Segregation of Eastern Filbert Blight Disease Response and Single Nucleotide Polymorphism Markers in Three European–American Interspecific Hybrid Hazelnut Populations

in Journal of the American Society for Horticultural Science
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  • 1 Department of Plant Biology, School of Environmental and Biological Sciences, Rutgers University, 59 Dudley Road, New Brunswick, NJ 08901
  • | 2 Center for Agroforestry, University of Missouri, 1111 Rollins Street, Columbia, MO 65211
  • | 3 Department of Plant Biology, School of Environmental and Biological Sciences, Rutgers University, 59 Dudley Road, New Brunswick, NJ 08901

The perennial stem canker disease eastern filbert blight (EFB), caused by Anisogramma anomala, is devastating to most trees of European hazelnut (Corylus avellana), as genetic resistance is rare in the species. The pathogen is harbored by the wild American hazelnut (Corylus americana) found throughout much of eastern North America. Wild American hazelnut is generally resistant or tolerant to EFB, and is fully cross compatible with C. avellana, the species grown commercially for its nuts, making it a valuable resource for disease resistance breeding. The objective of this study was to identify quantitative trait loci (QTLs) associated with EFB resistance and tolerance in these two species. Three unrelated EFB-resistant C. americana selections [Oregon State University (OSU) 533.069 from Pennsylvania, OSU 403.040 from Nebraska, and OSU 557.122 from Wisconsin] were crossed with C. avellana ‘Tonda di Giffoni’ (TdG), a cultivar from Italy known to be tolerant of EFB. Their progenies, each containing 124 trees, were exposed to A. anomala through field inoculations and natural spread over 7 years, then each tree was evaluated for cumulative disease response. Results showed that disease response of all three populations exhibited a roughly normal distribution, indicating that resistance/tolerance was under multigenic control. An average of 2869 total markers were used to construct each population’s linkage map following genotyping, which included an average of 121 published simple sequence repeat markers to anchor linkage groups (LGs) to those of previous studies. Linkage maps were constructed for each parent of each population and used to map QTLs associated with EFB response. The subsequent analysis resolved five EFB-related QTLs across the three populations, highlighting three genic regions. Unexpectedly, only one QTL was identified from one of the three resistant C. americana parents, located on LG11 of the map of OSU 403.040, whereas three QTLs were found in a similar region on LG10 across the three maps of TdG, and a fifth QTL was found on LG6 of one TdG map. The lack of strong QTLs identified from the three EFB-resistant C. americana parents suggests that their resistance may be highly quantitative and not resolved within the constraints of this study. In contrast, tolerance from TdG appears to be conferred by a limited number of genes with relatively strong effects. Based on prior mapping work in European and American hazelnut where R genes have been located on LG2, LG6, and LG7, the QTLs associated with resistance/tolerance on LG10 and LG11 represent novel resistance regions. These QTLs present new targets for marker aided breeding, especially when pyramiding EFB resistance genes is a goal.

Abstract

The perennial stem canker disease eastern filbert blight (EFB), caused by Anisogramma anomala, is devastating to most trees of European hazelnut (Corylus avellana), as genetic resistance is rare in the species. The pathogen is harbored by the wild American hazelnut (Corylus americana) found throughout much of eastern North America. Wild American hazelnut is generally resistant or tolerant to EFB, and is fully cross compatible with C. avellana, the species grown commercially for its nuts, making it a valuable resource for disease resistance breeding. The objective of this study was to identify quantitative trait loci (QTLs) associated with EFB resistance and tolerance in these two species. Three unrelated EFB-resistant C. americana selections [Oregon State University (OSU) 533.069 from Pennsylvania, OSU 403.040 from Nebraska, and OSU 557.122 from Wisconsin] were crossed with C. avellana ‘Tonda di Giffoni’ (TdG), a cultivar from Italy known to be tolerant of EFB. Their progenies, each containing 124 trees, were exposed to A. anomala through field inoculations and natural spread over 7 years, then each tree was evaluated for cumulative disease response. Results showed that disease response of all three populations exhibited a roughly normal distribution, indicating that resistance/tolerance was under multigenic control. An average of 2869 total markers were used to construct each population’s linkage map following genotyping, which included an average of 121 published simple sequence repeat markers to anchor linkage groups (LGs) to those of previous studies. Linkage maps were constructed for each parent of each population and used to map QTLs associated with EFB response. The subsequent analysis resolved five EFB-related QTLs across the three populations, highlighting three genic regions. Unexpectedly, only one QTL was identified from one of the three resistant C. americana parents, located on LG11 of the map of OSU 403.040, whereas three QTLs were found in a similar region on LG10 across the three maps of TdG, and a fifth QTL was found on LG6 of one TdG map. The lack of strong QTLs identified from the three EFB-resistant C. americana parents suggests that their resistance may be highly quantitative and not resolved within the constraints of this study. In contrast, tolerance from TdG appears to be conferred by a limited number of genes with relatively strong effects. Based on prior mapping work in European and American hazelnut where R genes have been located on LG2, LG6, and LG7, the QTLs associated with resistance/tolerance on LG10 and LG11 represent novel resistance regions. These QTLs present new targets for marker aided breeding, especially when pyramiding EFB resistance genes is a goal.

The Corylus genus comprises 13 species organized into four different subsections (Botta et al., 2019). These species are spread across a wide geographic area of the northern hemisphere, including Asia, Europe, and North America (Mehlenbacher, 1991). Although all species produce edible nuts, European hazelnut (C. avellana) is the species of commercial interest, mainly because of its superior traits. European hazelnut trees grow best in areas with mild summers and winters, often in areas bordered by major bodies of water (Mehlenbacher, 1991). Top European hazelnut producers worldwide include Turkey (776,046 t), Italy (98,530 t), Azerbaijan (53,793 t), the United States (39,920 t), Chile (35,000 t), China (29,318 t), and the Republic of Georgia (24,000 t) (Food and Agricultural Organization of the United Nations, 2019). Within the United States, 99% of European hazelnut production takes place in the Willamette Valley of Oregon (Lunde et al., 2000).

