Abstract
Lettuce downy mildew caused by Bremia lactucae is the most important disease of lettuce worldwide. Breeding for resistance to this disease is a major priority for most lettuce breeding programs. Many genes and factors for resistance to B. lactucae have been reported by multiple researchers over the past ~50 years. Their nomenclature has not been coordinated, resulting in duplications and gaps in nominations. We have reviewed the available information and rationalized it into 51 resistance genes and factors and 15 quantitative trait loci along with supporting documentation as well as genetic and molecular information. This involved multiple rounds of consultation with many of the original authors. This paper provides the foundation for naming additional genes for resistance to B. lactucae in the future as well as for deploying genes to provide more durable resistance.
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Introduction
Lettuce (Lactuca sativa) is one of the most widely consumed vegetable crops worldwide. It has an annual production of more than 3.6 billion tonnes with a value of more than $2.4 billion in the U.S. (USDA-NASS 2014). Downy mildew (DM) caused by the oomycete pathogen Bremia lactucae is the most important disease of lettuce that decreases quality of the marketable portion of the crop. The impact of this disease is often accentuated by postharvest losses that occur during transit and storage. DM can also increase the consequences of microbial contamination by human enteric pathogens (Simko et al. 2015a).
Strategies for control of DM include the combined use of resistant cultivars and fungicides as well as agronomic practices that reduce foliar humidity. The use of fungicides is constrained by high costs and the development of fungicide-resistant strains (Crute 1987; Schettini et al. 1991). Moreover, increasing restrictive regulations aimed at reducing pesticide applications are coming into force; in Europe several chemicals that are effective against B. lactucae will be redrawn from the market. The deployment of cultivars carrying dominant resistance genes (Dm genes) is the most effective method for controlling DM; however, pathogen variability has led to the rapid defeat of individual Dm genes (e.g. Ilott et al. 1987). Consequently, the search for new sources resistance to B. lactucae has been a continuous, long-term priority of lettuce breeding programs (Crute 1992; Lebeda et al. 2002, 2014). Over 50 genes for resistance have been reported so far and genetically characterized to varying extents (see below for references). In addition, many other sources of resistance have been identified in germplasm screens but have yet to be characterized genetically (e.g. Farrara and Michelmore 1987; Bonnier et al. 1994; Lebeda and Zinkernagel 2003; Beharav et al. 2006). As more resistance genes are characterized from these and other sources, it is likely that several hundred genes with efficacy against B. lactucae will be identified that will require a coordinated, rational nomination process.
This review compiles the knowledge of genetic resistance against B. lactucae, summarizing what is known of genes for resistance to B. lactucae that has been generated over more than 50 years of lettuce genetics and breeding (Supplemental Fig. 1). Resistance has been reported by multiple researchers leading to duplications in nominations as well as gaps in sequence. The extent of genetic characterization has varied. Genes characterized as single Mendelian loci were designated Dm genes, while those that were less well characterized genetically were often but not always termed R-factors. For this review we have rationalized the nomenclature of all of the Dm genes and R-factors reported so far and provide the foundation for future designation and use of Dm genes.
Historical overview of breeding for resistance to B. lactucae
Breeding for resistance to B. lactucae in cultivated lettuce has been carried out since the beginning of the last century. Initial breeding efforts utilized resistance identified in old lettuce cultivars (L. sativa). French traditional cultivars Gotte à Graine Blanche de Loos and Rosée Printanière were the first sources of resistance (referenced in Crute 1992). Subsequently, resistance was identified in several other cultivars such as Meikoningen, May Queen, Gotte à Forcer à Graine Noire, Bourguignonne Grosse Blonde d’Hiver and Blonde Lente à Monter (Jagger and Chandler 1933; Schultz and Röder 1938; Jagger and Whitaker 1940; Ogilvie 1944; Rodenburg et al. 1960). Later breeding efforts accessed resistance from wild Lactuca species. One of the first inter-specific crosses for this purpose was between L. sativa cv. Imperial D and DM–resistant L. serriola PI104854 (Whitaker et al. 1958). This resistance was used in breeding programs in California during the 50’s, that led to the crisphead cv. Calmar (cv. Great Lakes × USDA 45325; Welch et al. 1965) and subsequently cv. Salinas (cv. Calmar × Vanguard 75; Ryder 1979a, b) that is in the pedigree of many current crisphead cultivars (Mikel 2007, 2013). Contemporary breeding efforts are focused on introgression of new genes from wild species. L. serriola, the likely progenitor of cultivated lettuce, and, to a lesser extent, L. saligna have been used as donors of resistance genes (Jagger and Whitaker 1940; Crute and Johnson 1976a, b; Lebeda et al. 1980; Bonnier et al. 1994; Witsenboer et al. 1995; Maisonneuve et al. 1999; Jeuken and Lindhout 2002, Michelmore and Ochoa 2006, 2008; Mc Hale et al. 2009, Zhang et al. 2009). L. virosa also possesses race-specific resistance to B. lactucae (Lebeda and Boukema 1991; Lebeda et al. 2002, Maisonneuve et al. 1999), but its use in breeding programs has been restricted by infertility barriers between L. virosa and L. sativa (Maisonneuve 2003). Transfer of resistance from L. virosa to L. sativa has occasionally been enabled by embryo rescue (Maisonneuve 1987; Maisonneuve et al. 1995). Other wild species such as L. aculeata are potential sources of resistance that have yet to be used as donors in breeding programs (Jemelková et al. 2015). Currently, introgression of recently identified resistance from L. serriola, L. saligna and L. virosa through repeated backcrosses to L. sativa is being carried out by multiple public and commercial breeding programs resulting in a large increase in the number of resistance genes being deployed (e.g. Michelmore and Ochoa 2008; Michelmore et al. 2013a).
