HORTSCIENCE 53(5):624–627. 2018. https://doi.org/10.21273/HORTSCI12944-18 PRSV-W is transmitted in a nonpersistent manner by 24 species in 15 genera with , Aulacorthum solani, Aphis Inheritance of Resistance to craccivora, and Macrosiphum euphorbiae as natural vectors. PRSV-W is a Ringspot -Watermelon Strain in whose genome consists of unipartite, single- stranded, linear RNA. Its total genome size is Watermelon 12 kb, and the genome codes for eight pro- teins. PRSV-W is in the family . Nihat Guner PRSV-W induces pinwheel and scroll types Sakata Seed America, Inc., Morgan Hill, CA 95037 of cytoplasmic cylindrical inclusions in in- fected host cells (Tiwari and Rao, 2014). Type Zvezdana Pesic-VanEsbroeck W isolates are reported to infect 38 species in Department of Entomology and Plant Pathology, North Carolina State 11 genera of , and two species of University, Raleigh, NC 27695 Chenopodiaceae, with squash ( spp.), watermelon (C. lanatus), cucumber Luis A. Rivera-Burgos1 and Todd C. Wehner (Cucumis sativus), and melon (Cucumis melo) Department of Horticultural Science, North Carolina State University, among the commercially important natural hosts (Freitas and Rezende, 2008). The virus Raleigh, NC 27695 is not seed transmitted. It appears to overwinter Additional index words. Citrullus lanatus, single recessive gene, allelism test, plant in wild species of Cucurbitaceae and Cheno- introduction podiaceae (Purcifull and Hiebert, 1979). Symptoms of severe PRSV-W infection Abstract. Sources of resistance to the watermelon strain of papaya ringspot virus- in cucurbits include leaves with mosaic, watermelon strain (PRSV-W) have been identified within the watermelon (Citrullus puckering, blistering, and size reduction; lanatus) germplasm collection. Inheritance of the resistance to PRSV-W was studied in vines that are stunted; and fruit that are small, three Citrullus amarus (formerly C. lanatus var. citroides) PI accessions: PI 244017, PI knobby, malformed, and mottled (Tiwari and 244019, and PI 485583. Three susceptible parent lines, ‘Allsweet’, ‘Calhoun Gray’, and Rao, 2014). PRSV-W causes significant yield ‘New Hampshire Midget’, were crossed with resistant PI accessions to develop F1,F2, and reduction in watermelon, squash, melon, BC1 progenies in six families. A single recessive gene was found to control the resistance cucumber, and other cultivated cucurbits to PRSV-W in all three resistant PI accessions. Allelism tests indicated that the three PI (Turechek et al., 2010). accessions carry the same resistance allele to PRSV-W. The gene symbol ‘prv’ is proposed Researchers have screened cucurbit spe- for PRSV-W resistance in PI 244017, PI 244019, and PI 485583 in watermelon. cies other than watermelon for resistance to PRSV-W, and the inheritance of the resis- tance has been determined. Sources of re- Introduction are common (Ali et al., 2012; Chen et al., sistance to PRSV-W have been found in 2008; Morata and Puigdomenech, 2017; cucumber (C. sativus), melon (C. melo), and Watermelon [C. lanatus (Thunb.) Mat- Wehner et al., 2001). Virus diseases are squash (Cucurbita spp.). PRSV-W resistance sum. & Nakai] is a major cucurbit crop that destructive to the watermelon crop and are is controlled by a single recessive gene in accounts for 7.5% of the world area devoted difficult to control (Kone et al., 2017; Navas- cucumber (Tian et al., 2015) and a single to vegetable crops (FAO, 2015). Worldwide, Castillo et al., 2011). Chemical control of the dominant gene in melon (Pitrat and Lecoq, watermelons are grown on more than 3.4 vectors is not usually