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  Lettuce Dieback
Prepared by I. Simko et al.
  Pathogen Responsible
Lettuce necrotic stunt virus
  Description and Sympotoms
Lettuce dieback is a soil-borne disease caused by two closely related viruses from the family Tombusviridae (Obermeier et al., 2001) - Tomato Bushy Stunt Virus (TBSV) and Lettuce Necrotic Stunt Virus (LNSV) that was recently reclassified as Moroccan Pepper Virus (MPV) (Wintermantel and Hladky, 2013). The disease has been observed throughout the main lettuce producing areas of California and Arizona (Grube et al., 2005). Available evidence suggests that dieback disease is caused by the same or a similar Tombusvirus as the brown blight disease described in 1920s (Jagger, 1940; Wisler and Duffus, 2000). TBSV was also detected in Europe (Novák et al., 1981; Blancard et al., 2006), but no widespread distribution of the lettuce dieback disease has been reported outside the U.S.

Symptoms of lettuce dieback include mottling and necrosis of older leaves, stunting, and plant death. The characteristic symptoms usually appear after the plant has reached 6 to 8 weeks of age and render the plant unmarketable. A complete loss of the crop may occur in severely infected fields.
  Current Management
TBSV is an extremely persistent virus and that is likely to survive in soil and water for long periods of time (Wisler and Duffus, 2000). The virus has no known vector and it seems to move through infested soil and water (Martelli et al., 1988). While fungal vectors are not necessary for transmission, studies have yet to be conducted to determine if such vectors can facilitate or increase rates of virus transmission to lettuce. Previous studies have provided no evidence that either chemical treatment or rotation with non-host crops can effectively reduce, remove, or destroy the virus in infested soil (Wintermantel & Anchieta, 2003). Since there are no known cultural methods to prevent the disease in a lettuce crop grown in an infested field, genetic resistance remains the only option for disease control.
  Genetics of Resistance
Susceptibility to dieback is widespread in romaine, butterhead, Batavia, Latin, and leaf lettuces; however, modern iceberg-type cultivars remain completely free of symptoms when grown in infested soil (Grube and Ryder, 2003; Grube et al., 2005; Simko et al., 2009). The resistance in iceberg cultivars appears to have been originally introduced into the crisphead genepool from the cultivar Imperial over 70 years ago (Jagger et al., 1941; Wisler & Duffus, 2000). This suggests that the resistance is effective and highly durable despite extensive cultivation of crisphead cultivars. Genetic analysis using molecular markers identified a single dominant gene (Tvr1) as responsible for the dieback resistance in crisphead lettuce that mapped to chromosomal linkage group 2 (Grube et al., 2005; Simko et al., 2009). Sequencing of molecular markers closely linked to the Tvr1 gene revealed the presence of three haplotypes in cultivated lettuce, two of them associated with resistance (Simko et al., 2010b). One of the resistant haplotypes is predominant in modern iceberg lettuces (e.g. cv. Salinas and relatives), while the other one is present in the primitive accession PI 491224 that was used to introgress dieback resistance into romaine lettuces (Grube & Ryder, 2003; Simko et al., 2010a). Three additional haplotypes associated with disease resistance were identified in wild Lactuca species related to cultivated lettuce (L. saligna, L. serriola, and L. virosa) (Simko et al., 2010b).
  Genetic Marker Development
The Cntg10192 marker on linkage group 2 is linked to the Tvr1 gene (Simko et al., 2009; Simko et al., 2010a; Simko et al., 2010b). This marker was sequenced from 73 accessions of four Lactuca species (L. saligna, L. sativa, L. serriola, and L. virosa). The 349 bp fragment contains 11 SNPs that differentiate six haplotypes (Simko et al., 2010b). The Simko lab developed the High-resolution DNA melting (HRM) assay that can be used to distinguish four haplotypes identified in L. sativa and L. serriola (Simko et al., 2009; Simko et al., 2010b; Simko, 2013). The assay is based on a 185 bp fragment that encompasses three of the 11 SNPs. When more than 1,000 accessions from all horticultural types of lettuce were analyzed with the Cntg10192-based assay, the accuracy of detecting resistant and susceptible phenotypes was 100% (Simko, 2013). Application of marker-assisted selection can reduce the need for field screening and accelerate development of dieback resistant material.