Genetics of resistance and nomenclature of resistance genes
Extensive classical genetic studies have been carried out for the resistance of lettuce to B. lactucae. The gene-for-gene interaction between L. sativa and B. lactucae was first elaborated by Crute and Johnson (1976a, b). This interaction is now one of the best characterized gene-for-gene plant-pathogen relationships (Farrara et al. 1987; Hulbert and Michelmore 1985; Ilott et al. 1987, 1989). At least 28 Dm genes are currently known that provide high levels of resistance against specific isolates of B. lactucae (Table 1). Although most Dm genes confer complete resistance, some Dm genes show incomplete resistance that varies depending on the environmental conditions and the isolate of B. lactucae. Low temperature decreases the effectiveness of several Dm genes (Judelson and Michelmore 1992). Cultivars carrying Dm6 and Dm7 may exhibit partial resistance associated with macroscopically visible hypersensitive necrosis (Crute and Norwood 1978). Additionally, gene dosage affects the resistance phenotype of some Dm genes, for example Dm17 under high pathogen pressure (Maisonneuve et al. 1994). Some lettuce cultivars such as Iceberg and Grand Rapids exhibit resistance at the adult plant stage in the field that cannot be attributed to Dm genes (Milbrath 1923; Verhoeff 1960; Crute and Norwood 1981). This quantitative resistance phenotype (Norwood and Crute 1985; Grube and Ochoa 2005) has so far been shown to be inherited polygenically (Simko et al. 2013); transgressive segregation resulting in elevated resistance has been observed in progeny from cvs. Grand Rapids × Iceberg (Grube and Ochoa 2005; Simko et al. 2013). Some cultivars such as Green towers and Cobham Green have no known Dm genes and are used as susceptible lines to grow B. lactucae isolates; however, the European isolate Serr84/99 is avirulent on Cobham Green and there is some evidence suggesting polygenic resistance in this cultivar (Maisonneuve 2011b). Most accessions of L. saligna are completely resistant to isolates of B. lactucae derived from L. sativa; therefore, this species has been proposed to be a non-host for downy mildew (Bonnier et al. 1992; Petrželová et al. 2011; van Treuren et al. 2013); this complete resistance is in part determined by several quantitative trait loci (QTLs) operating at different developmental stages (Jeuken and Lindhout 2002; Jeuken et al. 2008, Zhang et al. 2009; Den Boer et al. 2013). However, the mechanism of resistance in L. saligna is still unresolved. Stacking of these QTLs in 10 pairwise combinations hardly showed an increase in the level of resistance suggesting that epistatic interactions play a role (De Boer et al. 2014; Den Boer 2014).
The genetic studies have resulted in the identification of numerous Dm genes and R-factors. In order to remove duplications in nomenclature and evaluate the genetic evidence for Dm genes and R-factors, we reviewed all the primary literature reporting resistance to B. lactucae in lettuce. When possible, this involved multiple rounds of consultation with the authors and with the lettuce genetics and breeding community at large. This resulted in the classification of 28 Dm genes and 23 R-factors that provide resistance to specific isolates of B. lactucae (Table 1). Resistance was assigned a Dm designation when supported by genetic evidence and mapped to a single locus in the lettuce genome. Resistances were designated as R-factors, when the resistance specificity as determined by reactions to isolates of B. lactucae indicated presence of new resistances genes; however, such resistances had not (yet) been shown to be monogenic or mapped. Over eighty percent of the Dm genes and R-factors were identified in wild Lactuca species collected in Europe (Table 1). Most of these resistances have been introgressed into cultivars of L. sativa as part of breeding programs in Europe and the USA. Parallel research and breeding efforts resulted in several duplicate designations for resistance from different sources. Seven resistances were therefore renamed to remove duplications and to fill in gaps in the sequence of designations; resistances identified in the same study were kept adjacent to the extent possible (Table 1). Fifteen major QTLs for resistance to B. lactucae have so far been identified (Table 2). The QTLs were renamed to be consistent with the convention for describing QTLs in lettuce, in which a QTL is prefixed with ‘q’ followed by capital letters indicating resistance to the disease (DMR in this case) and two numbers indicating the chromosomal linkage group followed by the number of the QTL on that linkage group.