Attempts to grow European hazelnut in the eastern United States have been made for more than 100 years, but the disease eastern filbert blight (EFB), caused by the fungus Anisogramma anomala, has continually hindered such efforts (Capik and Molnar, 2012; Fuller, 1908; Johnson and Pinkerton, 2002; Thompson et al., 1996). In the eastern United States, where the pathogen is harbored by the tolerant wild American hazelnut (C. americana), A. anomala is pervasive and genetically variable (Cai et al., 2013; Dunlevy et al., 2019; Johnson et al., 1996; Muehlbauer et al., 2019; Pinkerton et al., 1993; Tobia et al., 2017). American hazelnut can be found throughout much of eastern North America, from southern Canada in the north, through Florida and Oklahoma in the south, bordered by the Rocky Mountains on the west and the Atlantic Ocean on the east (Drumke, 1964; Gleason and Cronquist, 1963; Revord et al., 2020; Sathuvalli and Mehlenbacher, 2012). Although American hazelnut rarely shows signs or symptoms of EFB (Revord et al., 2020), most European hazelnut cultivars are highly susceptible, with EFB capable of killing host trees lacking genetic resistance within a few years following infection (Fuller, 1908; Johnson and Pinkerton, 2002; Johnson et al., 1996).

Genetic host resistance has been widely accepted as the most effective method to manage EFB (Chen et al., 2007; Lunde et al., 2006; Sathuvalli et al., 2010). ‘Gasaway’, an obsolete pollinizer with poor nut traits, was the first European cultivar identified with genetic resistance to EFB in the Pacific Northwest (Cameron, 1976; Mehlenbacher et al., 1991). This cultivar was shown to carry a dominant resistance allele in the heterozygous state at a single locus (Coyne et al., 1998; Mehlenbacher et al., 1991; Osterbauer et al., 1997; Sathuvalli et al., 2017). ‘Gasaway’ has been used extensively in the Oregon State University (OSU) breeding program to address EFB following the pathogen’s introduction to the Pacific Northwest in the 1960s, resulting in the release of a series of EFB-resistant cultivars and pollinizers (Botta et al., 2019; Davison and Davidson, 1973). Their use has revived the declining Oregon European hazelnut industry, which has expanded from 11,700 ha in 2009 to 34,000 ha in 2020 (N. Wiman, personal communication). Research conducted at OSU mapped the ‘Gasaway’ resistance gene (R-gene) to linkage group 6 (LG6) of the European hazelnut genetic map (Mehlenbacher et al., 2004; Sathuvalli and Mehlenbacher, 2013; Sathuvalli et al., 2012, 2017). Interestingly, although ‘Gasaway’ resistance is effective in controlling EFB in Oregon, cultivars carrying the R-gene are susceptible to EFB when grown in parts of the eastern United States, with recent research suggesting the presence of pathogenic variation (multiple strains) in eastern A. anomala populations (Capik and Molnar, 2012; Capik et al., 2013; Dunlevy et al., 2019; Molnar et al., 2010a, 2010b; Muehlbauer et al., 2018).

In an attempt to decrease reliance on one source of EFB resistance, multiple seed-based collection expeditions, primarily across eastern Europe and the Caucasus region, were made and thousands of cultivars, selections, and other germplasm have been screened for EFB response. Approximately 3% of the more than 5000 seedlings evaluated between OSU and Rutgers University (New Brunswick, NJ) have been deemed resistant to EFB (Capik et al., 2013; Chen et al., 2007; Colburn et al., 2015; Coyne et al., 1998; Leadbetter et al., 2016; Lunde et al., 2000; Molnar et al., 2007, 2010a, 2018; Sathuvalli et al., 2010). Fortunately, resistant C. avellana accessions have been identified that originate from many different countries and, more recently, R-genes have been mapped to several different LGs. For example, resistance from the Spanish cultivar Culpla, the Serbian cultivar Crvenje, the Russia selection OSU 495.072, and selection OSU 408.040 from Minnesota have all mapped to the same region as ‘Gasaway’ resistance on LG6 (Colburn et al., 2015; Sathuvalli et al., 2012). An additional eight sources of resistance with varying origins have also been assigned to LG6 based on simple sequence repeat (SSR) markers (Komaei Koma et al., 2021). Resistance in the Spanish cultivar Ratoli mapped to LG7 along with resistance from C. americana cultivar Rush, whereas resistance of the Georgian selection OSU 759.010 and Russian selection Rutgers H3R07P25 mapped to LG2 (Bhattarai et al., 2017; Honig et al., 2019; Sathuvalli et al., 2011a, 2011b). Şekerli et al. (2021) mapped four additional sources of resistance to LG7 and one additional source to LG2. Other sources of resistance, such as the Italian cultivar Tonda di Giffoni (TdG) and the OSU cultivar Sacajawea, appear to possess quantitative resistance [QR (high level of tolerance)] possibly controlled by several genes (Capik and Molnar, 2012; Chen et al., 2007; Mehlenbacher et al., 2008). In these accessions, disease incidence is reduced and, when present, cankers are smaller in size and occur less frequently.

Breeders have also looked beyond European hazelnut for resistance to EFB, as well as other important traits, such as enhanced climatic adaptation (primarily cold tolerance). For more than 100 years, breeders and growers in the eastern United States have made crosses between European and wild American hazelnuts in an attempt to combine the superior nut traits of the European species with the EFB tolerance of the wild American species. Breeding efforts were generally intermittent over the decades, and commercial cultivars were never developed (Molnar, 2011; Molnar et al., 2005). More recently, interspecific progenies and populations have been studied for their responses to EFB, with varying results from mostly susceptible to a significant proportion of the progeny expressing resistance (Chen et al., 2007; Coyne et al., 1998; Molnar and Capik, 2012; Molnar et al., 2009; Revord et al., 2020). More specifically, Molnar and Capik (2012) found that resistance was generally poorly transmitted from EFB-resistant C. americana parents to F1 progeny when crossed to susceptible C. avellana, with the exception of plants related to C. americana ‘Rush’, which was shown to transmit a single R-gene (Bhattarai et al., 2017; Chen et al., 2005; Sathuvalli et al., 2012). Later, Revord et al. (2020) examined EFB response across a much larger number of F1 hybrid populations of EFB-resistant C. americana crossed with susceptible and tolerant C. avellana and documented bimodal, normal, and no transmission distributions across the various progeny. The bimodal distribution category suggests that qualitative genes may be involved in EFB resistance, whereas the continuous and no transmission distributions suggest resistance is polygenic and sometimes not expressed at a sufficient level in the F1. These varied results also showed that the C. americana selection’s phenotype is not an accurate predictor of EFB response of its progeny. Test crosses are needed to better understand inheritance, presenting challenges for breeders of plants with long juvenile periods.

