Scientific Communication

Scientific communication

PINHEIRO, JB; SILVA, GO; OLIVEIRA, VR; AMARO, GB; MORAIS, AA. 2019. Prospection of genetic resistance resources to root-knot nematodes in cucurbit genotypes. Horticultura Brasileira 37: 343-347. DOI - http://dx.doi.org/10.1590/S0102-053620190314 Prospection of genetic resistance resources to root-knot nematodes in cucurbit genotypes Jadir B Pinheiro1ID; Giovani Olegario da Silva2ID; Valter R Oliveira1ID; Geovani Bernardo Amaro1ID; Alexandre Augusto de Morais 1 ID

1Embrapa Hortaliças, Brasília-DF, Brasil; [email protected]; [email protected]; [email protected]; alexandre. [email protected] 2Embrapa Hortaliças/SIN, Canoinhas-SC, Brasil; [email protected]

ABSTRACT RESUMO The aim of this research was to prospect genetic resistant Prospecção de fontes de resistência aos nematoides das galhas sources to root-knot-nematode in Cucurbitaceae accessions. Two em genótipos de cucurbitáceas assays were conducted, the first to evaluate the resistance to root- O objetivo desse trabalho foi prospectar fontes de resistência knot nematode, M. incognita race 1 in accessions of Lagenaria aos nematoide-das-galhas em acessos de cucurbitáceas. Foram vulgaris; Sicana odorifera; Cucurbita facifolia; Luffa sp.; Citrullus realizados dois experimentos, o primeiro para avaliar a resistência ao lanatus cv. Citroides; Lagenaria vulgaris; Cucurbita moschata; nematoide-das-galhas, M. incognita raça 1 em acessos das espécies Cucurbita moschata x Cucurbita maxima; Cucumis melo and Lagenaria vulgaris; Sicana odorífera; Cucurbita facifolia; Luffa Cucumis metuliferus. The second to evaluate the reaction to nematode sp.; Citrullus lanatus cv. Citroides; Lagenaria vulgaris; Cucurbita M. incognita race 1, M. javanica and M. enterolobii of the three moschata; Cucurbita moschata x Cucurbita máxima; Cucumis accessions of Cucumis metuliferus (‘Kino’) considered resistant to M. melo e Cucumis metuliferus. O segundo para avaliar a reação aos incognita race 1 in the first experiment. The assays were carried out nematoides M. incognita raça 1, M. javanica e M. enterolobii em três in a greenhouse at Embrapa Hortaliças in a completely randomized acessos de Cucumis metuliferus (‘Kino’) considerados resistentes design with six replications. The seedlings in pots were inoculated nd a M. incognita raça 1 no primeiro experimento. Os experimentos with 5000 eggs and juveniles of 2 stage (J2) of each Meloidogyne foram conduzidos em casa-de-vegetação na Embrapa Hortaliças, em species alone. Fifty-three and eighty-four days after inoculation, delineamento inteiramente casualizado com seis repetições. As mudas respectively in both experiments, the plants were evaluated for mantidas em vasos foram inoculadas com 5000 ovos e eventuais egg mass index (IMO), gall index (IG), number of eggs per gram juvenis de 2º estádio (J2) das espécies de Meloidogyne, isoladamente. of root (NEGR) and reproduction factor (RF). The melon Cucumis Cinquenta e três, e oitenta e quatro dias após a inoculação, para metuliferus known as ‘Kino’ was identified as genetic source of os dois experimentos respectivamente, as plantas foram avaliadas resistance to root-knot nematodes and can be explored in breeding quanto ao índice de massas de ovos (IMO), índice de galhas (IG), program as resistant rootstock. número de ovos por grama de raiz (NEGR) e fator de reprodução (FR). Verificou-se que a espécie de melão conhecida como ‘Kino’, é um recurso genético que pode ser explorado para a resistência a M. incognita raça 1, M. javanica e M. enterolobii com potencial uso como porta enxerto resistente.

Keywords: Cucurbitaceae, Meloidogyne incognita race 1, M. Palavras-chave: Cucurbitaceae, Meloidogyne incognita raça 1, M. javanica, M. enterolobii. javanica, M. enterolobii.