Some lettuce cultivars possess the same resistance specificity, despite the fact that their resistances were introgressed from different sources, sometimes even from different Lactuca species. Linkage analysis of Dm5 and Dm8 and parallel genetics of virulence in B. lactucae demonstrated that both resistances are controlled by the same gene (Norwood and Crute 1984; Hulbert and Michelmore 1985). These resistances were identified from different accessions of L. serriola collected from Turkey and Russia (Jagger and Whitaker 1940; Leeper et al. 1963; Lebeda et al. 1980) and have different molecular haplotypes (Witsenboer et al. 1995). Similarly, Dm38 and R24 cosegregate and share specificities (J. Schut, unpublished). Dm38 and R24 were introgressed from L. serriola sources from Czechoslovakia and Hungary, respectively (Bonnier et al. 1994; Maisonneuve et al. 1999). Similarly, Dm18 and R32 cosegregate and have the same specificity; both resistances were rendered ineffective simultaneously by a change in virulence in B. lactucae (Petrželová et al. 2013). Dm18 originated from L. serriola LS17, while R32 originated from L. saligna LJ81632, suggesting either conservation since the diversification of these Lactuca species or independent convergent evolution of these genes. Dm36 in cv. Ninja has been reported to be identical to Dm37 in cv. Discovery based on reactions to European isolates and had been named Rsal-1 (Maisonneuve 2007, 2011a); however, this conclusion is not supported by the reactions of Ninja and Discovery to Californian isolates (C. Tsuchida and L. Parra, unpublished). Both Dm36 and Dm37 were introgressed from accessions of L. saligna from Israel (B. Moreau, pers. comm.), but the identity of the donor for Dm36 is uncertain and both resistances may have originated from the same source. Resolution of the relationship of Dm36 to Dm37 awaits analysis at the sequence level.
The genetic location is known for 28 Dm genes. As in other plants, resistance genes are clustered in the lettuce genome. The known Dm genes are located in major resistance clusters (MRCs) along with genes determining resistance to other diseases (Table 1; Hulbert and Michelmore 1985; Farrara et al. 1987; Bonnier et al. 1994; Mc Hale et al. 2009; Christopoulou et al. 2015a, b). MRC1 contains Dm5/8, Dm10, Dm17, Dm25, Dm36, Dm37, Dm43, Dm45, as well as Tu and Mo2 for resistance to Turnip Mosaic Virus (TMV) and Lettuce Mosaic Virus (LMV) respectively, and qFUS1.1 and qFUS1.2 for resistance to wilt caused by Fusarium oxysporum f.sp. lactucae. MRC2 includes Dm1, Dm2, Dm3, Dm6, Dm14, Dm15, Dm16, Dm18, Dm50 and qDMR2.2, along with Tvr for resistance to Tomato Bushy Stunt Virus (TBSV), Ra for root aphid resistance, and qANT1 for resistance to anthracnose. MRC4 contains Dm4, Dm7, Dm11, Dm24, Dm38, Dm44 and Dm48 as well as qFUS4.1 for resistance to Fusarium wilt. MRC9A contains qDMR9.1, qDMR9.2 and qDMR9.3, and qVERT9.1 for resistance to wilt caused by Verticillium dahliae (Christopoulou et al. 2015a, b). Dm39 was initially mapped at a locus similar to MRC9A based on analysis of an interspecific F2 population derived from L. saligna CGN05271 × L. sativa cv. Olof (Jeuken and Lindhout 2002); however, this resistance phenotype turned out to be due to an interaction between a L. saligna-allele of Rin4 at MRC9A and the L. sativa-allele of Dm39 at MRC8C (Jeuken et al. 2009). In Arabidopsis Rin4 is a negative regulator of basal defense and known to be the target for three effectors of Pseudomonas syringae and guarded by two R-genes (Axtell and Staskawicz 2003; Mackey et al. 2002).
There has been only limited characterization of specific Dm genes at the molecular level. Each phenotypic MRC spans multiple megabases in the lettuce genome and encompasses complex clusters of genes encoding nucleotide binding-leucine rich repeat, receptor-like proteins (NLRs). Sequence analysis of 385 NLR-encoding genes in the reference lettuce genome identified 25 multigene families and 17 singletons of resistance gene candidates (RGCs) that could be classified as TNL- or CNL-encoding types, depending on the presence or absence of Toll interleukin 1 receptor domain (TIR) at the N-terminus Christopoulou et al. (2015b). Functional analysis of NLR-encoding genes that co-segregated with Dm phenotypes using RNAi demonstrated four NLR-encoding multigene families that were required for 13 Dm phenotypes (Table 1). Only two individual Dm genes have been cloned so far. The map-based cloning of Dm3, encoding a CNL type of NLR, was confirmed by transgenic complementation (Shen et al. 2002). Dm7 was identified on the basis of multiple EMS-induced mutations (Christopoulou et al. 2015a).
