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ASHS 2024 Annual Conference

 

USVL531-MDR: Watermelon Germplasm Line with Broad Resistance to Powdery Mildew and Phytophthora Fruit Rot

Authors:
Chandrasekar S. Kousik US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414, USA

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Jennifer Ikerd US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414, USA

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Mihir Mandal Oak Ridge Institute for Science and Education participant sponsored by US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414, USA

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Scott Adkins US Department of Agriculture-Agricultural Research Service, US Horticultural Research Laboratory, Fort Pierce, FL 34945, USA

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William W. Turechek US Department of Agriculture-Agricultural Research Service, US Horticultural Research Laboratory, Fort Pierce, FL 34945, USA

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USVL531-MDR is a multiple disease-resistant (MDR) watermelon (Citrullus mucosospermus; Syn: Citrullus lanatus var. lanatus) germplasm line that exhibits high levels of resistance to a broad range of isolates of cucurbit powdery mildew (Podosphaera xanthii) and Phytophthora capsica that cause Phytophthora fruit rot. In comparison, the watermelon cultivar Mickey Lee and watermelon germplasm line USVL677-PMS are highly susceptible to P. xanthii and P. capsici. The hypocotyls, cotyledons, and true leaves of USVL531-MDR are highly resistant to powdery mildew compared with those of USVL677-PMS and Mickey Lee, on which severe powdery mildew and abundant development of conidia can be observed. Resistance to Phytophthora fruit rot is expressed as significantly reduced or very small (≤0.7 mm) to no lesion development, rot, or pathogen sporulation on the fruit compared with large lesions, severe rot, and heavy sporulation on fruit of susceptible watermelon cultivars such as Mickey Lee and Sugar Baby. USVL531-MDR has uniform growth characteristics, fruit size, shape, and color. Commercial watermelon cultivar with resistance to both powdery mildew and Phytophthora fruit rot are not currently available; therefore, USVL531-MDR can be a useful source for incorporating resistance in commercially acceptable cultivars. USVL531-MDR can be easily crossed with commercial watermelon cultivars to develop breeding populations.

Origin

USVL531-MDR was derived from a US Plant Introduction (PI) of the watermelon collection maintained at the US Department of Agriculture-Agricultural Research Service (USDA-ARS), Plant Genetic Resources and Conservation unit, Griffin, GA. Specifically, PI 494531 was originally collected from Oyo, Nigeria, in 1984, and the PI number was assigned in 1985. It was initially classified as Citrullus lanatus var. lanatus; however, it was later reclassified as Citrullus mucosospermus (Fursa) Fursa (Chomicki and Renner 2015; Fursa 1981; Paris 2015; Renner et al. 2017). Additional details of the PI 494531 used to develop the germplasm line USVL531-MDR can be obtained from the US National Germplasm System website (https://npgsweb.ars-grin.gov/gringlobal/accessiondetail?id=1389467).

Powdery mildew of watermelon.

Powdery mildew of watermelon, which is caused by Podosphaera xanthii, is a common disease that occurs in most watermelon-growing regions and can lead to significant yield reduction (Keinath 2015; Keinath and DuBose 2004; McGrath 2017a; Zhang et al. 2011). The pathogen P. xanthii can infect the hypocotyl, cotyledons, true leaves, and fruit of watermelon (Ben-Naim and Cohen 2015; Davis et al. 2007; Jahn et al. 2002; Keinath and DuBose 2004; Kousik et al. 2011, 2018a; Mandal et al. 2020; McGrath 2017a). Powdery mildew on watermelon has been observed with increasing frequency (Keinath 2015; Keinath and Rennberger 2017; Kousik et al. 2011, 2016, 2018a, 2018b, 2019; Mercier et al. 2014; Rennberger et al. 2018) during the past 10 to 15 years. Additionally, powdery mildew on watermelon has been listed as an important research priority by the Watermelon Research and Development Group (Kousik et al. 2016). Fungicides are routinely applied to manage powdery mildew, and several effective ones are available (Keinath and DuBose 2004; Keinath 2015; Keinath and Rennberger 2017; McGrath 2017a). However, excessive reliance on fungicides is not economical or environmentally favorable, and the cucurbit powdery mildew pathogen has been shown to develop resistance to fungicides rapidly (Keinath et al. 2018; McGrath 2010). Currently, few commercial watermelon varieties and pollenizers with resistance to powdery mildew are available (Kousik et al. 2019). Several sources of resistance to powdery mildew identified in watermelon PIs (Davis et al. 2007; Kousik et al. 2018a, 2018b; Tetteh et al. 2010; Thomas et al. 2005) and germplasm and breeding lines have been developed (Ben-Naim and Cohen 2015; Kousik et al. 2018a). Regardless, the occurrence of multiple races of P. xanthii and appearance of new ones across the world complicate breeding efforts, creating a constant need for new germplasm resources (Cohen et al. 2004; Jahn et al. 2002; Kousik and Ikerd 2014; Lebeda et al. 2011, 2016; McCreight 2006; McGrath 2017a; Mercier et al. 2014; Pitrat et al. 1998; Tores et al. 2021). Most of the P. xanthii races have been classified based on melon (Cucumis melo) differentials and, thus far, seven races have been described using this system (Cohen et al. 2004; Jahn et al. 2002; Lebeda et al. 2011, 2016; McGrath 2017a; Pitrat et al. 1998). The characterization of races based on bitter gourd (Momordica charantia) differentials (Dhillon et al. 2018) and watermelon (Kousik and Ikerd 2014; Tores et al. 2021) have also been proposed. However, cucurbit powdery mildew race classification for watermelon is not yet as advanced as it is for melon. Currently, the two proposed races in the United States are based on the ability of isolates to infect two differential lines (USVL677-PMS and Mickey Lee) (Kousik and Ikerd 2014). Some researchers have also used the designation 1W or 2W based on the ability of the P. xanthii isolate to infect melon (Cucumis melo) differential PMR-45 and some watermelon genotypes (Davis et al. 2007; Mercier et al. 2014; Tetteh et al. 2010). Powdery mildew race 1 cannot infect PMR-45, whereas race 2 can. The race classification is based on melon differentials as race 1 or race 2, and the “W” indicates the ability of the race to infect watermelon. However, this classification is not based on watermelon differentials. Another plant pathogen, Golovinomyces cichoracearum, has also been reported to cause powdery mildew of cucurbits (McGrath 2017a). However, we have not detected this pathogen on watermelon in South Carolina for at least 10 years. Quick differentiation between the two powdery mildew pathogens can be accomplished by microscopically observing the conidia for fibrosin bodies (McGrath 2017a).

