2. Recommended and previous gene symbols for genes conferring resistance to Puccinia hordei in barley (Hordeum vulgare) and the accession numbers for seed stocks containing Rph genes. Gene symbol Recom. Rph1.a Rph2.b Rph3.c Rph4.d Rph5.e + Rph2.q Rph5.e Previous Rph1a Rph2b Rph3c Rph4d Oderbrucker Peruvian Estate Gold (Gull) Cultivar or pedigree USDA-ARS number Recom. CIho 940 CIho 935 PI 57700 CIho 1145 PI 39401 CIho 13806 Other Manchuria Peru CIho 3410 Egypt Sweden CIho 1024 Australia Argentina Cultivar origin or wild barley

Rph5e + Quinn Rph2 Rph5e Magnif 102
Rph6.f + Rph2.r+ Rph7.g Rph8.h Rph9.i Rph2.j Rph2.k Rph2.l Rph2.m Rph2.n Rph10.o Rph11.p Rph2.s Rph2.t
Rph6f + Bolivia Rph2 Rph5e Rph8 Rph9 Rph2b Rph2b Rph2b Rph2b Rph2b Rph10 Rph11 Rph2b Rph2b Rph2b Cebada Capa Egypt 4 Hor 2596 Batna Weider (No. 22) Juliaca Kwan Chilean D Clipper BC8 Clipper BC67 Ricardo Reka 1 Ariana Beni Olid Bowman*4/PI 466324 Berac*3/HS2986 HJ198*3/HS2310 Triumph PC249A PI 531901-1 Bowman*5/Tu 17 Bowman*4/PI 355447
PI 36360 PI 53911 CIho 6481 CIho 1243 CIho 3391 PI 39398 PI 39151 PI 39367 PI 48136 T39-3 T38-26 PI 45492 CIho 5051 CIho 14081 PI 235186 PI 466324 PI 531849 PI 531841 PI 268180 PI 584765 PI 584760 Tu 17a PI 355447
CIho 1257 North Africa CIho 6193 North Africa Egypt Ethiopia Algeria CIho 1021 Australia CIho 1114 Peru CIho 1016 India CIho 1433 Australia H. spontaneum H. spontaneum CIho 6306 Uruguay Australia CIho 2524 Tunisia CIho 10506 Libya H. spontaneum H. spontaneum H. spontaneum H. spontaneum CIMMYT sel. PI 531901 Egypt Tunisia 17 Tunisia H. spontaneum

Rph2.u Rph.v

Rph3.w Rph13.x Rph2.y Rph12.z Rph3.aa Rph14.ab Rph7.ac Rph15.ad
Tentative allele symbols are recommended for the Rph2 allele in these cultivars even though their Rph2 allele has not been studied in lines with only one Rph gene. References: Chicaiza, O., J.D. Franckowiak, and B.J. Steffenson. 1996. New sources of resistance to leaf rust in barley. pp. 706-708. In A.E. Slinkard, G.J. Scoles, and B.G. Rossnagel (eds.) Proc. Fifth Int. Oat Conf. & Seventh Int. Barley Genet. Symp., Saskatoon. Univ. of Saskatchewan, Saskatoon. Clifford, B.C., and A.C. Udeogalanya. 1976. Hypersensitive resistance of barley to brown rust (Puccinia hordei Otth). p. 27-29. In Proc. 4th Eur. Medit. Cereal Rusts Conf., Interlaken, Switzerland. Feuerstein, U., A.H.D. Brown, and J.J. Burdon. 1990. Linkage of rust resistance genes from wild barley (Hordeum spontaneum) with isozyme markers. Plant Breed. 104:318-324. Frecha, J.H. 1970. Inheritance of the resistance to Puccinia hordei Otth in barley. Bol. Genet. Inst. Fitotec., Castelar 7:1-8. Henderson, M.T. 1945. Studies of the sources of resistance and inheritance of reaction to leaf rust, Puccinia anomala Rostr., in barley. Ph.D. Thesis. Univ. of Minnesota, St. Paul. Jin, Y., G.H. Cui, B.J. Steffenson, and J.D. Franckowiak. 1996. New leaf rust resistance genes in barley and their allelic and linkage relationships with other Rph genes. Phytopathology 86:887-890. Jin, Y., G.D. Statler, J.D. Franckowiak, and B.J. Steffenson. 1993. Linkage between leaf rust resistance genes and morphological markers in barley. Phytopathology 83:230-233. Jin, Y., and B.J. Steffenson. 1994. Inheritance of resistance to Puccinia hordei in cultivated and wild barley. J. Hered. 85:451-454.