Implications for control of downy mildew
This review provides the foundation for naming Dm genes in future. Genetic dissection of R-factors into their Mendelian components will reveal the number and genomic position of the underlying Dm genes. Genetic dissection of QTLs will also reveal candidate genes, although they may not be of the NLR type. Germplasm screens will continue to identify many new sources of resistance that are likely to be conferred by new Dm genes. The International Bremia Evaluation Board (IBEB; http://www.worldseed.org/isf/ibeb.html) should be consulted in order to coordinate the naming of such new Dm genes. IBEB currently consists of representatives from Europe and the US who are knowledgeable of efforts to control DM in lettuce and genetics of resistance to B. lactucae. IBEB should therefore serve in an advisory capacity to avoid duplications and ensure sequential designation.
Genomic analyses show that the MRCs are complex clusters of multiple NLRs. One or more genes could be conferring a resistance phenotype depending on which isolate is used to detect it. Simple segregation analysis of the host alone does not reveal how many genes are effective at a single Mendelian locus. This can be revealed by segregation analysis of the virulence phenotype in B. lactucae; however, this is a slow and labor intensive process. The potential presence of multiple effective genes at a single locus has consequences; recombination at a MRC during backcross programs may result in loss of some Dm genes and parallel introgressions from the same source of resistance may result in different subsets of Dm genes being retained. There is some evidence for this occurring with Dm18 (Wroblewski et al. 2007). Detailed genetic analysis of MRCs may result in the identification of multiple Dm genes and require revision/splitting of current Dm designations.
Genome sequencing and assembly has revealed that all plant genomes contain many, usually hundreds, of NLR-encoding genes. Therefore, all plants have many resistance genes; even if active specificities have yet to be recognized. Consequently, avirulence factors recognized by additional Dm genes in the cultivars described in this paper may be identified in the future, particularly in isolates from L. serriola. Although these Dm genes are effective in limiting migration of isolates from L. serriola onto L. sativa, they are of marginal relevance to control of DM in cultivated lettuce; however, they will be relevant when introgression of a new resistance specificity from a wild species inadvertently replaces such Dm genes, and consequently introduces susceptibility to isolates from the wild species.
Resistance to DM can also be mediated by recessive genes. DMR6 in Arabidopsis is necessary for susceptibility to downy mildew; a recessive dmr6 allele derived by mutation results in resistance against Hyaloperonospora arabidopsidis (Van Damme et al. 2005, 2008). A DMR6 ortholog has been identified in lettuce, where its over-expression increases host susceptibility to B. lactucae (Stassen et al. 2012; Zeilmaker 2012). Natural variation in DMR6 that confers resistance to B. lactucae has yet to be identified.
The plethora of known resistance genes and those now in multiple public and commercial breeding pipelines provides the opportunity for rational deployment of resistance genes (Dm and QTLs; Michelmore et al. 2013b). Pyramids of resistance genes based the nomenclature proposed here that are effective against the diversity of B. lactucae should be generated so as to maximize the evolutionary hurdle required for B. lactucae to become virulent. Pyramids of dissimilar sets of resistance genes should be deployed in the different lettuce types so as to provide heterogeneity in the selection pressure acting on the pathogen population. This should result in more durable resistance to DM.
Abbreviations
- DM:
-
Downy mildew
- NLR:
-
Nucleotide binding-leucine rich repeat-receptor like protein
- MRC:
-
Major resistance cluster
- QTL:
-
Quantitative trait locus
- TNL:
-
NLR proteins with a Toll/interleukin receptor (TIR) domain at their N-terminus
- CNL:
-
NLR proteins lacking a TIR domain often with a coiled-coil (CC) N-terminal domain
- IBEB:
-
International Bremia Evaluation Board
- USDA:
-
United States Department of Agriculture
- DMR6:
-
Downy mildew resistance 6
- EMS:
-
Ethyl methanesulfonate
References
Axtell MJB, Staskawicz J (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112(3):369–377
Beharav A, Lewinsohn D, Lebeda A, Nevo E (2006) New wild Lactuca genetic resources with resistance against Bremia lactucae. Genet Resour Crop Evol 53:467–474