Phytophthora fruit rot of watermelon.

Phytophthora fruit rot caused by Phytophthora capsici is a major factor limiting watermelon production for the past 15 years in the southeastern United States, where more than 50% of the crop is grown (Kousik et al. 2014a, 2014b, 2016, 2017). Phytophthora fruit rot of watermelon was first reported from Colorado in 1940 (Wiant and Tucker 1940), but it is now prevalent in most watermelon-producing regions in the United States (Granke et al. 2012; Kousik et al. 2014a, 2016; McGrath 2017b). Phytophthora fruit rot of watermelon is considered a top research priority by the US National Watermelon Association, and this was noted in their latest call for proposals in 2022 (Kousik et al. 2016, 2022). Phytophthora fruit rot on watermelon can be a preharvest or postharvest problem (Kousik et al. 2016, 2017). Additionally, the watermelon fruit are susceptible at all stages of fruit development (Kousik et al. 2018c), thus making it necessary to protect the crop in the field and after harvest as well. Fungicides are routinely used to manage Phytophthora fruit rot of watermelon, and many effective ones are available to growers (Kousik et al. 2014b, 2017). However, resistance to fungicides in P. capsici populations have also been documented (Granke et al. 2012; Keinath 2007). Furthermore, under favorable conditions, P. capsici has been known to overwhelm some of the effective fungicides (Kousik et al. 2014b, 2017). The use of resistance to manage Phytophthora fruit rot would be optimal; however, although commercial resistant varieties are not yet available, several sources of resistance have been described (Kousik et al. 2012, 2014a). Extensive details of Phytophthora fruit rot of watermelon have been previously described (Kousik et al. 2012, 2014a, 2014b, 2017, 2018c, 2022).

The watermelon germplasm line USVL531-MDR with resistance to powdery mildew and Phytophthora fruit rot is being released because of great interest in its use in breeding and other programs. Several seed companies and university researchers are now working with USVL531-MDR after obtaining it through material transfer agreements; therefore, we decided to openly release it for use by the larger research community.

Development of USVL531-MDR.

Variability in the disease expression of plants within a PI to powdery mildew (Davis et al. 2007; Tetteh et al. 2010; Thomas et al. 2005), Phytophthora fruit rot (Kousik et al. 2012, 2014a), and several other viral diseases (Guner et al. 2002; Kousik et al. 2009; Strange et al. 2002) has been previously described. When using potential sources of resistance within a PI, it is necessary to develop pure lines for use in breeding programs and other downstream uses such as RNAseq (Mandal et al. 2018, 2020). During the original PI germplasm screen of the potential powdery mildew resistant lines conducted in 2011, PI 494531 exhibited varying levels of resistance; therefore, a pure line selection procedure was adopted to develop highly resistant homozygous individuals for use in breeding programs. When developing USVL531-MDR, 16 seedlings of PI 494531 were grown in a greenhouse in 6.4-cm square pots, inoculated, and evaluated for resistance to powdery mildew as previously described (Kousik et al. 2018a, 2018b). Resistance to powdery mildew in hypocotyls is not adequately documented; therefore, we evaluated hypocotyls in addition to cotyledons and true leaves of all plants for resistance. Commercial cultivars Dixie Lee, Sugar Baby, and Mickey Lee and the highly susceptible line USVL677-PMS (derived from PI 269677) were routinely included as susceptible controls for powdery mildew and Phytophthora fruit rot resistance screening. Powdery mildew-resistant seedlings that were given a rating of ≤2 using a scale of 0 to 10 for hypocotyl, cotyledons, and true leaves were transplanted into 11.4-L pots after screening for disease resistance (Kousik et al. 2014a, 2018a). Plants were allowed to grow in a greenhouse and self-pollinated by hand to obtain fruit. Fruit from individual plants were screened with the highly virulent isolate of Phytophthora capsici, RCZ-11, collected in South Carolina from zucchini squash that has been used extensively in various studies (Kousik et al. 2014a, 2014b, 2018c, 2022). The details of the isolate RCZ-11 used for screening for resistance to Phytophthora fruit rot have been described elsewhere (Kousik et al. 2018c, 2022). Each fruit was inoculated with a 7-mm agar plug from an actively growing colony of P. capsici and placed in a walk-in humid chamber (relative humidity >95%; temperature = 26 ± 2 °C) under continuous fluorescent lights (Kousik et al. 2014a, 2014b, 2022). Data of the lesion development and sporulation were recorded 5 d after fruit inoculations when large lesions and heavy sporulation were observed on fruit of susceptible cultivars (Mickey Lee, USVL677-PMS, or Sugar Baby). Seeds from highly resistant individual fruit were collected, and plants were grown and screened in the next generation for resistance to powdery mildew and after fruit formation for Phytophthora fruit rot. Therefore, we screened and selected individual plants for five successive generations for the two diseases to develop S5 lines; one of which was designated as ‘USVL531-MDR’.

Broad resistance to powdery mildew isolates in ‘USVL531-MDR’.

