Inheritance of resistance to yellow rust (Puccinia glumarum Erikss. & Henn.) in seven varieties of wheat

[ 21 ] Trans. Brit. mycol. Soc. 45 (I), 21-45 (1962).

INHERITANCE OF RESISTANCE TO YELLOW RUST (PUCCINIA GLUMARUM ERIKSS. & HENN.) IN SEVEN VARIETIES OF WHEAT By F. G. H. LUPTON

AND

R. C. F. MACER

Plant Breeding Institute, Cambridge The inheritance of resistance to four physiologic races of Puccinia glumarum has been studied in seven varieties of wheat. Using an assessment of the rust reaction of seedling plants in the F l , F 2 and Fa of a dialle! set of crosses between these varieties, seven genes conferring resistance have been identified at four loci. In general, resistance was found to be inherited as a dominant character although cases of recessive inheritance, particularly against aggressive physiologic races of the pathogen, also occurred. A systematic nomenclature for the genes conferring yellow rust resistance is proposed, and it is suggested that new, and genetically distinct, differential host varieties should be produced for the identification of physiologic races of P. glumarum.

Yellow rust (Puccinia glumarum Erikss. & Henn. = P. striiformis Westend)* is the most widespread and important rust disease of wheat in North-West Europe and in other reg-ions where wheat is grown under cool temperate conditions or at high altitudes. The disease occurs throughout Great Britain and is found in most years upon susceptible wheat varieties. In recent years the incidence of yellow rust has been reduced by the widespread cultivation of resistant varieties of autumn sown wheat (Triticum aestivum L.). In 1952 and 1956, however, rust developed extensively on the new, high yielding varieties Nord Desprez and Heine VII, respectively. Although much research has been carried out into the genetics of resistance to black stem rust (Puccinia graminis Pers. f.sp. tritici (Erikss. & Henn.)) in North America (Ausemus, 1943; Ausemus, Harrington, Worzella & Reitz, 1946; Plessers, 1954; Knott & Anderson, 1956; Knott, 1957a, b), in Australia (Watson & Waterhouse, 1949; Athwal & Watson, 1954), and in India (Sen & Joshi, 1955; Rao & Agrawal, 196oa, b), comparatively few investigations have been reported on the inheritance of resistance to yellow rust, and such information as is available does not concern the commercially important wheat varieties of North-West Europe. The first experiments upon the genetics of resistance to fungal diseases in plants were conducted by Biffen at Cambridge at the beginning of the century. These concerned the resistance of 'immature' and adult wheat plants to Puccinia glumarum in the field and demonstrated conclusively that the resistance of the variety Rivet (Triticum turgidum) in a cross with the

* Puccinia glumarum is considered invalid by Rylander, Jorstad & Nannfe!dt (1953); it is, however, retained here because of its common usage in the literature.

22

Transactions British Mycological Society

susceptible variety Red King (T. aestivum) was inherited as a recessive Mendelian factor, and also that the resistance was inherited independently of other characters (Biffen, 1906). In further studies, Biffen (1907) showed that the 'immunity' of American Club (T . compactum) was also inherited as a single Mendelian recessive factor in crosses with the susceptible varieties of T. aestivum, Preston, Tasmanian and Michigan Bronze. Resistance was also found to be recessive in one cross between two Hungarian varieties of T. aestivum, 'Red ' (resistant) and 'White' (susceptible). Later, Armstrong (1922) extended the range of varieties used in similar investigations and found that in each case resistance was inherited as a single recessive Mendelian factor. Rudorf ( I 930) laid the foundation for work on yellow rust carried out on seedling plants in the glasshouse. He found that resistanc e at the seedling stage was also simply inherited and defined a number of resistant reactiontypes. He showed that the hypersensitive reaction type of the variety Chinese 166, which he classed as 'immune', was unaffected by environmental conditions and was inherited as a dominant character both in crosses with susceptible varieties and with varieties showing less stable resistance reactions. Straib (1934), using eighteen physiologic races of P. glumarum, reported that the ' immunity ' of Chinese 166 was inherited as a dominant character determined by a single gene in each cross with which he worked, and was not influenced by the reaction of the ' nonimmune' parents, which included both resistant and susceptible varieties. Other types of resistance were demonstrated to be controlled by one or more dominant genes and it was also found that, in each of the crosses studied, the reaction towards one physiologic race of P. glumarum was inherited independently of that towards any other race. In one cross (R umkers Sommerdickkopf x Heines Kolben), transgression in the direction of enhanced susceptibility was demonstrated. Other investigators (Hubert, 1932; Favret & Vall ega, 1953; Pal, Sikka & Rao, 1956; Bahl & Kohli, 1960) have reported the behaviour of progenies of crosses between various pairs of wheat varieties. Information of this type provides valuable data concerning the genetic basis of resistance in certain varieties, but cannot reveal the relationship between genes for resistance carried by different varieties. The recent work of Singh & Swaminathan (1959), using a monosomic analysis technique, has demonstrated that three recessive genes situated on chromosomes IV, VI and IX of the variety Cometa Klein confer resistance to ten physiologic races of P. glumarum. This work, carried out in India, represents the most detailed analysis of the genetical control of resistance to yellow rust yet reported. MATERIALS AND EXPERIMENTAL TECHNIQUES

A diallel set of crosses, without reciprocals, was made between the 'seven wheat varieties Cappelle-Desprez, Chinese 166, Heine VII, Holdfast, Hybrid 46, Minister and Soissonais-Desprez. Tests of the seedling reactions to four physiologic races of P. glumarum were made on l'~ plants, on F2 populations, and (in the Fa) on the progenies of single F2 plants.

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

23

Wheat varieties The seven wheat varieties were selected first because they showed differing reaction-types to four British physiologic races of P. glumarum and, secondly, because they were important parents in wheat-improvement programmes being undertaken at the Plant Breeding Institute, Cambridge. Seed of the varieties was obtained from the collection of cereal varieties maintained at Cambridge. A brief description of each of these varieties is given below and the seedling rust-reaction-types observed during the period 1956-60 are summarized in the right-hand columns of Table 1. Table

I.

Reactions ofparental varieties and F1 hybrids to races 2 B, 5, 8 and 8B of Puccinia glumarum Hybrid 46

Holdfast

Heine VII

Chinese 166

Cappelle

0 0 0 0

0* 0 0 0

IV 0 0 IV

O-II 0 0 IV

0 0 0 0

III-IV 0 0 0

0

0* 0 0

0 0 0

Race Soissonais Minister Cappelle

2B 5

8 8B Chinese 166

2B 5

8 8B Heine VII

2B 5

8 8B Holdfast

0 0 0 IV

III-IV

2B

a a

a a a

8 8B

0 0

2B

a a a

8 8E 2B 5

8 8B

*

0

a a

5

2B

5

Soissonais

a

a a a a a a

IV

5

Minister

0 0 0

III-IV

8 8B Hybrid 46

O-II 0 0 IV

IV

a

0 III-IV 0

0

a

a

0 0

0* 0 0 0

O-II

o-r

0 IV

0 IV

0* 0

II-IV II-IV II-IV IV

a

a a

a

0 0

a a

a

0-1*

a a

0-1

o-r

a a a

o-r

a

0 IV

Data obtained using a stock of Hybrid 46 re-selected for resistance to physiologic race 2 B.