efficient to control the 1983). In squash, resistance to PRSV-W is million ha, with a production of more than disease. Cultural controls such as treatment controlled by a single recessive gene in 111 million Mg of fruit. China and the Mid- with mineral oil sprays, light-reflective sur- C. moschata (Bolanos-Herrera, 1994) and dle Eastern countries are the major producers faces, and cross-protection with weak PRSV-W by three partially dominant genes in C. maxima and consumers (FAO, 2015). In the United isolates show limited effectiveness and require (Maluf et al., 1997). States, watermelon is used fresh as a dessert additional input costs. Therefore, genetic re- Sources of resistance to PRSV-W have and in salads. Major production states in the sistance remains the simplest, most effective, been reported in watermelon. Strange et al. United States are Florida, California, Texas, and most efficient mean of limiting losses to (2002) screened the USDA watermelon Georgia, and North Carolina (USDA, 2017). these diseases (Ali et al., 2012; Levi et al., 2016; germplasm collection and reported PRSV-W Production increased from 1.2 million Mg in Nagendran et al., 2017; Yu et al., 2011). resistance in three PI accessions from South 1987 to 5.1 million Mg in 2017, with a farm PRSV-W affects all agricultural species Africa (PI 244017, PI 244018, and PI value of $579 million (USDA, 2017). of the Cucurbitaceae and is of great eco- 244019), three PI accessions from Zimbabwe Plant diseases caused by are a ma- nomic importance because of its destruc- (PI 482342, PI 482318, and PI 482379), one jor limiting factor in the commercial pro- tiveness (Ali et al., 2012; Morata and PI accession from Botswana (PI 485583), duction of watermelon worldwide. Around Puigdomenech, 2017). PRSV-W was first and one PI accession from Nigeria (PI the world, more than 10 viruses are known to described by Webb and Scott (1965) from 595203). All of the resistant PI accessions be a problem in watermelon production (Ali Asia in Sri Lanka (Bateson et al., 2002). For except PI 595203 are C. amarus (formerly et al., 2012; Wang et al., 2017). The major many years, PRSV-W was considered to be C. lanatus var. citroides). PI 595203 is Citrullus viruses affecting watermelon in the United the distinct potyvirus, WMV-1 (Webb and mucosospermus (Chomicki and Renner, 2015). States are PRSV-W [formerly Watermelon Scott, 1965). However, the P and W isolates Although there has been no report of mosaic virus-1 (WMV-1)], WMV [formerly were found to be indistinguishable serologi- inheritance for resistance to PRSV-W in -2 (WMV-2)], and cally (Gonsalves and Ishii, 1980) and now are watermelon accessions (PI 244017, PI Zucchini yellow mosaic virus. All three vi- considered to be strains of PRSV (Baker 244019, and PI 485583), Azevedo et al. ruses are nonpersistently transmitted by sev- et al., 1991; Purcifull and Hiebert, 1979; (2012) reported that PRSV-W resistance in eral species of , and mixed infections Purcifull et al., 1984). The main reason for watermelon accession PI 595201 was not the early confusion about the taxonomic a simple monogenic inheritance pattern, al- status of the W isolate was that it does not though additive effects were found. PI Received for publication 31 Jan. 2018. Accepted infect papaya. However, the P isolates infect 595203 was reported to have a low level of for publication 1 Mar. 2018. cucurbits in nature as well as papaya resistance in the extensive PRSV-W water- 1Corresponding author. E-mail: [email protected]. (Provvidenti, 1993). melon screening by Strange et al. (2002).

