Ann. appl. Biol. (1970), 66, 137-143 Printed in Great Britain

‘37

Breeding for mature -plant resistance to yellow rust in wheat

BY F. G. H. LUPTON AND R. JOHNSON Plant Breeding Institute, Trumpington, Cambridge

(Accepted 18 March 1970)

S U M M A R Y

In recent years several varieties of wheat, such as Rothwell Perdix and Maris Envoy, have shown good resistance to yellow rust when first produced, but because their resistance was determined by simply inherited major genes, they have later been severely attacked by newly arising physiologic races of the pathogen. Other varieties, such as Little Joss, Atle and Maris Widgeon, though slightly attacked by several races, have never suffered severe damage even when exposed to high levels of inoculum. The inheritance of this non- race-specific type of resistance was studied in a cross between Little Joss and a susceptible but shorter-strawed variety, Nord Desprez. Resistance appeared to be under complex control. It was found possible to select short-strawed resistant plants, using simple techniques in the field.

I N T R O D U C T I O N

The repeated appearance of new races of cereal leaf diseases, especially mildew in barley and yellow rust in wheat, has led to an increased interest in the selection of varieties with non-race-specific or ‘horizontal’ resistance to disease. Van der Plank (1963) drew attention to the importance of such resistance, and pointed out that where selection for resistance has been less intensive and has chiefly been based on natural infection in the field, the varieties obtained have shown a more stable disease reaction, and although they may not exhibit the near immunity commonly conferred by major genes, they rarely suffer severe attacks from newly arising races of pathogen. Van der Plank illustrates his point by reference to resistance of maize to Puccinia sorghi and of barley to P. graminis, but there appears to be no reason why similar resistance should not be found to pathogens in cases where recent breeding work has been mainly directed towards the production of varieties with simply inherited major genes. In view of the lack of published data the present paper discusses possible sources of non-race-specific resistance to yellow rust in wheat, and the results obtained from a pilot experiment designed to explore means of their exploitation.

S O U R C E S O F R E S I S T A N C E

Small plots of leading varieties and of their parents and more remote ancestors are grown each year at the Plant Breeding Institute. These plots show the improvements obtained by breeding and form a living pedigree chart in which modern varieties can be compared with successively older varieties, including those cultivated 50 or more years ago, from which the initial crosses were made.

138 F. G. H. LUPTON AND R. JOHNSON

Epidemics of yellow rust are induced throughout the breeding plots, by artificial inoculation of spreader rows with the more important physiologic races of P . strii- formis. Infection from these plots has spread to those in the living pedigree chart, and, as the spectrum of prevalent rust races has changed, has enabled observations to be made of the reactions of a range of modern and older varieties to a succession of races of P. striiformis (Table I).

Table I. Percentage leaf area infected with yellow rust, 1967-9 28. vi. 67 2. vii. 68 15. vii. 69

(Races 3/55 and (Races 3/55 and (Races 3/55, 58C 60 prevalent) 60 prevalent) and 60 prevalent)

Varieties introduced before 1920 and old land varieties Bon Fermier Browick Extra Kolben Heine Kolben Little Joss No6 Rampton Rivett Red Fife Saxo Squareheads Master Yeoman

75

5 5-10

0' I

0- I

95 10-15 50

5 2-3

1-2

25

5 5

25

0

1-2

1-2 I 0

I I

1-2

Varieties introduced between 1920 and 1950 Atle BersCe Desprez 80 Hatif Inversable Holdfast Hybrid 40 Jubilegem Prof. Delos Vilmorin 23 Vilmorin 27

Cappelle Desprez Charnplein Blite le Peuple Heine VII Heine 51 Hybrid 46 Joss Cambier Maris Beacon Maris Envoy Maris Nimrod Maris Ranger Maris Settler Maris Widgeon Minister Nord Desprez Peko Professeur Marchal Rothwell Perdix Viking Yga Blondeau