The objective of our study was to document disease response in F1 hybrid progenies between three unrelated EFB-resistant C. americana selections and the EFB-tolerant C. avellana TdG, and then generate single nucleotide polymorphism (SNP) markers through next-generation sequencing (NGS) to develop highly saturated linkage maps and identify QTLs for EFB resistance and tolerance in these three populations.

Materials and Methods

Population development.

Three interspecific F1 C. americana × C. avellana full-sib progenies (abbreviated as CRA, CRB, and CRC) were developed for this study, each containing 124 seedlings and their two parents. The maternal C. americana parents included OSU 533.069 [from Pennsylvania (seed lot OSU 88301)], OSU 403.040 [from Nebraska (seed lot OSU 87147)], and OSU 557.122 [from Wisconsin (seed lot OSU 89314)] for the CRA, CRB, and CRC populations, respectively. These accessions were originally selected by S. Mehlenbacher at OSU from a larger population of wild germplasm, as described in Sathuvalli and Mehlenbacher (2012). The accessions were also clonally propagated and evaluated at Rutgers University following field inoculations and natural spread and found to be resistant to EFB, showing no signs or symptoms of the disease (Capik and Molnar, 2012). The Italian TdG was chosen as the common C. avellana paternal parent. This cultivar is believed to possess QR to EFB, showing reduced incidence and severity of cankers, and also exhibiting highly desirable nut and kernel traits (Capik and Molnar, 2012; Coyne et al., 2000).

The C. americana female parent trees were located at Rutgers University Horticultural Research Farm #3 (East Brunswick, NJ). Pollen of TdG was collected in Jan. 2011 at OSU and stored at −28.9 °C, then shipped overnight on dry ice for use in pollinations in Feb. 2011. Hybridizations were conducted following the procedures of Mehlenbacher (1994). Nuts were harvested from trees in Sep. 2011 and stratified under moist conditions at 4 °C for 4 months, then germinated in a peat-based medium in a greenhouse (24/18 °C day/night with 16 h daylength). Trees were kept in the greenhouse during the spring months following procedures of Molnar and Capik (2012), then acclimated to outdoor conditions by moving them under 40% shade in June 2012. They were planted in the field in Nov. 2012 at the Rutgers Specialty Crop Research and Extension Center (Cream Ridge, NJ). Tree spacing was 1.0 m within rows and 3.0 m between rows. Herbicides were used to control weeds, but no insecticides or fungicides were sprayed. In addition to natural infections caused by EFB inoculum from other nearby European and American hazelnut research fields and later from cankers within the plot itself, trees were field inoculated by tying diseased stems into the canopy of each seedling tree each spring from 2013 to 2015 to help reduce the chance trees escaped infection (Molnar et al., 2007). By year 7, the trees would have had at least 5 successive years of exposure to EFB and opportunity for multiple years of perennial canker development within each tree.

Disease response phenotyping.

Total canker length (TCL) and total shoot length (TSL) were measured for each tree in Jan. 2019. TCL was determined by measuring every canker on each tree to the nearest inch and summing all individual canker lengths. TSL was determined by measuring each shoot (excluding young suckers and previous year’s growth that would not yet display any cankers) to the nearest foot and summing all shoot lengths. Both measures were converted to metric units (centimeters for TCL and meters for TSL), then underwent a square root transformation, as this was previously found to be best for equalizing the variance across the means (Coyne et al., 2000). Percent diseased wood (PDW) was used to represent host response and was calculated by dividing the transformed TCL by the transformed TSL. A histogram of PDW was generated for each population to help visualize disease response distributions and to allow for comparison among the three.

DNA preparation.

Leaf samples from the four parents were received from OSU in May 2018. Leaf samples from all 124 seedling trees per population were collected from the Rutgers Specialty Crop Research and Extension Center in June 2018. Leaf tissue was collected on dry ice and subsequently flash frozen in liquid nitrogen. Approximately 0.20 g of tissue per sample was ground with a bead mill (TissueLyser II; Qiagen, Hilden, Germany) while the tissue remained frozen. DNA extraction was performed using a kit (DNeasy Plant Mini Kit; Qiagen) following the manufacturer’s instructions. Samples were checked for DNA quantity and quality with a spectrophotometer (NanoDrop; Thermo Fisher Scientific, Waltham, MA), then diluted to 50 ng·μL−1 for double digest restriction-site associated DNA sequencing (ddRADseq) library preparation.

Library preparation and sequencing.