Cappelle-Desprez (Hybride du Joncquois X Vilmorin 27). This wheat, which was bred in France, at present accounts for 70-80 % of the winter wheat acreage grown in Great Britain. It is resistant both as a seedling and as an adult plant to physiologic races 5,8 and 8B of Puccinia glumarum but is seedling susceptible to race 2 B. The variety shows a moderate degree of adult plant resistance to the latter race and is rarely attacked

24

Transactions British Mycological Society

severely in the field. This variety will be referred to as 'Cappelle' throughout this paper. Chinese 166 (parentage unknown). Chinese 166 (also known as 'Chinese Winter ') was collected in Western China early in the century and has been used extensively as a differential host variety by Rudorf (1930), Gassner & Straib (1932), Manners (1950), and Fuchs (1960 a). It was also used by Rudorf (1930) and Straib (1934) in their investigations into the inheritance of yellow rust resistance. It is resistant to the four physiologic races used in this investigation and has always given a constant reaction of the hypersensitive type. This variety is distinct from the variety Chinese Spring, monosomic lines from which, developed by Sears (1954), have been used for black stem rust investigations by workers in North America, and for investigations with yellow rust by Singh & Swami nathan (1959) in India. Heine VII (Hybride a Courte Paille x Svalof Kronen). This German variety showed a high degree of resistance to physiologic races of P. glumarum in Great Britain until 1955, when it was severely attacked by a race later identified by Batts (1957) as race 8 B. The variety is susceptible to this physiologic race, both as a seedling and as an adult plant. Holdjast (Yeoman x White Fife). Holdfast was bred at Cambridge, and, because of its high bread-making quality, has been widely used in crossing programmes. It is seedling susceptible (reaction type III-IV) to the physiologic races used in these tests under most conditions, but at high temperatures it gives a I-II reaction-type (Manners, 1950). A similar effect of temperature has previously been reported in certain varieties by Straib (1940). Holdfast shows some degree of adult plant resistance in the field and is rarely attacked severely at the later stages of development when rust attacks are most damaging. Such resistance may be related to the high temperatures often occurring in June and July. Holdfast was chosen as a parent for use in this investigation because of its susceptibility to all races of the pathogen used and its importance in the breeding programmes. This choice was unfortunate from a genetical point of view, in that the reactions of some of the F2 populations of crosses involving Holdfast were influenced by temperature in a manner which complicated the interpretation of the results. Hybrid 46 (Benoist 40 x 'other hybrids '). This British variety has a very high level of resistance to rust in both the seedling and adult plant stages. The commercial stock used at the beginning of these experiments was later found to consist of a mixture of resistant and susceptible plants when inoculated with certain isolates of the physiologic race group 2, which were identified after the variety had been released. A re-selected resistant line has since been established and some crosses were repeated using this stock. Minister (Benoist 40 x Prof. Delos). The Belgian variety Minister is very resistant to P. glumarum under normal testing conditions. With low light intensities, however, pustules of reaction-type II occasionally develop on seedling plants. Soissonais-Despre; (Mon Desir x Hybride a Courte Paille). This French variety is very similar to Heine VII in its reaction to P. glumarum. It will be referred to as 'Soissonais' in this paper.

~

c

R

e:

~

Table

2.

Reactions

iffourteen differential host varieties to phy siologic races 2 B, 5, 8 and 8B of Puccinia glu marum

M ichigan Amb er Ble ro uge d' Ecosse Strubes D ickkopf Webs ter C.l. 3780 Ho lzap fels Fr ilh Vilmor in 23 He ines Kolben Cars tens Dickkopf V Spa lding's Pr olific Chinese 166 R ouge pro lifiqu e ba rb u T riticum dicoccum va r, tricoccum Gers te von Fong T ien He ils Dorn berger Frankengerste Estanzuela 7Sa Petkuser rye H ybrid 46 (re-selected stock 46 / 670 ) Cappelle He ine V II

Race 2t

R ace 2X·

Race 2B

III- IV III- IV IV III-IV IV IV 0 0 -11 O-II 00 I-IV IV III00 i i

IV IV IV II-IV IV IV 0 II-IV O-IV i-O O-IV

IV IV IV III IV IV 0 O- II O- II 00 II-IV

-

-

-

-

IV II-IV

-

-

-

Race st IV I II-IV IV III + 110 -1 0 IV II + 00 O-II IV 11100

R ace 5

Race 8t

R ace 7X.

R ace 8

R ace 8 B

IV IV IV III II-IV O -III 0 IV O-III 00 0-111

IV III - IV IV 0 -1 0-1 II 0-1 0 O-II O- II 00 0-11 IV 11100

IV IV IV 0+ II-IV i-O 0 IV 0 + i-O 0 +

IV IV IV O - II + II-IV 0 -1 0 -1 O-II O-II 00 O-II

IV IV IV 0 -11 + IV 0 -1 O-II 0 -11 O-II 00 O-II

-

-

0

-

-

III-IV 0 -1

-

0 0

-

0 IV

-

• R eactions to physiologic rac es repor ted by Fu chs ( l g6o a) . t Reactions to ph ysiologic races rep or ted by M anners (1950) .

p

~

o ~ ~

.§

~

0-1

-

ia

00

00

0 0

0 IV

~

!=tl

o ~

~~ N

va

26

Transactions British Mycological Society

Physiologic races of Puccinia glumarum Each of the four physiologic races used in these experiments was isolated in Great Britain. Physiologic race determinations, using eleven of the standard set of differential host varieties (Gassner & Straib, 1932) together with three additional varieties (T able 2), indicated that the cultures could be classified as physiologic races 5 and 8 (Manners, 1950) and 2B and 8B (Batts, 1957). Physiologic races 2B and 8B are more aggressive (sensu Zadoks, 1959) than are physiologic races 5 and 8, and they have also been the most frequently identified ph ysiologic races in Britain and North-West Europe in recent years (Zadoks, 1960). These physiologic races, which are sometimes referred to as the' Cappelle race ' (2B) and the 'Heine VII rac e ' (8 B), are closely related to, if not identical with, physiologic races 2 X and 7X characterized by Fuchs (1960 a). These identifications are based on small differences in the reactions of the differential host varieties, which may be attributed as much to slight differences in the environmental conditions under which the tests were conducted as to fundamental differences in the pathogenicity of the isolates of the fungus. The present set of differential host varieties is unsatisfactory in that specific reaction spectra are not always obtained with mor e recently collected ph ysiologic races of P. glumarum. In addition two varieties, Webster and Carstens DickkopfV, are unstable in reaction-type and are very sensitive to fluctu ations in temperature ; it is upon small differences in the reaction-type shown by these varieties that ph ysiologic races 7 and 8 are distinguished. Fuchs (1960 b) has recently suggested that both these varieties should be removed from the differential series and replaced by other varieties which would, in effect, result in physiologic races 7 and 8 being grouped together. Inoculation procedure These investigations were confined to an examination of the seedling reactions to P. glumarum in the glasshouse of FI , F2 and Fa hybrid populations. Differential host varieties and the parental varieties were used as controls with each set of inoculations. Between seven and ten seedlings were grown in No. I John Innes Compost in small (3 or 3t in.) clay pots and inoculated when the first leaf was well developed and about 7 em. in length. The' dry-dusting' method of inoculation, using a I: 50 mixture of uredospores and sterilized talc , applied with a cyclone sprayer (Macer, 1962), gave a very uniform deposition of spores. Large polythene covers, sheltering 100-130 pots standing in water, were used for the inoculations and were left in position for 48 hr. after the inoculation to act as humidity chambers. The plants were not pr e-tr eated or handled in any way before inoculation. All inoculations were carried out in a cool glasshouse during periods from mid-January to mid-May, or from September to mid-November, in each of the years 1956 to 1960. The most favourable and uniform conditions for rust development occurred during these periods. In 1958 a glasshouse, in which it was possible to control the temperature during the

