Seedlings of 431 accessions representing six and five Armenian natural populations of the wild Lactuca georgica and L. altaica, respectively, and 32, 23, and 20 populations of L. saligna, L. serriola, and L. aculeata, respectively (mostly Israeli natural populations), were screened at seedling stage for resistance to six highly virulent races of Bremia lactucae - the causal of lettuce downy mildew - that were found on several widely grown cultivars and represent the virulence spectrum in the main lettuce production areas in Europe and California. This study is likely the first detailed screening of resistance to B. lactucae races in natural populations of L. georgica and L. altaica. The highest average resistance probability and frequency of highly resistant accessions across races were detected in L. georgica. These were even higher than those shown by the germplasm of known non-host resistance (NHR) species L. saligna, which classified to the secondary lettuce gene pool (LGP-2). Thus, we suggest that L. georgica is a new LGP-2 source of resistance to B. lactucae. Our findings also support previous observations that L. aculeata, a species within the LGP-1, should be prioritized as a source of downy mildew resistance in domesticated lettuce (L. sativa) breeding programs, since some L. aculeata accessions expressed highly resistance across races. For L. serriola, the closest relative of cultivated lettuce, and for L. altaica, also a closer or even a primitive form of L. sativa, probabilities of resistance to each of the investigated B. lactucae races were very low.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Beharav, A., & Hellier, B. (2020). Bolting and flowering response of Lactuca georgica, a wild lettuce relative, to low temperatures. American Journal of Plant Sciences, 11, 2139–2154.
Beharav, A., Lewinsohn, D., Lebeda, A., & Nevo, E. (2006). New wild Lactuca genetic resources with resistance against Bremia lactucae. Genetic Resources and Crop Evolution, 53, 467–474.
Beharav, A., Ben-David, R., Doležalová, I., & Lebeda, A. (2008). Eco-geographical distribution of Lactuca saligna natural populations in Israel. Israel Journal of Plant Science, 56, 195–206.
Beharav, A., Ben-David, R., Doležalová, I., & Lebeda, A. (2010a). Eco-geographical distribution of Lactuca aculeata natural populations in North-Eastern Israel. Genetic Resources and Crop Evolution, 57, 679–686.
Beharav, A., Ben-David, R., Malarz, J., Stojakowska, A., Michalska, K., Doležalová, I., Lebeda, A., & Kisiel, W. (2010b). Variation of sesquiterpene lactones in Lactuca aculeata natural populations from Israel, Jordan and Turkey. Biochemical Systematics and Ecology, 38, 602–611.
Beharav, A., Ochoa, O., & Michelmore, R. (2014). Resistance in natural populations of three wild Lactuca species from Israel to highly virulent Californian isolates of Bremia lactucae. Genetic Resources and Crop Evolution, 61, 603–609.
Beharav, A., Stojakowska, A., Ben-David, R., Malarz, J., Michalska, K., & Kisiel, W. (2015). Variation of sesquiterpene lactone contents in Lactuca georgica natural populations from Armenia. Genetic Resources and Crop Evolution, 62, 431–441.
Beharav, A., Hellier, B., Richardson, K. L., Lebeda, A., & Kisha, T. (2018a). Genetic relationships and structured diversity of Lactuca georgica germplasm from Armenia and the Russian Federation among other members of Lactuca L., subsection Lactuca L., assessed by TRAP markers. Genetic Resources and Crop Evolution, 65, 1963–1978.
Beharav, A., Khalifa, S., & Nevo, E. (2018b). New insights into the range, morphology, and natural hybridization of wild Lactuca aculeata in Israel. Israel Journal of Plant Science, 65, 175–185.
Beharav, A., Malarz, J., Michalska, K., Ben-David, R., & Stojakowska, A. (2020). Variation of sesquiterpene lactone contents in Lactuca altaica natural populations from Armenia. Biochemical Systematics and Ecology, 90, 104030.
Bonnier, F. G. M., Reinink, K., & Groenwold, R. (1992). New sources of major gene resistance in Lactuca to Bremia lactucae. Euphytica, 61, 203–211.
Bonnier, F. G. M., Reinink, K., & Groenwold, R. (1994). Genetic analysis of Lactuca accessions with new major gene resistance to lettuce downy mildew. Phytopathology, 84, 462–468.
De Vries, I. M. (1990). Crossing experiments of lettuce cultivars and species (Lactuca sect. Lactuca, Compositae). Plant Systematics and Evolution, 171, 233–248.
Doležalová, I., Křístková, E., Lebeda, A., & Vinter, V. (2002). Description of morphological characters of wild Lactuca L. spp. genetic resources (English-Czech version). Horticultural Science (Prague), 29, 56–83.