Received on November 6, 2018; accepted on August 9, 2019

mong the Cucurbitaceae including the occurrence of nematodes, cucurbit crops and are the most common Aspecies cultivated in Brazil are with significant losses in crops due in the world and in Brazil (Pinheiro et the squashes (Cucurbita moschata), to high infestation. Despite low al., 2011, 2013). winter squash (Cucurbita maxima), natural mobility of the nematodes, the The Meloidogyne enterolobii specie summer squash (Cucurbita pepo), constant soil turnover and movement was discovered in Brazil parasitizing watermelon (Citrullus lanatus), melon of machinery in the crop areas has guava plants in São Francisco’s region, (Cucumis melo), cucumber (Cucumis favored its spread. Root-knot nematodes located in the lower middle Bahia, sativus), gherkin (Cucumis anguria) of the genus Meloidogyne are very causing serious damage. It also has and chayote (Sechium edule) (Ferreira, destructive to all cultivated cucurbit been identified as a parasite that 2008). The intensive cultivation of species. Meloidogyne incognita, M. affects various vegetable crops in other this group of vegetables has promoted javanica and M. arenaria are the most Brazilian regions, including cucurbits the development of several diseases, important root-knot nematode species in (Damaceno et al., 2016).

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Search for resistance to root M incognita race 1. The following In both experiments, seeds of nematodes in this family for the use of genotypes were evaluated: Bottle cucurbit genotypes were sown in 1.0 genes in biotechnological events or as Gourd (Lagenaria vulgaris); Sikana L plastic pots containing substrate rootstocks becomes important. Franco (Sicana odorifera); Malabar Gourd of savanna soil, washed sand, cattle et al. (2008) and Galatti et al. (2013) Gila (Cucurbita facifolia); Loofah manure and carbonized rice straw, in identified cucurbit species as sources variety (Nova Ponte) (Luffa sp.); Pig the ratio 1:1:1:1. The first trial was sown of resistance to M. incognita and with Watermelon (Citrullus lanatus cv. on October 10, 2012 and the second on potential for grafting. Ito et al. (2014), citroides); Cabacinha (Lagenaria April 28, 2014. Six days after direct also aiming to identify resistance to M. vulgaris); CNPH 001-Phyt-90- sowing of three seeds per pot, plantlets incognita and M. javanica in accessions Phyt92-1; CNPH 042-Phyt-90; CNPH were thinned, leaving only one plant of cucurbitaceae, identified resistant 043-Phyt-90 (Cucurbita moschata); per pot. Plants were inoculated with a and compatible accessions by grafting. hybrid pumpkin (Jabras) (Cucurbita suspension df 5000 eggs and juveniles of Pinheiro et al. (2011) evaluated 13 moschata x Cucurbita maxima); Melon second stage (J2) with the nematodes in squash cultivars for M. incognita, accessions: CNPH 86-276, CNPH 1962, cucurbit roots, in 5 mL water distributed observed that all squash cultivars were CNPH 86255, CNPH 87308, CNPH in the pot, around the plant stem. susceptible; the authors highlighted the 88442, CNPH 93696, CNPH 93696, Evaluations were performed 53 and need to seek for sources of resistance in CNPH 93731, CNPH 94253, CNPH 84 days after inoculation, respectively breeding programs. Similarly Pinheiro 92571, CNPH 98307, CNPH 01-963, for the 2012 and 2014 trials. The et al. (2013) evaluated the resistance of CNPH 11-1061, CNPH 11-1075, CNPH following traits were evaluated. Egg 25 accessions of melon and pumpkins 11-1076, CNPH 01-930, Neve Melon mass index (IMO): root systems to M. incognita race 1 and found and BRS Araguaia (Cucumis melo); and washed in running water and colored by that only the access ‘Kino’ (Cucumis Melon Kino. As susceptible standard immersion