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

27

incubation period, was completed and used for some of the tests on the F 2 populations and for all the tests on the F 2 plant progenies. The temperature during the testing of this material was maintained at 60° ± 5° F. Tests carried out before 1958 were unavoidably subject to a somewhat wider temperature fluctuation. Under the conditions of experiment, symptoms of the disease and the various resistance reactions were clearly visible 15-17 days after inoculation and scoring was always completed within 19 days of inoculation, Only the reactions on the first leaf were considered, and the scoring system used was based entirely upon a reaction-type rating on a scale from 0 to IV. The 0 reaction-type was defined as non-sporulating but included necrotic and chlorotic reactions of various intensity and also the hypersensitivity reaction of Chinese 166. Reaction types I-IV were characterized by an increasing amount of sporulation combined with a decreasing intensity of chlorosis and necrosis (Gassner & Straib, 1932). EXPERIMENTAL RESULTS

Reactions o]parental varieties The reactions of the parental varieties have already been described and are summarized in Table I. These reactions were obtained from the combined observations of many separate tests, as both the parental varieties and the differential host varieties were inoculated with each batch of hybrids. Reactions of F1 hybrids The number of grains available for these tests was limited and only three to five F 1 plants of each cross were inoculated with each physiologic race of P. glumarum. The results, given in Table I, show that resistance to races 5 and 8 was in all cases inherited as a dominant character. In the case of race 2 B, the resistance of Chinese 166, Heine VII, Hybrid 46 and Soissonais was dominant, but that of Minister was recessive. The resistance of Chinese 166 and Hybrid 46 to race 8B was dominant, but that of Cappelle and Minister was recessive. Reactions qf F2 populations Samples of the F 2 populations of each cross were inoculated separately with each of the physiologic races. The sample size varied, but for most crosses 150-200 seedlings were examined after inoculation with each race. In populations in which segregation occurred it was necessary to divide the plants into two groups, resistant and susceptible. Plants giving reaction-types 0 and I were therefore classified as resistant and those giving reaction-types III and IV were classified as susceptible. In general, the populations fell clearly into one or other of these classes and very few plants with the intermediate reaction-type II were found. Where such plants occurred, they were allocated to either the resistant or susceptible group after consideration of the reactions of the parental varieties grown as controls in each test. This resulted, in nearly every case, in the plants being classified as susceptible. The division between resistance and sus-

28

Transactions British Mycological Society

ceptibility has therefore been drawn, in effect, between reaction-types I and II (i.e. 0 and I, resistant; II, III and IV, susceptible) and not between reaction-types II and III, as has been done in many other investigations of resistance to the cereal rusts. On the basis of the reactions obtained from the inoculation of F 2 populations, a hypothesis is proposed concerning the genes determining the rust reactions of each parental variety to each physiologic race of P. glumarum. The genes concerned are indicated in Tables 3-6, together with the numbers of resistant and susceptible plants to be expected according to the hypothesis, and the probability of the results obtained agreeing with it. In allotting symbols to these genes, a system similar to th at adopted by Knott & Anderson (1956) in designating the factors determining resistance to black stem rust (Puccinia graminis f.sp. tritici) has been used. This system differs in some respects from that advocated by Ausemans et af. (1946) and also from that suggested in the report of the International Committee on Genic Symbols and Nomenclature (U.N.E.S.C.O. 1957). It offers, however, a simple and conveni ent system of nomenclature which can be adapted as necessary when the genetic analysis is extended to include further wheat varieties or physiologic races of P. glumarum. The symbol Yr has been used to designate all factors det ermining resistance to P. gfumarum. Numerical subscripts (e.g. Yr2B . l ) denote loci at which independently inherited factors determining resistance to different races or groups of races are found ; where two or more resistan ce alleles occur at one of these loci, th ey are indicated by lower case letter subscripts (e.g, Yr2B . 2a )' Dominant genes are indicated by capital letters and recessive genes by small letters. Physiologic race :2 B. The resistan ce of the varieties Chines e 166, H eine VII and Soissonais to race 2 B (T able 3) appears to be det ermined by single dominant genes. A single recessive gene determines th e resistance of Minister; Cappelle and Holdfast are both susceptible to this race. Since all plants of the F2 from the cross of Soissonais with Heine VII are resistant, it is likely that the reaction s of these varieties are determined by genes at the sam e locus. Provision al symbols have been allotted to the genes determining reactions to race 2 B as follows: Cappelle Chinese 166 Heine VII Holdfast

+

Yr2B . l Yr2 B . 2a

Hybrid 46 Segregating Minister Yrw. 3 Soissonais Y r w . 2b

+

The segregation for resistant and susceptible plants obtained following inoculation with race 2 B agrees satisfactorily with the hypothesis, except in the crosses of Minister with Holdfast and Cappelle. The excess of resistant plants observed in the cross with Holdfast probably arose as a consequence of the instability of reaction of this variety when fluctuations occur in the environment. The very large excess of resistant plants in the cross of Minister with Cappelle requires more careful consideration and will be discussed later.

Table 3. Reactions

O bsd . Expd. Ratio O

Obsd . Expd . Ratio

S

:

X'

P

Minister, YrOB. a

Obsd. Expd. Ratio

X'

P

31 35"3 I

S

R

S

12 3 64 '7

136 194'3 3

II 0'0

2 10 221'0

I

10 8 '7 1

120 112'1 13

0'21 o'7---{}'5 38 38 '4 IS

3 2,6 I

:

25 6 243 '8 13

4457' 7 I

4' 33 0'OS---{}'02

:

132.8 3

44S6'2 3

122 144-,8 3

3'26 O'I -0'OS

o-o-o-B

160 152'0 13

:

18 25' 9 3

3'00 O'I-O'OS

0'06 18 7 173'3 3

:

69'33 V ery low

129 13°'3 15

p

Obsd . Ex pd. Ratio

r----"---,

R

0·68 o' S- o'3

X'

Cappelle, +

,--A----.,

r----"---,

P

O bsd. Expd. Ratio

~-,

,.--'-----,

X'

Heine VII, Yr. B.oa

+

Soissonais, YrOIl .•b

Cappe lle,

110 IOS'7 3

27 35'0 3

2'24 O'2---{}' 1

16 7 S9'o I

70

178 ' 0 3 263 'S8 Very low

~

B H eine VII, Yr.B.oa

M in ister, Yr2B.3

X P

So issonais, Yr2B . 2b

2

Chi nese 166, Yr. 8.1

R H old fast, +

ofF 2 populations to race

12 8

49 44-'2 I

0,64 o' 5---{}'3

14' 36 < 0'00 1

71 4 8 '2 I

R 70 72'7 3

S

R

S

27 24' 3

103 [II'O 3

4S 3 7'0

: 0'43 o' 7---{}'S

116 1[ 6'0

I

0 0'0

: 2'3 1 0'2 -0'[

I

~

~: aq

~

; ~

o ~ t"""

.§

~

~ ~

o ~

~ ~

~

\0

u.J

Table 4, Reactions of F2 populations to race 5 Ch inese 166, YrS , !

Minister, Yr. ,.c

H ybrid 46, Yr•.• b· Yr. ..

o

Cappelle, Yr....