Bonnier FJM, Reinink K, Groenwold R (1992) New sources of major gene resistance in Lactuca to Bremia lactucae. Euphytica 61(3):203–211
Bonnier FJM, Reinink K, Groenwold R (1994) Genetic analysis of Lactuca accessions with new major gene resistance to lettuce downy mildew. Phytopathology 84:462–468
Channon AG, Smith Y (1970) Further studies on races of Bremia lactucae Regel. Hort Res 10:14–19
Christopoulou M, McHale LK, Kozik A, Reyes-Chin Wo S, Wroblewski T, Michelmore RW (2015a) Dissection of two complex clusters of resistance genes in lettuce (Lactuca sativa). Mol Plant Microbe Interact 28:751–765
Christopoulou M, Wo SRC, Kozik A, McHale LK, Truco MJ, Wroblewski T, Michelmore R (2015b) Genome-wide architecture of disease resistance genes in lettuce. G3: Genes|Genomes|Genetics 5(12):2655–2669
Crute IR (1987) The occurrence, characteristics, distribution, genetics, and control of a metalaxyl-resistant phenotypes of Bremia lactucae in the United Kingdom. Plant Dis 71:763–767
Crute IR (1992) The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica 63:95–102
Crute IR, Johnson AG (1976a) The genetic relationship between races of Bremia lactucae and cultivars of Lactuca sativa. Ann Appl Biol 83:125–137
Crute IR, Johnson AG (1976b) The development of a strategy for lettuce downy mildew resistance breeding. In: Proceedings of the EUCARPIA meeting on leafy vegetables, Institute for Horticultural Plant Breeding, Wageningen, Netherlands, 15–18 Mar 1976, pp 88–94
Crute IR, Lebeda A (1981) Evidence for a race-specific resistance factor in some lettuce (Lactuca sativa L.) cultivars previously considered to be universally susceptible to Bremia lactucae Regel. Theor Appl Genet 60:185–189
Crute IR, Lebeda A (1983) Two new specific resistance factors to Bremia lactucae identified in cultivars of lettuce. Tests of Agrochemicals and Cultivars No 4: 128–129. (Ann Appl Biol 102, Supplement)
Crute IR, Norwood JM (1978) Incomplete specific resistance to Bremia lactucae in lettuce. Ann Appl Biol 89:461–474
Crute IR, Norwood JM (1981) The identification and characterization of field resistance to lettuce downy mildew (Bremia lactucae Regel). Euphytica 30:707–717
Crute IR, Norwood JM, Gordon PL, Clay CM, Whenham RJ (1986) Diseases of lettuce - Biology, resistance and control, downy mildew. Annu Rep Natl Veg Res Stn. Wellesbourne, UK 36:51–53
Den Boer E (2014) Genetic investigation of the nonhost resistance of wild lettuce, Lactuca saligna, to lettuce downy mildew, Bremia lactucae. Ph.D. thesis. pp 99–124 Wageningen University NL. ISBN:978-94-6257-207-2. http://edepot.wur.nl/324386
Den Boer E, Zhang NW, Pelgrom KTB, Visser RGF, Niks RE, Jeuken MJW (2013) Fine mapping quantitative resistances to downy mildew in lettuce revealed multiple sub-QTLs with plant stage dependent effects reducing or even promoting the infection. Theor Appl Genet 126:2995–3007
Den Boer E, Pelgrom KTB, Zhang NW, Visser RGF, Niks RE, Jeuken MJW (2014) Effects of stacked quantitative resistances to downy mildew in lettuce do not simply add up. Theor Appl Genet 127:1805–1816
Farrara B, Michelmore RW (1987) Identification of new sources of resistance in Lactuca spp. HortScience 2:647–649
Farrara BF, Illot TW, Michelmore RW (1987) Genetic analysis of factors for resistance to downy mildew (Bremia lactucae) in species of lettuce (Lactuca sativa and L. serriola). Plant Pathol 36:499–514
Grube RC, Ochoa OE (2005) Comparative genetic analysis of field resistance to downy mildew in the lettuce Grand Rapids and Iceberg. Euphytica 142:205–215
Guenard M, Cadot V, Boulineau F, De Fontanges H (1999) Collaboration between breeders and GEVES-SNES for the harmonization and evaluation of a disease resistance test: Bremia lactucae of the lettuce. In: Lebeda A, Kristkova E (eds.) EUCARPIA leafy vegetables 1999, Proceedings of the EUCARPIA meeting on leafy vegetables genetics and breeding, Olomouc, 8–11 June 1999, pp 177–181
Hulbert SH, Michelmore RW (1985) Linkage analysis of genes for resistance to downy mildew (Bremia lactucae) in lettuce (Lactuca sativa). Theor Appl Genet 70:520–528
International Bremia Evaluation Board (IBEB) from the International Seed Federation (ISF). http://www.worldseed.org/isf/ibeb.html
Ilott TW, Durgan ME, Michelmore RW (1987) Genetics of virulence in Californian populations of Bremia lactucae (lettuce downy mildew). Phytopathology 77:1381–1386
Ilott TW, Hulbert SH, Michelmore RW (1989) Genetic analysis of the gene-for-gene interactions between lettuce (Lactuca sativa) and Bremia lactucae. Phytopathology 79:888–897
Jagger IC, Chandler N (1933) Physiologic forms of Bremia lactucae on lettuce. Phytopathology 23:18–19
