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Cucurbit Grafting Angela R. Davis a; Penelope Perkins-Veazie a; Yoshiteru Sakata b; Salvador López-Galarza c; Jose Vicente Maroto c; Sang-Gyu Lee d; Yun-Chan Huh d; Zhanyong Sun e; Alfredo Miguel f; Stephen R. King g; Roni Cohen h; Jung-Myung Lee i a United States Department of Agriculture, Agricultural Research Service, South Central Agricultural Research Laboratory, P.O. Box 159, Hwy 3 West, Lane, OK, U.S.A b National Institute of Vegetable and Tea Science, Kusawa-360, Ano, Tsu, Japan c Departamento de Producción Vegetal, ETSIA, Universidad Politécnica de Valencia, Co de Vera s/n, Valencia, Spain d National Horticultural Research Institute, Rural Development Administration, Suwon, Rep. of Korea e AVRDC-The World Vegetable Center, P.O. Box 42, Shanhua, Tainan, Taiwan f Instituto Valenciano de Investigaciones Agrarias, Apartado Oficial, Moncada, Valencia, Spain g Vegetable and Fruit Improvement Center, Department of Horticultural Sciences, Texas A&M University, College Station, TX, U.S.A h ARO, Newe Ya'ar Research Center P.O. Box 1021, Ramat Yishay, Israel i Dept. of Horticulture, Kyung Hee University, Suwon, Rep. of Korea

Online Publication Date: 01 January 2008

To cite this Article Davis, Angela R., Perkins-Veazie, Penelope, Sakata, Yoshiteru, López-Galarza, Salvador, Maroto, Jose Vicente, Lee, Sang-Gyu, Huh, Yun-Chan, Sun, Zhanyong, Miguel, Alfredo, King, Stephen R., Cohen, Roni and Lee, Jung- Myung(2008)'Cucurbit Grafting',Critical Reviews in Plant Sciences,27:1,50 — 74 To link to this Article: DOI: 10.1080/07352680802053940 URL: http://dx.doi.org/10.1080/07352680802053940

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Angela R. Davis,1 Penelope Perkins-Veazie,1 Yoshiteru Sakata,2 Salvador L´opez-Galarza,3 Jose Vicente Maroto,3 Sang-Gyu Lee,4 Yun-Chan Huh,4 Zhanyong Sun,5 Alfredo Miguel,6 Stephen R. King,7 Roni Cohen,8 and Jung-Myung Lee9 1United States Department of Agriculture, Agricultural Research Service, South Central Agricultural Research Laboratory, P.O. Box 159, Hwy 3 West, Lane, OK 74555, U.S.A. 2National Institute of Vegetable and Tea Science, Kusawa-360, Ano, Tsu, Mie 514-2392, Japan 3Departamento de Produccion´ Vegetal, ETSIA, Universidad Politecnica´ de Valencia, Co de Vera s/n 46022 Valencia, Spain 4National Horticultural Research Institute, Rural Development Administration, Suwon 441-440, Rep. of Korea 5AVRDC-The World Vegetable Center, P.O. Box 42, Shanhua, Tainan, 74199, Taiwan 6Instituto Valenciano de Investigaciones Agrarias, Apartado Oﬁcial, 46113 Moncada, Valencia, Spain 7Vegetable and Fruit Improvement Center, Department of Horticultural Sciences, Texas A&M University, College Station, TX 77843, U.S.A. 8ARO, Newe Ya’ar Research Center P.O. Box 1021, Ramat Yishay, 30095, Israel 9Dept. of Horticulture, Kyung Hee University, Suwon 449-701, Rep. of Korea

Table of Contents

I. CUCURBIT GRAFTING ...... 51 A. Introduction ...... 51 B. History ...... 52 C. Current Status ...... 53 D. Concerns Associated with Grafting ...... 53 E. Economic Feasibility ...... 53

II. WHY GRAFT CUCURBITS? ...... 54 A. Disease Control ...... 54 B. Cold/Heat Tolerance ...... 56 C. Wet/Flood/Drought/Salinity Tolerance ...... 56 D. Increased Efﬁciency of Land Usage ...... 56 Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 E. Effect of Grafting on Flowering and Harvest ...... 56 F. Nutrient Uptake ...... 57

III. PLANT PHYSIOLOGY ...... 57 A. Scion and Rootstock Physiology ...... 58 B. Vigor and Shape ...... 58 C. Yield and Size ...... 58 D. Quality ...... 59

IV. WHAT CUCURBITS ARE GRAFTED ...... 60 A. Watermelon ...... 60 B. Cucumber ...... 60

Address correspondence to Angela R. Davis, United States Department of Agriculture, Agricultural Research Service, South Central Agri- cultural Research Laboratory, P.O. Box 159, Hwy 3 West, Lane, OK 74555, U.S.A. E-mail: [email protected].

50 CUCURBIT GRAFTING 51

C. Melons ...... 61 D. Bitter Gourd ...... 61 E. Summer Squash ...... 61 F. Chinese Snake Gourd ...... 61 G. Commonly Used Rootstocks ...... 61

V. GRAFTING METHODS ...... 62 A. Tongue Approach/Approach Graft ...... 64 B. Hole Insertion/Terminal/Top Insertion Graft ...... 64 C. One Cotyledon/Slant/Splice/Tube Graft ...... 65 D. Cleft/Side Insertion Graft ...... 65 E. Pin Graft ...... 66 F. Double Graft ...... 66 G. Root Pruning ...... 66 H. Automated Graft ...... 66 I. Acclimatization ...... 67 J. Production of Rootstock and Scion ...... 67 K. Compatibility ...... 67

VI. CONCLUSION ...... 68

ACKNOWLEDGEMENTS ...... 68

REFERENCES ...... 68

option. Some seed companies now offer watermelon transplants Due to limited availability of arable land and high market de- grafted onto squash or bottle gourd rootstocks, and some trans- mand for off-season vegetables, cucurbits (plants in the family Cu- plant facilities offer grafting services. There have been thorough curbitaceae) are continuously cultivated under unfavorable condi- analyses of cucurbit grafting in other countries, but the literature tions in some countries. These conditions include environments that in English is limited. This review summarizes the state of the cucur- are too cold, wet, or dry, or are cool low-light winter greenhouses. bit grafting industry on a global level, translating work published Successive cropping can increase salinity, the incidence of cucurbit in many languages. pests, and soilborne diseases like fusarium wilt caused byFusarium spp. These conditions cause various physiological and patholog- Keywords Cucurbitaceae, watermelon, cantaloupe, cucumber, meth- ical disorders leading to severe crop loss. Chemical pest control ods, quality, yield

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 is expensive, not always effective, and can harm the environment. Grafting can overcome many of these problems. In fact, in many parts of the world, grafting is a routine technique in continuous cropping systems. It was first commonly used in Japan during the I. CUCURBIT GRAFTING late 1920s by grafting watermelon [Citrullus lanatus (Thunb.) Mat- sum. and Nakai] onto pumpkin [Cucurbita moschata Duchesne ex. A. Introduction Poir] rootstocks. Soon after, watermelons were grafted onto bottle The phase-out of methyl bromide fumigation drives the gourd [Lagenaria siceraria (Molina) Standl.] rootstocks. This prac- search for alternative methods of soilborne pathogen control in tice helped control declining yield due to soilborne diseases. China produces more than half the world’s watermelons and cucumbers vegetables. Although alternative pesticides and other physical (Cucumis sativus L.), and approximately 20% of these are grafted. treatments are being tested and developed, grafting with resis- Use of rootstocks can enhance plant vigor through vigorous attain- tant rootstocks offers one of the best methods to avoid soilborne ment of soil nutrients, avoidance of soil pathogens and tolerance of diseases. Additionally, grafting can affect vegetative growth, low soil temperatures, salinity, and wet-soil conditions. The type of flowering, fruit ripening date and quality, and provide higher rootstock affects cucurbit plant growth, yield, and fruit quality. Cu- curbit grafting is rare in the United States, but with continued loss yields, especially under low-temperature conditions. of quality disease-free farmland along with the phase-out of methyl Rootstock-scion combinations reportedly affect pH, flavor, bromide, the U.S. cucurbit industry sees grafting as an attractive sugar, color, carotenoid content, and texture of fruit. As early 52 A. R. DAVIS ET AL.

as 1949, Imazu recommended Cucurbita moschata as a root- TABLE 1 stock, since it confers resistance to fusarium wilt and improves Common and scientific names of crops used in this review and plant vigor. He noted however, that this rootstock caused in- names of commonly used cultivars and their scientific names ferior texture and flavor in grafted ‘Honey Dew’ (Cucumis melo var. inodorus) fruits. Fortunately, these quality effects Common name Scientific name are not always negative. Some rootstock-scion combinations African horned cucumber Cucumis metuliferus increase flesh firmness, along with sugar and lycopene con- Armenian cucumber, Cucumis melo var. flexuosus tent in watermelon (Davis and Perkins-Veazie, 2005). This snake melon study demonstrated that quality traits can be improved by Bitter gourd, bitter melon Momordica charantia selecting rootstock-scion combinations that complement each Bottle gourd Lagenaria siceraria other. Burr cucumber Sicyos angulatus It is not surprising that rootstocks have such a drastic impact Cantaloupe Cucumis melo L. var. on the scion and scion fruit, because they can enhance plant cantaloupensis vigor, improve disease resistance, improve tolerance of low soil Chinese snake gourd Trichosanthes kirilouii temperatures and/or salinity, and improve attainment of soil nu- Cucumber Cucumis sativus trients and water. Additionally, studies have shown that RNA, Figleaf gourd Cucurbita ficifolia protein, and small molecules, some causing signal transduction, Luffa Luffa cylindrica can translocate from the rootstock to the scion, directly affecting Melon Cucumis melo L. scion physiology. Muskmelon, netted melon Cucumis melo var. reticulatus Researchers in some countries have examined cucurbit graft- Oriental melon Cucumis melo L. ing for decades, but most of this information has not been trans- Oriental pickling melon Cucumis melo var. conomon lated into English. This review combines information on cu- Pumpkin Cucurbita maxima curbit grafting history, methods, disease resistance, and quality Pumpkin Cucurbita moschata issues. Reports are summarized from many countries and non- Pumpkin, summer squash Cucurbita pepo English sources. Table 1 lists the cultivars and species mentioned Squash Cucurbita spp. throughout this article with their common name for reference. Squash interspecific hybrid Cucurbita maxima x Cucurbita This timely review of cucurbit grafting provides a summary of moschata existing research as the U.S. searches for alternatives to methyl Watermelon Citrullus lanatus bromide for soilborne pathogen control. Wax gourd Benincasa hispida Winter melon, honeydew Cucumis melo var. inodorus B. History Cultivar name Scientific name Research on cucurbit grafting began in the 1920s with the ‘Bloomless’ Cucumis sativus use of Cucurbita moschata as a rootstock for watermelon. Ini- ‘Earl’s Favorite’ Cucumis melo L. var. tial reports by Tateishi (1927) and Sato and Takamatsu (1930) cantaloupensis described several studies and grafting applications at Kyusyu ‘Galia’ Cucumis melo var. saccharinus University. Tateishi (1931) reported on grafting of watermelon ‘Honey Dew’ Cucumis melo var. inodorus onto Cucurbita moschata rootstocks, a technique that was well ‘Shin-tosa’ Cucurbita maxima x Cucurbita known at the time. However, bottle gourd and wax gourd [Ben- moschata