Heine VII, Yr. ,..,

r---"-----. ,..------A----. ,------A------- , - - - " - - - - - - , , - - - - - " - - - ,

S

R Holdfast , +

Obsd ,

Expd. Ratio

194 189'7 3

S9 63'3 : I 8 0' 3 o' 7-o'S

i'"

p Soissonais, Yrs, 2b

OOOd, Expd, Ratio

212 216'5 15

Obsd, Expd, Ratio

x· p

Cappelle, Yr s , 3a

H ybrid 46, Yr. ,. b' Yr•.•

Obsd, Expd. Ratio X' p Obsd,

Expd, Ratio X'

p M inister, :Yr. ,.c

!I S 13 1'3 IS

l SI 14 1' 3 IS

:

0 9' 7 I

13 6'2

198 201'6

I7

13'4 : I 15 1'°3 0'3-0' 2

268 27 1' 0

3 0'0

I

8'00 0' 0 1-0'001

!l3

9 1'9

120'1 63

I

27' 0 9

Very low 122 122'8

Ratio

IS

p

25 8'7 I 32'68

86 9 2 '8 15

132 30 121'S 40' S 3 : I

9'47 0'0 1-0'00 1

Very low

Obsd , Exp d, X·

19 14' S I

1'4 9 0'3-0'2

X' p

H eine VII, Tr s , 2a

:

S

R

9 B'2 :

o' oB 0' 8-0'7

I

222 2 2 6 '0

S

R

109 12 113' 4 7,6 IS: I 2' 7S 0' 1-0'05 2

S9 63 '0 63

1'0 I

1' 2 9 0'3 -0' 2 2° 9 2 17'S 63

:

12 3'S 1

21'° 3

Very low 8S BS'o

° 0 '0

S

R 67 69'8 3

26 23' 2 : I 0'45 0'7-0'5

88 9 2 '8 IS

11

6'2 I

3'97 0'05-0'02 21 97 110' 6 7'4 I IS 26 '68

Very low

R 82 90 '8

3:

S

39 30 '2 I

3'43 0'1-0'05 135 13S' o

°

0 '0

Soissonais, Yr.,2b ~

R

S

114 48 121'S 4 0' S 3: I 1'93 0'2-0'1

~

~

~

~.

O:l

a·

§.:

~ B

S"

~

~ ......

~

4 0'0

~. Q

of F 2 populations to race 8

Table 5. Reactions Chinese 166, Yrs , 1

Mi niste r, Yr 8 • 3•

~ ~

Hold fast , +

Obsd, Expd, Ratio 2

X

p Soissonais , 1'r• . 2b

Obsd,

Expd . Rati o

X2

p

H eine VII, Yr• . 2a

Obsd , Expd. Ratio

R

S

R

S

130 109'5

16 36'5

125 " 2'5

25 37'S

3

: I 'S'4° < 0'00 '

135

129'4 15

p

6 3' 1

,66 159'415

[

o-r-c-og

Obsd. Expd,

Ratio

x2

p

H ybrid 46, Trs, 'b , 1'r• .•

l IS

2'9°

X'

Ca ppelle, 1'r•.•a

3 8,6 ,

: 3,89 0'OS-o'02

43 4S'9 IS

10 6'4-

92 9S·6 15

: I 5'82 0'02-0'0 1

H eine V II, Y rs , 2a

So issonais, Y ra. 2/)

42 42 '3 63

S

R

S

R

S

25 33'S

86 84.8

27 28'2

62 66 ,8

27 22'2

3:' 2,88 0'2-0'1

,

83

0'7 ,

91' 9

4 1'7 I

53 55'3 IS

: 0"3 0'8-0'7

106 106'0

R 109 100'5

3· , 6 0"-0'05 o 0'0

IS 6' 1

'S

: 13'86 < 0'001

:

3:

'

3:' 1 '06

0'3- 0 ' 2 178

' 78 ' 0

o 0 '0

.e.~... $:I)

(Jq

~

~

~

o 6 3'7 I

I'S2 0'3--0'2

::r: ~

~ ~

;:t

~

?:'

2

X p

5 S'4

: 0'03

"

7'8 '5: ' "40 0'3 -0'2

o 0'0

'4S ' 47 '0

82 8 1·6 IS

S

R 1' 4 "7'2

10 7 ' ° 9'3 63

' 02 [02'0

Cappelle, 1'rs , 3a

,-------'----, ,------A..--, ,-----A----, ~

4 10,6 I : 4'4 0 o 'OS-0 '02

0'2--0"

Ratio

X2 p

7'3

I

Obsd,

Obsd. Expd, Ratio

108'7 15

2'25

Expd .

Minister , 1'ra.a c

3: ' 5'S 7 0'02-0'0 1

H yb rid 46, Yr s , 3b.1'r. ..

2

0'0

o

~

f

I

o-q-o-B

W H

32

Transactions British Mycological Society

Physiologic race 5. The proportions of resistant plants obtained following inoculations of F2 populations with race 5 (Table 4) indicate that single dominant genes determine the reactions of Cappelle, Chinese 166, Heine VII, Minister and Soissonais and that two dominant genes determine the reaction of Hybrid 46. Since all plants in the two crosses Cappelle x Minister and Heine VII x Soissonais were resistant, it is likely that the reactions of each of these pairs of varieties are determined by genes at single loci. Similarly, since all plants in the crosses of Hybrid 46 with Minister and Cappelle were resistant, it seems probable that one of the genes carried by this variety is situated at the same locus as the gene carried by Minister and Cappelle. The genes concerned have been allocated provisional symbols thus: Cappelle Chinese 166 Heine VII Holdfast

Hybrid 46 Minister Soissonais

The data obtained supports this hypothesis satisfactorily, although an excess of susceptible plants was obtained from the crosses involving Heine VII. The high x2 values sometimes recorded occur because the expected numbers of resistant plants are, in fact, too small for the accurate application of this test. Physiologic race 8. The reactions obtained following inoculations with race 8 (Table 5) suggest that the genes determining reactions to this race are the same as those determining reactions to race 5. This result was not unexpected as the reactions obtained with these two races on the differential host varieties, and on numerous varieties and selections tested, suggest that the difference in pathogenicity of these races is not great. The genes determining reactions to race 8 have been allocated provisional symbols corresponding to those determining reactions to race 5, thus: Cappelle Chinese 166 Heine VII Holdfast

Hybrid 46 Minister Soissonais

This hypothesis is well supported by the data, though rather high X2 values were obtained with the crosses Chinese 166 x Holdfast and Cappelle x Soissonais. Physiologic race 8B. The proportions of resistant plants obtained following inoculations with race 8B (Table 6) were clearly very different from those obtained with race 8. They suggest that the reactions of Chinese 166 and Hybrid 46 are determined by single dominant genes, that of Minister by a single recessive and that of Cappelle by two recessive genes. All plants in the crosses of Cappelle with Minister and Hybrid 46 were resistant, although segregation occurred in the cross of Minister with Hybrid 46. It is therefore probable that one of the genes determining the reaction of Cappelle occurs at the same locus as that determining the reaction of Minister, and that the second gene occurs at the locus determining the

Table 6. Reactions of F 2 populations to race 8 B

""

Chinese 166, rrS8 ,1 ~

Holdfast,

+

Obsd. Expd, Ratio X'

P

+

Soissona is,

Heine VII,

+

CappeIIe,

rr&B ,3 a ' r r SB ,4a

rrBB .4b

-e !"

""

'-"

Minister,

r r8B

ae

13° 65 '3

0'3 1 O'5-
1°7 36 106'7 35'3 1 : 3 0'003 > 0' 9

:

13 1 195"7 I 3 85'0 V ery low

52 55'7

48 4 8 '7

I

I

R

S

R

139 120'7 3

22 4° '3

100 84'3 7

:

I

1I'06

<0'00 1 13 II'7

19 1 208 '5 I : 3 5"89 0 '02-0'01

121 114 '7 3

32 38'3

87 69' 5

176 18 7'3 55

42 3° ' 7 : 9 4'75 O'05-
216 216 '0

Obsd, Expd, Ratio X'

125 24 139'7 9'3 I : 15 25'80 Very low

135 134'1 13

Obsd, Expd. Ratio X·

137 138'1 13

P

rrSB,3a' rrSB ,fa

34 35'3 3

0'33 O'7-
33 3 1'9 : 3 0'05 0'9-<1.8

rrSB ,4 b

147 146'3 : 3 0'0 1 > 0 '9

Obsd. Expd, Ratio X'

p

~

43 46 '3

Obsd. Expd. Ratio

P

Hybrid 46,

142 138 '7 3

17 1 16 7'3 3

x'

S

R

I

Cappelle,

rr8.ll .3C

S

:

Hybrid 46 ,

Heine VII,

So issonais,

+

+

-

0 0'0

-

-

-

3° 3°'9 : 3 0'°4 0'9-<1,8

I : 0 '17 O'7-
:

I

1"37 O'3-
° 0'0

-

-

-

S

93 108'7 : 9 5"21 0 '02-0'05 28 28 ,6 : 9 0'03 0'9-<1,8

23 22'4 7

61 55 '7 : 9 1'15 0'3-0'2

38 43 '3 7

S

R ° 0'0

-

-

17° 170'0 -

0 0'0

-

S

0

log

0'0

1° 9'0

-

-

60 60'0

-

R

-

~

l::

(')

,----A-----, ~ ,-------A------ , - - - - - ' - - - - - , ~

R

Obsd. Expd. R atio X' P

P

Minister,

-

o

e:

~

.....