624 HORTSCIENCE VOL. 53(5) MAY 2018 The objective of this study was to de- 3-week-old plant with 800-mesh carborun- self-pollinated to generate F2 seeds. To con- termine the inheritance of PRSV-W resis- dum, then applying the inoculum to the leaf firm the allelism test conducted in F1 plants, tance in three resistant PI accessions (PI with a pestle which was rotated in a circular F2 progenies were planted, inoculated, and 244017, PI 244019, and PI 485583) and to motion 8–10 times as if painting the leaf with rated as before. test the resistance genes in the three PI inoculum. After inoculation, carborundum accessions for allelism. Based on previous was rinsed off the leaves to improve light Results studies in other cucurbits, we hypothesize interception, and the plants were maintained that the inheritance of the resistance to in aphid-proof cages. All ‘Gray Zucchini’ All crosses between susceptible parents PRSV-W follows the single gene mode of plants were seeded in Metro-Mix 200 and resistant parents produced uniformly inheritance. (Scotts-Sierra Horticultural Products Com- susceptible F1 progenies, indicating that pany, Marysville, OH) in 160 mm diameter PRSV-W resistance is a recessive trait. The Materials and Methods (1550 mL volume) clay pots. Plants were F2,BC1Ps, and BC1Pr progenies from all six fertilized weekly with 150 mg·kg–1 Peters crosses were tested to the expected ratios of Plant material. The parental lines used in Professional 20–20–20 N–P–K (Scotts- a single gene inheritance. The F2 segregation this study were watermelon cultivars All- Sierra Horticultural Products Company). data obtained from all crosses followed the sweet (ALS), New Hampshire Midget Inoculation and data collection. The pre- expected ratio of 3 susceptible :1 resistant, (NHM), and Calhoun Gray (CHG) that are viously described inoculation procedure to favoring the single gene inheritance hypoth- highly susceptible to PRSV-W; and PI maintain the PRSV-W isolate and increase esis (Table 1). All BC1Ps progenies also 244017, PI 244019, and PI 485583 that are inoculum in squash plants was also used for supported the expected ratio for a single highly resistant. PI accessions were obtained the inheritance study in watermelon (Guner recessive gene hypothesis, showing 1 suscep- from the Southern Regional Plant Introduc- et al., 2002). Plants were inoculated at the tible : 0 resistant ratio (Table 1). All BC1Pr tion Station at Griffin, GA. ALS, CHG, and first true leaf stage and weekly rated at least populations segregated 1 susceptible : 1 re- NHM were used as susceptible parents be- six times 2 weeks after the inoculation. We sistant ratio, which also confirms a single cause they have high fruit yield and quality used a scale of 1 to 9 on the basis of severity recessive gene mode of inheritance control- (Wehner, 2002). All crosses were made using of viral symptoms, where 0 = none, 1–2 = ling the resistance to PRSV-W in PI 244017, controlled, hand-pollination in the green- trace, 3–4 = slight, 5–6 = moderate, 7–8 = PI 244019, and PI 485583 (Table 1). The house of the Department of Horticultural severe, and 9 = plant dead (Guner et al., pooled F2 individuals segregated 436 suscep- Science at North Carolina State University 2002). After the last rating, plants were tested tible : 154 resistant with a c2 of 0.35 (df = 1), in Raleigh, NC. Six families were developed by using ELISA (Agdia Incorporated, showing that the data were consistent with from six crosses, ALS · PI 244019, ALS · PI Elkhart, IN) to determine the presence of a 3:1 ratio (Table 2). The P value for that c2 485583, CHG · PI 244019, NHM · PI the virus in the leaf tissue. Leaf tissue used also confirmed a good fit of the data to the 244017, NHM · PI 244019, and NHM · for testing was sampled from the top five predicted values (P value = 0.55). The 2 PI 485583. The F1 was self-pollinated and leaves of the