ddRADseq libraries of all 124 seedling trees and two parents per population were generated using a protocol modified from Poland et al. (2012). The first step of library preparation was a double restriction digest of 200 ng of DNA per sample with the methylation-sensitive rare-cutting enzyme PstI (NEB, Ipswich, MA) and methylation-sensitive common-cutting enzyme MspI at 37 °C for 2 h in a polymerase chain reaction (PCR) system (Applied Biosystems 9700 GeneAmp, Thermo Fisher Scientific). Both PstI adapters containing unique barcodes of 5 to 10 base pairs (bp) and common MspI Y-adapters were ligated to the digested DNA fragments in a mastermix containing 200 U of T4 DNA ligase, 2 μL of 10 × NEBuffer 4, and 4 μL of ATP (10 mm) (NEB) per sample by incubating at 22 °C for 2 h, followed by 20 min at 65 °C to inactivate the ligase. Ligated samples went through a size-selection cleanup by mixing 0.5 v/v solid phase reversible immobilization magnetic beads (Agencourt Ampure XP; Beckman Coulter, Brea, CA) with the samples. The 96-well plate was subsequently placed on a magnetic stand and the supernatant was removed. This was followed by a 70% ethanol wash to remove fragmented DNA <300 bp, which was repeated twice for a total of three washes. Samples then went through PCR amplification using primers with sequences that allow for binding to the flow cell during Illumina (San Diego, CA) sequencing. Each sample was amplified in a single PCR reaction with the following thermal cycling conditions: initial denaturation of 95 °C for 30 s, followed by 16 cycles of 95 °C for 30 s, 62 °C for 20 s, 68 °C for 15 s, with a final extension of 68 °C for 5 min. DNA library samples were quantified using a fluorometer (Qubit 3.0, Thermo Fisher Scientific), diluted to 5 ng·μL−1, and pooled in 48-plex. Another magnetic bead cleanup was performed on pooled libraries using the previously described procedure, except that the 70% ethanol wash was repeated only once. Final pooled libraries were quantified using the fluorometer and were checked for quality using high-resolution automated electrophoresis (2100 Bioanalyzer System; Agilent Technologies, Santa Clara, CA). Libraries were pooled so that all 124 progeny and two parent samples in each population were divided across three HiSEq. 2500 lanes per population (Illumina) (2 × 150 paired-end). NGS was conducted by Genewiz, Inc. (South Plainfield, NJ) with a 25% PhiX spike-in.

SNP calling.

The Stacks v1.47 pipeline was used to process the FASTQ files returned from sequencing into a set of SNP markers to be used for linkage map construction (Catchen et al., 2013). First, the process_radtags function was used to demultiplex reads by barcode sequence, remove reads with low-quality scores, rescue barcodes, and RAD-Tags using the –r option, and truncate reads to 100 bp in length. Quality filtering within process_radtags was done using default parameters (reads discarded with an average quality score below 90%, Stacks software manual). Outside of Stacks, the Burrows-Wheeler Aligner (BWA) software package was used to align filtered reads against the ‘Jefferson’ European hazelnut reference genome (Li and Durbin, 2009; Rowley et al., 2018). The Samtools program suite was then used to sort the sequence alignment/map (SAM) output files from BWA, select aligned reads, and convert them into binary alignment/map (BAM) files (Li et al., 2009). Returning to Stacks, the ref_map.pl function was then used to call SNP markers from the aligned BAM files through several programs. First, the pstacks program gathered loci based on their positions in the ‘Jefferson’ reference genome and called SNP markers for each accession. A minimum of three identical reads were required to form a stack and call a SNP marker. The cstacks program then generated a catalog of all loci from the parent accessions, compiling the loci based on alignment position. The sstacks program matched the reads of each sample against the generated catalog. Finally, the genotypes program within the Stacks software pipeline generated a set of markers and respective genotypes in a format that can be used in mapping programs, in this case JoinMap 4.1 (van Ooijen, 2006). Default parameters were used for all steps of ref_map.pl except for the final genotypes program where r was set to 0.90 so that loci missing data in more than 10% of the seedlings (fewer than 112 seedlings) were removed before further analysis.

SSR genotyping.

A total of 193 SSR markers developed across several studies and placed on previous European and American hazelnut genetic maps (Akin et al., 2016; Bassil et al., 2005; Bhattarai and Mehlenbacher, 2017, 2018; Boccacci et al., 2005; Colburn et al., 2015, 2017; Gürcan and Mehlenbacher, 2010; Gürcan et al., 2010a, 2010b; Ives et al., 2014; Mehlenbacher et al., 2006; Sathuvalli and Mehlenbacher, 2013; Sathuvalli et al., 2012) were screened as possible anchor markers for comparing the current study’s genetic linkage maps to previously reported maps (Beltramo et al., 2016; Bhattarai and Mehlenbacher, 2017; Colburn et al., 2015, 2017; Gürcan et al., 2010a; Honig et al., 2019; Ives et al., 2014; Mehlenbacher et al., 2006; Sathuvalli et al., 2011a, 2011b, 2012; Torello Marinoni et al., 2018). SSR genotyping PCR reactions included a total volume of 12.5 μL, with concentrations of 5 ng·μL−1 of genomic DNA, 1 × Immolase-Taq PCR buffer (Bioline; Meridian Life Science, Memphis, TN), 2.0 mm MgCl2, 0.25 mm dNTPs each, 0.5 pmol·μL−1 forward primer with 5'-M13(-21) addition (Schuelke, 2000), 1 pmol·μL−1 reverse primer with 5'-“PIG-tailing” addition (Brownstein et al., 1996), 1 pmol·μL−1 forward M13(-21) primer with FAM, NED, PET, or VIC fluorescent labels (Schuelke, 2000), and 0.5 U Immolase-Taq DNA polymerase (Bioline). Primers for SSR markers were synthesized by Integrated DNA Technologies (Coralville, IA). Thermalcycling conditions were as follows: initial denaturation at 94 °C for 5 min; 30 cycles of 94 °C for 30 s, 55 °C for 45 s, 72 °C for 45 s; 20 cycles of 94 °C for 30 s, 53 °C for 45 s, 72 °C for 45 s; with a final extension of 72 °C for 10 min. PCR products were then sized using capillary electrophoresis (Applied Biosystems 3500xl Genetic Analyzer; Thermo Fisher Scientific), Applied Biosystems LIZ 600 size standard v2.0 (Thermo Fisher Scientific), and Applied Biosystems Genemapper 5.0 software (Thermo Fisher Scientific). All SSR markers were scored codominantly.

Linkage map construction.

