Additive genes in wheat for resistance to stripe (yellow) rust (Puccinia striiformis Westend.)

CROP PROTECTION (1982) 1 (2), 181-189 © 1982 Butterworths

Additive genes in wheat for resistance to stripe (yellow) rust (Puccinia striiformis Westend.) E. L. SHARP

Department of Plant Pathology, Montana State University, Bozeman, M T 59717, USA AND E. FUCHS

Field and Grass Crops Protection Institute, Federal Biological Research Centre, Braunschweig, Federal Republic of Germany ABSTRACT. Forty-nine lines of wheat (F6 generation) containing minor additive genes conditioning resistance to stripe (yellow) rust (Puccinia striiformis Westend.) were evaluated to several virulence types (physiologic races) of the pathogen obtained from the USA and Europe. All wheat lines showed some level of resistance to all virulence types ofP. striiformisbut there were differences in level of resistance between crosses and between lines within a particular cross. Generally, all lines expressed the most resistance at the seedling stage when grown at higher temperatures (15°C during the dark period; 25°C during the light period) than at 2°C (dark period) and 20°C (light period). Lines with more resistance genes showed the most resistance, and this resistance was least sensitive to temperature change. Mature plants in the field had levels of resistance equal to, or greater than, those of their seedling counterparts. One parent of each cross evaluated was either a commercial cultivar or an advanced wheat selection, and was rated as susceptible. In many cases, these susceptible parents contributed to resistance in the progeny and thus the progeny showed transgressive segregation for resistance. Some parent cultivars, which were completely susceptible as seedlings and moderately resistant as mature plants, also contributed to seedling resistance in the progeny when combined with parents known to contain minor additive genes for resistance to P. striiformis. The advantages of using minor additive genes are discussed in relation to the control of stripe rust of wheat and to crop protection generally.

Introduction Control o f plant disease m a y be achieved by one or a combination of several methods: potentially, the most economical control of m a n y diseases of field crops is by the use of resistant cultivars. Unfortunately, the effectiveness of resistance has often been short-lived because of changes in specific pathogens which have allowed

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Additive genes for resistance to stripe rust

them to overcome the defence mechanisms of the hosts. This phenomenon has led to various approaches in attempts to obtain durable (i.e. long-lasting) resistance. Johnson (1981) has recently discussed durable resistance with particular reference to stripe (yellow) rust of wheat caused by Puccinia striiformis Westend. He advocated the use of parents that, through time and experience, are known to have durable resistance, as starting materials in breeding programmes. This paper presents evidence that wheat cultivars that normally appear to be susceptible can, also, often be utilized as sources of broadbased resistance, which appears to be durable. In earlier investigations in this laboratory, additive genes for resistance of wheat to stripe rust were found to occur in many wheat cultivars and lines (Lewellen, Sharp and Hehn, 1967). This resistance was referred to as 'minor-gene resistance', in which the effects of single genes, each of which had only a minor effect on resistance, were additive to give a useful level of resistance. The minor genes always behaved as recessives, were temperature-sensitive, usually conditioned higher levels of resistance at 15°C in the dark and 25°C in the light than at 2°C (dark) and 20°C (light) and, when accumulated in the same genotype, gave a wide range of infection types in the F2 generation when crossed to a completely susceptible wheat cultivar. One particular plant introduction of wheat, PI 178383, contained one major gene which conditioned a temperature-insensitive necrotic fleck reaction and three detectable minor genes conditioning other types of resistance to stripe rust. The minor resistance genes in PI 178383 were separated by developing lines from a cross between cv. Itana and PI 178383 which contained either one, two or three minor genes. These components conditioned reaction types 3-, 2,1; 1-, 0; and 0-, 00, respectively, at a temperature regime of 15°C (dark)/25°C (light) (Sharp, 1968). These lines were crossed with several susceptible or moderately resistant commercially grown wheat cultivars and the progenies were selected for resistance to cultures of P. striiformis occurring in the north-western USA. This selection procedure was followed in several selfed generations and several lines were developed from each cross. At the F6 generation, 49 different lines were selected for evaluation against different virulence types of P. striiformis occurring both in the United States and in Europe (Sharp, 1976). Data are presented in this paper on the reaction of the 49 wheat lines to several virulence types from widely separated regions. Materials and methods Wheat plants, each carrying one, two or three minor genes from PI 178383, were crossed with 12 different commercial wheat cultivars or advanced breeding lines. One entry (18/1) carried one detectable gene, four lines (12/21, 14/2, 15/2, 17/2) carried two minor genes and two lines (10/3, 11/3) carried all three minor genes. The various crosses and lines developed from the crosses are listed in Tables 1, 2 and 3. The 49 wheat lines, which were in the F6 generation, were evaluated with representative cultures of virulence types of P. striiformis from both the United States and Europe. Seedlings were uniformly inoculated with uredospores of the various virulence types in a settling tower and were then placed in a dew chamber for 24 h at 7°C. Before and after inoculation and incubation, the plants were grown in controlled-environment chambers at temperature regimes of either 2°C (dark)/20°C (light) or 15°C (dark)/25°C (light), with a photoperiod of 12 h, peak light intensity of about 26 900 Ix. The light intensity was gradually increased at the beginning of each