Jagger IC, Whitaker TW (1940) The inheritance of immunity from mildew (Bremia lactucae) in lettuce. Phytopathology 30:427–433
Jemelková M, Kitner M, Křístková E, Beharav A, Lebeda A (2015) Biodiversity of Lactuca aculeata germplasm assessed by SSR and AFLP markers, and resistance variation to Bremia lactucae. Biochem Syst Ecol 61:344–356
Jeuken M, Lindhout P (2002) Lactuca saligna, a non-host for lettuce downy mildew (Bremia lactucae), harbors a new race-specific Dm gene and three QTLs for resistance. Theor Appl Genet 105:384–391
Jeuken MJW, Pelgrom K, Stam P, Lindhout P (2008) Efficient QTL detection for non-host resistance in wild lettuce: backcross inbred lines versus F2 population. Theor Appl Genet 116:845–857
Jeuken MJW, Zhang NW, McHale LK, Pelgrom K, Den Boer E, Lindhout P, Michelmore RW, Visser RGF, Niks RE (2009) Rin4 causes hybrid necrosis and race-specific Resistance in an Interspecific lettuce hybrid. Plant Cell 21:3368–3378
Johnson AG, Crute IR, Gordon PL (1977) The genetics of race specific resistance in lettuce (Lactuca sativa) to downy mildew (Bremia lactucae). Ann Appl Biol 86:87–103
Johnson AG, Laxton SA, Crute IR, Gordon PL, Norwood JM (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
Judelson HS, Michelmore RW (1992) Temperature and genotype interactions in the expression of host-resistance in lettuce downy mildew. Physiol Mol Plant Pathol 40:233–245
Lebeda A (1984) Race-specific factors of resistance to Bremia lactucae in the world assortment of lettuce. Sci Hort 22:23–32
Lebeda A, Blok I (1991) Race-specific resistance genes to Bremia lactucae Regel in new Czechoslovak lettuce cultivars and location of resistance in a Lactuca serriola × Lactuca sativa hybrid. Arch Phytopathol Pflanzenschutz 27(1):65–72
Lebeda A, Boukema IW (1991) Further investigation of the specificity of interactions between wild Lactuca spp. and Bremia lactucae isolates from Lactuca serriola. J Phytopathol 133:57–64
Lebeda A, Zinkernagel V (2003) Characterization of new highly virulent German isolates of Bremia lactucae and efficiency of resistance in wild Lactuca spp. germplasm. J Phytopathol 151:274–282
Lebeda A, Crute IR, Blok I, Norwood JM (1980) The identification of factors determining race specific resistance to Bremia lactucae in some Czechoslovakian lettuce cultivars. Z. Pflanzenzüchtung 85:71–77
Lebeda A, Pink DAC, Astley D (2002) Aspects of the interactions between wild Lactuca spp. and related genera and lettuce downy mildew (Bremia lactucae). In: Spencer-Phillips PTN, Gisi U, Lebeda A (eds) Advances in downy mildew research. Kluwer Academic Publishers, Dordrecht, pp 85–117
Lebeda A, Křístková E, Kitner M, Mieslerová B, Jemelková M, Pink DAC (2014) Wild Lactuca species, their genetic diversity, resistance to diseases and pests, and exploitation in lettuce breeding. Eur J Plant Pathol 138:597–640
Leeper PW, Thompson RC, Whitaker TW (1963) Valmaine, a new downy mildew immune romaine lettuce variety. Texas and M University Agricultural Experimental Station L-610
Mackey D et al (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108(6):743–754
Maisonneuve B (1987) Utilisation de la culture in vitro d’embryons immatures pour les croisements interspécifiques entre Lactuca sativa L. et L. saligna L. ou L. virosa L.; étude des hybrides obtenus. Agronomie 7:313–319
Maisonneuve B (2003) Lactuca virosa, a source of disease resistance genes for lettuce breeding: results and difficulties for gene introgression. In: Van Hintum TJL, Lebeda A, Pink DA, Schut JW (eds.) EUCARPIA leafy vegetables, Noordwijkerhout, 19–21 Mar 2003, pp 61–67
Maisonneuve B (2007) New interpretation of the resistance to Bremia lactucae of some differential lettuce varieties. In: EUCARPIA leafy vegetables, Warwick HRI, 18–20 April 2007, p 17
Maisonneuve B (2011a) Improvement of the differential lettuce set for Bremia virulence evaluation: new sativa monogenic lines. In: EUCARPIA leafy vegetables, Université Lille Nord de France, Villeneuve d’Ascq, 24–26 Aug 2011, p 61
Maisonneuve B (2011b) Amélioration des Hôtes différentiels Bremia: obtention de lignées de laitue à résistance monogénique. Innov Agron 15:9–14
Maisonneuve B, Bellec Y, Anderson P, Michelmore RW (1994) Rapid mapping of two genes for resistance to downy mildew from Lactuca serriola to existing clusters of resistance genes. Theor Appl Genet 89:96–104
Maisonneuve B, Chupeau MC, Bellec Y, Chupeau Y (1995) Sexual and somatic hybridization in the genus Lactuca. Euphytica 85:281–285
Maisonneuve B, Bellec Y, Souche S, Lot H (1999) New resistance against downy mildew and lettuce mosaic potyvirus in wild Lactuca spp. In: Lebeda A, Kristkova E (eds) EUCARPIA leafy vegetables 1999, Proceedings of the EUCARPIA meeting on leafy vegetables genetics and breeding, Olomouc, 8–11 June 1999, pp 191–197