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 incasa hispida (Thunb.) Cogn.] became preferred rootstocks for watermelon grafting on account of their resistance to fusarium wilt, their high affinity for watermelon, and the highly stable growth of the plants after grafting (Sato and Takamatsu, 1930; cumis melo.L.var.conomon Makino) (Konno, 1919), makuwa Matsumoto, 1931; Tateishi, 1931; Kijima, 1933; Murata and melon (Cucumis melo var. makuwa Makino) (Jhoya, 1938), and Ohara, 1936; Kijima, 1938). ‘Earl’s Favorite’ (Cantalupensis Group) (Tanaka, 1942) neces- Pumpkin and squash (Cucurbita moschata, Cucurbita max- sitated grafting of these cultivars onto resistant rootstocks. Mat- ima Duchense ex. Lam., Cucurbita pepo L.), figleaf gourd sumoto (1931) reported that Cucurbita spp. and melon are com- (Cucurbita ficifolia Bouché), cucumber, and bottle gourd were patible with cucumber, and Imazu (1949) noted that Cucurbita reported as compatible with cantaloupe (Cucumis melo L. var. moschata, bottle gourd, wax gourd, and luffa [Luffa cylindrica cantalupensis)in1931 by Matsumoto. Compared to water- (L.) M. Roem.] were also compatible with cucumber. melon, progress on melon grafting (Cucumis melo L.) in Japan Cucumber grafting started in Japan around 1960 to strengthen was slow, since oriental melons (Cucumis melo L.) are rela- low-temperature tolerance and fusarium wilt resistance (Fujieda, tively tolerant to soilborne diseases. However, the occurrence 1994). Following the advances by Ishibashi (1959; 1963), which and spread of fusarium wilt in pickling melon ‘Etsu-uri’ (Cu- led to improved grafting techniques and the incubation of grafted CUCURBIT GRAFTING 53

seedlings, grafting cucumber became common in Japan in the Spain grows around 30 million grafted watermelon plants, 1960s (Sakamoto, 1965). approximately 50% of their crop (Hoyos, 2004). Twenty mil- Around the same time, grafting was explored in Europe. In lion watermelon and 5 to 6 million melon plants are grafted in France, research on cucurbit grafting started in the 1950s, with Italy (Amadio, 2004) annually. the grafting of cucumber and melon scion onto figleaf gourd Grafting is considered a good alternative to methyl bromide to control fusarium wilt. During the 1960s melon plants were for controlling cucumber soilborne diseases in Greece (Pavlou grafted onto Benincasa spp., to offset the effects of low soil et al., 2002). The United Nations Industrial Development Orga- temperatures in early greenhouse grown melons (Alabouvette nization (UNIDO) recently equipped Honduras and Guatemala et al., 1974; Louvet, 1974; CTIFL, 1985). In Spain, research on with 60,000 m2 of specialized greenhouses to produce 30 million grafted melon and watermelon started in 1976 and was com- grafted watermelon and melon plants. These greenhouses are ca- mercialized there by the end of the 1980s, concomitant with the pable of supplying 30% of the melon transplants in both coun- spread of commercial nurseries (Miguel, 1986; Garc´ıa-Jiménez tries (Amadio, 2004). It is estimated that approximately 2,000 et al., 1990; Miguel, 1993). Cucumber grafting in Spain be- ha of watermelon and 500 ha of melon are grown with grafted gan in the mid-1990s, but is increasing in importance (Hoyos, plants in Honduras, and 1,000 ha of grafted watermelon and 50 2001). ha of grafted melon are grown in Guatemala (Camacho, 2007). At the end of the 1980s melon and watermelon grafting exper- Morocco, Mexico, Cuba, and the U.S. have recently started look- iments were performed in Italy (Trentini and Maiolli, 1989). This ing at grafting as a viable option for cucurbit crops (Besri, 2004; technology was again introduced during the 1996–97 season as Pérez-Montesbravo, 2004), but at least 250 ha of grafted wa- a methyl bromide alternative (Leoni et al., 2004). termelon were planted in 2007 for the U.S. market (Chadwell, 2007) and approximately 1,000 ha of grafted watermelon and C. Current Status 100 ha of grafted melon are grown in Mexico (Camacho, 2007). In 1998, approximately 95% of watermelon and oriental mel- Ma (2008) estimated that about 10–20% of China’s watermelons ons were grafted onto squash or gourd rootstocks in Japan, Ko- are grafted (about 2-3M ha.). rea, and Taiwan (Lee and Oda, 2003). Table 2 demonstrates the latest statistics on cucurbit grafting volume and the percent of D. Concerns Associated with Grafting cucurbits grafted in multiple countries. France and Spain cur- The main problems associated with grafting are the time rently raise approximately 1% to 3% of their melon and cu- and labor required, cost, rootstocks rendered ineffective by oc- cumber crops using grafted plants (Erard, 2004; Hoyos, 2004). currence of newly migrated soilborne diseases or pests, and changes in fruit quality. Grafted seedlings are more expensive TABLE 2 than nongrafted seeds and seedlings. It is difficult for farmers to The most recent published data for amount of area under provide the intensive care required to raise newly grafted plants, cultivation of select cucurbit crops and percentages of total often requiring the added cost of a transplant facility that has crop grafted within stated country healing chambers and trained personnel. Changes in resistance to diseases or pests must be taken into Area under Grafted seedlings account as well as changes in fruit quality, which occur with cultivation used (%) some rootstocks. These problems should be regarded as impor- Country Crop (ha) Estimated values tant research topics, given that grafting cultivation is an indis- South Korea Watermelon 23,179 98 pensable production technique for sustainable agriculture. They

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 South Korea Cucumber 5,853 95 are mentioned in detail below. South Korea Oriental melon 7,077 95 France Melons not reported 1–3 E. Economic Feasibility France Cucumber not reported 1–3 The labor required, and the high cost of grafted seedlings Spain Melons not reported 1–3 make cucurbit grafting expensive. It is difficult for farmers Spain Cucumber not reported 1–3 who wish to perform the grafting to maintain adequate hu- Honduras Watermelon 2,000 not reported midity and low light levels while grafted plants heal. How- Honduras Melons 500 not reported ever, since some transplant facilities now offer grafting services Guatemala Watermelon 1,000 not reported and with improved grafting techniques and mechanization, pur- Guatemala Melons 50 not reported chase of grafted seedlings is becoming more affordable. Grafted United States Watermelon 250 not reported seedlings are more expensive than non-grafted seedlings, re- Mexico Watermelon 1,000 not reported flecting the cost of the rootstock seeds, which are often F hy- Mexico Melons 100 not reported 1 brids or triploids. There are added costs involved in the grafting Source: Erard, 2004; Hoyos, 2004; Camacho, 2007; Chadwell, 2007, operation: raising the grafted seedlings, and transporting them Huh, 2007. to growers’ fields (Taylor et al., 2006). Additionally, grafting 54 A. R. DAVIS ET AL.