0'Cl

S

; ~

~

~ ~

~

~ ~

~

?tl 0

~

~~ OJ OJ

34

Transactions British Mycological Society

reaction of Hybrid 46. The following symbols have been provisionally allocated to the genes determining reactions to race 8B: Cappelle YrSB. 3a• YrSB. 4a Chinese 166 YrSB. 1 Heine VII + Holdfast +

Hybrid 46 Minister Soissonais

YrSB.4b Yrs B. 3c

+

The data agree with this hypothesis, except that an excess of susceptible plants was obtained in the cross of Chinese 166 with Hybrid 46.

Reactions of F2 plant progenies In order to confirm the hypothesis built up on the basis of the reactions of F z populations, and also to determine the relationships between the genes determining reactions to different races, the reactions of F2 plant progenies from critical crosses were investigated. At least ten seedlings from each F2 plant progeny were used in tests with each of the physiologic races. Table 7. Reactions of F2 plant progenies from the cross Chinese 166 x Minister Races 2B and 8B

Total ,------A----.

Seg, 3 R: I S 15R : I S

R

Ra='F

R"S

3 IS ego 15R:

and 8

S

Total

{ Ob sd. Expd, (7:6 :2 : 1)

Seg. IR :3 S

S

Obsd.

Expd. (7 :8 : I)

19 0 0

0

0

0

19

21'9

19 0

7 0

0

26

25'0

19

21"9

7

18'7

5 5°

3'1

19

5 5 3'1

X = 1·63 2

,

6'3

}X2 = 1'59 P

= 0'5--0' 3

P = 0' 7--0'5

Data from the inoculation of progenies from the cross Chinese 166 x Minister are given in Table 7. All progenies react in the same way to each race and it may be concluded that the same two genes determine the reactions of these varieties to all four physiologic races. One of these genes gives a dominant resistance to all four races, and the other a dominant resistance to races 5 and 8 and a recessive resistance to races 2 B and 8E. If these data are considered in conjunction with the data obtained from the F2 populations, it is clear that the single dominant gene corresponds with the genes found to determine the reaction of Chinese 166 to each of the races. The genes provisionally designated Yr2B , 1' Yrs.1' Yrs. 1 and YrS B. 1 are thus identical, and will be designated collectively Yrl' It is also evident that the gene giving dominant resistance to races 5 and 8 and recessive resistance to races 2 Band 8 B corresponds with the genes previously found to determine the reaction of Minister to each of these races. Thus the genes designated Yr2B.3, YrS • 3c , YrS • 3c and YrS B . 3c are also identical and will be collectively designated Yr3c • The figures obtained from inoculation of progenies of the crosses of

Puccinia glumarwn. F. G. H. Lupton and R. C. F. Macer

35

Chinese r66 with Heine VII are given in Table 8. They show that two dominant genes determine reactions to races 2 B, 5 and 8 and that one of these genes alone determines reactions to race 8B. Considered in conjunction with the data from F 2 populations, this observation confirms that Table 8. Reactions of F2 plantprogenies from the cross Chinese 166 x Heine VII (a) To races 2B, 5 and 8

Total

Race 2B (

R

R

Races 5 and 8

Total

Seg. 3 R: 1S 15R: 1S

I7 0

R: 1S 1I seS g, 15SR:IS

0

I'

{ Obsd, Expd, (7:8: I)

17'1

Obsd.

I'

17'1

llO

19'5 2'4

0

0

20 0

0 2

1:1

1:10

1:1

39

19'5

2'4

,

\

Expd, (7: 8: 1)

S

lx'

= 0'09

JP> 0'9

I

P> 0'9

X' = 0'09

(b) To races 5,8 and 8B

Races 5 and 8 R

Seg. 3 R: 1S 15R: 1S

II

0

4 2

II

Race 8B { ieg. ;:lR: 1S

8 19 19'0

I'

{ Obsd, Total Expd. 7:8: 1

16,6

,

Total

,

(

Obsd,

S

Expd. (I: 2: I)

0 0 2

8'5

1'0

~'5

} X' = 3'°5 P = 0'3--0'2

2

2'4 I

P> o'g

X' = 0'09

Table g, Reactions of Fz plantprogenies from the cross Heine VII x Minister Races 5 and 8

Total

A

I

R

Race 8B { ieg. Total

1

R:3S

{ Obsd. Expd. (7:8: r)

Seg. 3 R: 1S 15R: I S

S

Obsd.

15 7 3

0 18 5

0

0 2

15 25 10

25

23

2

50

22'9

25'0

3' r

\

v-

X'

=

0'74

Expd. (I :2:1)

12'5 25'0 12'5

}X'P == 0'5--0'3 1"00

I

P = 0'7-0'5

a single dominant gene determines the resistance of Chinese 166 to all races and also shows that a single gene determines the resistance of Heine VII to rac,es 2 B, 5 and 8, Thus the genes designated YrZB. Za, Yr5 . Za and Yrs, 2a are Identical. The segregation obtained from the cross of 3-2

36

Transactions British Mycological Society

Minister with Heine VII, given in Table 9, confirms this hypothesis. A similar segregation was obtained from the cross of Minister with Soissonais (Table 10), indicating that the genes Yr2B • 2b, YrS • 2b' and YrS • 2b are identical. Since there is no evidence from any of the crosses examined that Table 10. Reactions of F2 plant progenies from the cross Soissonais x Minister Races 5 and 8

Total .--------"-----.

R

Race 8B { Total

~eg. I R:gS

{ Obsd. Expd, (7: 8: I)

Table

Seg. gR:IS 15R: I S

S

Obsd.

Expd. (1:2: I)

0 0 I

13 16

10'0 20'0 10'0

Ig 7 4

0 9 6

24

15

I

22'5

20'0

2'5

\

= 2'25

X2

v

P

II

Total I

Seg, gR:IS

S

Obsd.

Expd. (I :2: I)

4 0 0

0 12 0

0 0 3

4'7 9.6 4'7

4

12

3

4 12 3 19

R

4'7 2

X

Table

12.

= 1'42 = 0'5-0'3

= 0'5-O'g

Race 2B

{ Obsd. Expd. (I: 2: I)

}X2

4°

J

rr:

Total

= 1·80 = 0'5-o'g

Reactions of F2 progenies from the cross Holdfast x Heine VII

I I.

Races 5{ R and 8 ~eg. 3 R: I S

P

} X2

=

9.6 v

1'42 P

P

4'7 J

= 0'5-0'3

Reactions of F 2 plantprogenies from the cross Holdfast x Soissonais Race 2B

Total I

Races 5 {R and 8 ~eg. 3 R: I S

Total

{ Obsd. Expd. (I: 2: I)

R

Seg. 3 R: I S

4 0 0

0 240

0 12

4

24

12

20'0

10'0

10'0

,

S

Obsd.

