Recommended allele symbols for leaf rust resistance genes in barley

J.D. Franckowiak¹, Y. Jin², and B.J. Steffenson³

¹Department of Plant Sciences
³Department of Plant Pathology
North Dakota State University, Fargo, ND 58105, USA

²Plant 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; Jørgensen, 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	Cultivar or pedigree	USDA-ARS accession number	References
Rph1.a	Oderbrucker	CIho 940	Henderson, 1945; Waterhouse, 1948
Rph2.b	Peruvian	CIho 935	Levine and Cherewick, 1952; Starling, 1956; Steffenson and Jin, 1997
Rph3.c	Estate	PI 57700	Henderson, 1945; Roane and Starling, 1967
Rph4.d	Gold (Gull)	CIho 1145	Moseman and Reid, 1961; Roane, 1962
Rph5.e + Rph2.q+	Quinn	PI 39401	Roane and Starling, 1967; Starling, 1956
Rph5.e	Magnif 102	CIho 13806	Frecha, 1970; Yahyaoui and Sharp, 1987
Rph6.f + Rph2.r+	Bolivia	PI 36360	Henderson, 1945; Roane and Starling, 1967; Starling, 1956
Rph7.g	Cebada Capa	PI 53911	Johnson, 1968; Nover and Lehmann, 1974; Parlevliet, 1976; Starling, 1956
Rph8.h	Egypt 4	CIho 6481	Levine and Cherewick, 1952; Tan, 1977a
Rph9.i	Hor 2596	CIho 1243	Clifford and Udeogalanya, 1976; Tan, 1977a
Rph2.j	Batna	CIho 3391	Reinhold and Sharp, 1982; Starling, 1956; Steffenson and Jin, 1997
Rph2.k	Weider (No. 22)	PI 39398	Henderson, 1945; Sharp and Reinhold, 1982; Watson and Butler, 1947; Steffenson and Jin, 1997
Rph2.l	Juliaca	PI 39151	Levine and Cherewick, 1952; Starling, 1956
Rph2.m	Kwan	PI 39367	Henderson, 1945; Zloten, 1952; Steffenson and Jin, 1997
Rph2.n	Chilean D	PI 48136	Levine and Cherewick, 1952; Tan, 1977b
Rph10.o	Clipper BC8	T39-3	Feuerstein et al., 1990
Rph11.p	Clipper BC67	T38-26	Feuerstein et al., 1990
Rph2.s+	Ricardo	PI 45492	Henderson, 1945; Moseman and Roane, 1959; Zloten, 1952
Rph2.t+	Reka 1	CIho 5051	Levine and Cherewick, 1952; Starling, 1956; Moseman and Greeley, 1965
Rph2.u+	Ariana	CIho 14081	Sharp and Reinhold, 1982; Zloten, 1952
Rph.v	Beni Olid	PI 235186	Jin and Steffenson, 1994
Rph3.w	Bowman*4/PI 466324	PI 466324	Jin and Steffenson, 1994; Chiciaza et al., 1996
Rph13.x	Berac*3/HS2986	PI 531849	Jin and Steffenson, 1994; Jin et al., 1996
Rph2.y	HJ198*3/HS2310	PI 531841	Jin et al., 1995; Jin et al. 1996
Rph12.z	Triumph	PI 268180	Walther, 1987; Jin et al., 1993
Rph3.aa	PC249A	PI 584765	Jin (unpublished).
Rph14.ab	PI 531901-1	PI 584760	Jin et al., 1996
Rph7.ac	Bowman*4/Tu 17	Tu 17a	Chicaiza et al., 1996
Rph15.ad	Bowman*4/PI 355447	PI 355447	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		Cultivar or pedigree	USDA-ARS number		Cultivar origin or wild barley
Recom.	Previous		Recom.	Other
Rph1.a	Rph1a	Oderbrucker	CIho 940		Manchuria
Rph2.b	Rph2b	Peruvian	CIho 935		Peru
Rph3.c	Rph3c	Estate	PI 57700	CIho 3410	Egypt
Rph4.d	Rph4d	Gold (Gull)	CIho 1145		Sweden
Rph5.e + Rph2.q	Rph5e + Rph2	Quinn	PI 39401	CIho 1024	Australia
Rph5.e	Rph5e	Magnif 102	CIho 13806		Argentina
Rph6.f + Rph2.r+	Rph6f + Rph2	Bolivia	PI 36360	CIho 1257	North Africa
Rph7.g	Rph5e	Cebada Capa	PI 53911	CIho 6193	North Africa
Rph8.h	Rph8	Egypt 4	CIho 6481		Egypt
Rph9.i	Rph9	Hor 2596	CIho 1243		Ethiopia
Rph2.j	Rph2b	Batna	CIho 3391		Algeria
Rph2.k	Rph2b	Weider (No. 22)	PI 39398	CIho 1021	Australia
Rph2.l	Rph2b	Juliaca	PI 39151	CIho 1114	Peru
Rph2.m	Rph2b	Kwan	PI 39367	CIho 1016	India
Rph2.n	Rph2b	Chilean D	PI 48136	CIho 1433	Australia
Rph10.o	Rph10	Clipper BC8	T39-3		H. spontaneum
Rph11.p	Rph11	Clipper BC67	T38-26		H. spontaneum
Rph2.s+	Rph2b	Ricardo	PI 45492	CIho 6306	Uruguay
Rph2.t+	Rph2b	Reka 1	CIho 5051		Australia
Rph2.u+	Rph2b	Ariana	CIho 14081	CIho 2524	Tunisia
Rph.v		Beni Olid	PI 235186	CIho 10506	Libya
Rph3.w		Bowman*4/PI 466324	PI 466324		H. spontaneum
Rph13.x		Berac*3/HS2986	PI 531849		H. spontaneum
Rph2.y		HJ198*3/HS2310	PI 531841		H. spontaneum
Rph12.z		Triumph	PI 268180		H. spontaneum
Rph3.aa		PC249A	PI 584765		CIMMYT sel.
Rph14.ab		PI 531901-1	PI 584760	PI 531901	Egypt
Rph7.ac		Bowman*5/Tu 17	Tu 17a	Tunisia 17	Tunisia
Rph15.ad		Bowman*4/PI 355447	PI 355447		H. spontaneum

⁺ 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:

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