Mc Hale LK, Truco MJ, Kozik A, Wroblewski T, Ochoa OE, Lahre KA, Knapp SJ, Michelmore RW (2009) The genomic architecture of disease resistance in lettuce. Theor Appl Genet 118:565–580
Michelmore RW (2008) Genetic variation in lettuce. California leafy greens research program. http://calgreens.org/control/uploads/Michelmore_-_Genetic_variation_in_lettuce.pdf
Michelmore RW (2010) Genetic variation in lettuce. California leafy greens research program. http://calgreens.org/control/uploads/Michelmore_Variation_report_2009-2010_final_%282%291.pdf
Michelmore RW, Ochoa OE (1999) Lettuce Breeding. California leafy greens research program. Annual report (1998–1999), pp 38–49
Michelmore RW, Ochoa OE (2002) Lettuce Breeding. California leafy greens research program. Annual report (2001–2002), pp 52–64
Michelmore RW, Ochoa OE (2006) Breeding crisphead lettuce. California leafy greens research program. Annual report (2005–2006), pp 56–65
Michelmore RW, Ochoa OE (2008) Breeding crisphead and leafy lettuce. California leafy greens research program. http://calgreens.org/control/uploads/Michelmore_and_Ochoa_Breeding_Crisphead_Lettuce.pdf
Michelmore RW, Truco MJ, Ochoa OE (2011) Breeding crisphead and leafy lettuce. California leafy greens research program. http://calgreens.org/control/uploads/Michelmore_Breeding_Crisphead_and_Leafy_Lettuce.pdf
Michelmore RW, Truco MJ, Ochoa OE (2013a) Breeding crisphead and leafy lettuce. California leafy greens research program. http://calgreens.org/wp-content/uploads/2013/07/Michelmore-Lettuce-Breeding.pdf
Michelmore RW, Christopoulou M, Caldwell KS (2013b) Impacts of resistance gene genetics, function, and evolution on a durable future. Annu Rev Phytopathol 51(1):291–319
Mikel MA (2007) Genealogy of contemporary North American lettuce. HortScience 42:489–493
Mikel M (2013) Genetic composition of contemporary proprietary U.S. lettuce (Lactuca sativa L.) cultivars. Genet Resour Crop Evol 60:89–96
Milbrath DG (1923) Downy mildew on lettuce in California. J Agric Res [U.S.] 23:989–994
Moravec J, Křístková E, Lebeda A (1999) Leafy vegetable growing and breeding in the Czech Republic—history and the present time In: Lebeda A, Křístková E (eds) EUCARPIA leafy vegetables 1999, Proceedings of the EUCARPIA meeting on leafy vegetables genetics and breeding, Olomouc, 8–11 June 1999, pp 17–32
Norwood JM, Crute IR (1984) The genetic control and expression of specificity in Bremia lactucae (lettuce downy mildew). Plant Pathol 33:385–400
Norwood JM, Crute IR (1985) Further characterization of field resistance in lettuce in Bremia lactucae downy mildew. Plant Pathol 34:481–486
Norwood JM, Crute IR, Lebeda A (1981) The location and characteristics of novel sources of resistance to Bremia lactucae Regel (downy mildew) in wild Lactuca L. species. Euphytica 30:659–668
Norwood JM, Michelmore RW, Crute IR, Ingram DS (1983) The inheritance of specific virulence in Bremia lactucae (downy mildew) to match resistance factors 1, 2, 4, 6 and 11 in Lactuca sativa (lettuce). Plant Pathol 32:177–186
Ogilvie L (1944) Downy mildew of lettuce. A preliminary note on some greenhouse experiments. Report of the Agricultural and Horticultural Research Station, University of Bristol, pp 90–94
Paran I, Kesseli R, Michelmore R (1991) Identification of restriction fragment length polymorphism and random amplified polymorphic DNA markers linked to downy mildew resistance genes in lettuce, using near-isogenic lines. Genome 34:1021–1027
Petrželová I, Lebeda A, Beharav A (2011) Resistance to Bremia lactucae in natural populations of Lactuca saligna from some Middle Eastern countries and France. Ann Appl Biol 159:442–455
Petrželová I, Lebeda A, Kosman E (2013) Distribution, disease level and virulence variation of Bremia lactucae on Lactuca sativa in the Czech Republic in the period 1999–2011. J Phytopathol 161:503–514
Rodenburg CM, Basse H, Glaschke B, Drouzy J, Trébuchet G, Haigh JD, Watts LE, Huyskes JA (1960) Salatsorten, eine internationale monographie Sortenbeschreibungen Nr 3. Instituut voor Veredeling van Tuinbouwgewassen, Wageningen, Holland
Ryder EJ (1979a) ´Salinas´ lettuce. HortScience 14:283–284
Ryder EJ (1979b) ´Vanguard 75´ lettuce. HortScience 14:284–286
Schettini TM, Legg EJ, Michelmore RW (1991) Insensitivity to metalaxyl in California populations of Bremia lactucae and resistance of California lettuce cultivars to downy mildew. Phytopathology 81:64–70
Schultz H, Röder K (1938) Die Anfälligkeit verschiedener Varietäten and Sorten von Salat (Lactuca sativa L. and Lactuca serriola L.) gegen den Falschen Meltau (Bremia lactucae Regel). Züchter 10:185–194
Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OE, Lavelle DO, Wroblewski T, Meyers BC, Michelmore RW (2002) Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol Plant Microbe Interact 15(3):251–261
Simko I, Hayes RJ, Kramer M (2012) Computing integrated ratings from heterogeneous phenotypic assessments: a case study of lettuce postharvest quality and downy mildew resistance. Crop Sci 52:2131–2142
Simko I, Atallah A, Ochoa OE, Antonise R, Galeano CH, Truco MJ, Michelmore RW (2013) Identification of QTLs conferring resistance to downy mildew in legacy cultivars of lettuce. Sci Rep 3:2875
Simko I, Zhou Y, Brandl MT (2015a) Downy mildew disease promotes the colonization of romaine lettuce by Escherichia coli O157:H7 and Salmonella enterica. BMC Microbiol 15:19
Simko I, Ochoa OE, Pel MA, Tsuchida C, Font Forcada C, Hayes RJ, Truco MJ, Antonise R, Galeano CH, Michelmore RW (2015b) Resistance to downy mildew in lettuce cv. La Brillante is conferred by Dm50 gene and multiple QTLs. Phytopathology 105:1220–1228
Stassen JHM, Vergeer PWJ, Andel A, Van den Ackerveken G (2012) Effectors of the lettuce downy mildew Bremia lactucae enhance host susceptibility. In: Stassen JHM (eds.) In: Identification and functional analysis of downy mildew effectors in lettuce and Arabidopsis, pp 95–114, Proefschriftmaken. ISBN: 978-90-393-5843-6
Tjallingii F, Rodenburg CM (1967) Onderzoek van slarassen op vatbaarheid voor drie fysio’s van valse meeldauw (Bremia lactucae). Zaadbelangen 21:104–105
USDA-NASS (2014). http://www.nass.usda.gov/Publications/Ag_Statistics/2014/Ag%20Stats%202014_Complete%20Publication.pdf
Van Damme M, Andel A, Huibers RP, Panstruga R, Weisbeek PJ, Van den Ackerveken G (2005) Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica. Mol Plant Microbe Interact 18:583–592
Van Damme M, Huibers RP, Elberse J, Van Den Ackerveken G (2008) Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew. Plant J 54:785–793
Van Ettekoven K, Van der Arend A (1999) Identification and denomination of new races of Bremia lactucae. In: Lebeda A, Kristková E (eds) EUCARPIA leafy vegetables 1999, Proceedings of the EUCARPIA meeting on leafy vegetables genetics and breeding, Olomouc, 8–11 June 1999, pp 171–175
van Treuren R, Van der Arend A, Schut J (2013) Distribution of downy mildew (Bremia lactucae Regel) resistances in a genebank collection of lettuce and its wild relatives. Plant Genet Resour 11(01):15–25
Verhoeff K (1960) On the parasitism of Bremia lactucae Regel on lettuce. Tijdschr over Plantenz 66:133–203
Welch JE, Grogan RG, Zink FW, Kihara GM, Kimble KA (1965) Calmar: a new lettuce variety resistant to downy mildew. Calif Agric 19:3–4
Whitaker TW, Bohn GW, Welch FE, Grogan RG (1958) History and development of head lettuce resistant to downy mildew. Proc Am Soc Hortic Sci 72:410–416
Witsenboer H, Kesseli RV, Fortin MG, Stanghellini M, Michelmore RW (1995) Sources and genetic structure of a cluster of genes for resistance to three pathogens in lettuce. Theor Appl Genet 91:178–188
Wroblewski T, Piskurewicz U, Tomczak A, Ochoa O, Michelmore RW (2007) Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J 51:803–818
Yuen JE, Lorbeer JW (1983) A new gene for resistance to Bremia lactucae. Phytopathology 73(2):159–162
Zeilmaker T (2012) Functional and applied aspects of the DOWNY MILDEW RESISTANT 1 and 6 genes in Arabidopsis. Ph.D. Thesis, Utrecht University, pp 1–147
Zhang NW, Pelgrom K, Niks RE, Visser RG, Jeuken MJW (2009) Three combined quantitative trait loci from non-host Lactuca saligna are sufficient to provide complete resistance of lettuce against Bremia lactucae. Mol Plant Microbe Interact 22:1160–1168
Acknowledgments
We thank those in the lettuce genetics and breeding community who reviewed and commented on data for this paper. We thank Dr. R. van Treuren, Centre for Genetic Resources, the Netherlands (CGN), for input on germplasm information. L. Parra thanks Becas Chile for a Scholarship from the National Commission for Science Research and Technology (CONICYT, Chile). Additional financial support was provided by a grant to RWM from USDA NIFA SCRI # 2010-51181-21631 and to AL from MSM 6198959215 (Ministry of Education, Youth and Sports of the Czech Republic) and the internal Grant of Palacký University in Olomouc (IGA_PrF_2016_001).
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Parra, L., Maisonneuve, B., Lebeda, A. et al. Rationalization of genes for resistance to Bremia lactucae in lettuce. Euphytica 210, 309–326 (2016). https://doi.org/10.1007/s10681-016-1687-1
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DOI: https://doi.org/10.1007/s10681-016-1687-1