Expd. (1:2: I)

0

4 24 12 40

10'0 20'0 10'0

}X2 = 4.80 P

= 0'1-0-05

X2 = 4.80 P = 0'1-0'05

the genes carried by Heine VII and Soissonais are not themselves identical, they will be together designated Yr2• The varieties Heine VII and Soissonais have the common parent Hybride a Courte Paille, which shows reactions to the four physiologic races similar to those of Heine VII and

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

37

Soissonais, It therefore seems reasonable to suppose that all three varieties should carry the same gene for resistance. The hypothesis concerning the genes Yr1 , Yr2 and Yrs is confirmed by data obtained from progenies of the crosses of Heine VII and Soissonais with Holdfast, given in Tables I I and 12.

Table Ig. Reactions of F2 plant progenies from the cross Cappelle x Holdfast Race S R

1

(R

Race 8B

Total

7 R:9 S ~eg. I R:3S

J Obsd. I Expd. (7:8: I)

Seg. 3R: I S

S

Obsd.

Expd. (7:8: I)

6

16 =20

17'5 20'0

7 0

10

3 10

0

0

4

16

17

20'0

10'0

7

10'0 2

X

Total

,

A

,

= 3'45

P

4 40

}xP == 1'03 2

o'7~'S

2'5

= O'2~'1

Table 14. Reactions of F2 plant progenies from the cross Chinese 166 x Cappelle (a) To races 2 Band 8 Race 2B R

R

81~ 3 R: I S ace t ~eg. rsR:IS { Obsd. Total Expd. (1:2: I)

Total

,

(

Seg. 3 R: I S

S

Obsd.

Expd. (7:8: I)

16 15

17'S 20'0 2'5

IS 0 0

14 0

9

9

15

15

10

10'0

20'0

10'0

4°

0

lx' <= IP

18'28 0'001

v

X2

= 3'75

P = 0'2-0'1

(b) To races 8 and 8B Race 8

Total -,

R

Race 8B

Total

r

gR:IS Seg. IgR:gS 55R:9S S IR:gS ego 7 R:9 S S

{ Obsd. Expd. (7:8: I)

Seg. 3 R: I S rsR:rS

16

2

0

12

0 0

15

20'0

,

0

12

r I'g

7

8

9 2'5 I

P < 0'001

Expd. (37: 18: 8: r) 23'1

I

17'5

18'28

Obsd.

19

0

16

x2 =

S

40

5"0 0·6

X2 = 2'79 P = 0'5-0'3

Transactions British Mycological Society

38

Data from tests of progenies from the cross of Cappelle with Holdfast, given in Table 13, indicate that resistance of this cross to race 8B is determined by two recessive genes, one of which also determines dominant resistance to race 5. As Holdfast is susceptible to both races, these genes Table 15. Reactions of F2 plant progenies from the cross Cappelle x Heine VII (a) To races 2B and 5

, R

Race 5

r

Seg. 3 R: I S

6

3 R: I S ~eg, ISR: I S

{ Obsd, Total Expd. (I :2: I)

Total

Race 2B

0

8

0 6 4'7

9 9,6

X'

0

,

= 0'48

P

S

Obsd.

Expd. (7: 8: 1)

0

7

8'3

9

9'5 1'2

3 4 4'7

3 19

lx' == JP

2'93 0'3-0'2

lx' <= JP

20'6 0'001

lx' = .I =

0'3-0'2

J

= 0'8-0'7

(b) To races 2B and 8B

Total

Race 2B '--

I

R

S SBr~ ace 1Sego 7I R:9 R:3 S

J Obsd.

Total ( Expd. (I: 2: I)

R

Seg. 3 R: I S

2

3 2

3

S

6

S'3

7

9'5 1'2

4 4'7

19

6

9

9,6

,

'-

X'

= 0'4 8

P

Expd, (7:S: I)

2

4

6 4'7

Obsd,

J

= 0,8-0'7

(c) To races SB and 5

Total

Race SB

rR

3 R: I S Race 51 ~eg, 15 R: I S { Obsd, Total Expd. (7:8: I)

R

Seg, 7 R:9 S IR:3 S

4

3 2 2

3 0

4

7 10'0

7 8'7

S

6 1'3

=

19'3 0

Expd. (7:8: I)

8 9

8'7 10'0

3

1'3

P

2'93

20

!

;-

X'

Obsd.

P < 0'001

must be derived from Cappelle. Confirmation of the evidence concerning the genes determining the reactions of Cappelle may be obtained from consideration of data from crosses of this variety with Chinese 166, Heine VII and Soissonais, given in Tables 14-16. These data also confirm

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

39

the hypothesis put forward concerning the resistance genes carried by Chinese 166, Heine VII and Soissonais, When considered in conjunction with data from F 2 populations, it is evident that the dominant genes determining the reaction of Cappelle to races 5 and 8 are identical with each other and with one of the recessive genes determining its reaction to Table 16. Reactions qf F2 plant progenies from the cross Cappelle x Soissonais (a) To races 2B and 8

(R 3R: ' Ivace 8 ~ego 15 : IS R IS

l

R

Seg. 3 R: I S

S

S 0

2 II

0

0

Obsd, Total { Expd. (1:2: I)

Total

Race 2B

,

Obsd,

Expd, (7:8: I)

7

8 °7 10'0

Ilt

0

x = 2

1'3

13 10'0

5 5"0

2

P

ltO

It

5"0 I

v-

2'70

lXJ == 0'7-0'5 1'25

P

=

0'3-0'2

(b) To races 2B and 8B

Race 2 B

Total

"----~

Race 8B

r

, 7 R:9 S Seg, I R:3 S S

( Obsd. Total Expd. (I :2: I)

l

---'''---,

j{

Seg. 3 R: I S

S

Obsd.

2

4

2 0

8 8

7 2 13 10'0

2

5 5"0

0

4

It

ltO

Expd. (7: 8: 1 )

I::~ fXP2== 0'05-0'02 6'Sl 1'3

5"0

y-

2

X

= 2'70

P

= 0'3-0'2

(c) To races 8B and 8

Race 8B

, R

R

R

ace 8

j SSego

l

3 R: I S ISR: I S

{ Obsd. Total Expd. (7:8: I)

Total

A...

Seg. 7 R:9 S

4

Obsd.

Expd. (7:8: I)

2

7

2

Ilt

8'7 10'0

S

3

7 0

0

8

8

4

8'7 '--

X2

10'0 y-

= 6'SI

P

}x ==o'7-o'S 1'25 2

P

1'3 ltO

1°3 I

= o'OS-o'02

race 8B. Inoculation offifty F 2 plant progenies from the cross of Cappelle with Minister with races 2B, 8 and 8B confirm the observation made with F 2 populations that all plants from these crosses were resistant to the latter three races, and that resistance of this cross to race 2 B was determined by a single dominant gene. It therefore seems probable that the gene determining the reaction of Cappelle to races 5, 8 and 8B is allelic with the

40

Transactions British Mycological Society

factor Trac determining the reaction of Minister. This gene, Trac , also determines dominant resistance to races 5 and 8 and recessive resistance to race 8B. The Cappelle gene cannot, however, be identical with Tr3c , since it has been shown that Tr3c determines the resistance of Minister to race 2 B, to which Cappelle is susceptible . The gene determining the reactions of Cappelle to races 5, 8 and 8B has therefore been designated Tr3a • Consideration of the second gene determining the reactions of Cappelle to race 8B is made with data from crosses involving Hybrid 46. Table 17. Reactions of F2 plant progenies from the cross Holdfast x Hybrid 46 Races 5 and 8 R

Race 8B Total

{reg,

3R :I

{ObSd, Expd. (7:8: I)

S

Seg. 3R:IS ISR:IS

Total S

14 S

0 22

0

3

19

25

6 6

21'9

2S'O

3'1

\

X2

= 3'76

Y

P

0 0

Obsd,

Expd. ( I : 2: I)