in Phloxin B solution 0.5 g/L metuliferus) presented resistance. Also we used the tomato cultivar ‘Rutgers’. water for 15 minutes (Taylor & Sasser, for M. incognita, Sigüenza et al. (2005) In the second year, 3 accessions of 1978). The longer time for evaluation observed tolerance, but not resistance, ‘Kino’ were evaluated: Kino CPACT, after inoculation in the second trial was in C. moschata accessions, whereas C. Kino Bag and Kino Mendonça, necessary due to the slower development metuliferus rootstock presented little species identified as resistant in the of the nematodes, observing the roots of damage and low nematode population. first experiment, for the reaction to the susceptible Rutgers tomato control, These authors cite several examples nematodes of M. incognita race 1, probably by sowing season, with milder of grafting with cucurbit species, M. javanica and M. enterolobii. The temperatures. After that, the number for controlling Fusarium in melon, susceptibility standard was tomato of nematode egg masses was counted to increase plant vigor in melon and cultivar ‘Rutgers’ and Cucumis melo under a stereomicroscope in the root cucumber, and for the vine decline BRS Araguaia. system of each plant/replication. The disease (Monosporascus cannonballus) In both assays, females of root- IMO in the roots was obtained according in melon. Resistance to Meloidogyne knot nematode were collected from to Taylor & Sasser (1978) using a scale enterolobii was also been reported in tomato roots in the experimental area ranging from 0 to 5, where 0= roots hybrids of C. lanatus combined with of Embrapa Hortaliças; these females without egg masses; 1= 1 to 2 egg C. lanatus var. citroides (Damaceno et were previously identified by isoenzyme masses; 2= 3 to 10 egg masses; 3= 11 to al., 2016). standard (Carneiro & Almeida, 2001) 30 egg masses; 4= 31-100 egg masses The objective of this work was to and then subjected to perineal cutting and 5= over 100 egg masses. The gall prospect sources of resistance to gall to identify the species according to index (GI) was also evaluated, which is nematodes in cucurbits accessions. procedures described by Eisenback & the number of galls in each root system Hirschmann-Triantaphyllou (1991). of each plant/replication. The GI was After identification, the nematodes were represented by a scale ranging from 1 to MATERIAL AND METHODS multiplied in Rutgers tomato plants in 5, according to Taylor & Sasser (1978): a greenhouse. Meloidogyne races were 0= roots without galls; 1= 1-2 galls; 2= The experiments were conducted identified by the differentiating host test 3-10 galls; 3= 11-30 galls; 4= 31-100 in greenhouse and the evaluations according to Taylor & Sasser (1978). galls and 5= more than 100 galls. To were carried out at Embrapa Hortaliças After identification, inoculation was evaluate the number of eggs per gram Nematology Laboratory, Brasília, performed on ‘Rutgers’ tomatoes, which of roots (NEGR), at the end of the trial, Federal District, Brazil, from October were kept separately in a greenhouse the roots of all treatments were washed, to December 2012 and April to August for production and maintenance of dried at room temperature for five hours 2014, using a completely randomized the inoculum. About 45 days after and weighed before being processed design with six replications. inoculation, eggs and juveniles of according to Hussey & Barker technique Twenty-eight melon and squash second stage (J2) were extracted from (1973) modified by Bonetti & Ferraz genotypes were evaluated in the first the root systems of plants for immediate (1981). The reproductive factor (RF) of year for reaction to root-knot nematodes inoculation of the experiments. the root-knot nematode in the different