Jin, Y., B.J. Steffenson, and H.E. Bockelman. 1995. Evaluation of cultivated and wild barley for resistance to pathotypes of Puccinia hordei with wide virulence. Genet. Res. Crop Evol. 42:1-6. Johnson, R. 1968. The genetics of resistance of some barley varieties to Puccinia hordei. p. 160-162. In Proc. Eur. Medit. Cereal Rust Conf., Oeiras, Portugal. Jrgensen, J.H. 1993. Coordinator's report: Disease and pest resistance genes. BGN 22:110-134. Levine, M.N., and W.J. Cherewick. 1952. Studies on dwarf leaf rust of barley. U.S. Dept. Agr. Tech. Bull.1056. 17 p. Manisterski, J., and Y. Anikster. 1995. New resistance genes to the brown rust, Puccinia hordei, in wild barley from Israel. BGN 24:102-103. Moseman. J.G. 1972. Report on genes for resistance to pests. BGN 2:145-147. Moseman, J.G., and L.W. Greeley. 1965. New physiological strains of Puccinia hordei among physiological races identified in the United States from 1959 through 1964. Plant Dis. Rep. 49:575-578. Moseman, J.G., and D.A. Reid. 1961. Linkage relationship of genes conditioning resistance to leaf rust and powdery mildew. Crop Sci. 1:425-427. Moseman, J.G., and C.W. Roane. 1959. Physiologic races of barley leaf rust (Puccinia hordei) isolated in the United States from 1956 to 1958. Plant Dis. Rep. 43:1000-1003. Nover, I., and C.O. Lehmann. 1974. Resistenzeigenschaften im Gersten- und Weizensortiment Gatersleben. 18. Prfung von Sommergersten auf ihr Verhalten gegen Zwergrost (Puccinia hordei Otth). Kulturpflanze 22:25-43. Parlevliet, J.E. 1976. The genetics of seedling resistance to leaf rust, Puccinia hordei Otth, in some spring barley cultivars. Euphytica 25:249-254. Ramage, R.T. 1972. Report from the Barley Genetics Committee of the American Barley Research Workers' Conference. BGN 2:10-15. Reinhold, M., and E.L. Sharp. 1982. Virulence types of Puccinia hordei from North America, North Africa and the Middle East. Plant. Dis. 66:1009-1011. Roane, C.W. 1962. Inheritance of reaction to Puccinia hordei in barley. I. Genes for resistance among North American race differentiating varieties. Phytopathology 52:1288-1295. Roane, C.W. 1976. BGS070, Resistance to Puccinia hordei Otth. (Barley leaf rust), Rph1a. BGN 6:120. Roane, C.W., and T.M. Starling. 1967. Inheritance of reaction to Puccinia hordei in barley. II. Gene symbols for loci in differential cultivars. Phytopathology 57:66-68. Roane, C.W., and T.M. Starling. 1970. Inheritance of reaction to Puccinia hordei in barley. III. Genes in the cultivars Cebada Capa and Franger. Phytopathology 60:788-790. Sharp, E.L., and M. Reinhold. 1982. Resistance gene sources to Puccinia hordei in barley. Plant Dis. 66:1012-1013. Starling, T.M. 1956. Sources, inheritance, and linkage relationships of resistance to race 4 of leaf rust (Puccinia hordei Otth), race 9 of powdery mildew (Erysiphe graminis hordei El. Marchal), and certain agronomic characters in barley. Iowa State Coll. J. Sci. 30:438-439. Steffenson, B.J., and Y. Jin. 1997. A multi-allelic series at the Rph2 locus for leaf rust resistance in barley. Cereal Rusts Powdery Mildews Bull. (in press). Tan, B.H. 1977a. A new gene for resistance to Puccinia hordei in certain Ethiopian barleys. Cereal Rust Bull. 5:39-43. Tan, B.H. 1977b. Evaluation host differentials of Puccinia hordei. Cereal Rust Bull. 5:17-23. Walther, U. 1987. Inheritance of resistance to Puccinia hordei Otth in the spring barley variety Trumpf. Cereal Rusts Powdery Mildews Bull. 15:20-26. Walther, U., and C.O. Lehmann. 1980. Resistenzeigenschaften im Gersten- und Weizensortiment Gatersleben. 24. Prfung von Sommer und Wintergersten auf ihr Verhalten geganuber Zwergrost (Puccinia hordei Otth). Kulterpfanze 28:227-238. Waterhouse, W.L. 1948. Studies in the inheritance of resistance to rust of barley, II. J. Proc. Royal Soc. New South Wales 81:198-205. Watson, I.A., and F.C. Butler. 1947. Resistance to barley leaf rust (Puccinia anomala Rostr.). Linnean Soc. New South Wales, Proc. 72:379-386. Yahyaoui, A.H., and E.L. Sharp. 1987. Virulence spectrum of Puccinia hordei in North Africa and the Middle East. Plant Dis. 71:597-598. Yahyaoui, A.H., E.L. Sharp, and M. Reinhold. 1988. New sources of resistance to Puccinia hordei in barley land race cultivars. Phytopathology 78:905-908.

Zloten, R.R. 1952. The inheritance of reaction to leaf rust in barley. M.S. Thesis. University of Manitoba, Winnipeg.