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TABLE 1. Infection indices in F6 generations for cross of known one-minor-gene line with wheat cultivars and advanced selections Seedlings

Cross & Lines 18/1 x Lancer 1837 1841 1842 1844 1843 1840 18/1 x M t 6531 1856 1854 18/1 x Itana 1848 18/1 x Delmar 1864 1863 1865 18/1 x Mt 6930 1859 1806 1858 1860 18/1 x Wanser 1850 1851 1852 1849

Mature plantsT Reaction Severity Infection index* type (%) 15/25°C 2/20°C~ 1976 1977 1976 1977

1"0 1"0 1"1 1"2 1"6 2"8

1.6 2.0 1.9 1-9 2"1 2"9

0 0 2 0 0 0

0 0 0 0 0 0

0 0 1 0 0 0

0 0 0 0 0 0

1"0 1-3

1-5 2-2

0 0

0 0

0 0

0 0

1"3

3"0

5

5

1

50

1.1 2.2 3.6

3"0 2"8 3-3

0 0 2

3 3 3

0 0 t

5 25 10

2.2 2-4 2-5 2"8

2"9 2-6 2-7 3"1

2 0 0 2

5 3 3 5

1 0 0 t

50 5 5 50

2"4 2.4 2"6 2-6

2"6 2.8 2"7 3"0

5 2 2 5

5 8 5 5

1 t t 1

75 50 50 75

* Seedling infection indices: reaction types 00, 0 - = I=VR; 0, = 2 = R ; 1, 2, 3 - = 3 =MR; 3, 4=4=S. Evaluated with Clement virulence type (race 232E137). T Mature plants: both reaction type and severity rated on a scale from 0 to 9. Type 0=no infection; 1, 2, 3=R; 4, 5, 6=MR; 7, 8, 9=S; t=trace. Severity=% of leaf infected. Evaluated with Chinese 166 virulence type (race 4lE136) in 1976 and with Suwon-Omar virulence type (race 104E137) in 1977. Temperature regimes: 15/25°C indicates 15°C (dark)/25°C (light); 2/20°C indicates 2°C (dark)/20°C (light). l -

photoperiod and gradually decreased towards the end o f each period. At 14 or 20 days after inoculation, depending u p o n the t e m p e r a t u r e regimen, the plants were evaluated for stripe-rust reaction type. An infection index was assigned in which plants with reaction types 00 and 0 - - were assigned an infection index value of 1 (very resistant----VR); reaction types 0 and 1 -- were given a value o f 2 (resistant-----R);

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Additive genes for resistance to stripe rust TABLE 2. Infection indices in F6 generation for crosses of known two-minor-gene lines with wheat cultivars and advanced selections Seedlings

Cross & Line 12/2 x Gaines 1795 1876 15/2 x Gaines 1828 14/2 × Gaines 1808 14/2 × Mt 6531 1885 1886 1887 14/2 x Mt 6928 1812 1811 14/2 x Mt 6535 1878 1877 17/2 x N10B55 1832 17/2 × Delmar 1804 17/2 x Mt 6610 1801 14/2 x Itana 1818 15/2 x McCall 1826 1822

Mature plantsT Reaction Severity Infection index* type (%) 15/25°C 2/20°C~ 1976 1977 1976 1977