decreased the transplant survival rate by up to 60% in high- and there are additional claims of improved tolerance to some wind conditions. The resultant loss of transplants and the need foliar fungal and viral pathogens. for replanting greatly increases the cost of grafting in high-wind Fusarium wilt, caused by Fusarium oxysporum Schltdl., is areas (Davis and King, 2005; King and Davis, 2006). probably the most common and damaging soilborne disease In Japan, grafted seedlings are almost four times the cost of cucurbit crops worldwide. Grafting for fusarium resistance of seeds (0.4 US dollars per seed vs. 1.6 U.S. dollars per started in Japan in the 1920s to control F. oxysporum f. sp. grafted seedling) (Sakata, 2008). In the U.S. grafted seedless niveum Snyder & Hansen. The first rootstock used for water- watermelon transplants cost $1,743 more per hectare than non- melon were Cucurbita moschata,but bottle gourd soon became grafted seedless plants (Taylor et al., 2006). That is a differ- the preferred rootstock (Tateishi, 1927; Sato and Takamatsu, ence of around $0.50, or three times more per grafted plant. In 1930; Kijima, 1933; Murata and Ohara, 1936; Sakata et al., Spain, grafting costs are 0.25–0.35 Euros per plant, not including 2007). Possibly because of the widespread use of bottle gourd seed cost. This cost is similar in other Mediterranean countries rootstocks, there were reports of Fusarium spp. isolated from (López-Galarza, 2008). infected roots (Sato and Ito, 1962), which was later identified as F. oxysporum f. sp. lagenariae Matsuo & Yamamoto (Sakata et al., 2007). Selection for fusarium wilt resistance in bottle II. WHY GRAFT CUCURBITS? gourd rootstocks, and the adoption of squash interspecific hy- The primary motive for grafting cucurbits is to avoid damage brids (Cucurbita maxima × Cucurbita moschata) that demon- caused by soilborne pests and pathogens when genetic or chem- strate immunity to fusarium wilt, has prevented the reoccurrence ical approaches for disease management are not available (Oda, of this resistance breakdown. Additional rootstocks were identi- 2002a;b). Grafting a susceptible scion onto a resistant rootstock fied that confer high levels of fusarium resistance, including Cit- can provide a resistant cultivar without the prolonged screening rullus spp. (Huh et al., 2002) and several different Cucumis spp. and selection required to breed resistance into a cultivar. Further- and Cucurbita spp. (Igarashi et al., 1987; Trionfetti-Nisini et al., more, grafting allows rapid response to new pathogen races, and, 1999; Hirai et al., 2002). Use of these rootstocks has controlled in the short-term, provides a less expensive and more flexible fusarium wilt in cucumber (Komada and Ezuka, 1974; Pavlou, solution for controlling soilborne diseases than breeding new re- 2002; Tjamos et al., 2002), melon (Imazu, 1949; Bletsos, 2005; sistant cultivars. In addition, grafting may enhance tolerance to Xu et al., 2005c) and bitter gourd (Momordica charantia L.) abiotic stresses, increase yield, and result in more efficient water (Lin et al., 1998), in addition to watermelon. Grafting to control and nutrient use; extend harvest periods, and improve fruit yield fusarium wilt in watermelon and cucumber is a common prac- and quality (Shimada and Moritani, 1977; Romero et al., 1997; tice, but it is less common in melon. Control of F. oxysporum Oda, 2002a;b; Trionfetti-Nisini et al., 2002; Lee and Oda, 2003; f.sp. melonis Snyder & Hansen in melon has traditionally been Rivero et al., 2003, Hang et al., 2005). Rootstocks can also accomplished using host plant resistance (or “resistant culti- influence temperature tolerance, moisture extremes (drought, vars”) making grafting unnecessary (NIVOT, 2001; Yoshioka, flooding), and salt stress (Matsubara, 1989). 2001). However, with the increased prevalence of race 1,2, graft- A. Disease Control ing gives an economic advantage wherever race 1,2 is endemic In the U.S., crop rotation has been effective for cucurbit pest (Hirai et al., 2002; Trionfetti-Nisini et al., 2002). control for many years. However, many soilborne pathogens can A recent report showed that grafting melon onto squash inter- survive in the soil for up to 10 or more years without a host, lim- specific hybrids can provide resistance not only to F. oxysporum iting the effectiveness of rotation for some diseases. Fumigation f. sp. melonis race 1,2, but also to Didymella bryoniae (Fuckel) is effective at controlling persistent soilborne diseases, but the Rehm, the causal agent of gummy stem blight (Crino et al., Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 phase-out of methyl bromide as a soil fumigant has made the 2007). It was pointed out that while gummy stem blight is typi- search for alternatives necessary. In intensive farming regions, cally considered a foliar disease, D. bryoniae is a soil-inhabiting such as Asia and Europe, managing the potential buildup of soil fungus, and one of the primary sources of infection is through pathogens is a primary concern. Europe adopted methyl bro- the crown. It was speculated that providing resistant rootstock mide to control soilborne pathogens; while many parts of Asia on susceptible scions prevents primary sources of infection, re- used grafting for this purpose. Since the phase-out of this fu- sulting in reduced disease incidence. migant, grafting emerged as an effective alternative for cucurbit Monosporascus vine decline, caused by the soilborne crop production in Europe. In the U.S., however, grafting has not pathogen Monosporascus cannonballus Pollack & Uecker, is emerged as a viable alternative. One reason may be that methyl a serious melon disease that, in some regions, surpasses fusar- bromide continues to receive critical use exemptions for cucurbit ium wilt in pervasiveness (Lobo, 1990; Buzi et al., 2002; Fer- and solanceous crops (King et al., 2008). Most grafting litera- rer, 2003). It can also cause significant watermelon disease as ture on soilborne diseases comes from studies conducted in the well (Garc´ıa-Jiménez et al., 1994; Gennari et al., 1999; Buzi Mediterranean region and Southeast Asia. It has been reported et al., 2004). Host plant resistance to monosporascus vine de- that grafting can improve resistance or tolerance to more than ten cline has yet to emerge as a viable option, and with reduced different fungal, bacterial, and nematode soilborne pathogens, chemicals available, grafting is part of an integrated approach CUCURBIT GRAFTING 55

to controlling this disease. Disease incidence on grafted plants rotiodes isolates have been identified that infect watermelon and is not as predictable for monosporascus vine decline compared commonly used watermelon rootstocks (Shishido et al., 2006), to fusarium wilt resistance; however, grafting alone will reduce black root rot may become a problem on watermelon and pump- disease severity depending on the rootstock / scion combina- kin in the future. Summer cucumber production was complicated tion, time of year, and primary inoculum levels (Edelstein et al., by severe damage by P. sclerotiodes when Cucurbita moschata 1999; Cohen et al., 2005). The reason for these variable re- rootstocks were used in Northern regions of Japan (Shishido sults appears to be lack of true resistance in melon rootstocks et al., 2006). to M. cannonballus. These rootstocks are instead tolerant of ‘Bloomless’ rootstocks alter several characteristics of grafted the pathogen; their large root systems and the vigor afforded cucumbers, including their susceptibility to plant diseases. These the scion allows for crop development in the presence of this rootstocks caused increased powdery mildew damage (Po- pathogen (Cohen et al., 2000). Grafting along with additional dosphaera xanthii [Castagne] U. Braun & N. Shishkoff) and control strategies to reduce pathogen populations appears to be Corynespora leaf spot (Corynespora cassicola (Berk. & M. A. akey factor in reducing the disease severity of monosporascus Curtis) C. T. Wei) on cucumber scions (Hasama, 1992; Hasama vine decline. Watermelon tolerance to this disease has improved et al., 1993). through grafting onto tolerant rootstocks (Peris, 2004). Root knot nematodes can cause serious disease in cucurbit Phytophthora blight, caused by Phytophthora capsici Leo- crops. Grafting reduced nematode gall formation in cucumber nian, is a serious threat to cucurbit production worldwide. Cu- (Giannakou and Karpouzas, 2003), watermelon (Miguel et al., cumber, melon, watermelon, pumpkin, and squash are suscep- 2005), and melon fields (Siguenza et al., 2005). In some cases, tible, and the host range includes 49 different plant species the rootstocks appear to provide tolerance by providing extensive (Babadoost, 2005). Identification of genetic resistance to this root area and vigor (Giannakou and Karpouzas, 2003; Miguel disease has proven difficult, but certain rootstocks appear to be et al., 2005), but some rootstocks have genetic resistance that more tolerant than others. Takahashi and Kawagoe (1971) found is exhibited in the grafted plants (Hagitani and Toki, 1978; that certain rootstocks reduced phytophthora blight on cucum- Siguenza et al., 2005; Gu et al., 2006). bers, and Wang et al. (2004) showed improved cucumber toler- Increased tolerance to viral complexes (CMV, WMV-II, ance to this disease through grafting. It is probable that improved PRSV, and ZYMV) of grafted seedless watermelons compared tolerance to phytophthora blight is all grafting can achieve, since to nongrafted controls was reported by Wang et al. (2002). An- no cucurbit compatible rootstock with genetic resistance for P. other report demonstrated that grafted melon plants had im- capsici has been reported (Babadoost, 2005). The best control proved tolerance to Melon Necrotic Spot Virus (MNSV) (Wang option at present is to combine grafting with tolerant rootstocks et al., 2002). Similarly, in grafted tomato, plants were more tol- with cultural practices to mitigate disease pressure. erant to Tomato Yellow Leaf Curl Virus (Rivero et al., 2003). Verticillium dahlia Kleb. is another common soilborne It is presumed that the increased tolerance is due to increases pathogen that affects cucurbit crops in many regions. Grafting in vigor, photosynthesis, chlorophyll content, and/or peroxidase for control of verticillium wilt was studied for cucumber, melon, activity associated with the grafted plants. and watermelon (Alabouvette et al., 1974; Paplomatas et al., Two reports claim increased viral susceptibility of grafted 2002). While immunity to V . dahlia was not found in any root- cucurbits compared to nongrafted plants. Iwasaki et al. (1996) stocks, some were tolerate, and grafting onto these rootstocks reported grafted cucumbers to be more susceptible to certain can delay expression of disease for up to 20 days (Paplomatas combinations of viral infection, such as Cucumber Mosaic et al., 2002). This delay, when combined with additional control Virus (CMV), Watermelon Mosaic Virus II (WMV-II), Papaya strategies, will likely result in effective control of verticillium Ringspot Virus (PRSV), and Zucchini Yellows Mosaic Virus Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 wilt. While few reports demonstrate the effectiveness of combin- (ZYMV). These specific viral combinations caused severe wilting grafting with other control methods in cucurbit crops, high ing in grafted plants when compared to nongrafted controls. levels of control have been achieved in eggplant when grafting Boubourakas et al. (2004) reported one instance in which grafted was combined with soil treatments designed to lower inoculum watermelon was infected by Cucumber Green Mottle Mosaic pressure (Ioannou, 2001). Virus (CGMMV), while nongrafted plants were asymptomatic. Phomopsis sclerotiodes Kesteren commonly causes black Possible mechanisms explaining an increase in susceptibility to root rot in greenhouse-grown cucumbers (Cappelli et al., 2004), viruses have not been investigated. It is possible that a lack of and has also been shown to cause disease in melon, pump- graft compatibility weakens the scion, making grafted plants kin, bottle gourd and watermelon (Shishido et al., 2006). The more susceptible to viral infection, or plants could be infected pathogen can survive in soil and soil-less media and even on during the grafting operation. It will be interesting to determine plastic containers, making control difficult. Grafting was shown if new virus-resistant rootstocks, such as Ling and Levi’s (2007) to be an effective control measure for greenhouse grown cucum- ZYMV-Florida strain-resistant bottle gourd rootstocks will con- bers, even surpassing chemical control treatments in some in- fer virus resistance to the scion. stances (Wiggell and Simpson, 1969), as long as highly resistant Disease-resistance mechanisms afforded by grafting are not rootstocks were used (Alabouvette et al., 1974). Since P. scle- well understood. It is considered that fusarium wilt resistance 56 A. R. DAVIS ET AL.