14

12 '5 2 5'0 12·S

27 9

}x2 = 1'31 P

= O'3-Q'2

5°

I

= O' I-O' OS

Tests of F2 plant progenies from the cross of Holdfast with Hybrid 46 (Table 17) show that resistance of this cross to races 5 and 8 is determined by two genes, one of which also determines resistance to race 8B. Considered in conjunction with data from F2 populations, it seems that the genes rr5 . 4, rrs ,4' and rTSB • 4/, are identical; they hav e been collectively designated Tr4b . The recessive gene rrw. 4a carried by Cappelle is allelic with rr4 b and is renamed rr4a . The genes YrS • 3b and rrS • 3b are also identical; since they do not confer resistance to race 8 B, they form a third member of the allelic series including Tr3a and rrac carried by Cappelle and Minister, respectively, and have been collectively designated Yr3b ' DIS CUSSION

The literature on inheritance of resistance to yellow rust has been surveyed, but reference should be made again to the pioneer experiments of Biffen (1907) and Rudorf ( I 930), which laid the foundation for investigations in the field and under glasshouse conditions respectively. It is, however, remarkable that no co-ordinated study of the factors determining resistance to this disease has yet been published. The absenc e of such a study is largely due to the practical difficulties involved in handling the pathogen on a large scale. The reaction of some wheat varieties and hybrids to P. glumarum is affected by changes in environmental conditions. Controlled studies of the inherit ance of resistance to this organism have therefore only been possible since suitable facilities for testing on a large scale have become available. The data presented in this paper, though in no way comprehensive,

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

41

could form a basis for further investigations. The genes by which the resistance of the varieties to races 2B, 5, 8 and 8B of P. glumarum is determined are summarized in Table 18. A total of seven genes situated at four loci has been identified. Resistance is thus determined by a relatively simple major gene system, similar to that shown by Knott & Anderson (1956) to determine the reactions of T. aestivum and T. durum to P. graminis var. tritici (see also Knott, 1957 a, b). Table 18. Summary of genetic factors determining resistance to races 2 B, 5, 8 and 8B of Puccinia glumarum Chinese 166 Cappelle Hybrid 46 Minister Heine VII Soissonais Holdfast

Race 2 BRace 5 1"r1 * 1"r1 + 1"r3([ 1"r3b • 1"r4 b 1"r3C 1"r2 1"r2

+

Race 8 Race 8 B 1"r1 1"r1 1"r3([ }r3a .yr4a 1"r3b • 1"r4b 1"r4b 1"r3C yr 3c 1"r2 + 1"r2 +

+

+

'" Dominant factors indicated by capital letters and recessive factors indicated by small letters.

In contrast to the reports of many previous workers (Armstrong, 1922; Singh & Swaminathan, 1959; Bahl & Kohli, 1960), it has been found that resistance is in general inherited as a dominant character, though in two varieties, Cappelle and Minister, resistance to certain races is inherited as a recessive. A particularly interesting feature is that certain of the genes appear to determine dominant resistance to some races but recessive resistance to others. The gene 1"1"3c, carried by the variety Minister, determines dominant resistance to the less aggressive physiologic races 5 and 8 but recessive resistance to the more aggressive races 2B and 8B. Similarly, the gene 'Yr3 ,,, carried by Cappelle, determines dominant resistance to races 5 and 8 but recessive resistance to race 8 B. It appears possible that the rust reactions determined by these two genes are influenced by a gene dosage effect. Plants carrying either of these genes in a heterozygous condition exhibit resistance to the less aggressive physiologic races 5 and 8, though only homozygous plants show resistance to the more aggressive races 2Band 8 B. Similar observations were reported by Knott & Anderson (1956) in relation to resistance to races 15Band 56 of P. graminis f.sp. tritici. In this context, it is interesting to reconsider the anomalous segregation obtained when F 2 populations of the cross Minister x Cappelle were inoculated with race 2B of P. glumarum. According to the hypothesis summarized in Table 18, resistance in this cross is determined by a single recessive gene. In fact, as is shown by the data in Table 3, 167 plants were found to be resistant and only 70 susceptible. The gene 1"r3" carried by Cappelle is not able to confer resistance to race 2B. The presence of this gene in a heterozygous condition, however, could increase the effect of the gene 1"1"3c, carried by Minister, to a level at which heterozygous plants

42

Transactions British Mycological Society

exhibit resistance and a ratio of 3 resistant: I susceptible would thus be found in an F2 population of this cross. If this suggestion is correct, the expected numbers ofresistant and susceptible plants would be 180'75 and 57'25, respectively. The observations obtained would then give a X2 for goodness of fit Of2'3I (P = 0'1-0'2). The operation of a gene dosage effect could be explained in terms of a biochemical system controlling resistance; alternatively, it could be due to a variation in some anatomical attribute, such as thickness of mesophyll cell walls. The high specificity of the host-parasite relationship is, however, difficult to explain on the latter hypothesis. The observed segregation in reaction to race 2B in the cross of Minister with Cappelle shows that the phenomenon cannot be explained in terms of a pair of distinct but closely linked genes. The physiologic races used in this investigation were identified by a consideration of their reactions on the empirically selected standard set of differential host varieties, chosen because they served to differentiate between certain known races of P. glumarum; little or nothing is known of the genetic basis upon which their reactions to these races depend. The majority of these differentials were chosen by Gassner & Straib (1932) and Straib (1937) during investigations of physiologic races occurring in Germany, though they have been supplemented by further varieties, as races which could not be clearly distinguished on the original differentials have appeared (Batts, 1957; Fuchs, I96oa). The poor reproducibility of differential reactions obtained with these varieties has already caused some confusion in the identification of European physiologic races of P. glumarum. The most outstanding example of this concerns the physiologic race attacking the variety Heine VII, which was identified as race 8 B by Batts (1957) and as race 7X by Fuchs (I960a). A consideration of the genes which have now been identified demonstrates a more fundamental danger inherent in this procedure. Races 8 and 8B (7X), for example, give similar reactions on the Gassner & Straib differentials, and would not have been distinguished if an extra differential, Heine VII, had not been added to the series. It is clear, however, from the data given in Table 18, that there are considerable differences between the genes by which reactions to these races are determined. These indicate greater differences in pathogenicity between these races than might have been expected from their reactions on the present differential host varieties. If breeding for resistance to yellow rust is to be carried out on a systematic basis, it would be an advantage if the existing differentials could be replaced by varieties carrying known single genes or combinations of genes for yellow rust resistance. Furthermore, since the expression of major genes for resistance may, to some extent, be influenced by the genetic background of the host plant, it is desirable that the new differential varieties should be of similar genotype except for the genes determining rust reaction. The use of such synthesized lines as additional differential varieties would have certain advantages. It would, for example, ensure that when new physiologic races of P. glumarum were inoculated onto these lines, it would immediately be known which genes, or combi-