plant. Plants were classified as homogeneity c (with df = 5) for the F2 was backcrossed to their respective parental lines, resistant or susceptible based on their rank 0.99, indicating that all crosses represented to obtain progenies F2,BC1Ps,andBC1Pr for relative to the estimated mean value of the the same progeny and were homogenous all six crosses. Each family contained six disease severity scale (6.0) and ELISA test (Table 2). progenies: Ps,Pr,F1,F2,BC1Ps,andBC1Pr. results. Plants which did not have the virus in To determine whether the resistance For each of the six crosses, 180 plants were their system and had an average rating <6.0 genes of the PI accessions were allelic, we tested: 5 Ps,5Pr,10F1, 100 F2,30BC1Ps,and were considered resistant, and plants with performed the allelism test. The PI accessions 30 BC1Pr plants were used to test the in- the virus in their system and an average were crosses in all possible combination to heritance from each cross. rating >6.0 were considered susceptible generate F1 progenies (PI 244017 · PI Planting and management. The inheri- (Strange et al., 2002). 244019, PI 244017 · PI 244019, and PI tance study was performed in the greenhouse Statistical analysis. The c2 tests for 485583 · PI 244019). The progenies were of the Department of Plant Pathology at goodness-of-fit (P < 0.05) and homogeneity evaluated using the same inoculation pro- North Carolina State University in Raleigh, were used to examine segregation ratios cedure used in the inheritance study. Also, F2 NC. Greenhouse temperatures ranged from (susceptible:resistant) for each F2 and BC1 progenies were generated and tested to con- 23 to 43 C (0800–2000 h) and 12 to 24 C Pr progeny with the SAS statistical package firm allelic reactions observed in the F1 (20000–0800 h). We seeded directly in plas- (SAS Institute, Inc., Cary, NC) and the progenies. We observed that all F1 and F2 tic pots (100 · 100 m2 size, 600-mL volume) SASGene 1.2 program (Liu et al., 1997). progenies were resistant to PRSV-W, indi- filled with a soilless mix (Canadian sphag- Yates’ correction was used for those chi- cating that the resistance genes in all three num moss, perlite, vermiculite, processed square tests where counts were #5 for any resistant PI accessions are allelic (data not pine bark). We planted two seeds per pot class in the ratio. However, there was no shown). and thinned to one to ensure a uniform difference in the conclusion, so we presented experiment (Gusmini et al., 2017). the data without the correction to avoid the Discussion Inoculum preparation. The virus isolate tendency of Yate’s to overcorrect (Haviland, for this study was obtained from D.E. 1990). The PRSV has a serious impact on water- Purcifull, University of Florida, Gainesville, Allelism test. To determine the allelic melon production in the United States. Most FL. PRSV-W isolate 2052 was a severe iso- association between the resistance genes in of the time, PRSV-W outbreaks result in late described by Baker et al. (1991) and was the three PI accessions (PI 244017, PI losses through a reduction in growth, yield, maintained on ‘Gray Zucchini’ squash 244019, and PI 485583) we conducted the and fruit quality. There are two pathotypes of (Cucurbita pepo L.) from Seminis Vegetable allelism test in the greenhouses. The resistant this potyvirus: PRSV-P (papaya strain) that Seeds (Woodland, CA). The inoculum was PI accessions were crossed to each other in all infects papaya (Carica papaya) and most of prepared by grinding infected ‘Gray Zuc- possible combinations using controlled the cucurbitaceous crops (Cucurbitaceae), chini’ leaves using a mortar and pestle in pollinations to generate F1 progenies. All and PRSV-W (watermelon strain) that exclu- 0.02 M phosphate buffer, pH 7.0. Leaf to F1 hybrids derived from resistant · re- sively infects cucurbitaceous crops (Cucur- buffer ratio was 1:5 (1 g infected