The software JoinMap 4.1 was used to build genetic linkage maps through two different approaches. The first was the multipoint maximum likelihood (ML) algorithm for cross-pollinated (CP) populations described by van Ooijen (2011). In this approach, markers segregating in either parent (lmxll or nnxnp format) or both parents (abxcd or efxeg format) were used to first generate two parental maps that were combined into a single integrated map. SNP markers and anchoring SSR markers were combined into one dataset. Accessions missing >10% of marker data were removed from the analysis. Chi-square analysis was performed to test markers against their expected segregation ratios, and only those showing the most severe segregation distortion were removed from the analysis (P 0.0001), as moderate segregation distortion is normal in wide (interspecific) crosses and also among C. avellana cultivars in general (van Ooijen, 2006). Marker groups were established over a set of logarithm of odds (LOD) scores ranging from 2 to 35 in increments of one. A LOD score of ≥26 was selected to group loci into LGs. The multipoint ML algorithm was then used to determine the order of loci in each LG. Settings for ML mapping were as follows: five spatial sampling thresholds (0.1, 0.05, 0.03, 0.02, and 0.01) with three optimization runs for each, chain length of 1000, cooling control parameter of 0.001, and chain termination after 10,000 chains without improvement. Kosambi’s mapping function was used and distances are presented in centimorgans (cM).

The second approach was the two-way pseudo-testcross approach for CP species described by Grattapaglia and Sederoff (1994). Additional procedures for this approach were developed by Mehlenbacher et al. (2006) and used by Honig et al. (2019). Only the markers that fell into established LGs in the first approach were used in this approach. Once again, SNP markers and anchoring SSR markers were combined into one dataset. The markers were then formatted so that segregation of different alleles only occurred in one parent (lmxll or nnxnp), resulting in two subsets of markers segregating in a 1:1 ratio. The markers were then recoded as BC1 markers and used to construct linkage maps. Procedures and settings for constructing linkage maps were the same as those described in the first mapping approach. Markers linked in repulsion grouped far from those linked in coupling for each LG in each parent map. To combine them, the markers in repulsion were recoded as “dummy variables,” which allowed them to be placed on the same map as those in coupling and form a single group for each LG in each parent.

QTL mapping.

QTL mapping was performed using the final year of EFB response data (PDW following a square root transformation) using MapQTL 6.0 software (van Ooijen, 2009). Due to the perennial, internally spreading nature of the fungus, final canker and shoot lengths represent a cumulative measure of canker development from multiple exposures and spread within the canopy since the trees were planted in 2012. Although TCL was only measured once in 2019, the final measurement of EFB response captured multiple years of infection and disease expression. All markers from the two-way pseudo-testcross approach described previously were recoded in DH format to specifically address memory constraints that arise when using CP mapping populations (Honig et al., 2019). This method generated a separate map for each parent that was used for QTL mapping. A permutation test was used to establish the LOD threshold of significance with 1000 permutations and a significance level of 0.05. The mapping process started with interval mapping, in which the most significant putative QTL above the established LOD threshold was identified for each LG. These putative QTLs were then used as cofactors for subsequent rounds of multiple QTL mapping (MQM). MQM was conducted until QTL positions were fixed, with cofactor selection being modified between rounds based on LOD score changes.

Results

Disease response.

At the time of evaluation, EFB was widely present within the three progenies and adjacent European and American hazelnut fields (data not shown) providing confidence few trees would have escaped exposure to A. anomala. The EFB response in each population, as measured by PDW (following a square root transformation), followed a relatively normal distribution (Fig. 1A–C). Canker measurements for all three populations are summarized in Table 1. Because all three populations shared a paternal parent, differences among them can largely be attributed to the maternal parents and their interaction with paternal alleles. The CRA population had a higher mean PDW (34.7%) compared with the other two populations and was the only population that held no seedlings free of EFB. The CRB and CRC populations had similar PDW distributions and means (21.3% and 23.4%, respectively). The lower mean TSL in the CRA population (49.9 m) relative to the CRB and CRC populations (55.2 m and 55.2 m, respectively) may have contributed to the higher mean PDW seen in CRA. The CRA and CRB populations had similar mean canker lengths (32.8 cm and 33.0 cm, respectively) and mean canker numbers (8.0 and 8.1, respectively), and the CRC had a lower mean canker number (6.9) but cankers that were longer on average (47.8 cm).

Fig. 1.
Fig. 1.

Histograms of eastern filbert blight (EFB) response for three Corylus americana × Corylus avellana populations (A) CRA, (B) CRB, and (C) CRC as measured by percent diseased wood. Percent diseased wood was calculated by dividing the square root of the total canker length by the square root of the total shoot length.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Table 1.

Eastern filbert blight (EFB) response measurements of three Corylus americana × Corylus avellana progeny populations (CRA, CRB, and CRC).

Table 1.

Illumina sequencing.

Illumina sequencing reads from the current study are curated in the National Center for Biotechnology Information (Bethesda, MD) Sequence Read Archive (SRA) database [PRJNA755895 (Leinonen et al., 2011)]. The total number of raw reads and average reads per sample per population from the Illumina sequencing runs are shown in Table 2. Phred quality (Q) score values and percent of reads with Q score above 30 were similar across all three populations. For total sequencing data, CRA had the least amount of data, with ≈2.39 Gb per sample and 15,963,018 reads per sample, whereas CRC had the most data with ≈2.72 Gb per sample and 18,120,200 reads per sample. Parent accessions were sequenced 10 times each and therefore had ≈10 times the raw sequencing data relative to seedlings. Abundant parental read data were necessary to ensure accurate SNP calling in the Stacks pipeline.

Table 2.

Raw and filtered Illumina sequencing data for three Corylus americana × Corylus avellana progeny populations (CRA, CRB, and CRC).

Table 2.

Marker screening.

The process_radtags function in the Stacks pipeline was used to remove PhiX spike-in reads, and filter based on quality using default parameters (Table 2). The CRA population retained 1,269,525,152 reads, the CRB population retained 1,115,447,958 reads, and the CRC population retained 1,344,792,998 reads. One progeny individual in the CRB population had less than 1 million reads and was removed from further analysis. For the CRA population, 22,857 loci/SNP markers were found across all seedlings, of which 5604 SNP markers were scored in at least 90% of the seedlings and used for linkage map construction. For the CRB population, 23,741 loci/SNP markers were found, of which 5523 SNP markers were scored in at least 90% of seedlings. For the CRC population, 23,792 loci/SNP markers were found, of which 5746 SNP markers were scored in at least 90% of seedlings. Of the 193 SSR markers screened across all three populations, 124 were polymorphic in CRA, 121 were polymorphic in CRB, and 117 were polymorphic in CRC. Combining the SNP and SSR markers, a total of 5728, 5644, and 5863 for the CRA, CRB, and CRC populations, respectively, were used as input for linkage map construction in JoinMap, where markers were further filtered based on segregation distortion and identification of identical genotypes (Supplemental Tables 13). In the CRA, CRB, and CRC populations, 2576 markers, 2560 markers, and 2651 markers were removed, respectively, due to extreme segregation distortion (P 0.0001). Seventy-six, 63, and 79 duplicate markers (those having identical genotypes across all seedlings) were also removed, leaving 3076 markers, 3021 markers, and 3133 markers remaining, respectively. SNP and SSR marker allele segregation information is presented in Supplemental Tables 1 to 3.

