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Race-specific factors of resistance to Bremia lactucae in the world assortment of lettuce
Scientia Horticulturae, 22 (1984) 23--32 Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands
23
RACE-SPECIFIC FACTORS OF RESISTANCE TO BREMIA LACTUCAE IN THE WORLD ASSORTMENT OF LETTUCE
A. LEBEDA
Plant Breeding Station, 798 17 Smr2ice (Czechoslovakia) (Accepted for publication 31 May 1983)
ABSTRACT Lebeda, A., 1984. Race-specific factors of resistance to Bremia lactucae in the world assortment of lettuce. Scientia Hortic., 22: 23--32. The presence of race-specific factors of resistance to Bremia lactucae was studied in a set of more than 220 lettuce cultivars and lines. The results have proved general validity of a genetic model postulated for Lactuca sativa--Bremia lactucae relationships on the basis of gene-for-gene theory, The whole set was divided into 29 groups according to reaction and presence of resistance factors. Besides the group of "universally susceptible" cultivars, the most numerous are those carrying the factors: R2,4; R3; R12; R13; R14 and R3,7. A new, as yet u n k n o w n resistance factor(s) is supposed to occur in 'Kinemontepas'. The evolutionary aspects of this enormous genetic diversity of race-specific resistance in Lactuca sativa are discussed. Keywords: Bremia lactucae; downy mildew; Lactuca sativa; lettuce; resistance.
INTRODUCTION
In recent years, much progress has been made in the sphere of genetic relationships between lettuce (Lactuca sativa L.) and downy mildew (Bremia lactucae Regel). Crute and Johnson (1976a) were the first to interpret these interactions on the basis of the gene-for-gene theory (Person, 1959). An important step in the study on race-specific resistance of lettuce had been realised after this genetic model was postulated in the above-mentioned pathosystem. This had been preceded by more than 50 years of intensive research at the level of cultivar--race interaction (Jagger, 1924; Jagger and Whitaker, 1940; Channon and Smith, 1970; Ventura et al., 1971; Eenink, 1974; Globerson et al., 1974}. The establishment of a basic genetic model meant no stop in the research oriented towards better understanding of race-specific resistance of lettuce to Bremia lactucae (Blok and Van Der Schaaf-Van Waadenoyen Kernekarnp, 1977; Lebeda, 1979b, c; Osara and Crute, 1981). Recent papers (Lebeda et al., 1980; Osara and Crute, 1981; Crute and Lebeda, 1981; Lebeda, 1982)
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© 1984 Elsevier Science Publishers B.V.
24
show that it will be necessary to modify and revise some data and presumptions in the previous model (Crute and Johnson, 1976a; Johnson et al., 1977, 1978). The objective of this study was to verify the general validity of the genetic model of the L. sativa--B, lactucae relationship, to integrate some new results, and to consider the possibilities of applying some sources of racespecific resistance in lettuce breeding. MATERIALS AND METHODS
Tests were accomplished in the set of more than 220 cultivars and lines belonging to the world lettuce assortment. The plant material mainly originated from the lettuce germplasm collection of the Plant Breeding Station at Smr2ice. Further substantial lettuce seed samples were provided by the Research Institute of Vegetable Growing and Breeding in Olomouc, Czechoslovakia, and the National Vegetable Research Station, Wellesbourne, Great Britain. A total of 12 B. lactucae isolates (CS1--CS12) were used for inoculation. Their virulence phenotypes were determined in our previous papers (Lebeda, 1979a, d, 1980a, 1982). Verification and determination of resistance factors (R-factors) and their combinations in the set of lettuce cultivars studied was accomplished by means of p h e n o t y p e analysis, whilst interpretation of the results was made on the basis of the gene-for-gene theory (Person, 1959). The tests were carried out on fully expanded cotyledons of lettuce seedlings, grown in plastic trays (500 X 340 X 50 mm) lined with moist filter paper. Every isolate was used to test 20--30 seedlings of each cultivar in 2--3 replications. The seedlings were raised in a controlled chamber at 20--24°C. The isolates of B. lactucae were maintained and multiplied on susceptible cultivars, usually carrying the factors R2 or R4 or their combinations. Inoculum was prepared by washing 1--3-day-old spores from the surface of cotyledons with distilled water. Inoculum concentration was adjusted to 105 spores m1-1 . The seedlings were treated with inoculum by means of a glass sprayer. Incubation t o o k place at 14--16°C, under a 12-h photoperiod. Sporulation was recorded on the 6th to 14th day after inoculation. The cultivars were classified, according to the intensity of sporulation, as resistant or susceptible (Crute and Johnson, 1976a; Crute and Norwood, 1978). In some cases, when incomplete resistance was found, quantitative estimation of sporulation intensity was carried o u t using the method of Dickinson and Crute (1974). Occasionally, combined response was observed on the seedlings, referring to segregation or heterogeneity (Crute and Dickinson, 1976}. RESULTS
The results of the tests are given in Table I. The set of cultivars and newlyselected lines studied were divided into 29 groups according to the presence