Although many romaine types are susceptible to dieback, they are resistant to Fusarium oxysporum race 1. A major QTL for resistance to F. oxysporum is located on linkage group 2 close to Tvr1. Because F. oxysporum resistance at this location is conferred by the Valmaine allele and the dieback resistance comes from Salinas, there is the possibility that backcrossing to transfer dieback resistance into romaines from crispheads (or conversely resistance to F. oxysporum into crispheads from romaines) could inadvertently introduce susceptibility to the other disease. However, genetic analysis showed that the two resistances are not absolutely linked and lines have been identified that are resistant to both dieback and F. oxysporum (Michelmore & Truco, 2010). Such lines can now be used to breed romaine and crisphead lines that are resistant to both diseases.
  • Blancard, D., Lot, H., Maisonneuve, B. (2006). A colour atlas of diseases of lettuce and related salad crops. Observation, biology and control. Manson Publishing Ltd. - Academic Press, London, UK.
  • Grube, R.C., Ryder, E.J. (2003). Romaine lettuce breeding lines with resistance to lettuce dieback caused by tombusviruses. HortScience 38:627-628.
  • Grube, R.C., Wintermantel, W.M., Hand, P., Aburomia, R., Pink, D.A.C., Ryder, E.J. (2005). Genetic analysis and mapping of resistance to lettuce dieback: a soilborne disease caused by tombusviruses. Theor. Appl. Genet. 110:259-268.
  • Jagger, I.C. (1940). Brown blight of lettuce. Phytopathology 30:53-64.
  • Jagger, I.C., Whitaker, T.W., Uselman, J.J., Owen, W.M. (1941). The Imperial strains of lettuce. U. S. Dept. Agric. Circ. 596.
  • Martelli, G.P., Gallitelli, D., Russo, M. (1988). Tombusviruses. In The plant viruses Volume 3. Edited by: Koenig R. New York: Plenum pp 13-72.
  • Michelmore, R.W., Truco, M.-J. (2010). Breeding leaf lettuce. Report to the California Leafy Greens Research Board.
  • Novák, J.B., Nováková, J., Lanzová, J. (1981). Demonstration of tomato bushy stunt virus in lettuce. Ochr. Rostl. 17:241-245.
  • Obermeier, C., Sears, J.L., Liu, H.Y., Schlueter, K.O., Ryder, E.J., Duffus, J.E., Koike, S.T., Wisler, G.C. (2001). Characterization of distinct tombusviruses that cause diseases of lettuce and tomato in the western United States. Phytopathology 91:797-806.
  • Simko, I. (2013). Marker-assisted selection for disease resistance in lettuce. In: R.K. Varshney and R. Tuberosa, editors, Translational genomics for crop breeding, Vol. I: Biotic stresses. Wiley-Blackwell Publ., Hoboken, NJ.
  • Simko, I., Hayes, R.J., Subbarao, K.V., Sideman, R.G. (2010a). SM09A and SM09B: Romaine lettuce breeding lines resistant to dieback and with improved shelf life. HortScience 45:670-672.
  • Simko, I., Pechenick, D.A., McHale, L.K., Truco, M.J., Ochoa, O.E., Michelmore, R.W., Scheffler, B.E. (2009). Association mapping and marker-assisted selection of the lettuce dieback resistance gene Tvr1. BMC Plant Biol. 9:135.
  • Simko, I., Pechenick, D.A., McHale, L.K., Truco, M.J., Ochoa, O.E., Michelmore, R.W., Scheffler, B.E. (2010b). Development of molecular markers for marker-assisted selection of dieback disease resistance in lettuce (Lactuca sativa). Acta Hortic. 859:401-408.
  • • Wintermantel, W.M., Anchieta, A.G. (2003). Tombusvirus infection of lettuce is influenced by soil salinity. Proceedings of the 5th symposium of the international working group on plant viruses with fungal vectors: Zurich, Switzerland pp 131-134.
  • Wintermantel, W.M., Hladky, L.L. (2013). Complete genome sequence and biological characterization of Moroccan pepper virus (MPV) and reclassification of Lettuce necrotic stunt virus as MPV. Phytopathology 103:501-508.
  • Wisler, G.C., Duffus, J.E. (2000). A century of plant virus management in the Salinas Valley of California, 'East of Eden'. Virus Res. 71:161-169.
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