Linkage map construction.

Integrated maps from the multipoint ML approach for CP species in JoinMap 4.1 are presented in Supplemental Figs. 1 to 33. For the CRA population, 11 LGs formed, corresponding to the haploid chromosome number for European hazelnut. Results showed that 297 markers were not placed on the CRA LGs, leaving a total of 2779 markers across all LGs. The LGs in CRA ranged in size from 132 to 392 markers and 54 to 144 cM. The CRA map spanned a total distance of 1062 cM, with an average marker spacing of 0.38 cM. For the CRB population, 12 LGs formed, with LG2 being divided into two groups. Six seedlings were removed due to missing scores at >10% of markers. A total of 217 markers were not placed on the CRB LGs, leaving a total of 2804 markers across all LGs. LGs ranged in size from 61 to 377 markers and from 33 to 152 cM (with the two LG2 groups being the smallest). The CRB map spanned a total distance of 1123 cM, with an average marker spacing of 0.40 cM. For the CRC population, 11 LGs formed. One seedling was removed because of missing scores at >10% of markers. A total of 110 markers were not placed on the CRC LGs, leaving a total of 3023 markers across all groups. LGs ranged in size from 158 to 393 markers and from 72 to 156 cM. The CRC map spanned a total distance of 1252 cM, with an average marker spacing of 0.41 cM.

Assignment of LGs was made using the previously described SSR markers and their locations on the reference European hazelnut genetic map (Mehlenbacher et al., 2006). All the screened SSR markers showed successful amplification in these populations, and most of the markers were polymorphic in all three populations. There were an average of 9.7, 9.0, and 10.3 SSR markers per LG for CRA, CRB, and CRC, respectively. Only three SSR markers were assigned to LGs different from those of linkage maps of previous studies. GB372, previously assigned to LG2, mapped to LG7 in all three populations. B773, previously assigned to LG7, mapped to LG8 in all three populations. GB627, previously assigned to LG11, mapped to LG1 in the CRC population (the only population in which it was polymorphic). Previous studies have found reciprocal translocations occurring in TdG, as seen through the formation of tetravalents during meiosis (Salesses, 1973; Salesses and Bonnet, 1988), and a procedure has been established to disentangle the “pseudo-linkage” of markers that results from reciprocal translocations within European hazelnut (Torello Marinoni et al., 2018). In the present study, no evidence of reciprocal translocations was detected and LGs separated as expected during construction of linkage maps.

QTL mapping.

QTL mapping was conducted with separate parental maps and DH marker codes from the two-way pseudo-testcross approach. QTL results are displayed in Table 3 and Fig. 2A–E. The only QTL associated with EFB resistance/tolerance in the CRA population was on LG10 of the TdG parent map. This was most closely associated with SNP 4112, which had an LOD score of 8.00 and accounted for 25.7% of phenotypic variation. Multiple QTLs associated with EFB resistance/tolerance were identified in the CRB population. One QTL was found on LG11 of the OSU 403.040 map. This QTL was most closely associated with SNP 42098, which had an LOD score of 3.01 and controlled 9.5% of phenotypic variation. Two QTLs were found on the TdG parent map in the CRB population, one on LG6 and another on LG10. The first was most closely associated with SNP 93212, with an LOD score of 6.11 and controlling 17.1% of phenotypic variation, whereas the second was most closely associated with SNP 29308, with an LOD score of 6.70 and controlling 18.9% of phenotypic variation. The only QTL identified in the CRC population was also on LG10 of the TdG map. This was most closely associated with SNP 4778, with an LOD score of 4.77 and controlling 16.2% of phenotypic variation.

Fig. 2.
Fig. 2.

Graphs depicting logarithm of odds (LOD) scores for quantitative trait loci (QTL) detection along maps of linkage groups (LG) for three Corylus americana × Corylus avellana populations (CRA, CRB, and CRC). (A) QTL associated with single nucleotide polymorphism (SNP) 4112 on LG10 of ‘Tonda di Giffoni’ (TdG) in CRA population. (B) QTL associated with SNP 42098 on LG11 of OSU 403.040 in CRB population. (C) QTL associated with SNP 93212 on LG6 of TdG in CRB population. (D) QTL associated with SNP 29308 on LG10 of TdG in CRB population. (E) QTL associated with SNP 4778 on LG10 of TdG in CRC population. Map distances reported in centimorgans.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Table 3.

Single nucleotide polymorphism (SNP) marker quantitative trait loci (QTL) for eastern filbert blight resistance/tolerance detected in the parent maps of three Corylus americana × Corylus avellana populations (CRA, CRB, and CRC) based on percent diseased wood.

Table 3.

Discussion

In this study, dense genetic linkage maps were created of three interspecific hybrid C. americana × C. avellana populations using SNP markers from NGS technology anchored to known LGs using polymorphic SSR markers previously mapped in European hazelnut. The parents were three unrelated EFB-resistant C. americana selections that remained free of EFB in New Jersey under high disease pressure crossed with TdG, an EFB-tolerant cultivar of C. avellana, with an expectation that the progenies would segregate for disease response. After 7 years in the field, EFB was widely present in the plots and all three progenies expressed normally distributed disease responses typical of quantitative traits under the control of multiple genes (Fig. 1A–C). Subsequent analysis identified five QTLs across three genetic regions associated with EFB resistance/tolerance (Supplemental Figs. 10, 17, 21, 22, 32).