Gabrielian, E., & Zohary, D. (2004). Wild relatives of food crops native to Armenia and Nakhichevan. Flora Mediterranea, 14, 5–80.
Giesbers, A. K. J., Pelgrom, A. J. E., Visser, R. G. F., Niks, R. E., Van den Ackerveken, G., & Jeuken, M. J. W. (2017). Effector-mediated discovery of a novel resistance gene against Bremia lactucae in a nonhost lettuce species. New Phytologist, 216, 915–926.
Giesbers, A. K. J., den Boer, E., Braspenning, D. N. J., Bouten, T. P. H., Specken, J. W., van Kaauwen, M. P. W., Visser, R. G. F., Niks, R. E., & Jeuken, M. J. W. (2018). Bidirectional backcrosses between wild and cultivated lettuce identify loci involved in nonhost resistance to downy mildew. Theoretical and Applied Genetics, 131, 1761–1776.
Gower, J. C. (1971). A general coefficient of similarity and some of its properties. Biometrics, 27, 857–871.
Gower, J. C., & Legendre, P. (1986). Metric and Euclidean properties of dissimilarity coefficients. Journal of Classification, 3, 5–48.
Heath, M. C. (1991). Evolution of resistance to fungal parasitism in natural ecosystems. New Phytologist, 119, 331–343.
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. Biochemical Systematics and Ecology, 61, 344–356.
Jeuken, M., Peleman, J., & Lindhout, P. (2001). An integrated interspecific AFLP map of lettuce (Lactuca) based on two L. sativa × L. saligna F2 populations. Theoretical and Applied Genetics, 103, 638–647.
Kilian, N., Gemeinholzer, B., & Lack, H. W. (2009). Tribe Cichorieae. In V. A. Funk, A. Susanna, T. Stuessy & R Bayer (Eds), Systematics, evolution, and biogeography of the Compositae (chapter 10: pp. 343–383). Vienna: International Association for Plant Taxonomy.
Kitner, M., Lebeda, A., Doležalová, I., Maras, M., Křístková, E., Nevo, E., Pavlíček, T., Meglic, V., & Beharav, A. (2008). AFLP analysis of Lactuca saligna germplasm collections from four European and three Middle East countries. Israel Journal of Plant Science, 56, 185–193.
Kitner, M., Majesky, L., Křistková, E., Jemelková, M., Lebeda, A., & Beharav, A. (2015). Genetic structure and diversity in natural populations of three predominantly self-pollinating wild Lactuca species in Israel. Genetic Resources and Crop Evolution, 62, 991–1008.
Lebeda, A. (1986). Specificity of interactions between wild Lactuca spp. and Bremia lactucae isolates from Lactuca serriola. Journal of Phytopathology, 117, 54–64.
Lebeda, A., & Petrželová, I. (2010) Screening for resistance to lettuce downy mildew (Bremia lactucae). In: M. M. Spencer & A. Lebeda, (Eds), Mass Screening Techniques for Selecting Crops Resistant to Disease (chapter 15: pp. 245-256). Vienna: International Atomic Energy Agency (IAEA).
Lebeda, A., & Reinink, K. (1994). Histological characterization of resistance in Lactuca saligna to lettuce downy mildew (Bremia lactucae). Physiological and Molecular Plant Pathology, 44, 125–139.
Lebeda, A., Pink, D. A. C., & Astley, D. (2002). Aspects of the interactions between wild Lactuca spp. and related genera and lettuce downy mildew (Bremia lactucae). In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.), Advances in Downy Mildew Research (pp. 85–117). Dordrecht: Kluwer.
Lebeda, A., Ryder, E. J., Grube, R., Doležalová, I., & Křístková, E. (2007). Lettuce (Asteraceae; Lactuca spp.). In R. Singh, & F. L. Boca Raton (Eds.), Genetic Resources, Chromosome Engineering, and Crop Improvement Series, Vegetable Crops (Volume 3, Chapter 9: pp. 377–472). Boca Raton: CRC Press.
Lebeda, A., Kitner, M., Křístková, E., Doležalová, I., & Beharav, A. (2012). Genetic polymorphism in Lactuca aculeata populations and occurrence of natural putative hybrids between L. aculeata and L. serriola. Biochemical Systematics and Ecology, 42, 113–123.
Lebeda, A., Křístková, E., Kitner, M., Mieslerová, B., Jemelková, M., & Pink, D. A. C. (2014). Wild Lactuca species, their genetic diversity, resistance to diseases and pests, and exploitation in lettuce breeding. European Journal of Plant Pathology, 138, 597–640.