Two field trials were conducted at the US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory research farm in Charleston, SC, during Summer and Fall 2017 to confirm field resistance to powdery mildew in ‘USVL531-MDR’ as previously described (Kousik et al. 2018a). Each of the trials had five plants per genotype per replication with four replications. The experiments were arranged as a randomized complete block (replication) design with genotypes randomized within the blocks. Because powdery mildew occurs naturally in the Charleston area, the plots were not inoculated. Lower leaves of ‘USVL531-MDR’ and the susceptible checks (‘USVL677-PMS’ and ‘Mickey Lee’) were rated using an ordinal scale of 0 to 10 (Kousik et al. 2018a, 2018b), where 0 = no visible powdery mildew, 5 = 26% to 50%, and 10 = 98% to 100% of leaf area covered with abundant conidia and leaf dying or dead. During Summer 2017, the first rating was recorded 48 d after transplanting on May 17, followed by two additional ratings, for a total of three ratings. During the fall season, the first rating was recorded 3 d after transplanting on 19 Sep, followed by six additional ratings recorded once every week. Data were analyzed using the PROC GLIMMIX procedure of SAS (version 9.4; SAS Institute, Cary, NC). Area under disease progress curves were calculated for each plot using the disease severity data (Madden et al. 2007), and means were separated using the PDIFF option (α = 0.05). ‘USVL531-MDR’ was highly resistant to the local prevailing isolates of powdery mildew when compared with ‘USVL677-PMS’ or ‘Mickey Lee’ in both the field trials (Table 1). Abundant sporulation was observed on ‘USVL677-PMS’. During similar field trials conducted in Fort Pierce, FL, ‘USVL531-MDR’ was highly resistant to powdery mildew compared with ‘USVL677-PMS’ and ‘Mickey Lee’ (data not presented).

Table 1.

Powdery mildew [PM (Podosphaera xanthii)] severity on the germplasm line ‘USVL531-MDR’ developed by the US Department of Agriculture-Agricultural Research Service (USDA-ARS), US Vegetable Laboratory, and two susceptible checks (‘USVL677-PMS’ and ‘Mickey Lee’) during Summer and Fall 2017 field trials in Charleston, SC.

Table 1.

Similarly, greenhouse trials to confirm resistance of hypocotyls, cotyledons, and true leaves on seedlings of USVL531-MDR were conducted exactly as previously described (Kousik et al. 2018a). The trial had four replications with four plants per replication, and it was conducted two times. A randomized complete block design was used for these two trials. A conidial suspension (105 condia/mL in 0.02% Tween 20) of a local P. xanthii isolate B108ML was used for inoculations as described before (Kousik et al. 2018a, 2018b), and hypocotyls, cotyledons, and true leaves were rated using the same scale of 0 to 10 that was referenced previously. Disease severity rating data were converted to midpoint percentages and analyzed using the PROC GLIMMIX procedure of SAS. Mean separation was performed using the PDIFF option (α = 0.05). During both the greenhouse trials, USVL531-MDR had very low to no occurrence of powdery mildew on hypocotyl, cotyledon, or true leaves (Figs. 1 and 2). In comparison, severe powdery mildew was observed on ‘Mickey Lee’ and ‘USVL677-PMS’. Generally, ‘USVL677-PMS’ was significantly more susceptible than ‘Mickey Lee’ (Table 2).

Fig. 1.
Fig. 1.

High levels of resistance to powdery mildew observed on plant of ‘USVL531-MDR’ in the pot (right) compared with severe powdery mildew on hypocotyl and cotyledons of the susceptible check plants of ‘USVL677-PMR’ (left) during greenhouse studies.

Citation: HortScience 58, 4; 10.21273/HORTSCI16907-22

Fig. 2.
Fig. 2.

Severe powdery mildew development on true leaves of ‘USVL677-PMS’ compared with those of ‘USVL531-MDR’ displaying high levels of resistance. Inset shows cotyledon of ‘USVL531’ (left) displaying high levels of resistance to powdery mildew compared with cotyledon of ‘USVL677-PMS’ with severe powdery mildew (right) during greenhouse studies.

Citation: HortScience 58, 4; 10.21273/HORTSCI16907-22

Table 2.

Resistance to powdery mildew (Podosphaera xanthii) in germplasm USVL531-MDR compared with the susceptible line USVL677-PMS and cultivar Mickey Lee during two inoculated greenhouse trials in Charleston, SC.

Table 2.

Resistance of true leaves of ‘USVL531-MDR’ was assayed against five isolates of powdery mildew collected from FL, CA, GA, and NY, as previously described, using petri dish assays (Kousik et al. 2018a). Details of each of the individual powdery mildew isolates have been previously described (Kousik et al. 2018a). The experiment was conducted three times with two replications for each genotype in each experiment. A randomized complete block design was used to arrange the plates on the shelves, and powdery mildew severity was recorded 14 d after inoculation, as previously described (Kousik et al. 2018a). Data of powdery mildew severity on each of the true leaves were recorded using the same disease severity scale of 0 to 10 that was described previously. Disease severity ratings were converted to midpoint percentages and analyzed using the PROC GLIMMIX procedure of SAS, and means were separated using the PDIFF option (α = 0.05). Significant differences among the isolates (P = 0.0005) and a significant (P ≤ 0.0001) interaction between genotypes × isolates was observed. ‘USVL677-PMS’ was susceptible to all five isolates. Variability in powdery mildew severity among isolates was observed on ‘USVL677-PMS’, and the TRIXFRT isolate collected from fruit in FL was the least aggressive compared with GC1, which was also collected from FL. ‘USVL531-MDR’ was significantly resistant against all the five isolates compared with ‘USVL677-PMS’ (Table 3). No differences in disease severity were observed among the isolates on ‘USVL531-MDR’.

Table 3.

Broad resistance against five powdery mildew (Podosphaera xanthii) isolates collected from different states in germplasm ‘USVL531-MDR’ compared with the susceptible line ‘USVL677-PMS’ during three petri dish experiments.

Table 3.