25 of supposed race-specific R-factors and their combinations. In some cases, the cultivars were grouped according to t y p e of reaction. For better understanding, each of the incompatible reactions is accompanied by symbols of R-factors which are expected to control all of them. The first group contains the cultivars which are considered to be "universally susceptible" on the basis of up-to-date knowledge. The second group comprises the results of comparison between t w o origins of 'Blondine', differing from each other in their response to the isolates CS3 and CS5. The t w o types of different reactions were proved as a result of a detailed study on 5 origins of 'Blondine' (Lebeda, 1982). The compatibility to CS3 and CS5 of these origins was always characterised by limited sporulation. It may be supposed that the different behaviour of the origins of 'Blondine' is n o t due to another R-factor, b u t probably mainly to a modified action of R1 under the influence of genetic background or environment. The origins Zwaan and Tozers are in good agreement with the original genetic model of Crute and Johnson (1976a). The third group contains the cultivars possessing the combination of the factors R2,4 or R2. It seems impossible to distinguish the combinations of these factors using CS-isolates. The factor R3 is relatively frequent in the assortment. In some cultivars, we may even expect the combination of the factors R3,4, which was impossible to determine by means of the isolates used. The presence of the respective R-factors was proved in Groups 5--11 in accordance with the postulates of Crute and Johnson (1976a, b) for individual cultivars. Group 12 is the most numerous and also rather interesting, as it comprises the cultivars which have been considered as "universally susceptible" until now. This presumption was nullified as a result of the incompatible reaction with the isolate C86. A more detailed study has shown that these cultivars carry a hitherto u n k n o w n race-specific R-factor (Crute and Lebeda, 1981), which was designated as R 1 2 (Lebeda, 1982; Crute and Lebeda, 1983). Group 13 contains the cultivars carrying the factors R1 or R7, initially expected on the basis of their reaction with CS isolates. The cultivars were tested using the isolates Tv, IM43 and W5. The tests have shown that their genotype has none of 11 R-factors so far known. The existence of a new race-specific R-factor designated R13 has been proved (Lebeda, 1982; Crute and Lebeda, 1983}. Group 14 comprises the cultivars with identical response to CS isolates, b u t according to previous data they are n o t completely identical as far as R-factors are concerned. The cultivars are also expected to have another new race-specific factor R14 (Lebeda, 1982; Crute and Lebeda, 1983). With respect to the rather diverse interactions of the cultivars in question with other B. lactucae isolates (except for CS isolates) it may be supposed that other R-factors are involved (in parentheses). Combinations of known R-factors were found or proved in Groups 15--20. Only in some cultivars (e.g. 'Brioso', 'Portato', 'Bremex', 'Munex')
--
Magiola
+
-
Aehiles, Agilo, Andy, Apollo, Ardito, Atlas, Bessy No. 57, C o r y , D a w s o n s Mildura, Divalo, Egivo, Invemo, Kastaar, Kloek, Kondor, Kordaat, Korrect, Kwiek, Mildura, No. 60, Original, Proeftuins Blackp o o l T y p e 57, V a l e n t i n e , Van Der Bergs Secura
4
Valmaine
+
Amanda Plus, Amplus, Budas Hajtato, Deci Minor, Deciso, Knap, Kr~l bi~je (May King), Miranda, Sea Queen, T r i u m f , V[de~isk~, V i t e s s e
3
5
-
+
Lobjoits Green Cos
--
+
Varka, Valdor, Winterday
B l o n d i n e (British, Dr. C r u t e )
+
Attraction SperKngs, Bautzener Dauerkopf, Chrestia, Clauses Peson, Helga, Herkules Winter, Ivcto, KB-4, Kolos, Laltue ~ , Maiw~nder Winter, Mona, No. 39, Olof, Plenos, Presto, Resistent, Rexina, Silvester, Virilde, Wowo
R3
R3
R1
R1
CS1
Isolates
Blondine (Dutch, It. BIok)
2
1
Croup Cultlvars/lines
+
+
+
+
+
+
+
+
+
CS2
-
-
+
+
-
•
a
+
3
3
?
1
CS3
-
-
+
-
-
+
+
+
3
3
1
1
CS4
-
+
+
+
+
-
+
+
+
5
?
1
CS5
+
-
-
+
--
+
+
+
3
3
1
1
CS6
1
1
+
3 (_)3
+
--
-
+
+
+
CS7
+
-
-
+
+
+
+
+
+
3
3
CS8
+
+
+
+
+
+
+
+
+
CS9
+
+
+
+
--
-
+
+
+
1
1
CS10
+
+
+
+
+
+
•
+
+
CSll
--
-
-
+
-
+
+
+
5
3
3
1
1
CS12
R5
R3 (+4?)
R3 (+4?)
R2,4
R1
R1
R0
R0
RO
Postulated host genotype
R e a c t i o n s o f l e t t u c e c u l t i v a r s t o i s o l a t e s o f B r e m i a l a c t u c a e . + = s u s c e p t i b l e ; - = r e s i s t a n t ; ( - ) = i n c o m p l e t e r e s i s t a n c e ; (+) = m i x e d r e a c t i o n ; • = n o t t e s t e d
TABLE I
t~
+
+
Hilde-Asmer
New
+
+
Butterkopf, Exeello
Excellent,
Hilde-Tozer
+
+
Heart
Unrivalled
Constant
+
+
+
+
+
+
+
+
Atu'e lla , ~ A [ a ~
Market
+
+
AWU, Be~ga. Berga Orl~inal~ D~teniek~ Atmkce, Neusldler, Prado, Suzan, Tagerwiner Nova, Winter Butterkopf
+
-
+
+
+
Rll
R9
+
+
+
-
All the Year Round, Amerlka, Arctic King, Attraetie, Boheme Blonde Gro~e, Clauses Aurelia, Delta, d~Iivezo Vezzie~es, Dry Weather, Grosso, Hilds Capo, Hilde, I-lilds Savio, Ka~'aner Sommer, Magna, Maya, M~iniek~" MJj0 Merveilled d'Hiver, Neckarriensen, Ostinata, Relly, Rigoletto, Steran, Tenax, Viruzan, Wunder yon Stuttgart
-
Hilde
Capitan, Mondlan
serriola,
+
Tornado
Sucrine,
L.
-
Bourguignonne
9
×
+
Valverde
8
12
11
I0
--
Ruby
R7,13
Mesa
659,
+
Sabine
11
R6
+
•
•
•
•
•
•
+
+
-
+
+
+
.
II
_7,13
+
.
+
+
•
+
+
+
+
+
+
+
+
-
+ 9
.
_7,13
+
.