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 T. J. L. Van Hintum, A. Lebeda, D. A. C. Pink, & J. W. Schut (Eds.), Eucarpia Leafy Vegetables Conference (pp. 61–67). Noordwijkerhout, Netherlands, 19–21 Mar 2003.
Michalska, K., Beharav, A., & Kisiel, W. (2014). Sesquiterpene lactones from roots of Lactuca georgica. Phytochemistry Letters, 10, 10–12.
Michelmore, R., Ochoa, O., & Wong, J. (2009). Bremia lactucae and lettuce downy mildew. In S. Kamoun & K. Lamour (Eds.), Oomycete genetics and genomics: Diversity, plant and animal interactions, and Toolbo (pp. 241–262). Hoboken: John Wiley & Sons, Inc.
Parra, L., Maisonneuve, B., Lebeda, A., Schut, J., Christopoulou, M., Jeuken, M., McHale, L., Truco, M. J., Crute, I., & Michelmore, R. (2016). Rationalization of genes for resistance to Bremia lactucae in lettuce. Euphytica, 210, 309–326.
Parra, L., Nortman, K., Sah, A., Truco, M. J., Ochoa, O., & Michelmore, R. (2021). Identification and mapping of new genes for resistance to downy mildew in lettuce. Theoretical and Applied Genetics, 134, 519–528.
Petrželová, I., Lebeda, A., & Beharav, A. (2011). Resistance to Bremia lactucae in natural populations of Lactuca saligna from some middle eastern countries and France. Annals of Applied Biology, 159, 442–455.
SAS Institute Inc. (2012). SAS OnlineDoc, Version 9.4 for windows. Cary: SAS Institute.
Schulze-Lefert, P., & Panstruga, R. (2011). A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science, 16, 117–125.
Spring, O., Gomez-Zeledon, J., Hadziabdic, D., Trigiano, R. N., Tines, M., & Lebeda, A. (2018). Biological characteristics and assessment of virulence diversity in pathosystems of economically important biotrophic oomycetes. Critical Reviews in Plant Sciences, 37(6), 439–495.
Strugala, R., Delventhal, R., & Schaffrath, U. (2015). An organ-specific view on non-host resistance. Frontiers in Plant Science, 6, 526.
The Plant List, Version 1.1, (2013). http://www.theplantlist.org/. Accessed 26 January 2021.
van Treuren, R., van der Arend, A. J. M., & Schut, J. W. (2013). Distribution of downy mildew (Bremia Lactucae regel) resistances in a genebank collection of lettuce and its wild relatives. Plant Genetic Resources: Characterization and Utilization, 11, 15–25.
van Treuren, R., van Eekelen, H. D. L. M., Wehrens, R., & de Vos, R. C. H. (2018). Metabolite variation in the lettuce gene pool: Towards healthier crop varieties and food. Metabolomics, 14, 146.
Wood, K. J., Nur, M., Gil, J., Fletcher, K., Lakeman, K., Gann, D., Gothberg, A., Khuu, T., Kopetzky, J., Naqvi, S., Pandya, A., Zhang, C., Maisonneuve, B., Pel, M., & Michelmore, R. (2020). Effector prediction and characterization in the oomycete pathogen Bremia lactucae reveal host-recognized WY domain proteins that lack the canonical RXLR motif. PLoS Pathogens, 16(10), e1009012.
Zohary, D. (1991). The wild genetic resources of cultivated lettuce (Lactuca sativa L.). Euphytica, 53, 31–35.
AB wishes to thank Rijk Zwaan (De Lier, The Netherlands) for providing greenhouse facilities, support in assessment and cultivation of the Lactuca accessions, as well as screening for resistance to the B. lactucae races. Financial support by the Research Authority, and performing the statistical analysis by Mrs. Efrat Yaskil, the Statistics Consulting Unit, University of Haifa, Israel, are acknowledged. Valuable comments on the revised version of this manuscript by Dr. Roi Ben-David, Institute of Plant Sciences, Agriculture Research Organization (ARO), Volcani Center, Bet Dagan, Israel, are gratefully acknowledged.
The research reported in this article did not have human or animal subjects.
Conflict of interest
The authors declare that they have no Conflict of interest.
About this article
Cite this article
Beharav, A. Lactuca georgica, a new wild source of resistance to downy mildew: comparative study to other wild lettuce relatives. Eur J Plant Pathol 160, 127–136 (2021). https://doi.org/10.1007/s10658-021-02228-5
- Bremia lactucae
- Gene pools
- Lettuce breeding
- Non-host resistance
- Wild Lactuca species