is due to the inherent resistance of the rootstock, whereby the tolerance is related to higher antioxidative ability and membrane roots exclude the pathogen and prevent infection. However, Lee stability. Grafted watermelon seedlings under low temperature (1989) observed that adventitious rooting of the scion did not stress have higher antioxidants and antioxidative enzyme activ- always increase susceptibility. This observation was supported ities in leaves than self-rooted watermelon seedlings (Liu et al., by a report stating that substances associated with fusarium tol- 2003a; Liu et al., 2004a). erance are synthesized in the roots and translocated to the scion through the xylem (Biles et al., 1989). However, the author’s C. Wet/Flood/Drought/Salinity Tolerance observations revealed that in most instances, adventitious root- Grafting bitter melon onto luffa rootstock improved scion ing of the susceptible scion will result in symptom development flood tolerance (Liao and Lin, 1996). Nongrafted control water- in fusarium-infested soils. In the case of monosporascus vine melon and watermelon grafted onto wax gourd showed greater decline, phytophthora blight, and verticillium wilt, the root- resistance to drought stress than watermelon grafted onto bot- stocks were not resistant but were tolerant to the pathogens tle gourd (Sakata et al., 2007). A Cucurbita moschata cultivar, involved. In these instances it is presumed that the large root ‘Higata 2’, performed well even in waterlogged fields (Toki, area and increased vigor of the rootstock allow scion devel- 1972). opment in the presence of the disease. This may also explain Rootstocks can decrease the accumulation of Cl− and Na+ in why some researchers report an increased tolerance to certain Cucumis melo scion leaves (Romero et al., 1997). This may foliar diseases. Understanding the mechanisms of disease re- be due to the exclusion or decreased absorption of Cl− by sistance is important for their best utilization. When grafting is the roots and replacement or substitution of total K+ by to- used to improve tolerance to diseases such as monosporascus tal Na+in the leaves. Yang et al. (2006) demonstrated that root rot or verticillium wilt, additional control strategies are rec- grafted cucumber plants have higher net photosynthesis, stom- ommended to decrease the pathogens levels to a manageable atal conductance, and intercellular CO2 concentrations under number. NaCl stress than self-rooted plants. Under salt stress, watermelon grafted onto salt-tolerant rootstock demonstrated im- B. Cold/Heat Tolerance proved vigor and yield, and maintained good fruit quality com- One of the most striking effects of grafting is the in- pared to watermelon-watermelon-grafted controls (Liu et al., creased absorption of ions by grafted plants at low temperatures 2003b; 2004b;c). It was suggested that increased salt tolerance (Tachibana, 1982; Ahn et al., 1999). This enhanced mineral up- of grafted watermelon is linked to increased peroxidase activity take appears to be closely associated with the activity of enzymes and decreased superoxide dismutase activity (Liu et al., 2003a; responsible for absorption (Ahn et al., 1999). Ahn further sug- 2004a,b). gested that increased water absorption capacity of figleaf gourd root systems conferred cold root temperature protection to cucumber scions. D. Increased Efficiency of Land Usage Grafting is used to advance the planting date for water- Grafting can overcome problems of continuous cropping in melon during cool periods (Taussig et al., 1996; Miguel et al., protected culture, increasing land use efficiency. In continuous 2004). ‘Shin-tosa’-type (an interspecific hybrid, Cucurbita max- cropping systems, soilborne diseases accumulate over time (Lu, ima × Cucurbita moschata) rootstocks show superior growth 2002; Zhang and Ge, 2002; Wang et al., 2004; Xu et al., 2004; under low-temperature conditions. Cucurbita moschata are not Feng et al., 2006b; Gu et al., 2006; Zhang et al., 2006a). In ad- as resistant as ‘Shin-tosa’ (Okimura et al., 1986), but are more dition, grafted plants with strong root systems can adapt to less resistant than wax gourd and watermelon. Cucumber plants optimum soil conditions such as increased salt or low tempera- Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 grafted onto figleaf gourd are more cold-tolerant than cucumber- ture, and have a wider harvesting period (Zhang, 2002; Liu et al., ‘Shin-tosa’-grafted plants (Fujii, 1970). Marukawa and Takatsu 2004b; Hu et al., 2006; Yang et al., 2006). The productivity of (1969a) examined 81 Cucurbita spp. accessions for use as root- grafted cucumber in solar greenhouses has been extended from stocks under low-temperature conditions (minimum tempera- 3–4 months to 7–8 months during winter months (Hang et al., ture 8–10◦C). They found that figleaf gourd resulted in the earli- 2005). In Northern China, nearly 100% of cucumbers and wa- est harvest and greatest yield. Under low temperature conditions, termelons grown in solar greenhouses are grafted (Hang et al., grafted cucumber have higher net photosynthesis, stomatal con- 2005). ductance, and intercellular CO2 concentrations than self-rooted plants (Zhang, 2002; Hu et al., 2006). E. Effect of Grafting on Flowering and Harvest Early reports on cold tolerance mechanisms, state that grafted Enhanced flowering was noticed in wild cucurbit species cucumber plants with increased total lipids per gram fresh grafted onto squash interspecific rootstock (Nienhuis and Lower, weight, high unsaturated fatty acids, an increase in fatty acid to 1979; Nienhuis and Rhodes, 1977). Watermelon grafted onto total lipid ratio, and a reduced ratio of esterol to total lipids, had bottle gourd caused early formation of female flowers when higher low temperature tolerance (Horvath et al., 1983; Bulder compared to other rootstocks (Kurata, 1976b; Sakata et al., et al., 1990; 1991a;b). More recently it was reported that chilling 2007). In contrast, Yamasaki et al. (1994) reported that flowering CUCURBIT GRAFTING 57

is delayed in watermelon grafted onto bottle gourd rootstocks. mation efficiency, CO2 conductivity, dark reaction activity, and The differences in flower initiation are negligible when suitable photosynthetic rate in the scion (Sun et al., 2002; Zen et al., temperatures occur at the beginning of the growing season, but 2004; Qi et al., 2006; Wei et al., 2006;). Increased photosyn- with less than optimal conditions, grafting to these rootstocks thesis can often be realized under less than optimal growing can delay flowering for up to one week, resulting in an equal conditions, such as weak sunlight and low CO2 content in so- delay in fruit maturity (Miguel, 1997; Xu et al., 2005d). lar greenhouses during winter months, allowing grafted plants Blooming is caused mainly by emission of SiO2 from tri- to produce higher yields and sometimes improved fruit quality chomes, which appear on the fruit epidermis and cover the (Xu et al., 2005d; Hu et al., 2006; Xu et al., 2006a; Zhu et al., pericarp (Matsumoto, 1980; Aoyagi et al., 1986; Yamamoto 2006). et al., 1989). Cucumber varieties grafted onto a squash interspecific hybrid rootstock inhibited flowering (Satoh, 1996). It III. PLANT PHYSIOLOGY was suggested that the root may control floral transition by Cytokinins, a group of plant hormones principally synthe- the production of inhibitory factors in some day-neutral Cu- sized in roots, significantly influence cucurbit plant growth. curbitaceae plants. Blooming of cucumber fruit is almost com- Plants with vigorous root systems release more cytokinins into pletely suppressed when seedlings are grafted onto the cultivar the ascending xylem sap, resulting in increased yield (Kato and ‘Kitora’ (Cucurbita moschata) (Sakata et al., 2008). ‘Bloom- Lou, 1989). For example, cucumber plants grafted on pump- less’ fruits have a distinct appearance and a longer shelf life, kin rootstocks demonstrated a 2.2 times higher trans-zeatin root features that are in demand, thus allowing their sale at a higher content, and were higher in dry matter than self-rooted cucumber price. This caused a rapid shift from conventional rootstock cul- (Seong et al., 2003). tivars to rootstocks for ‘Bloomless’ production (Sakata et al., Cytokinin composition varies greatly between species. For 2007). example, only zeatin and dihydrozeatin are found in cucumber, whereas large quantities of isopentenyladenine and isopentenyl F. Nutrient Uptake adenosine are found in squash and gourd (Table 3). However, One advantage of grafting is the utilization of the root- the stem must play a role in cytokine production or transport stock’s vigorous root system. Grafting influences absorption and since a small portion of scion stem, approximately 15 to 20 cm translocation of phosphorus, nitrogen, magnesium, iron, and cal- in length, can effectively modify the composition of cytokinins cium (Gluscenko and Drobkov, 1952; Masuda and Gomi, 1984; in the ascending xylem sap (Lee et al., 2001a;b). Ikeda et al., 1986; Kim and Lee, 1989; Ruiz et al., 1997; Nie Messenger RNA (Ruiz-Medrano et al., 1999; Xoconostle- and Chen, 2000; Pulgar et al., 2000; Zhang, 2002; Hu et al., Cázares et al., 1999) and protein (Golecki et al., 1998; Gómez 2006; Yang et al., 2006). Absorption and translocation of other et al., 2005) from a rootstock can migrate through the phloem micronutrients such as iron and boron are also influenced by to the scion to accumulate in the phloem and apical tissues. the rootstock (Brown et al., 1971; Gomi and Masuda, 1981; It was suggested that RNA may move within the phloem as a Zaiter et al., 1987; Rivero et al., 2004). Concentrations of N, component of a plant information superhighway (Xoconostle- P, Ca, and Mg in exudates increased in grafted plants (Nie and Cázares et al., 1999). One mRNA, which was demonstrated to Chen, 2000). Ion influx allows increased light energy transfor- circulate through the phloem from a pumpkin rootstock to a

TABLE 3 Cytokinin composition in xylem sap collected from intact and grafted plants of cucumber, squash, and ﬁgleaf gourd plants Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 Cytokinin content (ng/ml sap)

Crop Zeatin Dihydo-zeatin Isopentenyl (Scion/rootstock) Zeatin riboside riboside adenine Total Cucumber (Cucumis sativus) 0.076 4.55 0.80 Trace 6.11 Squash A (Cucurbita moschata) Trace 3.67 0.43 3.63 7.73 Squash B (Cucurbita maxima)Trace 4.06 0.57 1.84 6.47 Figleaf gourd (Cucurbita ﬁcifolia) Trace 4.54 1.48 6.18 12.2 Cucumber/Cucumber 0.55 5.58 0.96 Trace 7.07 Cucumber/Squash A 1.65 4.29 0.20 Trace 6.14 Cucumber/Squash B Trace 5.36 0.19 Trace 5.55 Cucumber/Figleaf 1.49 5.08 0.65 Trace 7.22

Reprinted with permission from Horticultural Reviews (Lee and Oda, 2003). 58 A. R. DAVIS ET AL.