6
+
+
•
+
+
+
+
+
+
+
-
-
-
R10
9
R8
7,13
-
6
R12
11
9
8
--
12
( )R12 12 -2 (~)1 12 12 12 12 -
-
-
+
-
-
_7,13
-
6
+ + + +
+ + + +
+
+
+
+
+ +
+
+
+
+
+
+
11
9
8
4-
(_)7
+
+
+
--
+
-
--
-
_7,13
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
6
+
+
•
+
+
+
+
+
+
--
+
-
+
--
11
9
_I3
-
+
+
+
+
+
+
+
+
+
+
+
+
+
-I-
+
-
6
6
+
+
+
+
+
+
+
+
+
+
-
-
--
--
10
9
8
_7,13
-
R12
R12
R12
R12
R12
RI2
R12
R12
R12
Rll
RIO
R9
R8
R7
R6
t~
Bremex, Munex
Fila, I.a~o M o r a v a
18
19
Campan, No. 1177/3, Type 6234, Type 796A
IAtrganda, Pirat
17
_R1,7
__
11
-- 11
-- R l l
Rll
+
_R1,7
--
7
3
_
11
_ 11
_1,7
--
÷
4-
4-
4-
4-
4-
4-
+
+
R3
R14
R14
R14
R14
4-
_R7
--
-
Imperial Winter
Bianka
-
Majorette
16
1,7
+
--
Spartan Lakes
Brioso, Portato
÷
4-
-
Pan-~lej-eaj
R14
+
4-
-
4-
4-
Start
R14
R14
--
13
Liba, Valore
4-
•
.
--
4-
+
+
CS3
Muck
R14
R13
13
CS2
--
-
-
CS1
Isolates
Dua, Lednieky
Continuity, Empire, New York, Pennlake, Webbs Wonderful, Windermere
A u r o r a , Cavoli di N a p o l i , Dorian, Ootte Jaune d'or, Gravitas, Guldrottmingen, H u b a r d Mazket, Ou Laitue Oeuf, Primo, Wan-ShouYmm-Ye
15
14
13
Group Cuitivars/lines
T A B L E I (continued)
.
13
_
4-
+
_1,7
7
3
_1,7
4-
4-
4-
4-
÷
4-
4-
+
.
13 .
CS4
.
13
4-
+
_1,7
_7
4-
_1,7
4-
4-
4-
4-
4-
+
4-
+
.
. 13
CS5
.
.
13
-
--
11
-- 11
_1,7
7
3
_1,7
4-
4-
4-
4-
4-
4-
4-
4-
.
13
CS6
__
11
_ 11
_1,7
_7
__
3
1,7
4-
+
4-
+
4-
4-
+
4-
13
13
CS7
_
4-
+
_7
(_)7
3
_7
÷
4-
4-
4-
4-
4-
+
4-
4-
+
CS8
4-
+
+
+
÷
+
4-
4-
4-
4-
4-
4-
+
4-
4-
+
CS9
13
13
--
11
-- 11
+
+
4-
+
4-
4-
4-
4-
4-
4-
+
4-
--
-
CS10
+
4-
4-
+
4-
+
4-
4-
4-
4-
+
4-
+
+
4-
+
CSll
4-
4-
1,7
7
3
1,7
14
14
14
14
14
14
14
14
13
13
CS12
R l l OR R2,11
R2,11
R1,7
R2,7
R2,3
R1,2,7
R14
R 1 4 (+1 ?)
R14
R14
R 1 4 (+2)
R14(+2)
R 1 4 (+2,4)
R14
R13
R13
Postulated host genotype
Arclente
Type 5276A (Karma)
Kinemontepas
28
29
Diana
27
Corelli
25
Avonerisp
Edgar, Orba, Pallas, Wenda
24
26
_R3,7
_R3,7
CA!mAr
23
-
_R3,7
_R1,7
_R7
_R3,7
_R7
+
Avondefiance, Tina
22
3,11
Type 83, Type 700
(--)
_6,8
_6
_6
+
+
+
+
_R6
_11
+
R3,7
TroPPo, Type 796, Type 1596 (Mistra), Type 7780A, Type 22732
_
+ (+)
B 67, Brezan, Fedore, Gmda, Ilona, Kares, Marian, Mariska, Marty, Nina, Novaran, Olga, Plevanos, Profo& Reskia, Respons, Solito, Topsy, Type 11, 51, 61, 27, 70, 71, Type 4045, R3,7 Type 5611, Vex-a, Winny -Type ]3-255, Type D-286 _R3,7
21
20
3,7
.
_3,7
_1,7
7
_3,7
_3,7
_3,7
_7
+
_3,11
.
3,7 . _3,7
.
3,7
_3,7
_3,7
_3,7
_7
+
_3
.
_3,7
3,7
_3.7
1,7
(_)7
.
.
.
7
.
.
_6,7.8
_
_
_7,8
_7,8
_7
_7,8
_R6,8
+
.
_3,7
3,7
.
.
.
_3,6,7,6
1,6,7
_6,7,8
_3,7,8
_3,7,8
3,7
_7,8
_6,8
3,11
3,7
3,7 . _3,7
.
.
_
_
_
.
_3,7,8
_
3,7
7,8
_6,8
_3,11
_3,7
_3,7
3,7
.
3,7
(_)7
(_)7
3,7
_3,7
3,7
(_)7
+
_3
3,7
_3,7
3,7
.
+
+
+
+
+
+
+
+
+
+
+ +
7
.
_6,7
_6
_6
_7
+
+
_7
_6
_11
_
+ (+)
_6
_6
_6
+
+
+
+
_6
+
+
+ +
_3,6,7,8
_6,7
_6,7,8
_3,7,8
_3,7,8
_3,7
_7,8
_6,8
3,11
_
3,7 _3,7
R?