leaf to 5 mL sistant crosses were inoculated with bitaceae) (Freitas and Rezende, 2008; buffer). PRSV-W and phenotypically scored for Romay et al., 2014). The virus can be trans- To maintain the PRSV-W isolate and non-complementation using the same in- mitted in a nonpersistent, noncirculative increase inoculum, we used the rub method oculation procedure and rating system manner by several aphid species (Aphididae), (Guner et al., 2002). Squash plants were used in the inheritance study (Guner and also by mechanical inoculation, but not inoculated by dusting one leaf on each et al., 2002). Each F1 progeny was via seeds (Tiwari and Rao, 2014). Some of

HORTSCIENCE VOL. 53(5) MAY 2018 625 Table 1. Single locus goodness-of-fit test (P < 0.05) for resistance to Papaya ringspot virus-watermelon strain in watermelon. Progeny Susceptible Resistant Expectedz c2 df P value Allsweet (susceptible) · PI 244019 (resistant) y Ps 50 x Pr 05 F1 10 0 F2 69 27 3:1 0.50 1 0.47 BC1Ps 30 0 BC1Pr 14 15 1:1 0.03 1 0.85 Allsweet (susceptible) · PI 485583 (resistant) y Ps 50 x Pr 05 F1 10 0 F2 73 24 3:1 0.00 1 0.95 BC1Ps 27 0 BC1Pr 13 17 1:1 0.53 1 0.46 New Hampshire Midget (susceptible) · PI 244017 (resistant) y Ps 50 x Pr 05 F1 10 0 F2 73 27 3:1 0.21 1 0.64 BC1Ps 30 0 BC1Pr 16 14 1:1 0.13 1 0.71 New Hampshire Midget (susceptible) · PI 244019 (resistant) y Ps 50 x Pr 05 F1 10 0 F2 74 26 3:1 0.05 1 0.86 BC1Ps 30 0 BC1Pr 18 12 1:1 1.20 1 0.27 New Hampshire Midget (susceptible) · PI 485583 (resistant) y Ps 50 x Pr 05 F1 80 F2 72 28 3:1 0.48 1 0.48 BC1Ps 29 0 BC1Pr 14 15 1:1 0.03 1 0.85 Calhoun Gray (susceptible) · PI 244019 (resistant) y Ps 40 x Pr 05 F1 10 0 F2 75 24 3:1 0.28 1 0.59 BC1Ps 30 0 BC1Pr 16 14 1:1 0.13 1 0.71 zExpected was the hypothesized segregation ratio for single gene inheritance. y Ps was the susceptible parent. x Pr was the resistant parent.

Table 2. Pooled and homogeneity data from the six crosses for resistance to Papaya ringspot virus-watermelon strain in watermelon. Progeny Susceptible Resistant Expectedz c2 df P value Susceptible · Resistant crosses, pooled y Ps 29 0 x Pr 030 F1 58 0 F2 436 154 3:1 0.35 1 0.55 BC1Ps 176 0 BC1Pr 91 87 1:1 0.08 1 0.76 Homogeneity 1.18 5 0.99 zExpected was the hypothesized segregation ratio for single gene inheritance. y Ps was the susceptible parent. x Pr was the resistant parent. the symptoms consist of mosaic, the pres- et al., 2017; Romay et al., 2014; Turechek to PRSV-W. In this study, these three PI ence of blisters and deformations on leaves, et al., 2010). accessions were tested for the inheritance of fruit malformation with a change in color, It is common for plant breeders to identify PRSV-W on segregating progenies from and plant stunting. In the field, PRSV-W cultigens that serve as a source of resistance, crosses with susceptible lines. The inheri- outbreaks are quite difficult to control, although the genetic basis of the resistance tance data indicated that the resistance to leaving breeding for disease resistance as has not been previously determined. As PRSV-W, in all three resistant PI accessions, the most suitable method to control PRSV-W already reported, the PI watermelon acces- was controlled by a single recessive gene. epidemics. Hence, the use of commercial sions 244017, 244019, and 485583 showed Similar results were also reported on the cultivars with high resistance to PRSV-W high resistance to PRSV-W epidemics inheritance of the resistance to PRSV-W on would stabilize yield and improve fruit (Strange et al., 2002). However, it was not watermelon PI accession 595203 (Ma et al., quality in watermelon production areas determined whether these PI accessions carry 2005). In other cucurbitaceous crops, such as worldwide (Ali et al., 2012; Nagendran one or more genes controlling the resistance cucumber (C. sativus L.) and melon (C. melo L.),

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