cucumber scion, is a member of a RNA family shown to af- B. Vigor and Shape fect apical meristem development (Ruiz-Medrano et al., 1999). Most studies indicate that changes in the scion are con- Tiedemann et al. (1994) studied the phloem proteins that differed trolled by the rootstock through controlled uptake, synthesis, in Cucumis sativus grafted on Cucurbita ficifolia or on Cucurbita and translocation of water, minerals, and plant hormones (Lee, maxima. They found four proteins on SDS-PAGE gels in grafted 1994). Yetisir and Sari (2004) reported that out of 11 root- scions that do not appear in control plants, but matched the rootstocks tested on watermelon, all the grafted plants produced stock phloem protein pattern. Two of the proteins matched the more biomass than control plants. phloem protein 1 and phloem protein 2 molecular weights of the The scion variety obviously affects final size, yield, and qual- rootstock ity, but rootstock effects may drastically alter these characteristics. Tamada (1989) and Hagihara (2004) classified the species and cultivars of the rootstocks used in Japan on the basis of A. Scion and Rootstock Physiology plant vigor. In general, ‘Shin-tosa’ rootstocks are more vigorous The sequence of structural events involved in graft compat- than the bottle gourd rootstock cultivars. Most of the Cucurbita ibility of herbaceous plants begins with ruptured cells at the moschata cultivars are comparatively weak. Cultivars of Cu- graft interface collapsing to form a necrotic layer that disappears curbita pepo and watermelon range from vigorous to relatively during subsequent events (for a more thorough review see, weak, and wax gourd is medium to weak. Most combinations of Andrews and Marquez, 1993). Living cells from both root- watermelon and bottle gourd are acceptable, but a weak bottle stock and scion then extend into the necrotic zone. A callus gourd rootstock was recommended by Hagihara (2004) when bridge of interlacing parenchyma cells formed when cell di- using an extremely vigorous watermelon cultivar. vision ruptures and invades the necrotic layer. During these A study by Edelstein et al. (2004) showed that number of events the tensile strength of the graft increases due to phys- leaves, stem length, and fresh weight of melon plants increased ical cohesion between rootstock and scion. New vascular cam- using 22 different Cucurbita spp. rootstocks. Davis and Perkins- bium is differentiated from parenchyma cells, and secondary Veazie (2005) demonstrated that rootstocks affect the number of xylem and phloem are produced by the reconstituted cam- nodes and lateral branches, and that the vigor of grafted water- bium, providing a vascular connection between rootstock and melon plants was improved when grated onto a gourd rootstock. scion. They further showed that grafting did not affect length, circum- In some cucurbits, the stem (both the hypocotyl and the epi- ference, or diameter of fruit, but decreased weight of the fruit, cotyl) has a central pit or cavity with 6 vascular bundles located suggesting the fruit were less dense. in a definite position (Oda et al., 1993). Complete union of these six vascular bundles is sometimes impossible depending on the grafting methods used. Initial studies by Lu et al. (1996) indi- C. Yield and Size cated that the addition of exogenous plant hormones helps the Grafting can increase yield since grafted plants are resistant formation of graft unions by increasing the rate of formation to soilborne disease, have strong root systems, and increased and number of vascular bridges. The differentiation, and pos- photosynthesis (Xu et al., 2005b; Qi et al., 2006; Wu et al., sibly the induction, of the vascular bridge in Cucumis sativus 2006). Since grafted plants are healthier and live longer, the har- requires high levels of the auxin, indole-3-acetic acid (IAA), vesting period can be expanded dramatically. This advantage which induces callus proliferation from the two partners at the is more obvious under less optimal growing conditions (Hang graft union (Lu and Song 1999; Lu, 2000). Lu and Song (1999) et al., 2005). Cucumber plants grafted onto pumpkin rootstocks mentioned that IAA and zeatin plus zeatin riboside are required had 27% more marketable fruit per plant than self-rooted cucum- Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 for vascular bundle regeneration in the graft union. There is a ber (Seong et al., 2003). Salam et al. (2002) demonstrated a 3.5 positive correlation between the vigor of grafted watermelon times higher yield due to larger fruit size, more fruit per plant, and the similarity of protective isozymes (e.g., peroxidase and and improved plant survival rates. A squash interspecific hybrid superoxide dismutase) between grafted and regular seedlings rootstock increased watermelon yield and increased fruit size (Zhang et al., 2006b). (Miguel et al., 2004). Yetisir and Sari (2003) and Yetisir et al. Studies by Ruiz and Romero (1999) demonstrated that grafted (2003) tested multiple rootstocks (Cucurbita moschata, Cucur- melon plants had lower concentrations of nitrate, higher concen- bita maxima, squash interspecific hybrids, and bottle gourd) for tration of nitrate reductase activity, and lower contents of total effects on yield. They found that watermelon scions grated onto free amino acids and soluble proteins compared to the control. bottle gourd had 27–106% greater yield over control plants, but Organic N and fruit yield also increased significantly in the ma- the Cucurbita sp. rootstock decreased yield by 127–240%. In jority of grafted plants. These changes were attributed to dif- areview, Sakata et al. (2007) wrote that yield and fruit weight ferences in N utilization and assimilation between grafted and of ‘Shin-tosa’ grafted watermelons were higher than those with control plants. With these important physiological effects on the other rootstock. This was especially true in watermelon, and to a scion, it is not surprising that grafting affects scion vigor, yield, lesser extent in melon (Miguel et al., 2004). Higher yields were and fruit quality. not noted with grafted cucumber (Brajeul and Letard, 1998). CUCURBIT GRAFTING 59

To complicate the matter further, yield was not affected by root- opment (about 30% fruit growth) in seeded heirloom varieties stock in most scion / rootstock combinations with Cucumis melo and in Cucumis melo (Elmstrom and Davis, 1981; Chisholm scions (Koutsika-Sotiriou and Traka-Mavrona, 2002). It was and Picha, 1986; Hubbard et al., 1989), but was found to be suggested that this discrepancy in the literature demonstrated present at all stages of growth in grafted and non-grafted wa- the importance of optimizing rootstock / scion combinations for termelons (Liu et al., 2006). Acid invertase activity was high each cropping environment (Ruiz et al., 1997). during the first third of watermelon fruit development, and then In Cucurbita spp., yield is dependent mainly on plant vigor. had little activity during the last 5 days of ripening. Sucrose This may be why yield of ‘Shin-tosa’ grafted watermelon are synthase activity was moderately high in the first third of fruit higher than other combinations (Sakata et al., 2007). Yield of development, then remained low. Sucrose phosphate synthase plants with weak rootstocks are inferior to the yield of those increased during the second third of fruit development, and fell with vigorous ones. Even if plants with weak rootstocks are in the last five days of ripening. The low sugar content of grafted spaced widely and grown in fertile conditions, their yields are watermelon is correlated with low invertase, high sucrose syn- still low, due to few fruit per plant. In some cultivars, larger fruit thase activities, and low sucrose phosphate synthase activity, size caused marketability problems, mainly in ‘Galia’ (Cucumis and sugar transmembrane transportation capability (Qian et al., melo var. saccharinus Naud.) type melons (Miguel, 2004). 2004; Liu et al., 2006). The increase of sucrose in grafted plants The yield of bottle gourd-grafted watermelon is relatively was accompanied by an increase of sucrose phosphate synthase stable, as it is affected little by soil characteristics (Tamada, and sucrose synthase activities (Xu et al., 2006a). In addition, 1989). Wax gourd-grafted and watermelon-grafted watermelon it appears that sugar accumulation in mature fruit varies with are affected by soil conditions, and often show decreased yield rootstocks (Gao and Liao 2006; Xu et al., 2006b). in areas of low fertility or moisture (Sakata et al., 2007). Melon: Preharvest internal decay or internal breakdown and abnormal fruit fermentation occurred in oriental melons and melons when grafted onto vigorous squash interspecific hy- D. Quality brid (Muramatsu, 1981; Chung, 1995). Other abnormalities ob- Changes in grafted cucurbit fruit quality appear to be both served were reduced fruit soluble solids content and persistent rootstock, and scion-dependent, causing contradictory reports green color in the suture stripe (Lee, 1989; Lee et al., 1998). in the literature. Additionally, as watermelon and muskmelon Cucurbita spp. rootstock sometimes negatively affected melon (Cucumis melo var. reticulatus) maturity is often delayed in fruit quality (Brix, taste, texture) (Traka-Mavrona et al., 2000). grafted fruit, it is important to sample the fruit several days Although ‘Shin-tosa’ rootstock is resistant to fusarium wilt, it past the expected fully ripe date to make sure values for sug- is almost never used for melon in Japan because it causes re- ars do not simply represent delayed ripening (Miguel, 1997; Xu duced fruit quality, including low sugar content, and fibrous flesh et al., 2005d). This difference in maturation probably causes (Muramatsu, 1981). An off-taste and texture in winter melon additional contradictory reports in the literature. fruit grown in Greece in some of rootstock/scion combinations As early as the late 1940s, Imazu (1949) noted that Cu- were reported by Koutsika-Sotiriou and Traka-Mavrona (2002). curbita moschata rootstock caused inferior texture and flavor If Cucurbita spp. are used as a rootstock with ‘Earl’s Favorite’ in grafted ‘Honey Dew’ fruits, despite conferring resistance to melon, the fruit grow better than those on nongrafted plants, but fusarium wilt. Grafting reportedly caused a small reduction, ap- the quality of the fruit netting is poorer and the sugar content is 2 proximately 1◦Brix, in the sugar content of both watermelon and to 3◦Brix less (Kamiya and Tamura, 1964). Trionfetti-Nisini et melon (Taussig et al., 1996; Miguel, 1997; Lopez-Galarza et al., al. (2002) reported that of 13 commercial melon rootstocks and 2004; Xu et al., 2005d; Qi et al., 2006; Xu et al., 2006b). Nev- various Cucurbitaceae spp. rootstocks, many of them influenced Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 ertheless, when grown properly, fruits from grafted plants were quality (shape, size, Brix). Grafting was reported to increase vit- commercially marketable, and reduction in fruit quality was not rescence (glassy look to flesh) in melon (Taussig et al., 1996). found in the Spanish type melons or cucumber (Miguel, 1997; The photosynthesis rate of grafted melon plants decreases dra- Hoyos, 2001). matically during late stages of fruit development (Xu et al., Fortunately, under the best circumstances, and when using 2005a). This decrease of photosynthesis may be related to low specific rootstock/scion combinations, grafting can enhance fruit fruit quality. quality (total soluble solids, and carotenoid and ascorbic acid Watermelon: The most common complaints about grafted contents) (Davis and Perkins-Veazie, 2005; Xu et al., 2005b; watermelon quality are low Brix, insipid taste, increased number Alan et al., 2007; Alexopoulos et al., 2007). Breeding for im- of yellowish bands in the red flesh, and internal flesh breakdown proved rootstock/scion combinations and screening for combi- (Ryu et al., 1973; Lee and Oda, 2003; Davis et al., 2008). Tex- nations that result in high quality fruit, is beginning to decrease tural quality and firmness were lower in watermelon grafted the number of negative quality issues for grafted cucurbit crops onto ‘Shin-tosa’ than those grafted onto bottle gourd or con- (Davis et al., 2008). trol (Yamasaki et al., 1994). The deterioration of watermelon The primary sugars in watermelon are sucrose, fructose, and fruit quality on Cucurbita spp. rootstocks was attributed to vig- glucose. Sucrose appears only after initiation of color devel- orous nutritional uptake (Kato and Ogiwara, 1978; Shinbori 60 A. R. DAVIS ET AL.