In past studies, EFB resistance has only been mapped to regions on LG2, LG6, and LG7. The QTL discovered in the OSU 403.040 map (CRB) is the first identified on LG11, supporting that it is distinct from other sources. The only other mapped R-gene originating in C. americana is that of the cultivar Rush, which mapped to a region on LG7 (Bhattarai et al., 2017). In addition, the QTLs identified on LG10 of the three TdG maps also represent a new genetic region associated with EFB resistance/tolerance. The closest anchoring marker in each population was the SSR BR352, which was 2.44, 2.68, and 7.38 cM away from the QTL in CRA, CRB, and CRC, respectively. This indicates that they are likely the same R-gene or part of the same gene cluster in TdG.

This study also identified one QTL that mapped close to the ‘Gasaway’ resistance locus. This QTL was found on the TdG map of the CRB population and was ≈16 cM from SSR marker A614, which cosegregates with the ‘Gasaway’ resistance locus (Sathuvalli et al., 2012, 2017). ‘Gasaway’ EFB resistance is the most widely studied and has been mapped to LG6, as has resistance for many other C. avellana accessions, including OSU 408.040, ‘Culpla’, ‘Crvenje’, and OSU 495.072 (Colburn et al., 2015; Komaei Koma et al., 2021; Mehlenbacher et al., 2006; Sathuvalli et al., 2012). Because these sources of resistance map to the same or nearby loci, it is believed that the ‘Gasaway’ R-gene is part of a cluster for EFB resistance (Capik et al., 2013; Colburn et al., 2015).

Interestingly, the QTLs identified in this study originated largely in the European parent, TdG, with only one of the three genomic regions associated with EFB resistance originating in C. americana. For the case of TdG, previous studies in Oregon have found this cultivar to have one of the lowest disease severities among all European cultivars, with trees able to maintain vigor and produce nuts after infection (Coyne et al., 2000; Pinkerton et al., 1993). As such, TdG has been classified as a cultivar expressing QR. Further, Capik and Molnar (2012) found that TdG had a significantly lower proportion of diseased wood as well as smaller canker lengths than the susceptible cultivar Barcelona in New Jersey. Studies examining inheritance of resistance from TdG concluded that TdG can transmit QR effectively (Osterbauer et al., 1997; Revord et al., 2020). More specifically, when Revord et al. (2020) compared interspecific progenies that shared TdG as a parent with all interspecific progenies studied, they found the TdG progenies to have a lower average disease rating when comparing progenies with both continuous and bimodal distributions. Therefore, two QTL regions found in TdG in the current study are not unexpected based on the results of these previous studies.

The three QTLs identified on LG10 are in the same relative region of the TdG parent map and are classified as major QTLs accounting for 16.2% to 25.7% of phenotypic variation. As such, these three QTLs are likely associated with the same locus segregating in each of the three populations, which may be responsible for some or a large component of the tolerance observed when TdG is grown in the presence of A. anomala. In the future, additional crosses could be made between TdG and an EFB-susceptible accession to better clarify segregation of disease response of the progeny and help identify other loci that may be involved with disease expression.

The low number of QTLs detected from the C. americana parents is unexpected, as these trees were free of EFB after many years of exposure under high disease pressure (Capik and Molnar, 2012). There are a number of possible explanations as to why more QTLs were not detected from the tolerant C. americana parents. First, interspecific crosses have been reported to reduce recombination and thus shorten genetic distances in genetic linkage maps (Brennan et al., 2014; Chetelat et al., 2000; Manrique-Carpintero et al., 2016; Quillet et al., 1995; Rieseberg and Buerkle, 2002; Torello Marinoni et al., 2020). This is also evident in the current study when comparing CRA (1062 cM), CRB (1123 cM), and CRC (1252 cM) interspecific population map distances with the C. avellana intraspecific map (1383 cM) distance reported in Honig et al. (2019). Reduced recombination in the interspecific progeny populations may have masked minor effect QTL from the C. americana parents.

In addition, previous studies have shown that C. americana parents transmit resistance to offspring in an unpredictable manner when crossed with susceptible C. avellana. Further, the C. avellana parent can also contribute to the disease response of the interspecific progeny (Molnar and Capik, 2012; Muehlbauer et al., 2018; Revord et al., 2020; and the current study). It is possible that some C. americana sources of resistance are highly quantitative and a high proportion of alleles must be recovered to confer sufficient resistance in the offspring. Thus, when crossing to a C. avellana parent, not enough C. americana resistance alleles are present in the offspring to confer appreciable tolerance in the F1. Recent work by Molnar et al. (2021) and T.J. Molnar (unpublished) supports this latter hypothesis by demonstrating recovery of a high level of tolerance and resistance in many F2 progeny derived from crosses of resistant C. americana × susceptible C. avellana F1 hybrids. These recent results suggest additive gene action may be responsible for the observed responses and that resistance in C. americana is highly quantitative. Therefore, in our current study, resistance from C. americana may be from many loci, each with minor effects, but once crossed with C. avellana, their contributions may have been too small to detect under our experimental design and LOD threshold. Furthermore, resistance alleles from C. americana may be recessive, and would not be recovered until the F2 or later generations. Evaluations of the F2 and backcross progeny of the current CRA, CRB, and CRC populations will be needed to prove this hypothesis (currently being studied), but were beyond the scope of the current study.

A final possibility as to why QTLs were not detected from the C. americana parents could be due to inherent challenges and expenses of working with perennial tree species, especially those difficult to propagate by stem cuttings, which resulted in the current work being an unreplicated study (each seedling tree was a unique genotype). As such, field-level environmental variation may have presented a confounding variable in resolving minor loci associated with EFB tolerance. Although all trees were planted in the same field, differences in soil characteristics and/or exposure to A. anomala over time may have contributed variation to EFB response among progeny and introduced confounding effects related to minor QTL estimates.