R3,6,7,8
R1,4,6,7
R6,7,8
R3,7,8
R3,7,8
R2,3,7
R7,8
R6,8
R3,11
R3,7
R3,7 R3,7
t~ ~D
30 was it necessary to change the effective combinations of R-factors according to latest knowledge (Osara and Crute, 1981). A new, b u t as y e t u n k n o w n combination of the factors R3,11 is supposed to occur in the lines Type 700 and Type 83 of Group 21 ('Sluis en Groot' and 'Ploeg', respectively). The previously-introduced combination of R-factors should also have been slightly modified in 'Correli' and 'Diana'. Based on the tests of Osara and Crute (1981) and results given in Table I, these cultivars are supposed to have a combination of the factors R3,7,8. Resistance of 'Ardente' (Group 27) is likely to consist of the factor R4,6,7 postulated before, and the factor R1. The expected combination of R-factors in 'Karma' of Group 28 (Type 5276) has been mentioned in our previous paper (Lebeda, 1980b). An unexpected response was found in 'Kinemontepas' (Group 29), which showed resistance to all the isolates used. The isolate CS2 induced limited sporulation only (quantitatively estimated up to 16%) accompanied by yellowing of cotyledons. In contrast with previous data based on the presence of the factor R7 (Crute, 1979), eventually in combination with R1, R2 and R4 (I.R. Crute, personal communication, 1981), it should be suggested that the resistance of this cultivar is controlled by one or more unknown factors. Its precise determination can be made after re-testing with a larger set of isolates possessing various virulence phenotypes. DISCUSSION The original genetic model of the L. sativa--B, lactucae relationship (Crute and Johnson, 1976a, b) suggested the known race-specific R-factors of lettuce to have had different genetic sources. Five of them have been widely used. The results published in the present paper and before (Crute and Lebeda, 1981, 1983; Lebeda, 1982) show that there are 3 new R-factors and that still others can be expected. The question arises, h o w many real ancestors participated in the origin and development of lettuce cultivars and which of them have been donors of R-factors. It seems probable that there have been more progenitors than previously supposed by Crute and Johnson (1976a, b) and referred to in literature. The development of lettuce cultivars was concentrated in the Mediterranean area; e.g. in Egypt, lettuce was grown as early as 2400 BC (Whitaker, 1975). It may be supposed that the development of cultivated lettuce types was rather local and was realized through continual selection of wild types of Lactuca serriola (Lindqvist, 1960), or others. The origin o f a number of cultivars and/or R-factors from L. serriola is precisely exemplified (Crute and Johnson, 1976a, b), b u t of many cultivars or types the origin is n o t exactly known. As stated before, it should be supposed that the breeding-process was based on a great variety of progenitors. It is necessary to point out h e r e that Crute and Johnson's model (1976a, b) mostly comprised genetic resources used in lettuce breeding in the U.S.A.
31
and Western Europe in particular. It seems possible that the lettuce cultivars developed in Central, Southern and Eastern Europe have been of different origin and, consequently, possess a different genetic background of resistance. This can be due to a specific genotype or a long-term host-pathogen co-evolution. The assortments of less-studied wild types and landraces coming from certain areas of Central, Southern and Eastern Europe or from other places (Asia, Africa) may help in the "quest for request", dealing with an enormous diversity of race-specific R-factors. In our opinion, a certain genetic resemblance among B. lactucae isolates, especially those used in Western Europe to study resistance, gave no possibility of the discovery of u n k n o w n R-factors. The problem can be solved by using pathogen isolates found in other places where a study of genetic relationships has been neglected. It may be supposed that some of the new R-factors have n o t been interacting with corresponding pathogen populations, which could lead to a virulence within the scope of a given specific relationship. It is necessary to test the large sets of commercial cultivars and landraces, as well as wild lettuce types and pathogen isolates, belonging to as great a number of B. lactucae populations as a possible means of understanding further details of the complex relationships and degree of variability within this pathosystem. Such a study would provide us with new knowledge and contribute to explanation of a difficult problem dealing with evolutional relationships between host and pathogen. ACKNOWLEDGEMENTS
The author thanks Dr. I.R. Crute for his fruitful discussion and critical remarks, and Miss J. Potomkov~ for preparing the English text of the paper.
REFERENCES Blok, I. and Van Der Schaaf-Van Waadenoyen Kernekamp, K., 1977. Problemen rond Bremia in sla. Zaadbelangen, 31 : 57--60. Channon, A.G. and Smith, Y., 1970. Further studies on races of Bremia lactucae Regel. Hortic. Res., 10: 14--19. Crute, I.R., 1979. Lettuce mildew -- destroyer of quality. ARC Res. Rev., 5: 1--4. Crute, I.R. and Dickinson, C.H., 1976. The behaviour of Bremia lactucae on cultivars of Lactuca sativa and on other composites. Ann. Appl. Biol., 82: 433--450. Crute, I.R. and Johnson, A.G., 1976a. The genetic relationship between races of Bremia lactucae and cultivarsof Lactuca sativa. Ann. Appl. Biol., 83: 125--137. Crute, I.R. and Johnson, A.G., 1976b. The development of a strategy for lettuce d o w n y mildew resistance breeding. Proc. Eucarpia Meet. Leafy Vegetables, Wageningen, pp. 88--94. Crute, I.R. and Lebeda, A., 1981. Evidence for a race-specific resistance factor in some lettuce (Lactuca sativa L.) cultivarspreviously considered to be universally susceptible to Bremia lactucae Regel. Theor. Appl. Genet., 60: 185--189. Crute, I.R. and Lebeda, A., 1983. T w o new specific resistance factors to Bremia lactucae identified in cultivars of lettuce. Tests of Agrochemicals and Cultivars No. 4, Suppl. Ann. Appl. Biol., 102: 128--129.
