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Genetic Analysis of Resistance to Tomato Late Blight in Solanum Pimpinellifolium Accession PI 163245

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Genetic Analysis of Resistance to Tomato Late Blight in Solanum Pimpinellifolium Accession PI 163245 Plant Breeding, 135, 391–398 (2016) doi:10.1111/pbr.12366 © 2016 Blackwell Verlag GmbH Genetic analysis of resistance to tomato late blight in Solanum pimpinellifolium accession PI 163245 E RIK W. OHLSON and M AJID R. FOOLAD* Department of Plant Science and the Intercollege Graduate Degree Program in Genetics, The Pennsylvania State University, University Park, PA 16802, USA; *Corresponding author, E-mail: [email protected] With 3 figures and 1 table Received October 9, 2015 / Accepted February 6, 2016 Communicated by M. Havey Abstract and Goodwin 1997, Mayton et al. 2001, Smart and Fry 2001). Late blight (LB), caused by Phytophthora infestans, is one of the most However, many strains of P. infestans have developed resistance devastating diseases of tomato (Solanum lycopersicum) worldwide. Due to phenylamides, one of the few effective systemic treatments to the emergence of new and aggressive P. infestans isolates, identifying for controlling LB infection (Gisi and Cohen 1996, Goodwin new genetic resistance to LB is a priority in tomato breeding. Recently, et al. 1996). While application of preventative control measures we reported the identification of several Solanum pimpinellifolium acces- such as mefenoxam or copper-based fungicides can be effective, sions with strong LB resistance. In this study, we investigated the utility frequent applications have financial and environmental conse- of resistant accession PI 163245 for tomato breeding by examining heri- 2 quences and may only prevent infection by certain genotypes of tability (h ) of resistance and the response to selection for resistance. the pathogen (McGrath et al. 2013). Identifying new sources of Estimates of h2 based on F :F and F :F parent : offspring correla- 2 3 3 4 LB resistance and incorporating resistance into elite breeding tion analyses averaged 0.79 and 0.94, respectively, suggesting the herita- ble nature of LB resistance in PI 163245. Analysis of response to lines and hybrid cultivars is an effective strategy to counter new 2 aggressive strains of P. infestans and reduce fungicide applica- selection for resistance from F2 to F4 generations indicated a realized h of 0.63, confirming the utility of this resistance in tomato breeding. Two tions (Foolad et al. 2008, Nowicki et al. 2013). methods of estimating the minimum number of loci involved indicated Three LB resistance genes are currently known for use in the presence of one major resistance locus. Currently, genetic mapping tomato breeding: Ph-1, Ph-2 and Ph-3. Ph-1, located on chromo- and breeding efforts are underway to further confirm the viability of this some 7, is a dominant resistance gene initially identified in accession for improving tomato LB resistance. accessions West Virginia 19 and 731 (Bonde and Murphy 1952, Ph-1 Key words: disease resistance — parent–offspring regression Gallegly and Marvel 1955, Peirce 1971). While provides P. infestans analysis — qualitative resistance — resistance breeding — resistance to race T-0, it is ineffective against the Solanum lycopersicum L. — vertical resistance predominant race T-1, and as a result, the gene is no longer use- ful in breeding for LB resistance (Peirce 1971, Foolad et al. 2014). The resistance genes Ph-2 and Ph-3 are currently the most effective forms of LB resistance in tomato. Ph-2 confers The cultivated tomato, Solanum lycopersicum L., is the most partial resistance and was first identified in the tomato accession popular and economically important vegetable crop in the world, West Virginia 700 (Gallegly and Marvel 1955), and subse- valued at almost $60 billion annually (faostat3.fao.org). It is sec- quently mapped to the long arm of chromosome 10 (Moreau ond only to potato in volume consumed and accounts for a sig- et al. 1998). While Ph-2 is not considered a particularly strong nificant portion of vitamins and minerals in many diets form of LB resistance (Goodwin et al. 1995, Black et al. 1996, (faostat3.fao.org). However, tomato is susceptible to more than Foolad et al. 2014), a very high level of resistance is obtained 200 diseases caused by fungi, bacteria, viruses and nematodes when it is combined with Ph-3 (Gardner and Panthee 2010a,b, (Lukyanenko 1991). As such, breeding for disease resistance is Panthee and Gardner 2010). Ph-3 was identified in the Solanum vital for improving yield and ensuring adequate production to pimpinellifolium accession L3708 (a.k.a. LA1269 and PI meet worldwide demand. One disease of particular importance is 365957) (AVDRC, 1994), located on the long arm of chromo- late blight (LB), caused by the oomycete Phytophthora infestans some 9 (Chunwongse et al. 1998), and recently fine mapped and (Mont.) de Bary, which is responsible for approximately 7% of cloned (Zhang et al. 2013, 2014). Furthermore, a second minor tomato yield losses annually in the United States and accounts LB resistance QTL was recently identified in L3708 and mapped for similar losses