Basil (Ocimum sp.) is a highly diverse genus (Vieira et al., 2003) that includes at least 64 species (Paton et al., 1999), several of which are among the most widely cultivated and consumed herbs worldwide (Simon et al., 1990). In the United States, Israel, and Europe, commercial sweet basil is readily identified by a distinct phenotype and chemotype used in the fresh, dried, and culinary industries (De Masi et al., 2006; Simon et al., 1990). Downy mildew has become a devastating disease of commercial sweet basil around the world and has severely impacted major growing regions in the United States since 2007 (Roberts et al., 2009; Wyenandt et al., 2010). A genus-specific host range limits P. belbahrii infection to basil species and excludes other members of the Lamiaceae family (Belbahri et al., 2005; Thines et al., 2009). Pathogenesis occurs during extended periods of leaf wetness and high humidity, which facilitate sporangia germination and entry through host stomata (Garibaldi et al., 2007; Koroch et al., 2013). Persistence of these environmental conditions results in profuse sporulation from the abaxial leaf surface and rapid disease progress leading to complete crop loss (Roberts et al., 2009). The capacity of P. belbahrii to persist on both seed (Garibaldi et al., 2004a) and transplants (Farahani-Kofoet et al., 2012) provides versatility to this species of downy mildew, which has facilitated its worldwide dissemination (Blomquist et al., 2009; Garibaldi et al., 2004b; Kanetic and Vasiliou, 2014; Martinez-de la Parte et al., 2009; McLeod et al., 2006; Nagy and Horvath, 2011).
Conventional and organic control methods have been explored and several conventional fungicides have resulted in reduced disease severity; however, organic controls tested to date remain ineffective (Homa et al., 2014; Mersha et al., 2012). The efficacy of chemical control agents is dependent on many factors including host developmental stage, application rate/interval, environmental conditions, and inoculum levels. The foliar application of pesticides in sweet basil has a number of disadvantages including the chemical residuals (Gilardi et al., 2013), pathogen selection pressure (Cohen et al., 2013), and increased resources required for repeated applications. The existence of P. belbahrii races has not been reported. However, recent discovery of oospores (Cohen et al., 2013) suggests the potential for sexual reproduction and eventual evolution of new pathogen races. Integration of downy mildew–resistant sweet basil cultivars into pest management strategies represents a more sustainable control strategy that is advantageous to environmental, public health, and economic interests.
Host resistance to basil downy mildew was first reported in 2010 from field evaluations in which all O. basilicum cultivars and breeding lines were highly susceptible (Wyenandt et al., 2010). Sporulation was reduced in multiple cultivars of O. ×citriodorum, while sporulation and chlorosis were absent on leaves of three similar cultivars of O. americanum (Wyenandt et al., 2010). To confirm these field observations and identify new sources of resistance and tolerance to basil downy mildew, a rapid screening protocol using a controlled environment was developed (Pyne et al., 2014).
Greenhouse evaluations of the U.S. Department of Agriculture National Plant Germplasm System (USDA-NPGS) germplasm demonstrated extensive susceptibility among O. basilicum accessions with the exception of accessions PI 172996, PI 172997, and PI 172998. Sporulation was not observed on leaves of these accessions. However, presence of disease symptoms (i.e., chlorosis and necrosis) in greenhouse screenings (Pyne et al., 2014) and presence of sporulation in field evaluations (James E. Simon, unpublished data) diminished the breeding value of these lines. Greenhouse screening has been essential to the identification of multiple resistant Ocimum accessions such as PI 652053 (Farahani-Kofoet et al., 2014; Pyne et al., 2014). However, these accessions are different species from O. basilicum and breeding is limited by sexual incompatibility and F1 hybrid sterility. The commercial cultivar Mrihani [Ocimum sp. (Horizon Seed Co., Williams, OR)] is a methyl chavicol chemotype with highly serrate and undulate leaves that was initially identified as downy mildew resistant using the rapid screening approach (Pyne et al., 2014). Despite a substantial difference in aroma, flavor, and phenotype, this cultivar is sexually compatible with sweet basil and could be used to facilitate the development of subsequent generations from a fertile F1.
For disease resistance breeding strategies to be most effective, they must be supported by inheritance studies that measure disease response across multiple generations, environments, and years (Holland et al., 2003). Such studies can be used to determine number of genes involved and elucidate gene action, which is essential to the adoption of an effective breeding method. True leaf downy mildew resistance in Brassica species has been attributed to a single dominant gene in multiple reports (Farnham et al., 2002; Jensen et al., 1999; Mahajan et al., 1995; Monteiro et al., 2005; Natti et al., 1967). Carlsson et al. (2004) determined a single recessive gene to be responsible for resistance in cotyledons of Brassica oleracea. Traits controlled by Mendelian genes are advantageous to plant breeders because rapid gain can be achieved with fewer selection cycles. However, in many cases gene action is complicated by multiple genes acting independently or interacting in a nonallelic or epistatic fashion (Hayman, 1958; Jinks and Jones, 1957; Mather and Jinks, 1971).
Peronospora belbahrii is an emerging pathogen of Ocimum species and inheritance of resistance has not been characterized. When prior knowledge of gene action is unavailable, it is important that an appropriate mating design is selected to capture as much genetic variation as possible through use of multiple populations from the same or different parents (Mather and Jinks, 1971). The development of six related generations derived from two inbred lines with differential response to a particular trait of interest provides a metrical system for partitioning of gene effects using scaling tests (Hayman, 1958; Mather and Jinks, 1971). This classic mating design has proven effective in determinations of heritability and gene action when characterizing new sources of disease resistance (Tetteh et al., 2013a, 2013b). The objective of this study was to investigate the mode of inheritance for resistance to downy mildew in a segregating full-sibling sweet basil family. Results provide the basis by which to design the appropriate breeding and selection strategies for the development of downy mildew resistance in sweet basil.
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