32 Crute, I.R. and Norwood, J.M., 1978. Incomplete specific resistance to Bremia lactucae in lettuce. Ann. Appl. Biol., 89: 467--474. Dickinson, C.H. and Crute, I.R., 1974. The influence of seedling age and development on infection o f lettuce by Bremia lactucae. Ann. Appl. Biol., 76: 49--61. Eenink, A.H., 1974. Resistance in Lactuca against Bremia lactucae Regel. Euphytica, 23: 411--416. Globerson, D., Netzer, D. and Tjallingii, F., 1974. Mode of inheritance of resistance in lettuce (l~ctuca sativa L.) to three Israeli and four Dutch races of downy mildew (Bremia lactucae Reg.). Euphytica, 23: 54--60. Jagger, I.C., 1924. I m m u n i t y to mildew (Bremia lactucae Reg.) and its inheritance in lettuce. Phytopathology, 14: 122. Jagger, I.C. and Whitaker, T.W., 1940. The inheritance of immunity from mildew (Bremm lactucae) in lettuce. Phytopathology, 30: 427--433. Johnson, A.G., Crute, I.R. and Gordon, P.L., 1977. The genetics of race-specific resistance in lettuce (Lactuca sativa) to downy mildew (Brem~ lactucae). Ann. Appl. Biol., 86: 87--103. Johnson, A.G., Crute, I.R., Gordon, P.L. and Norwood, J.M., 1978. Further work on the genetics of race-specific resistance in lettuce (Lactuca sativa) to downy mildew (Bremia lactucae). Ann. Appl. Biol., 89: 257--264. Lebeda, A., 1979a. Identification of races of Brem~ lactucae in Czechoslovakia. Phytopathol. Z., 94: 208--217. Lebeda, A., 1979b. New sources of resistance to two German races of Brem~ lactucae. Z. Pflanzenzuecht., 82: 286--288. Lebeda, A., 1979c. Resistance of Lactuca sativa L. varieties to two German and one Czechoslovakian race of downy mildew (Brem~ lactucae). Z. Pflanzenzuecht., 82: 361--365. Lebeda, A., 1979d. The occurrence of new races of Bremia lactucae in Czechoslovakia. Z. Pflanzenkr. Pflanzenschutz, 86: 729--734. Lebeda, A., 1980a. Establishment of virulence phenotypes in races of Bremia lactucae CS1;N1,N5 and N6. Phytopathol. Z., 97: 289--294. Lebeda, A., 1980b. Genetic constitution of resistance to lettuce downy mildew (Bremk~ lactucae) in new Dutch lettuce lines and cultivars. Z. Pflanzenzuecht., 85: 259--262. Lebeda, A., 1982. Biology and genetics of Lactuca sativa--Bremia lactucae interaction and its role in lettuce resistance breeding. Ph.D. Thesis, Research Institute for Plant Production, Praha, pp. 1--311. Lebeda, A., Crute, I.R., Blok, I. and Norwood, J.M., 1980. The identification of factors determining race-specific resistance to Bremia lactucae in some Czechoslovakian lettuce cultivars. Z. Pflanzenzuecht., 85: 71--77. Lindqvist, K., 1960. On the origin of cultivated lettuce. Hereditas, 46: 319--349. Osara, K. and Crute, I.R., 1981. Variation for specific virulence in the Finnish Bremia lactucae population. Ann. Agric. Fenn., 20: 198--209. Person, C., 1959. Gene-for-gene relationships in host--parasite systems. Can. J. Bot., 37: 1101--1130. Ventura, J., Netzer, D. and Globerson, D., 1971. Inheritance of resistance in lettuce to race 3 of downy mildew (Bremi~ lactucae Regel). J. Am. Soc. Hortic. Sci., 96: 103--104. Whitaker, T.V., 1975. The lettuce story. Evolution of a weedy cinderella. West. Grower Shiper, 46: 6--11.
23
RACE-SPECIFIC FACTORS OF RESISTANCE TO BREMIA LACTUCAE IN THE WORLD ASSORTMENT OF LETTUCE
A. LEBEDA
Plant Breeding Station, 798 17 Smr2ice (Czechoslovakia) (Accepted for publication 31 May 1983)
ABSTRACT Lebeda, A., 1984. Race-specific factors of resistance to Bremia lactucae in the world assortment of lettuce. Scientia Hortic., 22: 23--32. The presence of race-specific factors of resistance to Bremia lactucae was studied in a set of more than 220 lettuce cultivars and lines. The results have proved general validity of a genetic model postulated for Lactuca sativa--Bremia lactucae relationships on the basis of gene-for-gene theory, The whole set was divided into 29 groups according to reaction and presence of resistance factors. Besides the group of "universally susceptible" cultivars, the most numerous are those carrying the factors: R2,4; R3; R12; R13; R14 and R3,7. A new, as yet u n k n o w n resistance factor(s) is supposed to occur in 'Kinemontepas'. The evolutionary aspects of this enormous genetic diversity of race-specific resistance in Lactuca sativa are discussed. Keywords: Bremia lactucae; downy mildew; Lactuca sativa; lettuce; resistance.
INTRODUCTION
In recent years, much progress has been made in the sphere of genetic relationships between lettuce (Lactuca sativa L.) and downy mildew (Bremia lactucae Regel). Crute and Johnson (1976a) were the first to interpret these interactions on the basis of the gene-for-gene theory (Person, 1959). An important step in the study on race-specific resistance of lettuce had been realised after this genetic model was postulated in the above-mentioned pathosystem. This had been preceded by more than 50 years of intensive research at the level of cultivar--race interaction (Jagger, 1924; Jagger and Whitaker, 1940; Channon and Smith, 1970; Ventura et al., 1971; Eenink, 1974; Globerson et al., 1974}. The establishment of a basic genetic model meant no stop in the research oriented towards better understanding of race-specific resistance of lettuce to Bremia lactucae (Blok and Van Der Schaaf-Van Waadenoyen Kernekarnp, 1977; Lebeda, 1979b, c; Osara and Crute, 1981). Recent papers (Lebeda et al., 1980; Osara and Crute, 1981; Crute and Lebeda, 1981; Lebeda, 1982)
0304-4238/84/$03.00
© 1984 Elsevier Science Publishers B.V.