344 Hortic. bras., Brasília, v.37, n.3, July - September 2019 Prospection of genetic resistance resources to root-knot nematodes in cucurbit genotypes

genotypes was obtained by dividing Genes statistical program (Cruz, 2013). this trait was very influenced by the the final and initial population densities experimental conditions and, therefore, (RF = Pf/Pi) (Oostenbrink, 1966). We that gives a low reliability to the considered as initial population (Pi) RESULTS AND DISCUSSION estimates. Although, the other traits the inoculum, quantified and calibrated presented reduced CV, ranging from to contain 5000 eggs and juveniles of In the first trial, for all traits, 1.00 to 4.64. The melon genotype ‘Kino’ second stage (J2) nematodes per pot. significant differences were noticed presented to be resistant to M. incognita Statistical analyzes, analysis of (P=0.05) among genotypes. The race 1, meanwhile all other genotypes variance and grouping of means by coefficients of variation (CV) were were susceptible (Table 1). Scott & Knott were performed using the higher for NEGR, indicating that In the second trial, statistical

Table 1. Reaction of cucurbit genotypes to M. incognita race 1 (first trial). Brasilia, Embrapa Hortaliças, 2018. Genotypes IMO1 GI1 NEGR2 RF3 Reaction4 Bottle Gourd 3.50 c 5.00 b 731.65 a 9.78 b S Sikana 4.00 d 5.00 b 1471.02 a 8.02 b S Malabar Gourd Gila 5.00 e 5.00 b 6553.25 b 25.37 d S Loofah variety Nova Ponte 4.83 e 5.00 b 3751.36 a 18.98 c S Pig Watermelon 2.66 b 5.00 b 164.61 a 2.45 a S CNPH-001-Phyt-90, Phy92-1 5.00 e 5.00 b 17747.70 b 36.82 e S CNPH-042-Phyt-90 4.83 e 5.00 b 13781.54 b 38.48 e S CNPH-043-Phyt-90 5.00 e 5.00 b 6994.19 b 17.43 c S Jabras 5.00 e 5.00 b 2506.24 a 24.10 c S CNPH 86-276 5.00 e 5.00 b 3884.2 a 26.07 d S CNPH 1962 4.33 d 5.00 b 8979.32 b 15.48 c S CNPH 86255 4.33 d 5.00 b 1975.45 a 19.33 c S CNPH 87308 4.83 e 5.00 b 1784.88 a 9.58 b S CNPH 88442 3.50 c 5.00 b 1140.68 a 6.33 b S CNPH 93696 4.16 d 5.00 b 3649.71 a 15.23 c S CNPH 93731 3.00 b 5.00 b 4130.42 a 9.62 b S CNPH 94253 4.66 e 5.00 b 2110.19 a 16.57 c S CNPH 94254 5.00 e 5.00 b 3145.40 a 21.12 c S CNPH 98071 5.00 e 5.00 b 6895.01 b 17.75 c S CNPH 98307 5.00 e 5.00 b 4583.54 a 21.25 c S CNPH 01-963 3.66 c 5.00 b 745.90 a 7.47 b S CNPH 11-1061 4.80 e 5.00 b 5746.49 b 27.98 d S CNPH 11-1075 4.66 e 5.00 b 3793.32 a 14.40 c S CNPH 11-1076 4.50 e 5.00 b 2995.79 a 17.08 c S Kino 1.00 a 1.83 a 196.98 a 0.57 a R Neve Melon 4.16 d 5.00 b 1764.02 a 5.77 b S CNPH 01-930 5.00 e 5.00 b 98938.87 c 34.52 e S BRS Araguaia 4.50 e 5.00 b 2779.94 a 18.92 c S Rutgers 5.00 e 5.00 b 2171.39 a 11.43 b S Mean 4.34 4.89 7417.69 17.17 - CV (%) 4.64 1.00 60.37 4.04 - 1Egg and gall mass index (IMO and IG, respectively), according to Taylor & Sasser (1978). 0= roots without egg mass and/or gall; 1= roots with 1-2 egg masses and/or galls; 2= roots with 3-10 egg masses and/or galls; 3= roots with 11-30 egg masses and/or galls; 4= roots with 31-100 egg masses and/or galls; and 5= roots with more than 100 egg masses and/or galls; 2NEGR= number of eggs per gram of roots; 3RF (reproduction factor)= final population/initial population; 4Resistance reactions according to Oostenbrink (1966). I= immune (RF= 0); R= resistant (RF<1) and S= susceptible (RF>1). Means followed by same letters in the column, do not differ from each other by Scott-Knott test (p<0.05).