et al., 1981; Masuda et al., 1986). In heated greenhouse ex- fruits from grafted plants tend to be shorter and show decreased periments, grafted watermelon on five rootstocks (bottle gourd firmness and shelf life (Lee, 1989; Lee et al., 1999). and Cucurbita pepo) were more vigorous and out yielded the non-grafted controls by 25 to 95% (Ioannou et al., 2002). It was also found that fruit quality [external and internal appearance, IV. WHAT CUCURBITS ARE GRAFTED intensity of red, presence of fibrous tissue, cracks, cavities, ab- A. Watermelon normalities in the rind and organoleptic index (reflecting taste), Watermelon is an important crop in Asian countries. The texture, and Brix] was superior in nongrafted plants. A complex total area harvested in China was 2.2 million hectares in 2005 study on the effect of grafting and cytokinin-induced fruit set- (FAOSTAT, 2005). This counts for more than half the world ting on color and sugar development in triploid watermelon was watermelon production. In 2005, Korea ranked ninth in total reported by Liao and Lin (1996). They demonstrated that de- world production, about 850,000 metric tons. In Spain all the spite the loss of other quality traits, fruit from grafted plants set triploid cultivars and diploid pollinizer are grafted (Camacho with CPPU had a total Brix content similar to fruit from control and Fernandez, 2000; Hoyos, 2004; Miguel, 2004). Watermelon plants. is the most commonly grafted cucurbit in Italy (Amadio, 2007). Quality (Brix, lycopene, flesh firmness, rind thickness, and Watermelon was first grafted onto Cucurbita moschata and fruit shape) of watermelon was greatly affected by grafting shortly afterwards onto bottle gourd to control soilborne dis- et al (Yetisir and Sari, 2003; Yetisir ., 2003; Davis and Perkins- eases caused by successive cropping (Ashita, 1927; Tateishi, Veazie, 2005). Flesh firmness was increased slightly, lycopene 1927; Sakata et al., 2007). Remarkable yield increases of more was typically higher, and Brix typically lower in watermelon than 200% derived from growing grafted plants under protected fruit from grafted plants using gourd rootstocks (Davis and structures attracted the interest of many growers (Lee and Oda, Perkins-Veazie, 2005). The total sugar content of watermelons 2003). As a result, the area for protected cultivation increased in grafted onto bottle gourd rootstock was reported to be lower Japan, Korea, and China, and the demand for grafted seedlings et al et al than in self-rooted watermelons (Yao ., 2003; Qian ., markedly increased despite their high cost. In fact, grafting tech- et al Cucurbita 2004; Liu ., 2006). They reported that sp. root- niques are often developed with watermelon in mind. stock decreased the quality of watermelon fruit, but that fruit Squash interspecific hybrids, bottle gourd, and Cucurbita spp. from scion grafted onto bottle gourd differed only slightly from are often used as alternate rootstocks for watermelon to pre- et al control fruit. Miguel . (2004) found no difference in solu- vent disease infection. However, rootstocks of Cucurbita spp. ble solids concentrations of watermelon fruit from scions grafted often lower fruit quality (Kato and Ogiwara, 1978; Shinbori et al onto a squash interspecific hybrid versus control, but Salam . et al., 1981; Masuda et al., 1986). Wild type watermelon is (2002) showed a marked increase in watermelon TSS content used as a rootstock to prevent the occurrence of fusarium wilt et al when grafted onto bottle gourd. Perkins-Veazie . (2008) in grafted plants. It has a good graft compatibility with water- demonstrated that grafting watermelon could increase lycopene melon, leading to increased fruit quality (Huh et al., 2002), but it and total carotenoids by 20%, and increase amino acids, es- is susceptible to low temperature and high moisture injury. Burr pecially citrulline [a nonessential amino acid with vasodilation cucumber (Sicyos angulatus L.) is fairly resistant to wilt disease et al properties (Lee ., 1996)], by up to 35%. and adaptable during low temperature, but it has poor and slow Cucumis sativus and Cucurbita pepo: For crops harvested seed germination, making grafting difficult and inefficient (Lee at an immature stage such as cucumber, grafting has few re- et al., 1999). Wax gourd has good graft compatibility with wa- ported negative effects on fruit quality, although increased firm- termelon but is susceptible to low temperature stress that can ness and shortening of fruit have been noted (Muramatsu, 1981). Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 delay development and blooming period of the grafted plants As mentioned above, ‘Bloomless’ cucumber fruits have gained (Kurada, 1974; Ko, 1999; Huh, 2000; Sakata, 2007). a prominent market-share. However Sakata et al. (2008) report inconsistency in the literature on ‘Bloomless’ cucumber texture. Some reports show they have less desirable texture due B. Cucumber to tougher skin and softer flesh (Inayama, 1993a,b; Yamamoto Cucumber is a popular vegetable in China with over 1.7 mil- et al., 1996). Questions remain as to whether traditional cucum- lion hectares of cucumber and gherkins harvested in 2005 (FAO- bers taste better than ‘Bloomless’ fruits (Horie et al., 2004). STAT, 2005). About 50% of China’s cucumbers are grown in The main reason for selecting rootstocks for cucumber culti- plastic tunnels during the spring and fall season, and in solar vars is to increase yield, produce ‘Bloomless’ fruit, and achieve greenhouses during winter months in Northern China. Almost stable production. However, it has been suggested that differ- all cucumbers grown in solar greenhouse are grafted. ent rootstocks affect grafted cucumber quality characteristics Growing cucumbers under protected environments started in such as fruit shape, skin and flesh color and texture, firmness, the 1960s with the introduction of commercial plastic films, rind thickness, and ascorbic acid and soluble solids content enabling year-round production of several horticultural crops. (Inayama, 1989; Choi et al., 1992; Kang et al., 1992; Robinson Compared to watermelons and melons, cucumbers do not man- and Decker-Walters, 1997; Zhu et al., 2006b). Summer squash ifest an extensive spread of soilborne diseases, especially when CUCURBIT GRAFTING 61

grown outdoors in the summer. Cucumber cultivars developed One of the most serious problems in greenhouse production for winter greenhouses are more susceptible to various dis- of oriental melon is nematode control (Ko, 1999). Rootstocks eases and unfavorable environmental conditions than those in- with good to excellent nematode resistance are required for suc- tended for open field cultivation. Other advantages of grafting cessive melon production in many areas of Korea. Limited suc- are low temperature tolerance, yield increase, ease of manage- cess was obtained with ‘Andong,’ a burr cucumber rootstock. ment, higher fruit quality, ‘Bloomless’ fruit, and extension of Finding alternative rootstocks for nematode control is an im- harvest period in hydroponic systems (Asao et al., 1999). portant area of research and burr and African horned cucum- Cucurbita spp. and figleaf gourd are commonly used as root- bers (Cucumis metuliferus E. Meyer ex Naudin) are considered stocks for cucumber. Figleaf gourd is by far the most popular of promising (Igarashi et al., 1987). Grafted melons in Spain are the two species. mostly ‘Galia,’ cantaloupe, and Armenian cucumber (Cucumis Figleaf gourd is a common rootstock for cucumber since melo var. flexuosus Naud) types (Miguel, 2004). Cantaloupe the two species are highly compatible. This rootstock pos- types are grafted in France and Italy (Taussig et al., 1996; Buzi sesses good to high fusarium wilt (Ko, 1999), phytophthra, root et al., 2002). knot nematode resistance and low soil temperature tolerance (Marukawa and Takatsu, 1969a; Ahn et al., 1999; Lee and Oda, D. Bitter Gourd 2003). It also has good water and nutrients absorption (Shimada Bitter gourd is native to India and is grown throughout Asia. and Moritani, 1977; Masuda and Gomi, 1984) even at low tem- Both immature fruit and vine tips are nutritious and edible. The peratures (Tachibana 1987; 1989). The disadvantage of figleaf main problem with bitter gourd production is fusarium wilt and as a rootstock is its rapid seedling growth, making the optimal low temperatures during winter production (Lin et al., 1998). grafting window short. In addition, the germination rate is low Luffa (Luffa spp.), figleaf gourd, and pumpkin are common root- and not uniform (Hang et al., 2005). stocks for bitter gourd (Lin, 2004). Luffa has been widely used Squash interspecific hybrid rootstocks are more tolerant to during summer production since it is resistant to fusarium wilt high temperature conditions and are commonly used for cu- and has good tolerance to heat and flooding. Figleaf gourd and cumber during summer plantings. Cucumber grafted onto cer- pumpkin are used by farmers during low temperature winter pro- tain cultigens of Cucurbita moschata produced fruits with shiny duction. Since figleaf gourd does not have good heat tolerance, skin compared to fruit from nongrafted plants or from cucum- bitter gourd-figleaf grafted plants often show premature decay ber grafted onto other Cucurbita spp. (Fujieda, 1994). The shiny during hot weather. To overcome this problem, figleaf gourd and ‘Bloomless’ fruits are successful in the Japanese market, but not luffa, are often used together. Figleaf gourd roots will support in Korea. In France, squash interspecific hybrids or Cucurbita fi- the scion early and as temperatures rise, luffa roots support the cifolia are used as rootstocks for cucumber (Brajeul and Letard, plant. Cleft grafting is a good method for grafting bitter gourd 1998). In Spain the best rootstocks for cucumber have been the (Lin, 2004). squash interspecific hybrids (Hoyos, 2001). E. Summer Squash Burr cucumber is fairly resistant to wilt disease and adaptable Summer squash is grown widely under protected culture during low temperature. However, it has poor and slow seed during winter in China. Grafted plants are more compact and germination, making grafting difficult and inefficient (Takeuchi tolerant to low soil temperature, and fruit are uniform and and Nagai, 1977; Hagitani and Toki, 1978; Toki, 1978). straight. This fruit shape is preferred by Chinese customers. The most commonly used rootstocks are figleaf gourd and Cucurbita C. Melons spp. (Hang et al., 2005). In Spain and Italy, all grafted melon plants are now on squash Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 interspecific hybrids, but B. hispida or Cucurbita maxima was used in commercial production before the introduction of the F. Chinese Snake Gourd hybrids (Bianco, 1990; Chaux and Foury, 1994; Messiaen et al., Chinese snake gourd (Trichosanthes kirilouii Maxim) is a 1994; Miguel and Maroto, 1996; Fritsch, 2002). In Italy, cultivars dioecious crop. Female and male plants are indistinguishable of Cucurbita maxima tolerant to Monosporascus vine decline before transplanting. Farmers sometimes use male plants for (Gennari, 1999) are used except in places where this disease is rootstocks and female shoots for scions to increase fruit yield not prevalent. Locations where Monosporascus vine decline is (Li et al., 2006). Grafting onto wax gourd improves fusarium not an issue, Cucumis melo lines resistant to Fusarium oxyspo- wilt resistance (Lü et al., 2004). rum f. sp. melonis are used (Buzi et al., 2004). Grafting is a must in oriental melon cultivation since their G. Commonly Used Rootstocks roots are sensitive to low soil temperatures. However, grafting Tables 4 and 5 demonstrate the various uses of different root- onto vigorous rootstocks induces undesirable physiological dis- stocks. Marukawa and Yamamuro (1967) examined 84 cultivars orders such as vigorous vegetative growth, delayed fruit maturity and accessions of Cucurbita spp. for use as potential water- and harvesting, uneven maturity, and internal fruit breakdown melon rootstocks. They concluded the following: 1) about 20% (Chang, 1995). of the tested lines of Cucurbita maxima, Cucurbita moschata, 62 A. R. DAVIS ET AL.