Nevertheless, the QTLs identified here represent valuable additions to the overall effort to better understand EFB responses in C. avellana and C. americana, and hybrid germplasm that will improve efforts to breed new cultivars expressing durable resistance. This study identified several QTLs associated with resistance/tolerance to EFB from both C. americana and C. avellana. Commercial European hazelnut orchards typically consist of a relatively small number of clonally propagated cultivars, which are expected to be in production for more than 35 years. Anisogramma anomala has been shown to be genetically diverse in the eastern United States (Dunlevy et al., 2019; Muehlbauer et al., 2019) and relatively uniform in the Pacific Northwest where it was introduced (Tobia et al., 2017). Consequently, a diverse range of R-genes should be used in breeding efforts to reduce selection pressure on the pathogen and help manage EFB in the long term. Because of the high degree of resistance found in the American hazelnut (Revord et al., 2020) and augmented tolerance and resistance observed in new hybrid F2 populations (Molnar et al., 2021), it is suggested that breeders continue to investigate the wild American hazelnut species as a parent for development of accessions with durable EFB resistance.

Further, additional work is needed to study the molecular basis of resistance among different sources, whether these mechanisms are involved in pathogen recognition, signal transduction, or the defense response. This would help make R-gene pyramiding from multiple previously identified sources (see Mehlenbacher and Molnar, 2021) more effective by strengthening a single resistance mechanism or combining different resistance mechanisms into a single cultivar. Gene pyramiding for resistance to EFB will support the emerging European and American hazelnut industry in the eastern United States and help in the long-term management of EFB in the Pacific Northwest.

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Supplemental Fig. 1.
Supplemental Fig. 1.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 1. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 2.
Supplemental Fig. 2.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 2. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 3.
Supplemental Fig. 3.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 3. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 4.
Supplemental Fig. 4.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 4. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 5.
Supplemental Fig. 5.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 5. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 6.
Supplemental Fig. 6.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 6. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 7.
Supplemental Fig. 7.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 7. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 8.
Supplemental Fig. 8.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 8. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 9.
Supplemental Fig. 9.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 9. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 10.
Supplemental Fig. 10.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 10. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 11.
Supplemental Fig. 11.

Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 11. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 12.
Supplemental Fig. 12.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 1. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 13.
Supplemental Fig. 13.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 2. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 14.
Supplemental Fig. 14.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 3. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 15.
Supplemental Fig. 15.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 4. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 16.
Supplemental Fig. 16.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 5. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 17.
Supplemental Fig. 17.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 6. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 18.
Supplemental Fig. 18.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 7. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 19.
Supplemental Fig. 19.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 8. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 20.
Supplemental Fig. 20.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 9. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 21.
Supplemental Fig. 21.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 10. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 22.
Supplemental Fig. 22.

Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 11. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 23.
Supplemental Fig. 23.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 1. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 24.
Supplemental Fig. 24.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 2. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 25.
Supplemental Fig. 25.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 3. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 26.
Supplemental Fig. 26.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 4. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 27.
Supplemental Fig. 27.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 5. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 28.
Supplemental Fig. 28.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 6. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 29.
Supplemental Fig. 29.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 7. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 30.
Supplemental Fig. 30.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 8. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 31.
Supplemental Fig. 31.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 9. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 32.
Supplemental Fig. 32.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 10. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Supplemental Fig. 33.
Supplemental Fig. 33.

Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 11. Simple sequence repeat markers are in bolded italics.

Citation: Journal of the American Society for Horticultural Science 147, 4; 10.21273/JASHS05112-22

Contributor Notes

This work is supported by the New Jersey Agricultural Experiment Station, Hatch Act Funds, the U.S. Department of Agriculture (USDA) National Institute of Food and Agriculture Specialty Crops Research Initiative, Grant Number 2016-51181-25412, as well as the University of Missouri Center for Agroforestry and the USDA, Agricultural Research Service (ARS), Dale Bumpers Small Farm Research Center, Agreement numbers 58-6020-6-001 and 58-6020-0-007 from USDA, ARS.

We thank David Hlubik and Emil Milan for assistance in the disease phenotyping conducted in this study. We also thank Shawn Mehlenbacher of Oregon State University for access to the hazelnut reference genome, simple sequence repeat markers, and pollen.

T.J.M. is the corresponding author. E-mail: thomas.molnar@rutgers.edu.

  • View in gallery

    Histograms of eastern filbert blight (EFB) response for three Corylus americana × Corylus avellana populations (A) CRA, (B) CRB, and (C) CRC as measured by percent diseased wood. Percent diseased wood was calculated by dividing the square root of the total canker length by the square root of the total shoot length.

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    Graphs depicting logarithm of odds (LOD) scores for quantitative trait loci (QTL) detection along maps of linkage groups (LG) for three Corylus americana × Corylus avellana populations (CRA, CRB, and CRC). (A) QTL associated with single nucleotide polymorphism (SNP) 4112 on LG10 of ‘Tonda di Giffoni’ (TdG) in CRA population. (B) QTL associated with SNP 42098 on LG11 of OSU 403.040 in CRB population. (C) QTL associated with SNP 93212 on LG6 of TdG in CRB population. (D) QTL associated with SNP 29308 on LG10 of TdG in CRB population. (E) QTL associated with SNP 4778 on LG10 of TdG in CRC population. Map distances reported in centimorgans.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 1. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 2. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 3. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 4. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 5. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 6. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 7. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 8. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 9. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 10. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

  • View in gallery

    Corylus americana OSU 533.069 × Corylus avellana ‘Tonda di Giffoni’ (CRA) linkage group 11. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 1. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 2. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 3. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 4. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 5. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 6. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 7. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 8. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 9. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 10. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

  • View in gallery

    Corylus americana OSU 403.040 × Corylus avellana ‘Tonda di Giffoni’ (CRB) linkage group 11. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

  • View in gallery

    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 1. Simple sequence repeat markers are in bolded italics.

  • View in gallery

    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 2. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 3. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 4. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 5. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 6. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 7. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 8. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 9. Simple sequence repeat markers are in bolded italics.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 10. Simple sequence repeat markers are in bolded italics. Quantitative trait loci (QTL) regions are highlighted black.

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    Corylus americana OSU 557.122 × Corylus avellana ‘Tonda di Giffoni’ (CRC) linkage group 11. Simple sequence repeat markers are in bolded italics.

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