In other studies, ‘USVL531-MDR’ was resistant to 11 different powdery mildew isolates collected from different states (Kousik and Ikerd 2014). These 11 different powdery mildew isolates belonged to two races based on the two watermelon differentials ‘USVL677-PMS’ and ‘Mickey Lee’ (Kousik and Ikerd 2014). In recent studies using a local SC isolate, severe powdery mildew infection and development on true leaves over time were observed on ‘USVL677-PMS’ compared with ‘USVL531-MDR’, which was highly resistant. Microscopic observations of cleared leaves stained with trypan blue demonstrated that powdery mildew did not colonize ‘USVL531-MDR’ leaves; in comparison, ‘USVL-677’ leaves were highly colonized by P. xanthii (Mandal et al. 2020). During the same study, resistance genes expressed during P. xanthii בUSVL531-MDR’ interaction over time after inoculation have been identified and described. A potential resistance gene conditioning resistance to powdery mildew in ‘USVL531-MDR’ was identified on chromosome 2 as ClaPMR2, Citrullus lanatus PM Resistance gene 2 {Chr2: 26750001.26753327 (−)}, which encodes for an NBS-LRR resistance protein with homology to the Arabidopsis thaliana powdery mildew resistance protein RPW8. Based on single nucleotide polymorphisms associated with the ClaPMR2 locus (Cla019831), a polymerase chain reaction-based cleaved amplified polymorphic sequence (CAPS) marker has been developed to genotype ‘USVL531-MDR’ and ‘USVL677-PMS’, and the F2 population of ‘USVL531-MDR’ × ‘USVL677-PMS’ (Mandal et al. 2020). The CAPS marker identified the resistant and susceptible phenotype with 98% accuracy. ‘USVL531-MDR’, when used as a rootstock for grafting, also provided powdery mildew resistance to a susceptible scion ‘Mickey Lee’ when grafted on it (Kousik et al. 2018b). Relatively higher melatonin content was detected in leaves of ‘USVL531-MDR’ compared with those of ‘USVL677-PMS’ (Mandal et al. 2018). A high-quality genome assembly of ‘USVL531-MDR’ based on 100X PacBio reads (developed by Boyce Thomson Institute, Cornell University, Ithaca, NY) is also available for use in future studies (http://cucurbitgenomics.org/v2/ftp/genome/watermelon/USVL531/).

Resistance to Phytophthora capsici isolates in USVL531-MDR.

‘USVL-531-MDR’ has been evaluated extensively for resistance to P. capsici isolates. In routine studies after the development of ‘USVL531-MDR’, lesions on inoculated fruit of ‘USVL531-MDR’ were barely noticeable around the inoculum plug and were generally <1 cm in diameter (range, 0–1 cm diameter) compared with USVL677-PMS and cultivars Dixie Lee or Mickey Lee, which had fruit rot lesions that were large (>9 cm) and covered 80% of the visible surface of fruits. No pathogen sporulation occurred on inoculated fruit of ‘USVL531-MDR’, whereas heavy sporulation was observed on fruit of ‘USVL677-PMS’ and ‘Mickey Lee’. ‘USVL531-MDR’ was highly resistant to 20 isolates of the Phytophthora fruit rot causal agent P. capsici collected from different states in the United States, including FL, GA, NC, SC, MI, and NY (Kousik et al. 2022). Extensive genetic variability was observed among these 20 isolates. Furthermore, these 20 isolates belonged to the two different mating types (A1 and A2) and had differing levels of sensitivity to fungicides, especially mefenoxam and cyazofamid (Kousik et al. 2022). Additionally, fruit of ‘USVL531-MDR’ were resistant to the local SC P. capsici isolate RCZ-11 at all stages of development (Kousik et al. 2018c). The genetics of resistance to Phytophthora fruit rot in ‘USVL51-MDR’ appears to be complex; therefore, a recombinant inbred line population has also been developed using ‘USVL531-MDR’ as a parent for fine-mapping the chromosomal regions involved in resistance.

Description of USVL531-MDR Plants

Data of the horticultural characteristics of ‘USVL531-MDR’ were collected from plants grown in experimental fields in Charleston, SC, and Fort Pierce, FL. Plants of ‘USVL531-MDR’ have a runner growth habit with lobed leaves. The germplasm line is monoecious, with each plant producing five to six (mean, 5.6) almost round fruits (mean, 13.2 × 12.7 cm). The fruit color is green with slightly darker green stripes. The color of the fruit rind determined using a Konica Minolta Chroma Meter (CR-400 with 8-mm aperture and 2° viewing angle) and the CIE L*a*b* color data software (CM-S100w SpectraMagic NX, version 1.7; Konica Minolta, Tokyo, Japan) is medium green, with mean color coordinate readings of L* = 46.18, a* = −13.96, and b* = 20.18. The darker green stripes on the rind had mean color coordinate readings of L* = 34.91, a* = −8.57, and b* = 9.57. Fruit flesh is very firm and cream white-colored, with mean color coordinate readings of L* = 62.27, a* = −1.00, b* = 5.51. ‘USVL531-MDR’ has medium sized, white to cream-colored egusi-type seeds with a black border. Each fruit generally weighs approximately 1 kg (1.2 kg) in field tests conducted at Fort Pierce, FL. The brix value for mature fruit, on average, was very low (3.14%) and ranged from 2.3 to 3.7. The line can be easily crossed with commercial cultivated-type watermelon to produce F1 and F2 populations for breeding purposes.

PI 494531 was reported to have some level of resistance to bacterial fruit blotch and was given a rating of 3 using a scale of 1 to 9 for increasing disease severity (https://npgsweb.ars-grin.gov/gringlobal/method?id=496555). The original accession was given a rating of 3.7 using a scale of 1 to 9 for tolerance to gummy stem blight (https://npgsweb.ars-grin.gov/gringlobal/accessiondetail?id=1389467). Recently, we observed that ‘USVL531-MDR’ was resistant to Cucurbit leaf crumple virus when inoculated with Agrobacterium infectious clones (Kousik et al., data not shown). Overall, the germplasm line ‘USVL531-MDR’ can serve as a valuable resource for watermelon breeding programs aimed at incorporating resistance to multiple diseases.

