Rationalization of Genes for Resistance to Bremia Lactucae in Lettuce
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Euphytica DOI 10.1007/s10681-016-1687-1 REVIEW Rationalization of genes for resistance to Bremia lactucae in lettuce Lorena Parra . Brigitte Maisonneuve . Ales Lebeda . Johan Schut . Marilena Christopoulou . Marieke Jeuken . Leah McHale . Maria-Jose Truco . Ian Crute . Richard Michelmore Received: 12 December 2015 / Accepted: 29 March 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Lettuce downy mildew caused by Bremia molecular information. This involved multiple rounds lactucae is the most important disease of lettuce of consultation with many of the original authors. This worldwide. Breeding for resistance to this disease is a paper provides the foundation for naming additional major priority for most lettuce breeding programs. genes for resistance to B. lactucae in the future as well Many genes and factors for resistance to B. lactucae as for deploying genes to provide more durable have been reported by multiple researchers over the resistance. past *50 years. Their nomenclature has not been coordinated, resulting in duplications and gaps in Keywords Lactuca spp. Á Resistance genes Á Lettuce nominations. We have reviewed the available infor- downy mildew Á Dm gene Á Quantitative trait locus Á mation and rationalized it into 51 resistance genes and Plant breeding factors and 15 quantitative trait loci along with supporting documentation as well as genetic and Abbreviations DM Downy mildew NLR Nucleotide binding-leucine rich repeat- Electronic supplementary material The online version of this article (doi:10.1007/s10681-016-1687-1) contains supple- receptor like protein mentary material, which is available to authorized users. L. Parra Á M. Christopoulou Á M.-J. Truco Á M. Jeuken R. Michelmore (&) Laboratory of Plant Breeding, Wageningen University, The Genome Center and Department of Plant Sciences, Wageningen 6700 AJ, The Netherlands University of California, Davis, CA 95616, USA e-mail: [email protected] L. McHale Department of Horticulture and Crop Science, Ohio State B. Maisonneuve University, Columbus, OH 43210, USA INRA, Ge´ne´tique et Ame´lioration des Fruits et Le´gumes, Domaine Saint Maurice, CS60094, I. Crute 84143 Montfavet Cedex, France Agriculture and Horticulture Development Board, Stoneleigh Park, Kenilworth, Warwickshire CV8 2TL, A. Lebeda UK Department of Botany, Palacky´ University, Sˇlechtitelu˚ 27, 78371 Olomouc, Czech Republic J. Schut Rijk Zwaan, De Lier 2678 ZG, The Netherlands 123 Euphytica MRC Major resistance cluster genetically (e.g. Farrara and Michelmore 1987; Bon- QTL Quantitative trait locus nier et al. 1994; Lebeda and Zinkernagel 2003; TNL NLR proteins with a Toll/interleukin Beharav et al. 2006). As more resistance genes are receptor (TIR) domain at their N-terminus characterized from these and other sources, it is likely CNL NLR proteins lacking a TIR domain often that several hundred genes with efficacy against B. with a coiled-coil (CC) N-terminal domain lactucae will be identified that will require a coordi- IBEB International Bremia Evaluation Board nated, rational nomination process. USDA United States Department of Agriculture This review compiles the knowledge of genetic DMR6 Downy mildew resistance 6 resistance against B. lactucae, summarizing what is EMS Ethyl methanesulfonate 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). Resis- tance has been reported by multiple researchers Introduction leading to duplications in nominations as well as gaps in sequence. The extent of genetic characterization has Lettuce (Lactuca sativa) is one of the most widely varied. Genes characterized as single Mendelian loci consumed vegetable crops worldwide. It has an annual were designated Dm genes, while those that were less production of more than 3.6 billion tonnes with a value well characterized genetically were often but not of more than $2.4 billion in the U.S. (USDA-NASS always termed R-factors. For this review we have 2014). Downy mildew (DM) caused by the oomycete rationalized the nomenclature of all of the Dm genes pathogen Bremia lactucae is the most important and R-factors reported so far and provide the founda- disease of lettuce that decreases quality of the tion for future designation and use of Dm genes. 