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Table 2. Reaction of cucurbit genotypes to M. incognita race 1, M. javanica and M. enterolobii (second trial). Brasilia, Embrapa Hortaliças, 2018. 1IMO 1IG 2NEGR 3FR 4Reaction Genotypes M. incognita race 1 Kino CPACT 5.00 b 2.17 a 142.79 a 0.08 a R Kino BAG 3.83 a 2.83 b 67.17 a 0.06 a R Kino Mendonça 4.00 a 2.67 b 60.41 a 0.03 a R BRS Araguaia 5.00 b 4.50 c 1452.26 b 1.83 b S Rutgers 5.00 b 5.00 c 1070.83 b 5.12 c S Mean 4.56 3.43 558.69 1.42 - CV (%) 2.02 5.87 47.57 14.85 - M. javanica Kino CPACT 1.67 a 1.00 a 48.41 a 0.02 a R Kino BAG 1.83 a 1.00 a 143.47 a 0.05 a R Kino Mendonça 1.83 a 1.33 a 36.57 a 0.07 a R BRS Araguaia 5.00 b 4.83 b 2142.89 b 4.25 b S Rutgers 5.00 b 5.00 b 1884.05 b 6.58 c S Mean 3.06 2.63 851.07 2.19 - CV (%) 8.38 6.57 36.57 9.25 - M. enterolobii Kino CPACT 2.83 a 2.17 b 38.69 a 0.04 a R Kino BAG 4.33 b 2.33 b 26.74 a 0.03 a R Kino Mendonça 2.33 a 1.67 a 11.76 a 0.02 a R BRS Araguaia 5.00 b 4.83 c 2857.89 c 1.28 b S Rutgers 5.00 b 4.33 c 554.24 b 1.87 c S Mean 3.90 3.06 697.86 0.64 - CV (%) 7.70 7.38 90.76 13.37 - 1Egg and gall mass index (IMO and IG, respectively), according to Taylor & Sasser (1978). 0= roots without egg mass and/or gall; 1= roots with 1-2 egg masses and/or galls; 2= roots with 3-10 egg masses and/or galls; 3= roots with 11-30 egg masses and/or galls; 4= roots with 31-100 egg masses and/or galls; and 5= roots with more than 100 egg masses and/or galls; 2NEGR= number of eggs per gram of roots; 3RF (reproduction factor)= final population/initial population; 4Resistance reactions according to Oostenbrink (1966). I= immune (FR= 0); R= resistant (FR<1) and S= susceptible (FR>1). Means followed by same letters in the column do not differ from each other by Scott-Knott test (p<0.05). significance was observed (P=0.05) in to this species, emphasizing the need presented little damage and a low all traits on the evaluated genotypes. of resistance sources against root- nematode population. The authors In the same way as in the first assay, knot nematode in squash breeding pointed that high prices and restrictions the coefficients of variation (CV) were programs. Similarly, Pinheiro et al. of nematicides in grafting could become higher for NEGR in the evaluation of (2013) evaluated the resistance of an economically viable method for the all nematode species. We also observed 25 melon and pumpkin accessions control of root-knot nematodes. The the resistance of ‘Kino’ melon for the to Meloidogyne incognita race 1 and results obtained for C. metuliferus by three evaluated accessions and for observed that only the accession ‘Kino’ Sigüenza et al. corroborate the results three species of root-knot nematodes presented resistance. obtained in our study, where a low (Table 2). This fact confirms that ‘Kino’ Sigüenza et al. (2005) evaluated reproduction factor was observed for melon is a potential genetic resource of the use of Cucurbita moschata and both experiments and nematode species resistance against root-knot nematode Cucumis metuliferus as rootstocks (Tables 1 and 2). species. for the management of Meloidogyne Franco et al. (2008) studied Pinheiro et al. (2011) evaluated incognita, and verified thatC. moschata the reaction to M. incognita of 16 the behavior of 13 commercial squash rootstocks inoculated with the nematode Cucurbitaceae genotypes with potential cultivars for resistance to Meloidogyne were tolerant but not resistant. The for grafting with muskmelon. The incognita race 1 and all were susceptible inoculated C. metuliferus rootstock genotypes were evaluated based on