Availability

Small amounts of seed of ‘USVL531-MDR’ produced by hand self-pollination in a greenhouse are available for distribution to interested research personnel and plant breeders. Address all requests to Shaker Kousik, US Vegetable Laboratory, US Department of Agriculture-Agricultural Research Service, 2700 Savannah Highway, Charleston, SC 29414 (e-mail: shaker.kousik@usda.gov). Seed of USVL531-MDR will also be submitted to the National Plant Germplasm System, where they will be available for research purposes, including the development and commercialization of new cultivars. It is requested that appropriate recognition of the source be given when this germplasm contributes to research or development of a new breeding line or cultivar.

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  • Kousik, CS & Ikerd, JL 2014 Evidence for cucurbit powdery mildew pathogen races based on watermelon differentials 32 34 Havey, M, Weng, Y, Day, B & Grumet, R Proceedings of Cucurbitaceae 2014. American Society of Horticultural Science Alexandria, VA

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ling, K, Adkins, S, Webster, CG & Turechek, WW 2014a Phytophthora fruit rot-resistant watermelon germplasm lines: USVL489-PFR, USVL782-PFR, USVL203-PFR, and USVL020-PFR HortScience. 49 101 104 https://doi.org/10.21273/HORTSCI.49.1.101

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL & Harrison, HF 2014b Development of pre- and postharvest Phytophthora fruit rot on watermelons treated with fungicides in the field Plant Health Progress 15 3 145 150 Online (Bergh). https://doi.org/10.1094/PHP-RS-14-0009

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Brusca, J & Turechek, WW 2016 Diseases and disease management strategies take top research priority in the Watermelon Research and Development Group members survey (2014 to 2015) Plant Health Prog. 17 53 58 https://apsjournals.apsnet.org/doi/pdf/10.1094/PHP-S-15-0047

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ji, P, Egel, DS & Quesada-Ocampo, LM 2017 Fungicide rotation programs for managing Phytophthora fruit rot of watermelon in Southeastern United States Plant Health Prog. 18 28 34 https://doi.org/10.1094/PHP-RS-16-0059

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL, Mandal, MK, Adkins, S & Turechek, WW 2018a Watermelon germplasm lines: USVL608-PMR, USVL255-PMR, USVL313-PMR and USVL585-PMR with broad resistance to powdery mildew HortScience. 53 8 1212 1217 https://doi.org/10.21273/HORTSCI12979-18

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Mandal, MK & Hassell, R 2018b Powdery mildew resistant rootstocks that impart tolerance to grafted susceptible watermelon scion seedlings Plant Dis. 102 1290 1298 https://doi.org/10.1094/PDIS-09-17-1384-RE

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Iker, JL & Turechek, WW 2018c Development of Phytophthora fruit rot caused by Phytophthora capsici on resistant and susceptible watermelon fruit of different ages Plant Dis. 102 370 374 https://doi.org/10.1094/PDIS-06-17-0898-RE

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL & Mandal, MK 2019 Relative susceptibility of commercial watermelon varieties to powdery mildew Crop Prot. 125 104910 https://doi.org/10.1016/j.cropro.2019.104910

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL, Wechter, WP, Branham, SE & Turechek, WW 2022 Broad resistance to post-harvest fruit rot in USVL watermelon germplasm lines to isolates of Phytophthora capsici from across USA Plant Dis. 106 711 719 https://doi.org/10.1094/PDIS-11-20-2480-RE

    • Search Google Scholar
    • Export Citation
  • Lebeda, A, Kristkova, E & Sedlakova, B 2011 Gaps and perspectives of pathotype and race determination in Golovinomyces cichoracearum and Podosphaera xanthii Mycoscience. 52 159 164 https://doi.org/10.1007/S10267-010-0098-8

    • Search Google Scholar
    • Export Citation
  • Lebeda, A, Kristkova, E, Sedlakova, B, McCreight, JD & Coffey, MD 2016 Cucurbit powdery mildews: Methodology for objective determination and denomination of races Eur J Plant Pathol. 144 399 410 https://doi.org/10.1007/s10658-015-0776-7

    • Search Google Scholar
    • Export Citation
  • Madden, LV, Hughes, G & Van den Bosch, F 2007 The study of plant disease epidemics The American Phytopathological Society, APS Press St. Paul, MN

    • Search Google Scholar
    • Export Citation
  • Mandal, MK, Suren, H, Ward, B, Boroujerdi, A & Kousik, CS 2018 Differential roles of melatonin in plant-host resistance and pathogen suppression in cucurbits J Pineal Res. 65 3 e12505 https://doi.org/10.1111/jpi.12505

    • Search Google Scholar
    • Export Citation
  • Mandal, MK, Suren, H & Kousik, CS 2020 Elucidation of resistance signaling and identification of powdery mildew resistant mapping loci (ClaPMR2) during watermelon-Podosphaera xanthii interaction using RNA-Seq and whole-genome resequencing approach Sci Rep. 10 14038 https://doi.org/10.1038/s41598-020-70932-z. https://www.nature.com/articles/s41598-020-70932-z#Sec16

    • Search Google Scholar
    • Export Citation
  • McCreight, JD 2006 Melon-powdery mildew interactions reveal variation in melon cultigens and Podosphaera xanthii races 1 and 2 J Am Soc Hortic Sci. 131 1 59 65

    • Search Google Scholar
    • Export Citation
  • McGrath, MT 2010 Managing Cucurbit powdery mildew organically Online eOrganic article: http://www.extension.org/pages/30604/managing-cucurbit-powdery-mildew-organically. Last accessed on 7 Jan 2018

    • Search Google Scholar
    • Export Citation
  • McGrath, MT 2017a Powdery mildew 62 64 Keinath, AP, Wintermantel, WM & Zitter, TA Compendium of cucurbit diseases and pests Second Edition APS Press St. Paul, MN

    • Search Google Scholar
    • Export Citation
  • McGrath, MT 2017b Phytophthora fruit rot 102 104 Keinath, AP, Wintermantel, WM & Zitter, TA Compendium of cucurbit diseases and pests 2nd ed APS Press St. Paul. MN