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 Historical overview of breeding for resistance to B. the consequences of microbial contamination by lactucae human enteric pathogens (Simko et al. 2015a). Strategies for control of DM include the combined Breeding for resistance to B. lactucae in cultivated use of resistant cultivars and fungicides as well as lettuce has been carried out since the beginning of the agronomic practices that reduce foliar humidity. The last century. Initial breeding efforts utilized resistance use of fungicides is constrained by high costs and the identified in old lettuce cultivars (L. sativa). French development of fungicide-resistant strains (Crute traditional cultivars Gotte a` Graine Blanche de Loos 1987; Schettini et al. 1991). Moreover, increasing and Rose´e Printanie`re were the first sources of restrictive regulations aimed at reducing pesticide resistance (referenced in Crute 1992). Subsequently, applications are coming into force; in Europe several resistance was identified in several other cultivars such chemicals that are effective against B. lactucae will be as Meikoningen, May Queen, Gotte a` Forcer a` Graine redrawn from the market. The deployment of cultivars Noire, Bourguignonne Grosse Blonde d’Hiver and carrying dominant resistance genes (Dm genes) is the Blonde Lente a` Monter (Jagger and Chandler 1933; most effective method for controlling DM; however, Schultz and Ro¨der 1938; Jagger and Whitaker 1940; pathogen variability has led to the rapid defeat of Ogilvie 1944; Rodenburg et al. 1960). Later breeding individual Dm genes (e.g. Ilott et al. 1987). Conse- efforts accessed resistance from wild Lactuca species. quently, the search for new sources resistance to B. One of the first inter-specific crosses for this purpose lactucae has been a continuous, long-term priority of was between L. sativa cv. Imperial D and DM– lettuce breeding programs (Crute 1992; Lebeda et al. resistant L. serriola PI104854 (Whitaker et al. 1958). 2002, 2014). Over 50 genes for resistance have been This resistance was used in breeding programs in reported so far and genetically characterized to California during the 50’s, that led to the crisphead cv. varying extents (see below for references). In addition, Calmar (cv. Great Lakes 9 USDA 45325; Welch et al. many other sources of resistance have been identified 1965) and subsequently cv. Salinas (cv. Calmar 9 in germplasm screens but have yet to be characterized Vanguard 75; Ryder 1979a, b) that is in the pedigree of 123 Euphytica many current crisphead cultivars (Mikel 2007, 2013). Michelmore 1992). Cultivars carrying Dm6 and Dm7 Contemporary breeding efforts are focused on intro- may exhibit partial resistance associated with macro- gression of new genes from wild species. L. serriola, scopically visible hypersensitive necrosis (Crute and the likely progenitor of cultivated lettuce, and, to a Norwood 1978). Additionally, gene dosage affects the lesser extent, L. saligna have been used as donors of resistance phenotype of some Dm genes, for example resistance genes (Jagger and Whitaker 1940; Crute Dm17 under high pathogen pressure (Maisonneuve and Johnson 1976a, b; Lebeda et al. 1980; Bonnier et al. 1994). Some lettuce cultivars such as Iceberg and et al. 1994; Witsenboer et al. 1995; Maisonneuve et al. Grand Rapids exhibit resistance at the adult plant stage 1999; Jeuken and Lindhout 2002, Michelmore and in the field that cannot be attributed to Dm genes Ochoa 2006, 2008; Mc Hale et al. 2009, Zhang et al. (Milbrath 1923; Verhoeff 1960; Crute and Norwood 2009). L. virosa also possesses race-specific resistance 1981). This quantitative resistance phenotype (Nor- to B. lactucae (Lebeda and Boukema 1991; Lebeda wood and Crute 1985; Grube and Ochoa 2005) has so et al. 2002, Maisonneuve et al. 1999), but its use in far been shown to be inherited polygenically (Simko breeding programs has been restricted by infertility et al. 2013); transgressive segregation resulting in barriers between L. virosa and L. sativa (Maisonneuve elevated resistance has been observed in progeny from 2003). Transfer of resistance from L. virosa to L. cvs. Grand Rapids 9 Iceberg (Grube and Ochoa 2005; sativa has occasionally been enabled by embryo Simko et al. 2013). Some cultivars such as Green rescue (Maisonneuve 1987; Maisonneuve et al. towers and Cobham Green have no known Dm genes 1995). Other wild species such as L. aculeata are and are used as susceptible lines to grow B. lactucae potential sources of resistance that have yet to be used isolates; however, the European isolate Serr84/99 is as donors in breeding programs (Jemelkova´ et al. avirulent on Cobham Green and there is some 2015). Currently, introgression of recently identified evidence suggesting polygenic resistance in this resistance from L. serriola, L. saligna and L. virosa cultivar (Maisonneuve 2011b). Most accessions of L. through repeated backcrosses to L. sativa is being saligna are completely resistant to isolates of B. carried out by multiple public and commercial breed- lactucae derived from L. sativa; therefore, this species ing programs resulting in a large increase in the has been proposed to be a non-host for downy mildew number of resistance genes being deployed (e.g. (Bonnier et al. 1992; Petrzˇelova´ et al. 2011; van Michelmore and Ochoa 2008; Michelmore et al. Treuren et al. 2013); this complete resistance is in part 2013a). determined by several quantitative trait loci (QTLs) operating at different developmental stages (Jeuken and Lindhout 2002; Jeuken et al. 2008, Zhang et al. Genetics of resistance and nomenclature 2009; Den Boer et al. 2013). However, the mechanism of resistance genes of resistance in L.