24
show that it will be necessary to modify and revise some data and presumptions in the previous model (Crute and Johnson, 1976a; Johnson et al., 1977, 1978). The objective of this study was to verify the general validity of the genetic model of the L. sativa--B, lactucae relationship, to integrate some new results, and to consider the possibilities of applying some sources of racespecific resistance in lettuce breeding. MATERIALS AND METHODS
Tests were accomplished in the set of more than 220 cultivars and lines belonging to the world lettuce assortment. The plant material mainly originated from the lettuce germplasm collection of the Plant Breeding Station at Smr2ice. Further substantial lettuce seed samples were provided by the Research Institute of Vegetable Growing and Breeding in Olomouc, Czechoslovakia, and the National Vegetable Research Station, Wellesbourne, Great Britain. A total of 12 B. lactucae isolates (CS1--CS12) were used for inoculation. Their virulence phenotypes were determined in our previous papers (Lebeda, 1979a, d, 1980a, 1982). Verification and determination of resistance factors (R-factors) and their combinations in the set of lettuce cultivars studied was accomplished by means of p h e n o t y p e analysis, whilst interpretation of the results was made on the basis of the gene-for-gene theory (Person, 1959). The tests were carried out on fully expanded cotyledons of lettuce seedlings, grown in plastic trays (500 X 340 X 50 mm) lined with moist filter paper. Every isolate was used to test 20--30 seedlings of each cultivar in 2--3 replications. The seedlings were raised in a controlled chamber at 20--24°C. The isolates of B. lactucae were maintained and multiplied on susceptible cultivars, usually carrying the factors R2 or R4 or their combinations. Inoculum was prepared by washing 1--3-day-old spores from the surface of cotyledons with distilled water. Inoculum concentration was adjusted to 105 spores m1-1 . The seedlings were treated with inoculum by means of a glass sprayer. Incubation t o o k place at 14--16°C, under a 12-h photoperiod. Sporulation was recorded on the 6th to 14th day after inoculation. The cultivars were classified, according to the intensity of sporulation, as resistant or susceptible (Crute and Johnson, 1976a; Crute and Norwood, 1978). In some cases, when incomplete resistance was found, quantitative estimation of sporulation intensity was carried o u t using the method of Dickinson and Crute (1974). Occasionally, combined response was observed on the seedlings, referring to segregation or heterogeneity (Crute and Dickinson, 1976}. RESULTS
The results of the tests are given in Table I. The set of cultivars and newlyselected lines studied were divided into 29 groups according to the presence
25 of supposed race-specific R-factors and their combinations. In some cases, the cultivars were grouped according to t y p e of reaction. For better understanding, each of the incompatible reactions is accompanied by symbols of R-factors which are expected to control all of them. The first group contains the cultivars which are considered to be "universally susceptible" on the basis of up-to-date knowledge. The second group comprises the results of comparison between t w o origins of 'Blondine', differing from each other in their response to the isolates CS3 and CS5. The t w o types of different reactions were proved as a result of a detailed study on 5 origins of 'Blondine' (Lebeda, 1982). The compatibility to CS3 and CS5 of these origins was always characterised by limited sporulation. It may be supposed that the different behaviour of the origins of 'Blondine' is n o t due to another R-factor, b u t probably mainly to a modified action of R1 under the influence of genetic background or environment. The origins Zwaan and Tozers are in good agreement with the original genetic model of Crute and Johnson (1976a). The third group contains the cultivars possessing the combination of the factors R2,4 or R2. It seems impossible to distinguish the combinations of these factors using CS-isolates. The factor R3 is relatively frequent in the assortment. In some cultivars, we may even expect the combination of the factors R3,4, which was impossible to determine by means of the isolates used. The presence of the respective R-factors was proved in Groups 5--11 in accordance with the postulates of Crute and Johnson (1976a, b) for individual cultivars. Group 12 is the most numerous and also rather interesting, as it comprises the cultivars which have been considered as "universally susceptible" until now. This presumption was nullified as a result of the incompatible reaction with the isolate C86. A more detailed study has shown that these cultivars carry a hitherto u n k n o w n race-specific R-factor (Crute and Lebeda, 1981), which was designated as R 1 2 (Lebeda, 1982; Crute and Lebeda, 1983). Group 13 contains the cultivars carrying the factors R1 or R7, initially expected on the basis of their reaction with CS isolates. The cultivars were tested using the isolates Tv, IM43 and W5. The tests have shown that their genotype has none of 11 R-factors so far known. The existence of a new race-specific R-factor designated R13 has been proved (Lebeda, 1982; Crute and Lebeda, 1983}. Group 14 comprises the cultivars with identical response to CS isolates, b u t according to previous data they are n o t completely identical as far as R-factors are concerned. The cultivars are also expected to have another new race-specific factor R14 (Lebeda, 1982; Crute and Lebeda, 1983). With respect to the rather diverse interactions of the cultivars in question with other B. lactucae isolates (except for CS isolates) it may be supposed that other R-factors are involved (in parentheses). Combinations of known R-factors were found or proved in Groups 15--20. Only in some cultivars (e.g. 'Brioso', 'Portato', 'Bremex', 'Munex')
--
Magiola
+
-
Aehiles, Agilo, Andy, Apollo, Ardito, Atlas, Bessy No. 57, C o r y , D a w s o n s Mildura, Divalo, Egivo, Invemo, Kastaar, Kloek, Kondor, Kordaat, Korrect, Kwiek, Mildura, No. 60, Original, Proeftuins Blackp o o l T y p e 57, V a l e n t i n e , Van Der Bergs Secura
4
Valmaine
+
Amanda Plus, Amplus, Budas Hajtato, Deci Minor, Deciso, Knap, Kr~l bi~je (May King), Miranda, Sea Queen, T r i u m f , V[de~isk~, V i t e s s e
3
5
-
+
Lobjoits Green Cos
--
+
Varka, Valdor, Winterday
B l o n d i n e (British, Dr. C r u t e )
+
Attraction SperKngs, Bautzener Dauerkopf, Chrestia, Clauses Peson, Helga, Herkules Winter, Ivcto, KB-4, Kolos, Laltue ~ , Maiw~nder Winter, Mona, No. 39, Olof, Plenos, Presto, Resistent, Rexina, Silvester, Virilde, Wowo
R3
R3
R1
R1
CS1
Isolates
Blondine (Dutch, It. BIok)
2
1
Croup Cultlvars/lines
+
+
+
+
+
+
+
+
+
CS2
-
-
+
+
-
•
a
+
3
3
?
1
CS3
-
-
+
-
-
+
+
+
3
3
1
1
CS4
-
+
+
+
+
-
+
+
+
5
?
1
CS5
+
-
-
+
--
+
+
+
3
3
1
1
CS6
1
1
+
3 (_)3
+
--
-
+
+
+
CS7
+
-
-
+
+
+
+
+
+
3
3
CS8
+
+
+
+
+
+
+
+
+
CS9
+
+
+
+
--
-
+
+
+
1
1
CS10
+
+
+
+
+
+
•
+
+
CSll
--
-
-
+
-
+
+
+
5
3
3
1
1
CS12
R5
R3 (+4?)