1"0 3"5

1"0 3"5

0 2

0 8

0 t

0 75

1-0

1.0

0

0

0

0

2"8

3-6

0

3

0

5

1.1 1.1 1"2

1.6 1"6 1.2

0 0 0

0 0"8 0

0 0 0

0 0-25** 0

1"1 1-8

1-6 2"3

0 0

0 3

0 0

0 1

1.4 1.4

1-7 2.0

2 0

0 3

1 0

0 1

1-2

1.9

0

0

0

0

1"4

2.1

0

0

0

0

1.7

1"9

0

0

0

0

2.1

2.5

0

3

0

1

3.0 3.8

3.3 4.0

5 5

0 8

1 25

0 75

*~ Segregating or mixed seed *, T, I As in Table 1

reaction types 1, 2 and 3 - - were scored as 3 (moderately r e s i s t a n t = M R ) ; reaction types 3 and 4 were scored as 4 ( s u s c e p t i b l e = S ) . Detailed descriptions of the individual reaction types have been given in an earlier publication (Volin and Sharp, 1973). All the F6 seedling wheat lines were evaluated after inoculation with P. striiformis cultures of seven virulence types, which included cultures with virulence to all cultivars in the world differential set of varieties (Johnson, Stubbs, Fuchs and Chamberlain, 1972), used for determining physiologic races of P. striiformis, with the exception of cv. Lee. T h e three P. striiformis cultures used from the U S A were

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TABLE 3. Infection indices in F6 generation for cross of known three-minor-gene lines with wheat cultivars and advanced selections Seedlings

Cross & Line 11/3 x M t 6535 1870 1873 1872 1871 1790 1869 11/3 x Lancer 1836 1835 10/3 x Delmar 1781 1783 11-3 x Delmar 1788 11/3 x Mt 6610 1787

Mature plantst Reaction Severity Infection index* type (%) 15/25°C 2/20°C~ 1976 1977 1976 1977

1"0 1"0 1"0 1"0 1"1 1"1

1"0 1"0 1"2 1"3 1"4 1-7

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

1.0 1.2

1"5 1"1

0 0

0 3

0 0

0 5

1.0 1.8

1"2 1"6

0 5

0 0

0 1

0 0

1-4

2"1

2

0

1

0

1-1

1"3

0

0

0

0

*, t, I As in Table 1 especially characterized by virulence on wheat cvs Vilmorin, M o r o and Chinese 166, and are designated the Vilmorin, the M o r o and the Chinese 166 races, respectively, in this paper. T h e four European cultures used were similarly characterized by virulence on cvs Chinese 166, Heines Kolben, S u w o n - O m a r and Clement. Using the nomenclature of Johnson et al. (1972) the designations for the European cultures would be races 41E136, 36E132, 108E141 and 232E137, respectively. At least 50 individual plants o f each wheat line were grown at 15°C (dark)/25°C (light) before and after dew incubation, and were scored after inoculation with a specific virulence type. T h e virulence type especially characterized by virulence on Chinese 166, race 41E136, was evaluated at two temperature regimes (2°C (dark)/20°C (light), and 15°C (dark)/25°C (light)) in the seedling stage, and at the mature-plant stage in the field at Braunschweig, Federal Republic of G e r m a n y in 1976. In 1977 race 104E137, a rust culture virulent on Strubes Dickkopf, Vilmorin and S u w o n - O m a r of the world differential varieties, was used in the field for evaluations o f the F6 wheat lines. A 0-9 scale was used for field assessments of reaction type: rust severity was recorded as apparent percentage o f leaf infection. Results Testing of the various F6 wheat lines with cultures o f P . striiformis showed that some lines were still segregating for infection type and there was not, therefore, a uniform

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Additive genes for resistance to stripe rust

reaction to stripe rust within particular lines. For this reason, infection indices for each line are given as accumulated values for the 50 or more plants scored. In general, each wheat line within a specific cross reacted similarly to the different virulence types of P. striiformis evaluated. However, there were differences in the reaction pattern between lines of particular crosses, as illustrated in Figure 1. For example, one line from the cross between 18/1 and cv. Lancer, indicated by the stippled bar in Figure 1, gave a higher infection index with all but one of the virulence types tested. In most crosses there was evidence of additive gene action. Parent 18/1 had an infection index of 3 while the other parent, cv. Lancer, had an

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FIGURE 1. Infection indices for four selected F6 wheat lines developed from crossing 18/1 x Lancer evaluated with seven virulence types of Puccinia striiformis. Infection indices for parents 18/1 and Lancer=3 MR and 4 S, respectively. 4 S=susceptible; 3 MR=moderately resistant; 2 R=resistant; 1 VR=very resistant.