elsewhere in the world (Nowicki et al. 2012). to chromosome 2 (Chen et al. 2014). Despite the strong LB Identification and exploitation of new sources of genetic resis- resistance conferred by Ph-3, tomato cultivars containing this tance to LB is a priority in tomato breeding due to the occur- resistance gene alone have displayed susceptibility to LB when rence of new, more aggressive strains of the pathogen (Foolad exposed to intense disease pressure or particularly aggressive et al. 2008, 2014). P. infestans isolates (Chunwongse et al. 2002, Foolad et al. Phytophthora infestans, the causal agent of the Irish Potato 2008; R. G. Gardner, personal communication). Consequently, Famine, is one of the most destructive diseases of tomato and identification and introgression of additional forms of genetic potato (Solanum tuberosum L.) worldwide, and capable of resistance into new tomato cultivars is expected to be desirable destroying susceptible tomato and potato crops within 7–10 days and may increase the durability of LB resistance. of first colonization (Foolad et al. 2008, Nowicki et al. 2012). Additional LB resistance genes/QTLs have been identified and Until the late 1970s, LB was effectively controlled using fre- studied in several wild species of tomato, but have yet to be quent fungicide application and proper cultural practices (Fry effectively utilized in breeding. For example, race non-specific 392 E. W. OHLSON AND M. R. FOOLAD resistance QTLs were reported in Solanum habrochaites progeny, which were used for disease evaluation and estimation of accession LA2099 on all 12 chromosomes (Brouwer et al. heritability of LB resistance (described below). In all disease-screening 2004). The three strongest QTLs were fine mapped to chromo- experiments, in addition to the parental lines and filial populations, somes 4, 5 and 11 (Brouwer and St. Clair 2004). Resistance was several inbred lines, including NC 84173 (LB susceptible), New Yorker also reported in the S. habrochaites accession BGH6902 and as (containing Ph-1), NC 63EB (Ph-2), NC 870 (Ph-3) and NC 03220 (Ph-2 + Ph-3), were used as control genotypes. Seed of the control lines many as 28 QTLs were detected to contribute to the observed was kindly provided by R.G. Gardner, North Carolina State University, resistance (Abreu et al. 2008). However, the quantitative nature Mills River, NC. of the resistance reported in these accessions has limited their usefulness in tomato breeding. Traditional breeding strategies Inoculum preparation: The P. infestans isolate RS2009T1, belonging and marker-assisted selection (MAS) have been unable to utilize to the US clonal lineage US-23, race T-1 and mating type A1, was used these LB resistance QTLs without introducing undesirable char- in all disease evaluations. RS2009T1 was originally collected from a acteristics from S. habrochaites, including small fruit size, poor commercial tomato field in Rock Springs, PA, in 2009. This clonal growth habit, and late maturity due to linkage drag (Brouwer lineage was selected for its aggressive infection rates in tomato and its and St. Clair 2004). Additionally, effects of these QTLs were widespread natural occurrence throughout the north-eastern USA often relatively small and had low heritability (Abreu et al. (Gugino and Foolad 2013, Foolad et al. 2014, Gugino et al. 2014). The 2008). Resistance to LB has also been reported on chromosome P. infestans isolate was established on susceptible tomato leaflets placed 9 6 in the wild tomato species Solanum pennellii, although this abaxial (lower) side up in 100 15 mm Petri dishes. The Petri dishes contained a thin layer of 1.7% water agar to maintain high humidity. QTL is linked to the SP allele and it has been suggested this The infected tomato leaflets were maintained in an incubator at 14–16°C, resistance is potentially a result of indeterminate growth habit 100% humidity and 12-h photoperiod for 7–11 days. The inoculum was rather than a true resistance gene (Smart et al. 2007). Recently, prepared by placing the leaflets in 4°C distilled water and incubating at new LB resistance genes were identified and mapped to chromo- 4°C for 1 h to facilitate zoospore release. After briefly vortexing the somes 1 and 10 in S. pimpinellifolium accession PI 270443, inoculum to dislodge sporangia, the suspension was filtered through which displays strong LB resistance comparable to Ph-2 + Ph-3 cheesecloth to remove leaf debris, and subsequently adjusted to 10 000 combined (Merk et al. 2012). sporangia/ml using a light microscope and haemocytometer. Solanum pimpinellifolium is the most closely related wild = tomato species to the cultivated tomato (Miller and Tanksley F2 disease evaluation: The F2 population (n 560), parental lines and 1990, Peralta and Spooner 2000) and is the most well-utilized control genotypes were grown in 72-cell seedling flats in an isolated, source of LB resistance in tomato breeding. In order to identify environmentally controlled greenhouse section. For each of the parental additional sources of LB resistance, a screening of 67 and control lines, four replications of six plants were grown and placed on opposite ends and sides of the greenhouse section.
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