    • Search Google Scholar
    • Export Citation
  • Mercier, J, Muscara, MJ & Davis, AR 2014 First Report of Podosphaera xanthii race 1W causing powdery mildew of watermelon in California Plant Dis. 98 158 https://doi.org/10.1094/PDIS-05-13-0552-PDN

    • Search Google Scholar
    • Export Citation
  • Paris, HS 2015 Origin and emergence of the sweet dessert watermelon, Citrullus lanatus Ann. Bot. (Oxford). 116 133 148

  • Pitrat, M, Dogimont, C & Bardin, M 1998 Resistance to fungal diseases of foliage in melon 167 173 McCreight, JD Cucurbitaceae ’98 ASHS Press Alexandria, VA

    • Search Google Scholar
    • Export Citation
  • Rennberger, G, Gerard, P & Keinath, AP 2018 Occurrence of foliar pathogens of watermelon on commercial farms in South Carolina estimated with stratified cluster sampling Plant Dis. 102 11 2285 2295 https://apsjournals.apsnet.org/doi/10.1094/PDIS-03-18-0468-RE

    • Search Google Scholar
    • Export Citation
  • Renner, SS, Sousa, A & Chomicki, G 2017 Chromosome numbers, Sudanese wild forms, and classification of the watermelon genus Citrullus, with 50 names allocated to seven biological species Taxon. 66 1393 1405 https://doi.org/10.12705/666.7

    • Search Google Scholar
    • Export Citation
  • Strange, BE, Guner, N, Pesic-VanEsbroeck, Z & Wehner, TC 2002 Screening the watermelon germplasm collection for resistance to Papaya ringspot virus type-W Crop Sci. 42 1324 1330 https://doi.org/10.2135/cropsci2002.1324

    • Search Google Scholar
    • Export Citation
  • Tetteh, AY, Wehner, TC & Davis, AR 2010 Identifying resistance to powdery mildew race 2W in the USDA-ARS watermelon germplasm collection Crop Sci. 50 933 939 https://doi.org/10.2135/cropsci2009.03.0135

    • Search Google Scholar
    • Export Citation
  • Thomas, CE, Levi, A & Caniglia, E 2005 Evaluation of U.S. plant introductions of watermelon for resistance to powdery mildew HortScience. 40 154 156 https://doi.org/10.21273/HORTSCI.40.1.154

    • Search Google Scholar
    • Export Citation
  • Tores, JA, Fernández-Ortuño, D, Daniel Jiménez, D, Guiderdone, S & Bellón-Doña, D 2021 Evidence of physiological races of Podosphaera xanthii in watermelon in Southern Europe EUCARPA, Cucurbitaceae. P6-5, Page 81. https://cucurbit.info/wp-content/uploads/2021/09/cuc2021procee dings.pdf

    • Search Google Scholar
    • Export Citation
  • Wiant, JS & Tucker, CM 1940 A rot of winter queen watermelon caused by Phytophthora capsici J Agric Res. 60 73 88

  • Zhang, H, Guo, S, Gong, G, Ren, Y, Davis, AR & Xu, Y 2011 Sources of resistance to race 2WF powdery mildew in US watermelon plant introductions HortScience. 46 1349 1352 https://doi.org/10.21273/HORTSCI.46.10.1349

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  • Fig. 1.

    High levels of resistance to powdery mildew observed on plant of ‘USVL531-MDR’ in the pot (right) compared with severe powdery mildew on hypocotyl and cotyledons of the susceptible check plants of ‘USVL677-PMR’ (left) during greenhouse studies.

  • Fig. 2.

    Severe powdery mildew development on true leaves of ‘USVL677-PMS’ compared with those of ‘USVL531-MDR’ displaying high levels of resistance. Inset shows cotyledon of ‘USVL531’ (left) displaying high levels of resistance to powdery mildew compared with cotyledon of ‘USVL677-PMS’ with severe powdery mildew (right) during greenhouse studies.

  • Ben-Naim, Y & Cohen, Y 2015 Inheritance of resistance to powdery mildew race 1W in watermelon Phytopathology. 105 1446 1457 https://doi.org/10.1094/PHYTO-02-15-0048-R

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  • Chomicki, G & Renner, SS 2015 Watermelon origin solved with molecular phylogenetics including Linnaean material: Another example of museonomics New Phytol. 205 526 532 https://doi.org/10.1111/nph.13163

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  • Davis, AR, Levi, A, Tetteh, A, Wehner, TC, Russo, V & Pitrat, M 2007 Evaluation of watermelon and related species for resistance to race 1W Powdery mildew J Am Soc Hortic Sci. 132 790 795 https://doi.org/10.21273/JASHS.132.6.790

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  • Guner, N, Strange, BE, Wehner, TC & Pesic-VanEsbroeck, Z 2002 Methods for screening watermelon for resistance to Papaya ringspot virus type-W Scientia Hortic. 94 297 307 https://doi.org/10.1016/S0304-4238(02)00007-9

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  • Jahn, M, Munger, HM & McCreight, JD 2002 Breeding cucurbit crops for powdery mildew resistance 239 248 Chapter 15 Belanger, RR, Bushnell, WR, Dik, AJ & Carver, TLW The powdery mildews. A comprehensive treatise. APS Press St. Paul MN

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  • Keinath, AP & DuBose, VB 2004 Evaluation of fungicides for prevention and management of powdery mildew on watermelon Crop Prot. 23 35 42 https://doi.org/10.1016/S0261-2194(03)00165-0

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  • Keinath, AP 2007 Sensitivity of populations of Phytophthora capsici from South Carolina to mefenoxam, dimethomorph, zoxamide and cymoxanil Plant Dis. 91 743 748 https://doi.org/10.1094/PDIS-91-6-0743

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  • Keinath, AP 2015 Efficacy of fungicides against powdery mildew on watermelon caused by Podosphaera xanthii Crop Prot. 75 70 76 https://doi.org/10.1016/j.cropro.2015.05.013