infection index of 4: however, three of the four F6 lines tested had infection indices of between 1 and 2, and the index of the fourth one was near 2. This shows that cv. Lancer, although appearing to be susceptible, contributed genes which were responsible for greater resistance. Although all the lines investigated showed additive gene action, some combinations had greater effects on resistance than others, Figure 2 shows infection indices for four lines developed from a cross of 18/1 x cv. Wanser. The infection indices are generally higher than those of the progenies from 18/1 x cv. Lancer but the trends are similar. Although the results obtained with the different virulence types were somewhat variable, all lines showed at least moderate resistance. Infection indices for all 49 wheat lines evaluated with the different virulence types in the seedling stage at two temperature profiles and as mature plants in the field are given in Tables 1-3. More resistance was expressed in these lines at the higher temperature regime, 15/25°C, than at lower temperatures. However, in lines with two or three resistance genes the effect of temperature was less evident than in those

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carrying a single gene. T h e infection index was also less in lines with more resistance genes. In 1976, field conditions were unusually dry and this is reflected in the results for this year. T h e rust development in the field was considerably greater in 1977 and these results generally agree better with results obtained in the seedling tests. For mature plants in the field, the percentage of lines with one, two or three detectable minor genes exhibiting some rust were 45, 24, and 17 respectively in 1976 and 60, 41 and 9 in 1977 (Tables 1, 2 and 3). T h e highest reaction type noted in the field in 1976 was intermediate. In some lines, greater resistance was noted for the mature plants than for seedlings. Infection indices obtained in 1977 for the various crosses of cv. Gaines with

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FIGURE2. Infection indices for four selected F6 wheat lines developed from crossing 18/1 × Wanser evaluated with seven virulence types of Puccinia striiformis. Infection indices for parents 18/1 and Wanser=3 MR and 4 S, respectively. 4 S=susceptible; 3 MR=moderately resistant; 2 R = resistant; 1 VR=very resistant.

different parents, each containing two detectable genes, are given in Table 2. One line (1795), from the cross 12/2 x cv. Gaines, was very resistant both as seedlings and as mature plants, whereas another line from the same cross (1876), was quite susceptible as a seedling and when mature. Plants from 15/2 x cv. Gaines (line 1828) were very resistant as seedlings at both temperature profiles and also when mature. Seedlings from the cross 14/2 x cv. Gaines (line 1808) were moderately susceptible at 2/20°C and moderately resistant at 15/25°C, but mature plants were very resistant in the field. Gaines is always susceptible as a seedling but is moderately resistant at maturity. However, cv. Gaines can contribute genes for resistance at the seedling stage when they are combined with additive genes for stripe rust resistance from other wheat lines.

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Additive genes for resistance to stripe rust

Discussion Many wheat cultivars and lines contain stripe rust resistance factors of minor effect which combine additively with those of other cultivars to give a useful level of resistance. Although such wheats appear to have a spectrum of resistance to several virulence types ofP. striiformis, this study involved only a few virulence types. Volin (1971) evaluated minor-gene lines developed from the cross of cv. Itana and PI 178383 after inoculation with 11 physiologic races from the north-western USA and detected no evidence for specificity of reaction. Stubbs (1977) tested the same lines in international nurseries over a period of several years and reported that they reacted similarly with all physiologic races involved. Furthermore, wheat cv. Crest, which contains additive resistance genes from PI 178383, has been grown extensively for over 10 years in Montana, USA, and still gives an adequate control of stripe rust. The additive gene resistance to stripe rust discussed in this paper appears to be conditioned by a number of polygenes, of which each has an individual minor effect. Such genes can be combined to provide effective resistance through crossing suitable lines or cultivars and judicious selection. Several progenies from crosses exhibited marked resistance only after several generations of selection: this was probably attributable to the many heterozygous gene loci which were present in the early generations and which became homozygous in later generations so that maximum resistance was expressed. It appears that an appropriate genetic background must be established before the minor, additive resistance genes can be detected by conventional genetic procedures. However, once resistant plants can be identified, resistant lines eventually can be selected for homozygosity for resistance. In any study of a host-parasite system it is desirable to know the genotypic basis for infection type. In research on the resistance components of PI 178383, three minor genes at a temperature regime of 15°C (dark)/25°C (light) conditioned 00 or 0 - infection types. These infection types are very similar and differ from each other only in the amount of necrosis produced on inoculated leaves, but in neither infection type does necrosis span the entire width of the leaf. The resistance conditioned by two detectable minor genes was rated at 0 or 1 - ; these infection types are also quite similar to each other. The necrosis in the (0) infection type does span the entire width of the leaf and (1 --) differs only in that occasional pustules are produced on infected leaves. The presence of one detectable minor gene resulted in infection types 1, 2 and 3--. These three infection types are quite similar to each other in that necrosis is exhibited in each, but there are varying amounts of necrosis in comparison to sporulation. The actual length and physiological age of the leaf can sometimes determine whether a rating of 1, 2 or 3 - is recorded. Evidence to date indicates that additive gene resistance is durable, but only time will tell to what extent this is so. A number of step-wise changes in the pathogen would be necessary to overcome the resistance factors, and six genes for resistance in some of the selected wheat lines have been detected using different temperature regimes. There may be considerably more resistance factors involved in build-up of the genetic background. To utilize additive minor resistance genes effectively it is necessary to avoid epistatic genes of major effect in parental materials, because these will mask the presence of minor genes. Extremely susceptible wheat cultivars should not be used as parents, although moderately susceptible varieties can be a source of valuable additive minor genes. Between the two extremes of the most resistant and the most