TABLE 4 Response of cucurbits to biological and environmental stresses Nematode Graft compatibility Fusarium Rootstock M. M. Low temp High salt Oriental and scion Ia II III IV incognita halpa tolerance tolerance Watermelon Cucumber melon Rootstockb Shintozwa HRc HR HR HR S S HR HR HCd HC HC Hongtozwa HR HR HR SR S S MR MR SC HC HC Figleaf gourd MR SR MR SR S S HR HR IC HC IC Bottle gourd MR HR HR SR S S SR MR HC HC IC Wax gourd HR MR HR HR S SR SR SR HC HC — Bur cucumber HR HR HR HR S HR SR SR HC MC HC AH cucumbere HR HR HR HR S MR SR ? HR HC HC Scion Watermelon S SR HR HR HR SR S SR — — — Cucumber HR SR HR HR S S HR SR — — — Oriental melon HR HR S HR S S S S — — —

Reprinted with permission from Horticultural Reviews (Lee and Oda, 2003). a I, Fusarium oxysporum f. sp. niveum II; F. oxysporum f. sp. cucumerinum; III, F. oxysporum f. sp. melonis; and IV, F. oxysporum f. sp. lagenariae. bShintozwa (Cucurbita maxima x Cucurbita moschata), Hongtozwa (Cucurbita moschata), ﬁgleaf gourd (Cucurbita ﬁcifolia), bottle gourd (Lagenaria siceraria), wax gourd (Benincasa hispida), bur cucumber (Sicyos angulatus), and AH cucumber (Cucumis metuliferus), respectively. cHR, highly resistant; MR, moderately resistant; SR, slightly resistant; and S, susceptible. d HC, highly compatible; MC, moderately compatible; SC, slightly compatible; and IC, incompatible. eAH: African horned cucumber. Source: Ko (1999).

and Cucurbita pepo were compatible with watermelon; 2) figleaf V. GRAFTING METHODS gourd was incompatible with watermelon; and 3) the accessions The survival rate of grafted plants depends on compatibility ‘Kinshi Uri’ (Cucurbita pepo), ‘Bizen Chirimen,’ and ‘No. 8’ between scion and rootstock, quality and age of seedlings, (Cucurbita moschata) were suitable rootstocks for watermelon. quality of the joined section, and post-grafting management. The squash interspecific hybrids are the most commonly used Different grafting techniques are adapted for different scions cucurbit rootstocks, but some cultivars of Cucurbita moschata, and rootstocks depending on grafting objectives, farmers’ expe- Cucurbita pepo, and Citrullus spp. are increasing in importance rience, and post-grafting management conditions. When scion (Miguel and Maroto; 1996; Paplomatas et al., 2002; Miguel, and rootstock have hollow hypocotyls, the hole insertion and one 2004). Bottle gourd and wax gourd are suitable rootstocks for cotyledon grafting methods are preferred (Hang et al., 2005). watermelon because they are resistant to fusarium wilt, have high In contrast, tongue approach and cleft techniques, which have Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 affinity for watermelon, and they provide stable plant growth high survival rates, are often chosen by inexperienced farmers after grafting (Sato and Takamatsu, 1930; Matsumoto, 1931; who have plenty of space and adequate labor. In contrast, the Tateishi, 1931; Kijima, 1933; Murata and Ohara, 1936; Kijima, one cotyledon and the hole insertion grafts require experienced 1938). Bottle gourd is not used in Spain because of its suscep- labor, specialized tools, and a healing chamber to obtain high tibility to monosporascus vine decline (Garc´ıa-Jiménez et al., survival rates. Cleft, one cotyledon, and hole insertion methods, 1994), but in Italy it is used as well as Cucurbita moschata which have high grafting positions, increase separation of and squash interspecific hybrids (Morra, 1997; Buzi et al., scion from the ground. This decreases the opportunity of scion 2004). adventitious roots contracting soilborne diseases (Hang et al., Burr cucumber, which shows fusarium wilt and nematode 2005). resistance, low temperature tolerance, and tolerance of excess In manual grafting, the grafting and post-grafting operations water, was tested extensively for use as a rootstock for cucum- require three to four people, each assigned to a specific step in ber (Hagitani and Toki, 1978; Toki, 1978). However, it was not the process (Lee and Oda, 2003). Automation requires one to adopted because of its susceptibility to damping-off and gummy three people to oversee the entire process. Below is a review stem blight (Takeuchi and Nagai, 1977), uneven germination, of the published grafting methods, both manual and automated, and its thin hypocotyl makes grafting difficult (Tataki, 2004). and their pre- and post-grafting requirements. CUCURBIT GRAFTING 63

TABLE 5 Rootstocks for cucurbitaceous crops and some related characteristics Scion/Rootstock Cultivar Major characteristics Possible disadvantage Watermelon Bottle gourd (Lagenaria FR Dantos, Partner, Vigorous root system, resistant to New fusarium race, siceraria) Renshi, FR Combi, fusarium and low temperature susceptible TanTan anthracnose Squash (Cucurbita Chinkyo, No. 8, Keumkang Vigorous root system, resistant to Poor fruit shape and moschata) fusarium and low temperature quality Interspecific hybrid squash Shintozwa, Shintozwa #1, Vigorous root system, resistant to Reduced fertigation (Cucurbita maxima × C. Shintozwa #2, Chulgap fusarium and low temperature required; reduced moschata) excellent vigor and high quality temperature tolerance Pumpkins (Cucurbita pepo)Keumsakwa, Unyong, Vigorous root system, resistant to Poor fruit shape and Super Unyong fusarium and low temperature quality Wintermelon (Benincasa Lion, Best, Donga Good disease resistance Incompatibility hispida) Watermelon (Citrullus Kanggang, Res. #1, Fusarium tolerance, but not Not enough vigor and lanatus) Tuffness, Kyohgoh. resistance disease resistance African horned cucumber NHRI-1 Excellent fusarium resistance and Medium to poor graft (Cucumis metuliferus) good nematode tolerance compatibility Cucumbers Figleaf gourd (Cucurbita Heukjong, Black Seeded, Good low temperature tolerance Fruit quality may be ficifolia) Figleaf gourd and disease resistance reduced Squash (Cucurbita Butternut, Unyong #1, Good fusarium tolerance and Affected moschata) Super Unyong ‘bloomless’ fruit skin byPhytophthora Interspecific hybrid squash Shintozwa, Keumtozwa, Good fusarium and low Slight quality reduction (Cucurbita maxima x C. Ferro RZ, 64-05 RZ, temperature tolerance expected moschata) Gangryuk Shinwha, Chulgap Bur cucumber (Sicyos Andong Good fusarium tolerance, low and Reduced yield angulatus) high soil moisture tolerance and nematode tolerance African horned cucumber NHRI-1 Excellent fusarium resistance and Weak temperature (Cucumis metuliferus) good nematode tolerance tolerance Melons-Oriental Melons Squash (Cucurbita Baekkukzwa, No. 8, Good fusarium and low Phytophthora infection

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 moschata) Keumkang, Hongtozwa temperature tolerance Interspeciﬁc hybrid squash Shintozwa, Shintozwa #1, Good fusarium resistance, low and Phytophthora infection, (Cucubita maxima x C. Shintozwa #2 high soil temperature tolerance, poor fruit quality moschata) and high soil moisture tolerance Pumpkin (Cucurbita pepo)Keumsakwa, Unyong, Good fusarium resistance, low and Phytophthora infection Super Unyong high soil temperature tolerance, and high soil moisture tolerance Melon (Cucumis melo) Rootstock #1, Kangyoung, Fusarium tolerance and good fruit Phytophthora problem Keonkak, Keumgang quality African horned cucumber NHRI-1 Good fusarium tolerance, low and Weak temperature (Cucumis metuliferus) high soil moisture tolerance and tolerance nematode tolerance

Reprinted with permission from Horticultural Reviews (Lee and Oda, 2003). Source: Asao et al. (1999); Chung (1995); Igarashi, Kanno, and Kawaide (1987); Gomi and Masuda (1981); Kang, Choi, and Lee, 1992; Kim and Lee (1989); Ko (1999); Matsuo, Ichiuchi, and Kohyama (1985); Lee (1989; 1994; 2000); Lee et al. (1998); Oda (1999); Oh (2000); Tachibana (1981). 64 A. R. DAVIS ET AL.

TABLE 6 Efﬁciency and savings of labor by using three different grafting methods Labor Labor saved Treatment (min/100 plants) (%) PG 46.0 35.8 HIG 60.3 15.6 TAG 71.4 0

PG (Pin grafting), HIG (Hole insertion grafting), TAG (Tongue approach grafting).

Methods continue to evolve to overcome existing and developing problems, to increase survival rate, and decrease labor. The following methods are summarized from Hassell and Memmott (2008), Kapiel et al. (2004), Lee (1994), Lee et al. (1998), Lee and Oda (2003), and Oda (1999). Table 6 shows the efﬁciency of three of the main grafting techniques.