346 Hortic. bras., Brasília, v.37, n.3, July - September 2019 Prospection of genetic resistance resources to root-knot nematodes in cucurbit genotypes the reproduction factor being observed lanatus), were resistant to M. incognita. BRAZ, LT. 2008. Avaliação de genótipos that the loofah, pumpkin ‘Goianinha’, The best compatibility occurred with de cucurbitáceas quanto à resistência à Meloidogyne incognita. Horticultura pumpkin ‘Mini Paulista’, melon the “Canary Melon” rootstocks, which Brasileira 26: S3650-3654. ‘Redondo Amarelo’ and watermelon had 100% establishment, followed by FERREIRA, MAJF. 2008. Abóboras e morangas. Charleston Gray were resistant the pumpkin ‘Mini Paulista’ with 94%. In: BARBIERI, RL; STUMPF, ERT. Origem genotypes. Loofah, watermelon ‘Charleston Gray’ e evolução de plantas cultivadas. Brasília: Embrapa Informação Tecnológica, p.59-88. and pumpkin ‘Goianinha’ had low Ito et al. (2014) evaluated 33 GALATTI, FS; FRANCO, AJ; ITO, LA; cucurbit accessions to the nematodes M. establishment percentages: 66%, 62% CHARLO, HO; GAION, LA; BRAZ, LT. incognita and M. javanica and verified and 50% respectively. 2013. Rootstocks resistant to Meloidogyne Thus, we concluded that the species incognita and compatibility of grafting in net that melon genotypes CNPH 01-930, melon. Revista Ceres 60: 432-436. CNPH 01-962, CNPH 01-963, ‘Redondo ‘Kino’ is a genetic resource that can be HUSSEY, RS; BARKER, KR. 1973. A Gaucho’ and Wax Gourd (Benincasa exploited for resistance to the root-knot comparison of methods of collecting inocula of hispida) were considered resistant to nematodes M. incognita race 1, M. Meloidogyne spp. Including a new technique. M. incognita with reproduction factors javanica and M. enterolobii. Plant Disease Reporter 57: 1025-1028. ITO, LA; GAION, LA; GALATTI, FS; BRAZ, less than 1 (FR<1); ‘Redondo Amarelo’ LT; SANTOS, JM. 2014. Resistência de melon, ‘Charleston Gray’ watermelon, porta-enxertos de cucurbitáceas a nematóides ‘Coréia’ progeny (Citrullus lanatus), REFERENCES e compatibilidade da enxertia em melão. and Trichosanthes cucumerins, were Horticultura Brasileira 32: 297-302. OOSTENBRINK, M. 1966. Major characteristics resistant to M. javanica. Benincasa BONETTI, JIS; FERRAZ, S. 1981. Modificações of the relation between nematodes and plants. hispida was resistant to both species. do método de Hussey & Barker para extração Mededelingen Landbouw 4: 1-46. Grafting compatibilities between de ovos de Meloidogyne exigua em raízes de PINHEIRO, JB; AMARO, GB; CARVALHO, cafeeiro. Fitopatologia Brasileira 6: 553p. resistant rootstocks and muskmelons ADF; SOUSA, NYC. 2011. Reação de CARNEIRO, RMDG; ALMEIDA, MRA. 2001. cultivares de abóboras a Meloidogyne were greater than 98%. However, the Técnica de eletroforese usada no estudo incognita raça 1. In: Anais do 6º Congresso classification of melon accessions de enzimas dos nematoides de galhas para Brasileiro de Melhoramento de Plantas. CNPH 01-930, CNPH 01-962, CNPH identificação de espécies. Nematologia Resumo expandido. 4p. CD ROM. 01-963 to be resistant to M. incognita Brasileira 25: 35-44. PINHEIRO, JB; RODRIGUES, CS; PEREIRA, RB; AMARO, GB; OLIVEIRA, VR; differ from the results of this study, CRUZ CD. 2013. Genes: a software package for analysis in experimental statistics and CARVALHO, ADF. 2013. Reação de which were considered susceptible. quantitative genetics. Acta Scientiarum Cucurbitáceas a Meloidogyne incognita raça In a similar study, Galatti et al. Agronomy 35: 271-276. 1. In: Anais do 7º Congresso Brasileiro de Melhoramento de Plantas. Uberlândia-MG. (2013) evaluated 16 cucurbit accessions DAMACENO, LS; QUEIROZ, MA; DIAS, RCS; CASTRO, JMC; TEIXEIRA, FA. 2016. p. 952-955. for M. incognita and performed a graft Avaliação de parentais e F1s em melancia SIGÜENZA, C; SCHOCHOW, M; TURINI, compatibility study with a muskmelon quanto à reação ao Meloidogyne enterolobii. T; PLOEG, A. 2005. Use of Cucumis cultivar and found that the genotypes Revista Caatinga 29: 296-304. metuliferus as a rootstock for melon to manage Meloidogyne incognita. Journal of loofah (Luffa cylindrica), pumpkin EISENBACK, JD; HIRSCHMANN- Nematology 37: 276-280. ‘Goianinha’ and pumpkin ‘Mini TRIANTAPHYLLOU, H. 1991. Root-knot TAYLOR, A; SASSER, JN. 1978. Biology, nematodes: Meloidogyne species and races. identification and control of root-knot Paulista’ (Cucurbita moschata ), melon In: WR, NICKLE (ed). Manual of Agricultural ‘Redondo Amarelo’ (Cucumis melo), nematodes (Meloidogyne species). USA: Nematology, New York. p.191-274. North Caroline State University Graphics. Charleston Gray watermelon (Citrullus FRANCO, AJ; CHARLO, HCO; GALATTI, FS; 111p.

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