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susceptible there is abundant germplasm that can be utilized effectively in breeding for resistance to stripe rust. Some advantages of using resistance involving minor, additive genes are that it can readily be followed in a breeding programme and is easily manipulated by using different temperature regimes. Effective resistance can be obtained by crossing commercial wheat cultivars which normally appear to be susceptible (Krupinsky and Sharp, 1979). This not only avoids introducing undesirable traits which are often associated with resistant parents of exotic or non-agronomic types, but also increases the probability of obtaining progeny with adapted agronomic traits suitable for cultivar development. T h e method of identifying and exploiting minor additive resistance genes should be applicable to other host-parasite systems and appears to be worthy of further use in protection of plants from disease. Acknowledgement Research facilitated by a Senior Scientist Award from the Alexander von H u m b o l d t Foundation to the first author. Montana Agricultural Experiment Station Journal Series, Paper No. 1212. References JOHNSON,R. (1981). Durable resistance: differentiation of, genetic control, and attainment in plant breeding. Phytopathology 71, 567-568. JOHNSON,R., STUBBS,R.W., FUCHS,E. ANDCHAMBERLAIN,N.H. (1972). Nomenclature for physiologic races of Puccinia striiformis infecting wheat. Transactions of the British Mycological Society 58, 475-480. KRUPINSKY,J.M. ANDSHARP,E.L. (1979). Reselection for improved resistance of wheat to stripe rust. Phytopathology 69, 400-404. LEWELLEN,R.T., SHARP,E.L. ANDHEHN,E.R. (1967). Major and minor genes in wheat for resistance to Puccinia striiformis and their responses to temperature changes. Canadian Journal of Botany 45, 2155-2172. SHARP, E.L. (1968). Interaction of minor host genes and environment in conditioning resistance to stripe rust. In: Proceedings of the Second European and Mediterranean Cereal Rusts Conference, Oeiras, Portugal, 1968, pp. 158-159. (ed. by J.C. Santiago). Oeiras, Portugal: European and Mediterranean Cereal Rusts Foundation. SHARP, E.L. (1976). Broad based resistance to stripe rust in wheat. In: Proceedings of the Fourth European and Mediterranean Cereal Rusts Conference, Interlaken, Switzerland, 1976, pp. 159-161. (ed. by A. Br6nnimann). Interlaken: European and Mediterranean Cereal Rusts Foundation. STUBBS,R.W. (1977). Observations on horizontal resistance to yellow rust (Puccinia striiformis f. sp. tritici). Cereal Rusts Bulletin 5, 27-32. VOLIN, R.B. (1971). Physiological Race Determination and Environmental Factors Affecting the Development of Infection Type in Stripe Rust (Puccinia striiformis West.). PhD thesis, Montana State University, Bozeman, Montana, USA. 90 pp. VOLIN,R.B. ANDSHARP,E.L. (1973). Physiologicspecializationand pathogen aggressivenessin stripe rust. Phytopathology 63, 699-703. Received 2 September 1981