R3 (+4?)
R2,4
R1
R1
R0
R0
RO
Postulated host genotype
R e a c t i o n s o f l e t t u c e c u l t i v a r s t o i s o l a t e s o f B r e m i a l a c t u c a e . + = s u s c e p t i b l e ; - = r e s i s t a n t ; ( - ) = i n c o m p l e t e r e s i s t a n c e ; (+) = m i x e d r e a c t i o n ; • = n o t t e s t e d
TABLE I
t~
+
+
Hilde-Asmer
New
+
+
Butterkopf, Exeello
Excellent,
Hilde-Tozer
+
+
Heart
Unrivalled
Constant
+
+
+
+
+
+
+
+
Atu'e lla , ~ A [ a ~
Market
+
+
AWU, Be~ga. Berga Orl~inal~ D~teniek~ Atmkce, Neusldler, Prado, Suzan, Tagerwiner Nova, Winter Butterkopf
+
-
+
+
+
Rll
R9
+
+
+
-
All the Year Round, Amerlka, Arctic King, Attraetie, Boheme Blonde Gro~e, Clauses Aurelia, Delta, d~Iivezo Vezzie~es, Dry Weather, Grosso, Hilds Capo, Hilde, I-lilds Savio, Ka~'aner Sommer, Magna, Maya, M~iniek~" MJj0 Merveilled d'Hiver, Neckarriensen, Ostinata, Relly, Rigoletto, Steran, Tenax, Viruzan, Wunder yon Stuttgart
-
Hilde
Capitan, Mondlan
serriola,
+
Tornado
Sucrine,
L.
-
Bourguignonne
9
×
+
Valverde
8
12
11
I0
--
Ruby
R7,13
Mesa
659,
+
Sabine
11
R6
+
•
•
•
•
•
•
+
+
-
+
+
+
.
II
_7,13
+
.
+
+
•
+
+
+
+
+
+
+
+
-
+ 9
.
_7,13
+
.
6
+
+
•
+
+
+
+
+
+
+
-
-
-
R10
9
R8
7,13
-
6
R12
11
9
8
--
12
( )R12 12 -2 (~)1 12 12 12 12 -
-
-
+
-
-
_7,13
-
6
+ + + +
+ + + +
+
+
+
+
+ +
+
+
+
+
+
+
11
9
8
4-
(_)7
+
+
+
--
+
-
--
-
_7,13
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
6
+
+
•
+
+
+
+
+
+
--
+
-
+
--
11
9
_I3
-
+
+
+
+
+
+
+
+
+
+
+
+
+
-I-
+
-
6
6
+
+
+
+
+
+
+
+
+
+
-
-
--
--
10
9
8
_7,13
-
R12
R12
R12
R12
R12
RI2
R12
R12
R12
Rll
RIO
R9
R8
R7
R6
t~
Bremex, Munex
Fila, I.a~o M o r a v a
18
19
Campan, No. 1177/3, Type 6234, Type 796A
IAtrganda, Pirat
17
_R1,7
__
11
-- 11
-- R l l
Rll
+
_R1,7
--
7
3
_
11
_ 11
_1,7
--
÷
4-
4-
4-
4-
4-
4-
+
+
R3
R14
R14
R14
R14
4-
_R7
--
-
Imperial Winter
Bianka
-
Majorette
16
1,7
+
--
Spartan Lakes
Brioso, Portato
÷
4-
-
Pan-~lej-eaj
R14
+
4-
-
4-
4-
Start
R14
R14
--
13
Liba, Valore
4-
•
.
--
4-
+
+
CS3
Muck
R14
R13
13
CS2
--
-
-
CS1
Isolates
Dua, Lednieky
Continuity, Empire, New York, Pennlake, Webbs Wonderful, Windermere
A u r o r a , Cavoli di N a p o l i , Dorian, Ootte Jaune d'or, Gravitas, Guldrottmingen, H u b a r d Mazket, Ou Laitue Oeuf, Primo, Wan-ShouYmm-Ye
15
14
13
Group Cuitivars/lines
T A B L E I (continued)
.
13
_
4-
+
_1,7
7
3
_1,7
4-
4-
4-
4-
÷
4-
4-
+
.
13 .
CS4
.
13
4-
+
_1,7
_7
4-
_1,7
4-
4-
4-
4-
4-
+
4-
+
.
. 13
CS5
.
.
13
-
--
11
-- 11
_1,7
7
3
_1,7
4-
4-
4-
4-
4-
4-
4-
4-
.
13
CS6
__
11
_ 11
_1,7
_7
__
3
1,7
4-
+
4-
+
4-
4-
+
4-
13
13
CS7
_
4-
+
_7
(_)7
3
_7
÷
4-
4-
4-
4-
4-
+
4-
4-
+
CS8
4-
+
+
+
÷
+
4-
4-
4-
4-
4-
4-
+
4-
4-
+
CS9
13
13
--
11
-- 11
+
+
4-
+
4-
4-
4-
4-
4-
4-
+
4-
--
-
CS10
+
4-
4-
+
4-
+
4-
4-
4-
4-
+
4-
+
+
4-
+
CSll
4-
4-
1,7
7
3
1,7
14
14
14
14
14
14
14
14
13
13
CS12
R l l OR R2,11
R2,11
R1,7
R2,7
R2,3
R1,2,7
R14
R 1 4 (+1 ?)