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

43

nations of genes, continued to confer resistance. Such data could rapidly be absorbed into plant breeding programmes. It is realized, however, that the efficient behaviour of a differential host variety may be influenced by other factors than the presence of major genes for resistance. It has been shown, for example, by Green, Knott, Watson & Pugsley (1960) that the transference of genes for black stem rust resistance in wheat to a common variety by back-crossing was in certain cases accompanied by changes in the level of resistance expressed. These workers suggest, however, that this change in expression of resistance may have occurred as a result of the presence, in the genotype of the recurrent parent, of a gene allelic to the gene transferred but determining a lesser degree of resistance. They go on to stress the value of lines back-crossed to a very susceptible variety in the identification of genes or physiologic races, emphasizing in particular the advantages gained from the elimination of epistasis. As a first stage in the production of a new set of differential host varieties for P. glumarum, wheat lines homozygous for each of the genetic factors are being identified and the factors transferred by back-crossing to a common parent. The synthesis of a set of differential varieties each carrying known genes for rust resistance assumes the existence of complementary genetic systems for resistance and virulence in host and pathogen. This does not necessarily imply a simple gene for gene system as suggested by Flor ( I 956). Indeed, the indication of a multiple allele system at certain loci suggests that a more complex relationship probably obtains. No direct analysis of genes for aggressiveness in the pathogen can be attempted with P. glumarum, however, owing to the absence of a known sexual phase in its life cycle. It is hoped that the data presented in this paper may form the basis for further genetical studies incorporating additional resistant wheat varieties and an increased range of physiologic races of the pathogen. We would like to express our appreciation of help received from Dr]. G. Manners and the late Dr C. C. V. Batts in providing isolates of Puccinia glumarum, to Dr G. D. H. Bell, Director of the Plant Breeding Institute, for his interest and support throughout these investigations and also to Mr H. P. Hughes for his technical assistance. REFERENCES ARMSTRONG, S. F. (1922). The Mendelian inheritance of susceptibility and resistance to yellow rust (Puccinia glumarum Erikss, et Henn.) in wheat. ]. agric. Sci. 12, 57-96. ATHWAL, D. S. & WATSON, 1. A. (1954)' Inheritance of the genetic relationship of resistance possessed by two Kenya wheats to races of Puccinia graminis tritici. Proc. Linn. Soc. N.S. W. 79, 1-14. AUSEMUS, E. R. (1943). Breeding for disease resistance in wheat, oats, barley and flax. Bot. Rev. 9, 207-260. AUSEMUS, E. R., HARRINGTON,]. B., WORZELLA, W. W. & REITZ, L. P. (1946). A summary of genetic studies in hexaploid and tetraploid wheats. ]. Amer. Soc. Agron. 38, 1082-1099. BAHL, P. N. & KOHLI, S. P. (1960). Inheritance of seedling resistance to some Indian races of yellow rust in intervarietal crosses of Triticum aestiuum. Indian]. Genet. 20, 4 2-47.

44

Transactions British Mycological Society

BATTS, C. C. V. (1957). The reaction of wheat varieties to yellow rust, Puccinia glumarum, 1951-1956. J. nat. Inst. agric. Bot. 7-18. BIFFEN, R. H. (1906). Mendel's laws of inheritance and wheat breeding. J. agric. Sci. 1,4-48. BIFFEN, R. H. (1907). Studies in the inheritance of disease resistance. J. agric. Sci. 2, 109- 12 7. FAVRET, E. A. & VALLEGA,j. (1953)' Inheritance of resistance to Argentine races of Puccinia glumarum in the wheat 'Chino 166'. Phytopathology, 43, 471 (Abstr.). FLOR, H. H. (1956). The complementary genetic systems in flax and flax rust. Advanc. Genet. 8, 29-54. FUCHS, E. (1960a). Physiologische Rassen bei Gelbrost (Puccinia glumarum (Schm.) Erikss. et Henn.) auf Weizen. NachrBl. dtsch. PflSchDienst, Stuttgart, 12, 49-63. FUCHS, E. (1960b). Personal communication. GASSNER, G. & STRAIB, W. (1932). Die Bestimmung der biologischen Rassen des Weizengelbrostes (Puccinia glumarum f. sp. tritici (Schmidt) Erikss. u. Henn.), Arb. biol. Abt. (Anst.-Reichsanst.), Berl. 20, 141-163. GREEN, G.J., KNOTT, D. R., WATSON, I. A. & PUGSLEY, A. T. (1960). Seedling reactions to stem rust of lines of Marquis wheat with substituted genes for rust resistance. Ganad. J. Plant Sci. 40, 525-538. HUBERT, K. (1932). Beitrage zur Ziichtung rostresistenter Weizen. Z. Zucht. A, 18, 19-52. HYLANDER, N., J0RSTAD, I. & NANNFELDT, ]. A. (1953). Enumeratio Uredinearum Scandinavicarum. Op, bot. (Bot. Notiser (Suppl.)), I, 1-102. KNOTT, D. R. (1957a). The inheritance of rust resistance. II. The inheritance of stem rust resistance in six additional varieties of common wheat. Ganad. J. Plant Sci. 37, 177- 1 9 2. KNOTT, D. R. (1957b). The inheritance of rust resistance. Ill. The inheritance of stem rust resistance in nine Kenya varieties of common wheat. Ganad. J. Plant Sci. 37, 366-3 84. KNOTT, D. R. & ANDERSON, R. G. (1956). The inheritance of rust resistance. I. The inheritance of stem rust resistance in ten varieties of common wheat. Ganad. J. agric. Sci. 36, 174-195. MACER, R. C. F. (1962). Observations upon seedling reactions to Puccinia glumarum (Schm.) Erikss. & Henn. and the inheritance of yellow rust resistance in wheat. Proc. and. European Yellow Rust Gonj. 1960. Tech. Ber. Ned. Graan-Gentrum, no. 5. MANNERS,j. G. (1950). Studies on the physiologic specialization of yellow rust (Puccinia glumarum (Schm.) Erikss. & Henn.) in Great Britain. Ann. appl. Biol. 37, 187-214. PAL,B. P., SIKKA, S. M. & RAO, M. V. (1956). Inheritance studies in wheat. Indian J. Genet. 16, 32-46. PLESSERS, A. G. (1954). Genetic studies of stem rust reaction in crosses of Lee wheat with Chinese monosomic testers. Agric. Inst. Rev. 9, 37. RAO, M. V. & AGRAWAL, R. K. (1960a). Inheritance studies in wheat. V. Inheritance of seedling reaction to physiologic races 40 and 75 of stem rust in some in tervarietal crosses of Triticum aestivum. Indian J. Genet. 20, 48-52. RAO, M. V. & AGRAWAL, R. K. (1960b). Inheritance studies in wheat. VI. Inheritance of seedling reaction to physiologic race 42 and biotype 42 B of stem rust in some intervarietal crosses of Triticum aestivum. Indian J. Genet. 20, 53-57. RunORF, W. (1930). Beitrage zur Immunitatzuchtung gegen Puccinia glumarum tritici (Streifenrost des Weizens). Phytopath, Z. I, 465-526. SEARS, E. R. (1954). The aneuploids of common wheat. Res. Bull. Univ. Mo. no. 572. SEN, S. & JOSHI, M. G. (1955). Inheritance of resistance to black rust in wheat. Indian J. Genet. 15, 36-46. SINGH, M. P. & SWAMINATHAN, M. S. (1959). Monosomic analysis in bread wheat. III. Identification of chromosomes carrying genes for resistance to two races of yellow rust in Cometa Klein. Indian]. Genet. 19, 171-175. STRAIB, W. (1934). Untersuchungen zur Genetik der Gelbrostresistenz des Weizens. Phytopath, Z. 7, 427-477. STRAIB, W. (1937). Die Untersuchungsergebnisse zur Frage der biologischen Spezialisierung des Gelbrostes (Puccinia glumarum) und ihre Bedeutung fur die Pflanzenziichtung. Zuchter.9, 118-129.

Puccinia glumarum. F. G. H. Lupton and R. C. F. Macer

45

STRAIB, W. (1940). Der Einfluss des Entwicklungsstadiums und der Temperatur auf das GeIbrostverhaIten des Weizens. Phytopath, Z. 12, 113-168. V.N.E.S.C.O. (1957). Report of the International Committee on genic symbols and nomenclature. C.R. Un. Int. Sci. Bioi. Paris, B, no. 30. WATSON, I. A. & WATERHOUSE, W. L. (1949). Australian rust studies. VII. Some recent observations on wheat stem rust in Australia. Proc. Linn. Soc. N.S. W. 74, 115- 131. ZADOKS, J. C. (1959). On the formation of physiological races in plant parasites. Euphytica,8, I04-II6. ZADOKS, J. C. (1960). Preliminary report on the 'Yellow rust trials project' in 1959. Tech. s«. Ned. Graan-Centram, no. 3.

(Accepted for publication 18 January 196 I)