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  • Keinath, AP & Rennberger, G 2017 Powdery mildew on watermelon Clemson Cooperative Extension Publication. Fact sheet. LGP 1019. Powdery Mildew on Watermelon, Land-Grant Press (clemson.edu). https://lgpress.clemson.edu/publication/powdery-mildew-on-watermelon/. [accessed 18 Jan 2023]

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  • Keinath, AP, Rennberger, G & Kousik, CS 2018 First report of resistance to boscalid in Podosphaera xanthii, cucurbit powdery mildew, in South Carolina Plant Health Progress 19 220 221 Online (Bergh). https://doi.org/10.1094/PHP-03-18-0009-BR

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  • Kousik, CS, Adkins, S, Turechek, WW & Roberts, PD 2009 Sources of resistance in U.S. plant introductions (PI) to watermelon vine decline Caused by Squash Vein Yellowing Virus HortScience. 44 256 262 https://doi.org/10.21273/HORTSCI.44.2.256

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  • Kousik, CS, Donahoo, RS, Webster, CG, Turechek, WW, Adkins, ST & Roberts, PD 2011 Outbreak of cucurbit powdery mildew on watermelon fruit caused by Podosphaera xanthii in southwest Florida Plant Dis. 95 1586 https://doi.org/10.1094/PDIS-06-11-0521

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  • Kousik, CS, Ikerd, JL, Wechter, WP, Harrison, HF & Levi, A 2012 Resistance to Phytophthora fruit rot of watermelon caused by Phytophthora capsici in U.S. plant introductions HortScience. 47 1682 1689 https://doi.org/10.21273/ HORTSCI.47.12.1682

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    • Export Citation
  • Kousik, CS & Ikerd, JL 2014 Evidence for cucurbit powdery mildew pathogen races based on watermelon differentials 32 34 Havey, M, Weng, Y, Day, B & Grumet, R Proceedings of Cucurbitaceae 2014. American Society of Horticultural Science Alexandria, VA

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ling, K, Adkins, S, Webster, CG & Turechek, WW 2014a Phytophthora fruit rot-resistant watermelon germplasm lines: USVL489-PFR, USVL782-PFR, USVL203-PFR, and USVL020-PFR HortScience. 49 101 104 https://doi.org/10.21273/HORTSCI.49.1.101

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL & Harrison, HF 2014b Development of pre- and postharvest Phytophthora fruit rot on watermelons treated with fungicides in the field Plant Health Progress 15 3 145 150 Online (Bergh). https://doi.org/10.1094/PHP-RS-14-0009

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Brusca, J & Turechek, WW 2016 Diseases and disease management strategies take top research priority in the Watermelon Research and Development Group members survey (2014 to 2015) Plant Health Prog. 17 53 58 https://apsjournals.apsnet.org/doi/pdf/10.1094/PHP-S-15-0047

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ji, P, Egel, DS & Quesada-Ocampo, LM 2017 Fungicide rotation programs for managing Phytophthora fruit rot of watermelon in Southeastern United States Plant Health Prog. 18 28 34 https://doi.org/10.1094/PHP-RS-16-0059

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL, Mandal, MK, Adkins, S & Turechek, WW 2018a Watermelon germplasm lines: USVL608-PMR, USVL255-PMR, USVL313-PMR and USVL585-PMR with broad resistance to powdery mildew HortScience. 53 8 1212 1217 https://doi.org/10.21273/HORTSCI12979-18

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Mandal, MK & Hassell, R 2018b Powdery mildew resistant rootstocks that impart tolerance to grafted susceptible watermelon scion seedlings Plant Dis. 102 1290 1298 https://doi.org/10.1094/PDIS-09-17-1384-RE

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Iker, JL & Turechek, WW 2018c Development of Phytophthora fruit rot caused by Phytophthora capsici on resistant and susceptible watermelon fruit of different ages Plant Dis. 102 370 374 https://doi.org/10.1094/PDIS-06-17-0898-RE

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL & Mandal, MK 2019 Relative susceptibility of commercial watermelon varieties to powdery mildew Crop Prot. 125 104910 https://doi.org/10.1016/j.cropro.2019.104910

    • Search Google Scholar
    • Export Citation
  • Kousik, CS, Ikerd, JL, Wechter, WP, Branham, SE & Turechek, WW 2022 Broad resistance to post-harvest fruit rot in USVL watermelon germplasm lines to isolates of Phytophthora capsici from across USA Plant Dis. 106 711 719 https://doi.org/10.1094/PDIS-11-20-2480-RE

    • Search Google Scholar
    • Export Citation
  • Lebeda, A, Kristkova, E & Sedlakova, B 2011 Gaps and perspectives of pathotype and race determination in Golovinomyces cichoracearum and Podosphaera xanthii Mycoscience. 52 159 164 https://doi.org/10.1007/S10267-010-0098-8

    • Search Google Scholar
    • Export Citation
  • Lebeda, A, Kristkova, E, Sedlakova, B, McCreight, JD & Coffey, MD 2016 Cucurbit powdery mildews: Methodology for objective determination and denomination of races Eur J Plant Pathol. 144 399 410 https://doi.org/10.1007/s10658-015-0776-7

    • Search Google Scholar
    • Export Citation
  • Madden, LV, Hughes, G & Van den Bosch, F 2007 The study of plant disease epidemics The American Phytopathological Society, APS Press St. Paul, MN

    • Search Google Scholar
    • Export Citation
  • Mandal, MK, Suren, H, Ward, B, Boroujerdi, A & Kousik, CS 2018 Differential roles of melatonin in plant-host resistance and pathogen suppression in cucurbits J Pineal Res. 65 3 e12505 https://doi.org/10.1111/jpi.12505

    • Search Google Scholar
    • Export Citation
  • Mandal, MK, Suren, H & Kousik, CS 2020 Elucidation of resistance signaling and identification of powdery mildew resistant mapping loci (ClaPMR2) during watermelon-Podosphaera xanthii interaction using RNA-Seq and whole-genome resequencing approach Sci Rep. 10 14038 https://doi.org/10.1038/s41598-020-70932-z. https://www.nature.com/articles/s41598-020-70932-z#Sec16