0 1-2

95 95 40 60 20 0

50 2-3

Varieties introduced after 1950 25-30 25-30

40 70 10-15

0

- 0 0 0'1 0 0

2-3 0 80 5-10 0'1

90 40-50 5-60

0 0

25 25 5

5

5

1-2

0-1

0-1

5-10 25

25 25

0

0

0'1 - 0 0 0 0 1-2 0

25 1-2 0-1

50 5

15

20 0'1

I 0 2 0'1

30 0'1 I 0 0'1 0'1 0'1

0'1 0.1 60 30 5 20 2

I 0 I 0 0'1

5-10 5 0 20 30 0 0'1 0'1

5 0 0' I

0

25 0'1 0.1

50 5

60 0.1

20 20

Breeding for resistance to yellow rust I39 The common races in the field from 1967 to 1969 were race 3/55 (Ubels, Stubbs &

s’Jacob, 1965), race 60 (Macer & Doling, 1966) and, in 1969 only, race 58 C (Chamber- lain, Doodson & Johnson, 1970).

The general level of rust infection on the plots was highest in 1967, lowest in 1968, and intermediate in 1969, but although the levels of infection varied from year to year the ranking of the varieties for susceptibility tended to remain unchanged. The most marked departure from this situation is shown by Maris Envoy and Maris Settler which are completely resistant to races 3/55 and 60 as seedlings and therefore remained free of rust in 1967 and 1968. In 1969, however, they were severely attacked by the newly discovered race 58 C, to which they are seedling-susceptible. They illustrate the behaviour of varieties whose resistance is too heavily dependent on major genes or what van der Plank (1963) has described as ‘vertical’ resistance. Similar ‘ vertical ’ resistance was shown by Rothwell Perdix, which was completely resistant until the advent of race 60 in 1966 (Macer & Doling, 1966), and by Nord Desprez and Heine VII, which were resistant in Britain until the arrival of races 2 B and 8 B in 1951 and 1955 respectively (Batts, 1957). In contrast to the behaviour of these varieties, both Minister and Maris Nimrod are seedling-susceptible to race 58 C and seedling-resistant to races 3/55 and 60, but their infection levels remained very low in 1969. This type of resistance at the adult plant stage, following susceptibility at the seedling stage, is exhibited by many of the varieties in Table I. Amongst these are the recently introduced Elite le Peuple, Joss Cambier and Maris Widgeon, the older varieties Atle, BersCe and Vilmorin 27, and some of the much older varieties such as Browick, Squareheads Master, Yeoman and Little Joss. It is noteworthy that Maris Widgeon is more resistant than either of its parents, Cappelle Desprez and Holdfast (Table I), as was earlier reported by Lupton & Bingham (1969).

The older varieties, though susceptible as seedlings to a succession of races of P. striiformis, have maintained consistently high resistance in the field, similar to that reported earlier by Manners (1950). This suggests that they possess non-race-specific resistance which could be used in breeding. Little is known of the genetics of this type of resistance, but it is commonly assumed to be polygenic.

S E L E C T I O N F O R F I E L D RESISTANCE I N A H Y B R I D P O P U L A T I O N

To determine the most convenient method of selection within crosses segregating for non-race-specific resistance, a pilot cross was made between the short-strawed highly susceptible variety Nord Desprez and the taller variety Little Joss with its high level of non-race-specific resistance.

The F, of this cross, grown in 1965, was severely rusted, as was Nord Desprez itself. The F,, grown in 1966, was exposed in the field to a severe epiphytotic of yellow rust in which races 2B, 8B and 60 predominated. The cross was severely attacked, but 5 % of the population of 2500 plants were selected as showing some field resistance. The progenies of these and of a small number of susceptible plants were grown as F, single-plant cultures in 1967, and were again exposed to a severe epi- phytotic, in which race 3/55 was predominant. Some of the progenies of plants selected as resistant in F, were susceptible in F, and were probably derived from plants which had escaped infection in 1966. The remainder showed varying degrees of

30

20

10

-

30

0.6 8.3

1 L 20 e .- C

n c

0 10 Z

F. G. H. LUPTON AND R. JOHNSON

1 .o Little Joss 0.7

( a ) F3, 1967

7 13 I L , 9.0 16.0 25.0

Nord Desprez 25.3

( b ) Fq. 1968

17

\ 31

1 2 2

150

100

0.1 ~~~

0.25 1.0 4.0 9.0

98 F (c) Fs, 1969

Little JOSS 0.7

Nord Desprez 48.5

yo leaf area rusted

Fig. I . Number of progenies or groups of progenies from single plants of the cross Little Joss x Nord Desprez selected as resistant to yellow rust in FI, F3 and F4 showing different percentages of leaf area attacked. (a) F,, 1967. Progenies of F, plants selected as resistant. (b) F4, 1968. Progeny means of groups of five single plants selected from F3 families having less than 4 % of their leaf area rusted, or segregating widely for rust reaction. (c) F,, 1969. Progenies of single plants selected from resistant F4 families.