R14
R14
R 1 4 (+2)
R14(+2)
R 1 4 (+2,4)
R14
R13
R13
Postulated host genotype
Arclente
Type 5276A (Karma)
Kinemontepas
28
29
Diana
27
Corelli
25
Avonerisp
Edgar, Orba, Pallas, Wenda
24
26
_R3,7
_R3,7
CA!mAr
23
-
_R3,7
_R1,7
_R7
_R3,7
_R7
+
Avondefiance, Tina
22
3,11
Type 83, Type 700
(--)
_6,8
_6
_6
+
+
+
+
_R6
_11
+
R3,7
TroPPo, Type 796, Type 1596 (Mistra), Type 7780A, Type 22732
_
+ (+)
B 67, Brezan, Fedore, Gmda, Ilona, Kares, Marian, Mariska, Marty, Nina, Novaran, Olga, Plevanos, Profo& Reskia, Respons, Solito, Topsy, Type 11, 51, 61, 27, 70, 71, Type 4045, R3,7 Type 5611, Vex-a, Winny -Type ]3-255, Type D-286 _R3,7
21
20
3,7
.
_3,7
_1,7
7
_3,7
_3,7
_3,7
_7
+
_3,11
.
3,7 . _3,7
.
3,7
_3,7
_3,7
_3,7
_7
+
_3
.
_3,7
3,7
_3.7
1,7
(_)7
.
.
.
7
.
.
_6,7.8
_
_
_7,8
_7,8
_7
_7,8
_R6,8
+
.
_3,7
3,7
.
.
.
_3,6,7,6
1,6,7
_6,7,8
_3,7,8
_3,7,8
3,7
_7,8
_6,8
3,11
3,7
3,7 . _3,7
.
.
_
_
_
.
_3,7,8
_
3,7
7,8
_6,8
_3,11
_3,7
_3,7
3,7
.
3,7
(_)7
(_)7
3,7
_3,7
3,7
(_)7
+
_3
3,7
_3,7
3,7
.
+
+
+
+
+
+
+
+
+
+
+ +
7
.
_6,7
_6
_6
_7
+
+
_7
_6
_11
_
+ (+)
_6
_6
_6
+
+
+
+
_6
+
+
+ +
_3,6,7,8
_6,7
_6,7,8
_3,7,8
_3,7,8
_3,7
_7,8
_6,8
3,11
_
3,7 _3,7
R?
R3,6,7,8
R1,4,6,7
R6,7,8
R3,7,8
R3,7,8
R2,3,7
R7,8
R6,8
R3,11
R3,7
R3,7 R3,7
t~ ~D
30 was it necessary to change the effective combinations of R-factors according to latest knowledge (Osara and Crute, 1981). A new, b u t as y e t u n k n o w n combination of the factors R3,11 is supposed to occur in the lines Type 700 and Type 83 of Group 21 ('Sluis en Groot' and 'Ploeg', respectively). The previously-introduced combination of R-factors should also have been slightly modified in 'Correli' and 'Diana'. Based on the tests of Osara and Crute (1981) and results given in Table I, these cultivars are supposed to have a combination of the factors R3,7,8. Resistance of 'Ardente' (Group 27) is likely to consist of the factor R4,6,7 postulated before, and the factor R1. The expected combination of R-factors in 'Karma' of Group 28 (Type 5276) has been mentioned in our previous paper (Lebeda, 1980b). An unexpected response was found in 'Kinemontepas' (Group 29), which showed resistance to all the isolates used. The isolate CS2 induced limited sporulation only (quantitatively estimated up to 16%) accompanied by yellowing of cotyledons. In contrast with previous data based on the presence of the factor R7 (Crute, 1979), eventually in combination with R1, R2 and R4 (I.R. Crute, personal communication, 1981), it should be suggested that the resistance of this cultivar is controlled by one or more unknown factors. Its precise determination can be made after re-testing with a larger set of isolates possessing various virulence phenotypes. DISCUSSION The original genetic model of the L. sativa--B, lactucae relationship (Crute and Johnson, 1976a, b) suggested the known race-specific R-factors of lettuce to have had different genetic sources. Five of them have been widely used. The results published in the present paper and before (Crute and Lebeda, 1981, 1983; Lebeda, 1982) show that there are 3 new R-factors and that still others can be expected. The question arises, h o w many real ancestors participated in the origin and development of lettuce cultivars and which of them have been donors of R-factors. It seems probable that there have been more progenitors than previously supposed by Crute and Johnson (1976a, b) and referred to in literature. The development of lettuce cultivars was concentrated in the Mediterranean area; e.g. in Egypt, lettuce was grown as early as 2400 BC (Whitaker, 1975). It may be supposed that the development of cultivated lettuce types was rather local and was realized through continual selection of wild types of Lactuca serriola (Lindqvist, 1960), or others. The origin o f a number of cultivars and/or R-factors from L. serriola is precisely exemplified (Crute and Johnson, 1976a, b), b u t of many cultivars or types the origin is n o t exactly known. As stated before, it should be supposed that the breeding-process was based on a great variety of progenitors. It is necessary to point out h e r e that Crute and Johnson's model (1976a, b) mostly comprised genetic resources used in lettuce breeding in the U.S.A.
31
and Western Europe in particular. It seems possible that the lettuce cultivars developed in Central, Southern and Eastern Europe have been of different origin and, consequently, possess a different genetic background of resistance. This can be due to a specific genotype or a long-term host-pathogen co-evolution. The assortments of less-studied wild types and landraces coming from certain areas of Central, Southern and Eastern Europe or from other places (Asia, Africa) may help in the "quest for request", dealing with an enormous diversity of race-specific R-factors. In our opinion, a certain genetic resemblance among B. lactucae isolates, especially those used in Western Europe to study resistance, gave no possibility of the discovery of u n k n o w n R-factors. The problem can be solved by using pathogen isolates found in other places where a study of genetic relationships has been neglected. It may be supposed that some of the new R-factors have n o t been interacting with corresponding pathogen populations, which could lead to a virulence within the scope of a given specific relationship. It is necessary to test the large sets of commercial cultivars and landraces, as well as wild lettuce types and pathogen isolates, belonging to as great a number of B. lactucae populations as a possible means of understanding further details of the complex relationships and degree of variability within this pathosystem. Such a study would provide us with new knowledge and contribute to explanation of a difficult problem dealing with evolutional relationships between host and pathogen. ACKNOWLEDGEMENTS
The author thanks Dr. I.R. Crute for his fruitful discussion and critical remarks, and Miss J. Potomkov~ for preparing the English text of the paper.
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