    • Search Google Scholar
    • Export Citation
  • McCreight, JD 2006 Melon-powdery mildew interactions reveal variation in melon cultigens and Podosphaera xanthii races 1 and 2 J Am Soc Hortic Sci. 131 1 59 65

    • Search Google Scholar
    • Export Citation
  • McGrath, MT 2010 Managing Cucurbit powdery mildew organically Online eOrganic article: http://www.extension.org/pages/30604/managing-cucurbit-powdery-mildew-organically. Last accessed on 7 Jan 2018

    • Search Google Scholar
    • Export Citation
  • McGrath, MT 2017a Powdery mildew 62 64 Keinath, AP, Wintermantel, WM & Zitter, TA Compendium of cucurbit diseases and pests Second Edition APS Press St. Paul, MN

    • Search Google Scholar
    • Export Citation
  • McGrath, MT 2017b Phytophthora fruit rot 102 104 Keinath, AP, Wintermantel, WM & Zitter, TA Compendium of cucurbit diseases and pests 2nd ed APS Press St. Paul. MN

    • Search Google Scholar
    • Export Citation
  • Mercier, J, Muscara, MJ & Davis, AR 2014 First Report of Podosphaera xanthii race 1W causing powdery mildew of watermelon in California Plant Dis. 98 158 https://doi.org/10.1094/PDIS-05-13-0552-PDN

    • Search Google Scholar
    • Export Citation
  • Paris, HS 2015 Origin and emergence of the sweet dessert watermelon, Citrullus lanatus Ann. Bot. (Oxford). 116 133 148

  • Pitrat, M, Dogimont, C & Bardin, M 1998 Resistance to fungal diseases of foliage in melon 167 173 McCreight, JD Cucurbitaceae ’98 ASHS Press Alexandria, VA

    • Search Google Scholar
    • Export Citation
  • Rennberger, G, Gerard, P & Keinath, AP 2018 Occurrence of foliar pathogens of watermelon on commercial farms in South Carolina estimated with stratified cluster sampling Plant Dis. 102 11 2285 2295 https://apsjournals.apsnet.org/doi/10.1094/PDIS-03-18-0468-RE

    • Search Google Scholar
    • Export Citation
  • Renner, SS, Sousa, A & Chomicki, G 2017 Chromosome numbers, Sudanese wild forms, and classification of the watermelon genus Citrullus, with 50 names allocated to seven biological species Taxon. 66 1393 1405 https://doi.org/10.12705/666.7

    • Search Google Scholar
    • Export Citation
  • Strange, BE, Guner, N, Pesic-VanEsbroeck, Z & Wehner, TC 2002 Screening the watermelon germplasm collection for resistance to Papaya ringspot virus type-W Crop Sci. 42 1324 1330 https://doi.org/10.2135/cropsci2002.1324

    • Search Google Scholar
    • Export Citation
  • Tetteh, AY, Wehner, TC & Davis, AR 2010 Identifying resistance to powdery mildew race 2W in the USDA-ARS watermelon germplasm collection Crop Sci. 50 933 939 https://doi.org/10.2135/cropsci2009.03.0135

    • Search Google Scholar
    • Export Citation
  • Thomas, CE, Levi, A & Caniglia, E 2005 Evaluation of U.S. plant introductions of watermelon for resistance to powdery mildew HortScience. 40 154 156 https://doi.org/10.21273/HORTSCI.40.1.154

    • Search Google Scholar
    • Export Citation
  • Tores, JA, Fernández-Ortuño, D, Daniel Jiménez, D, Guiderdone, S & Bellón-Doña, D 2021 Evidence of physiological races of Podosphaera xanthii in watermelon in Southern Europe EUCARPA, Cucurbitaceae. P6-5, Page 81. https://cucurbit.info/wp-content/uploads/2021/09/cuc2021procee dings.pdf

    • Search Google Scholar
    • Export Citation
  • Wiant, JS & Tucker, CM 1940 A rot of winter queen watermelon caused by Phytophthora capsici J Agric Res. 60 73 88

  • Zhang, H, Guo, S, Gong, G, Ren, Y, Davis, AR & Xu, Y 2011 Sources of resistance to race 2WF powdery mildew in US watermelon plant introductions HortScience. 46 1349 1352 https://doi.org/10.21273/HORTSCI.46.10.1349

    • Search Google Scholar
    • Export Citation
Chandrasekar S. Kousik US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414, USA

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Jennifer Ikerd US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414, USA

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Mihir Mandal Oak Ridge Institute for Science and Education participant sponsored by US Department of Agriculture-Agricultural Research Service, US Vegetable Laboratory, Charleston, SC 29414, USA

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Scott Adkins US Department of Agriculture-Agricultural Research Service, US Horticultural Research Laboratory, Fort Pierce, FL 34945, USA

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William W. Turechek US Department of Agriculture-Agricultural Research Service, US Horticultural Research Laboratory, Fort Pierce, FL 34945, USA

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Contributor Notes

We acknowledge the technical assistance of Jerry Johnson, Stephen Mayo, Carrie Vanderspool, and the numerous student workers over the years with conducting the greenhouse and field experiments. We appreciate the critical review of this manuscript by Dr. Sharon Andreason and Dr. Dennis Katuuramu prior to submission. Financial support was provided in part by US Department of Agriculture NIFA SCRI CucCAP grant award 2015-51181-24285 and CuCCAP2 award 2020-51181-32139.

The use of trade, firm or corporation names in this publication is for the convenience of the reader. Such use does not constitute an official endorsement or approval by the US Department of Agriculture or the Agricultural Research Service of any product or service to the exclusion of others that may also be suitable.

Current address for M.M.: US Department of Agriculture-Agricultural Research Service, Crops Pathology and Genetics, University of California, Davis, CA, USA.

C.S.K. is the corresponding author. E-mail: shaker.kousik@usda.gov.

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