Breeding for resistance to yellow rust 141

resistance mostly distributed between those of the two parents (Fig. Ia). The progenies of susceptible F, plants were all more or less susceptible in F,.

The progenies which had obviously been misclassified in F, were eliminated. Five plants were selected from each of the F, lines that had less than 4% of the leaf area rusted, or which were segregating widely for rust reaction, and sown as single plant progenies in F4. The level of rust epiphytotic was much less severe in this year, 1968, and the crop was badly lodged. Scoring for disease susceptibility was, therefore, difficult and it was only possible to obtain mean scores for the five single plant cultures derived from each F, line. The results (Fig. I b ) again show a distribution of degrees

Table 2. Percentage leaf area rusted and height of progenies of representative F, plants from the cross Nord Desprex x Little Joss

Leaf area rusted (%)

Plants scored as resistant in Fz

Plants scored as susceptible in F S

F, F4 F, single plant progenies mean mean I A

\

2-9 1-1 0.7 2.4 4.0 1.1

0 5 0.8 0'0

0.8 0 1 2.3 0.3 0.0 0.4 2'1 0'1 1'5 2.6 0 2 0'2

5.8 0.5 0.5 1.6 1.0 0.4 0.8 0 1 0'2 12.2~ 0.7 10.2 2-5 00 00

35.0 22.0 47.5 12.4 9'3 29'5 15.5 21.5 44.6 15.0 2.6 19.0 41.5 21.5 20.5 6.8 2.7 0.5 26.8 0.6 0.7 24.0 1.7 2.6

1967 1968

3-1 3'5 1.5 1.7 0.6 0.8 2'4 4'3 0.5 0.7 3" 3'7 2.4 3'4 1.5 1.9 0.8 1.8 0 .3 0.3 102 11.3

50 0 56.0 41.0 45.0 63-5 67.5 31.1 39'5 41'0 42.5 0 7 19.6 3'4 4'0 3'0 5'7

00 00

14'4 6.4 I '2

4'5

3 '9

2.3 3'3 0.9 18.5

57'5 47'0 67.5 55'0 50.0

4'5 7'6

1'0

6.9

0 1

22'0

Individual plots, 1969

32.0 9 5 6.4 5.6 I .6 7'5 11.7

4'2 2.3 25.1

75'0 60.0 700 58.5 600 29'5 6.7 10.6

6.5

0 1

Nord Desprez

Little Joss

25'3 8.3 33'5 42'5 50'0 52'5 55'0 37'0 47'5 52'5 55'0 57'5

0.7 0.6 0'2 0.4 0.5 0.7 0.9 0.4 0 5 0.6 0 8 1.9

Height (em) *

* Progeny segregating widely in F, and retained for further observation

of susceptibility mostly ranging between those of the parental varieties, but with some evidence of transgression towards levels of infection lower than that of Little Joss. This effect is possibly spurious, however, since pairs of plots of Little Joss and Nord Desprez were sown near to one another, thus exposing Little Joss to a higher than average inoculum potential.

The progenies of five plants selected from each of the F4 lines were grown in F5 as single-plant cultures in 1969. They were exposed to a severe epiphytotic in which races

142 F. G. H. LUPTON AND R. JOHNSON

3/55 and 58C were predominant. Levels of infection ranged between those of the parents but were skewed strongly towards that of Little Joss (Fig. I c). Some progenies showed a uniform level of resistance, but in others a wide variation in the reactions of the component lines was seen, indicating that further segregation for rust reaction had occurred (Table 2). The segregation between F, families derived from typical F, plants is shown in Table 2, which also demonstrates the good agreement, allowing for seasonal differences in level of infection, found between observations made in successive years. This is further demonstrated by the highly significant correlations between mean levels of rust attack on F, progenies in successive years (Table 3).

T o determine the possibility of combining the non-race-specific resistance of Little Joss with desirable field characters from Nord Desprez, straw heights of all selections were recorded in 1967 and 1969. There was no correlation of disease resistance with the tall straw of Little Joss (Table 3), and it was possible to select F, lines combining disease resistance with short straw and other desirable field characters of Nord Desprez (Table 2). Plant height was strongly heritable.

Table 3. Correlation coefficients between log % leaf area rusted and height (Data based on gz comparisons of Fz plant progenies)

Log rust Fa 1967

0'437""' F d 1968 Log. rust

Log. rust 0.661""" 0.704'"" F, 1969

0.045 0.014 0.007 1967 Height

Height 0.085 0.182 0.150 0.6 I 3 *** I 969

+"" P <O'OOI,

D I S C U S S I O N

The evidence presented indicates that non-race-specific resistance to P. striiformis may be found in many wheat varieties both old and new. The data do not permit an accurate description of the genetic control of this resistance in Little Joss but it was apparently complex. There was some indication of transgressive levels of resi- stance (Fig. I b), although as was pointed out, the inoculum levels may have been lower on the hybrid plots than on the control. A less equivocal example of transgressive levels of resistance is described in Maris Widgeon, which is more resistant than either of its parents, and there are similar reports in the literature (Pope, 1968; Johnson, Wolfe & Scott, 1969). In the cross of Little Joss with Nord Desprez it was also evident from the reaction of the F, that control of resistance was recessive. Both these observations are in contrast to the situation found with major genes for resistance, which are usually dominant and epistatic to genes determining lower levels of resistance (Lupton & Macer, 1962; Macer, 1964).

The differences between these two types of resistance and in their genetic control necessitate different approaches in breeding programmes. The non-race-specific type of resistance found in Little Joss cannot be selected in seedling populations, and for

Breeding for resistance to yellow rust I43 accurate studies requires a control of inoculum level which is difficult to achieve. Comparative studies can, however, be made over a range of inoculum levels although resistance is much more plastic in its expression than that due to major genes, and very high levels of inoculum can cause quite high levels of infection, thus reducing precision in selection. I t is encouraging therefore to note that resistance from Little Joss was handled successfully in a breeding programme using simple visual methods of selection and artificially created epiphytotics of yellow rust in the field.

REFERENCES

BATTS, C. C. V. (1957). The reaction of wheat varieties to yellow rust, Puccinia striiformis,

CHAMBERLAIN, N. H., DOODSON, J . K. &JOHNSON, R. (1970). Race 58C of Puccinia stri$ormis-

JOHNSON, R., WOLFE, M. S. & SCOTT, P. R. (1969). Pathology section, Rep. PI. Breed. Inst.,

LUPTON, F. G. H. & BINGHAM, J. (1969). Winter wheat. Rep. PI. Breed. Inst., 1968, pp. 51-5. LUPTON, F. G. H. & MACER, R. C. F. (1962). Inheritance of resistance to yellow rust (Puccinia

MACER, R. C. F. (1964). Developments in cereal pathology. Rep. PZ. Breed. Inst., 1966-7,

MACER, R. C. F. & DOLING, D. A. (1966). Identification and possible origin of a race of Puccinia

MANNERS, J. G. (1950). Studies on the physiologic specialization of yellow rust Puccinia

POPE, W. K. (1968). Interaction of minor genes for resistance to stripe rust in wheat. Proc.

UBELS, E., STUBBS, R. W. & S’JACOB, J. C. (1965). Some new races of Puccinia striiformis,

VAN DER PLANK, J. E. (1963). Plant diseases; epidemics and control. 349 pp. New York and

19j1-6. J . natn. Inst. ugric. Bat. 8, 7-18.

wheat yellow rust. Trans. Br. mycol. SOC. 55 (in the Press).

1968, pp. 113-23.

glumarum Erikss. & Henn.) Trans. Br. mycol. SOC. 45, 21-45.

PP. 5-33.

striiformis isolated in 1966. Nature, Lond. 212, 643.

glumarum (Schm.) Erikss. & Henn. in Great Britain. Ann. uppl. Biol. 37, 187-214.

3rd. int. Wheat Genet. Symp. Canberra, Australia, pp. 25 1-7.

Tijdschr. PlZiekt. 71, 14-19.

London: Academic Press.