A. Tongue Approach/Approach Graft The advantage of the tongue approach, which is sometimes called approach graft (TAG), is that it is easy and requires a low FIG. 1. The tongue approach grafting method. Step 1, preparing the rootstock; relative humidity microclimate after grafting. Because of this, step 2, preparing the scion; step 3, joining the scion to the rootstock; step 4, securing the joining with a metal strip; and step 5, removing the scion roots. it is often adapted by farmers. Although this method requires Reprinted with permission from HortScience (Hassell and Memmott, 2008). more space and labor compared to other methods, high seedling survival rate can be attained even by beginners. However, the ing. If the top of the rootstock was left on, it should be re- grafting position is close to the ground making it easy for ad- moved ﬁve days after grafting. The scion hypocotyls are cut off ventitious roots from the scion to reach the soil. Moreover, this seven to ten days after grafting at just below the graft union. method is not suitable for rootstocks with hollow hypocotyls, Grafted plants are maintained in the greenhouse until ready for since scions may form adventitious roots inside the hypocotyls. transplanting. This is at least two days after removing the scion Therefore the TAG method is good for rootstocks with high solid roots. A humidity chamber is not required (Lee, 1994; Lee et hypocotyls. al., 1998; Oda, 1999; Lee and Oda, 2003; Hassell and Memmott, This method originated in the Netherlands (Ishibashi, 1965), 2008). and is now widespread in Japan, Spain, France, and Italy (Bianco, 1990; Morra, 1997; Brajeul and Letard, 1998; Miguel and Maroto, 2000; Buzi et al., 2002; Lee and Oda, 2003). It is B. Hole Insertion/Terminal/Top Insertion Graft easy to use, has a high success rate, and the grafted seedlings The hole insertion graft (HIG), also known as terminal graft and top insertion graft, is the most popular cucurbit grafting

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 have a uniform growth rate. The scions and rootstocks should be approximately the same method in China. This method is easy, has high survival rates, diameter in the TAG method. This is usually the case after and the grafted plants have fewer incidents of soilborne disease the rootstock has fully developed cotyledons and the scion has because of the high graft union (Xiao and Yan, 2004; Hang cotyledons and the first true leaf. The rootstock is cut through et al. 2005). One person can produce 1,500 or more grafts/day the hypocotyl at a 35◦ to 45◦ angle (Figure 1). The growing and post-grafting acclimatization is simple. This method was point may remain by only cutting downward halfway through described in 1970 by Fujii and has recently been adopted by the hypocotyl, or it may be removed with a grafting knife or nurseries (Sakata et al., 2007). A modified HIG method, where razorblade. The scion is also cut at an angle (upward if the the root system is removed from the rootstock, was originally growing tip of the rootstock remains attached) and joined to developed for watermelon grafting (Utsugi, 1973) and will be the rootstock with the cut surfaces aligned. Lead strips, alu- discussed below under ‘Root Pruning.’ minum foil, or grafting clips are used to hold the grafts together. Normally rootstock seed are sown 2–4 days before scion When metal strips are used they can remain on the plant once seeds. Rootstocks are ready for grafting when both cotyledons the plant has healed. However, the grafting clips need to be and first true leaf start to develop (about 7 to 10 days after sow- removed once the union is healed. There is an additional cost ing). The rootstock’s growing point is removed (Figure 2), a cut ◦ ◦ for clips, and for labor to remove them 15–20 days after graft- is made and then drilled at a 35 to 45 angle using a bamboo CUCURBIT GRAFTING 65

FIG. 3. The one cotyledon grafting method. Step 1, preparing the scion; step 2, preparing the rootstock; step 3, joining the plants; step 4, securing the joined region with a grafting clip. Reprinted with permission from HortScience (Hassell and Memmott, 2008).

Sakata et al., 2007). This method is suitable when rootstock and scion are of a similar size. The rootstock should be grafted when cotyledons and the first true leaf start to develop (about 7 to 10 days after sowing). One cotyledon and the growing tip are removed (Figure 3). The seedling is cut at a slant from the base of one cotyledon to 0.8–1.0 cm below the other cotyledon, removing one cotyledon and the growing tip. The length of cut on the scion hypocotyl should match that of the rootstock and should be at a 35◦ to 45◦ angle. The scion is attached to the rootstock FIG. 2. The hole insertion grafting method. Step 1, preparation of the scion; step 2, removing the growing tip of the rootstock; step 3, drilling out the growing and fixed tightly by a grafting tube or clip (Oda, 1999; Lee and tip and creating a hole for the scion; step 4, joining the scion and rootstock; step Oda, 2003). Grafted plants should be maintained in the dark at ◦ 5, the joined plants. Reprinted with permission from HortScience (Hassell and 25 C and 100% humidity for three days or until the junction Memmott, 2008). has healed, before moving them into a greenhouse maintained at 21◦Cto30◦C. Plants should not be more than 33 days old or plastic gimlet. The scion hypocotyl is cut to form a 7–8 mil- before transplanting (Lee, 1994; Lee et al., 1998; Kapeil et al., limeter long wedge. The scion is then inserted into the prepared 2004). This approach requires good post-grafting management rootstock hole. This method does not require additional labor since scions easily fall off at an early stage. OCG is called tube for clipping, transplanting, cutting off remaining scion roots, or grating when the joined plants are held together with a length of clip removal. It does require a higher skill level compared to tube instead of a grafting clip (Hassell and Memmott, 2008). TAG, and requires a suitable environmentally controlled humid or healing chamber. D. Cleft/Side Insertion Graft To achieve a high rate of success, relative humidity should be The cleft graft (CG) also known as the side insertion graft maintained at approximately 95%. After the healing process is was the initial grafting method used for cucumber and water- complete, grafted plants are transferred and maintained at 21– melon (Ishibashi, 1959). The CG has largely been replaced by Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 ◦ 36 Cinthe greenhouse until junction is healed. Plants should OCG, HIG, and TAG, because of the higher success rate and the not be older than 33 days before transplanting (Lee, 1994; Lee uniform growth obtained from those methods (Amadio, 2004). et al., 1998; Lee and Oda, 2003; Kapeil et al., 2004; Hassell and However, in Italy and France CG is still one of the most com- Memmott, 2008). The main problem with HIG is that the size mon techniques (Bianco, 1990; Morra, 1997; Brajeul and Letard, of the rootstock hole is limited by rootstock size. Therefore, the 1998; Buzi et al., 2002). scion size has to be controlled, narrowing the grafting period. The CG method is suitable for rootstocks with wide hypocotyls. This method is simple and easy to learn, and is suit- C. One Cotyledon/Slant/Splice/Tube Graft able for preventing soilborne diseases since the grafting junction The one cotyledon graft (OCG) also known as slant, splice, or is high on the hypocotyl. When cotyledons and the first true leaf tube graft is commonly used, and has recently been adopted by start to develop (about 7 to 10 days after sowing) the rootstock is commercial plug seedling nurseries (Fujii, 1970, Sakata et al., ready to graft. The growing tip of the rootstock can be removed 2007). The procedure is performed by hand, machine, or robot, during grafting or around five days after the grafted plants are and is applicable to most vegetables. This approach is pre- removed from their high humidity chamber (Figure 4). A slit ferred when rootstocks have thin stems, i.e. watermelon, cu- is cut on the rootstock hypocotyl with a razor blade and held cumbers, and oriental melons (Yoshioka, 2001; Amadio, 2004; open with a toothpick. The width of the cut varies depending 66 A. R. DAVIS ET AL.

FIG. 4. The cleft grafting method. Step 1, preparing the scion; step 2, preparing the rootstock; step 3, opening up the rootstock hypocotyl; step 4, inserting the scion; step 5, securing the joined plants with a grafting clip. Reprinted with permission from HortScience (Hassell and Memmott, 2008).

on the diameter of the scion’s hypocotyl. The scion hypocotyl F. Double Graft ◦ ◦ is cut from both sides at a 35 to 45 angle and then inserted Double grafting is used when a perfect rootstock for a speciﬁc into the slit in the rootstock. The toothpick is removed. Then the scion is unavailable. For example, if the rootstock is too large two cut surfaces are matched and held together with a grafting and an intermediate sized stem is needed to bridge the rootstock clip or silicone sleeve. Grafted plants should be transferred to and scion. The scion is ﬁrst grafted onto a middle rootstock (Fig. a humidity chamber or healing room. Plants should be main- 5). The middle rootstock is then grafted onto another rootstock, tained in the greenhouse until the junction is healed, and should which has good resistance to soilborne diseases. Unfortunately not be more than 33 days old before transplanting (Lee, 1994; this method increases labor and cost while decreasing survival Lee et al., 1998; Oda, 1999; Lee and Oda, 2003; Hassell and rate (Lee et al., 1998). Memmott, 2008). G. Root Pruning E. Pin Graft Root pruning hole insertion grafting, and root pruning one cotyledon grafting employ the same procedures as the HIG and This method is similar to OCG, except that specially designed OCG methods except the rootstock hypocotyl is cut to remove pins are used instead of grafting clips to secure the graft union. the roots. This induces adventitious root growth, increases the The cotyledons of the rootstock and scion are cut horizontally, production of primary roots, and enhances the plant’s tolerance and a ceramic pin is inserted into the cut surface (Figure 5). This to cold and heat thus ensuring vigorous growth (Lee and Oda, helps align and secure the joined sections. This method’s limiting 2003). At present, more than 40% of watermelon grafting in factor is that the scion and rootstock should be approximately Japan is performed with this method. However, this added pro- the same diameter so the cambial regions are in close contact. cedure necessitates an exclusive grafting facility and is more This method is easy, reducing labor cost, but ceramic pins add dependent on soil conditions (Yoshida and Harada, 1972; Lee expense, and a special environmentally-controlled chamber is et al., 2001b; Xu et al. 2002, Zhu et al. 2006a).

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 needed to acclimatize the grafted plants (Lee et al., 1998).

H. Automated Graft The ﬁrst semiautomatic cucumber grafting system was com- mercialized in 1993 and others have been developed since. A simple grafting machine can produce 350–600 grafts per hour with 2 operators, whereas manual grafting techniques produce about 1,000 grafts per person per day (Masanao, 1996; Suzuki et al., 1998; Lee and Oda, 2003; Gu, 2006). That is an increase of 400 to 3,000 grafted plants per person per day. In Spain, automated methods represent less than 5% of the total cucurbit grafts, but is much higher in Japan. Grafting robots are being developed in Japan and Korea that are more forgiving or seedling uniformity and require less labor to operate than older grafting machines. They are expensive and require highly FIG. 5. Demonstration of Pin Grafting (1) and Double Grafting (2). uniform germination. The robots typically use the root pruning CUCURBIT GRAFTING 67

OCG method (Masanao and Hisaya, 1996; Suzuki et al., 1998; ide) to minimize possible microorganism damage (Hassell and Tiezhon and Liming, 2002; Lee and Oda, 2003). Kubota et al. Memmott, 2008). (2008) report a fully automated grafting robot for cucurbits with scion and rootstock feeders that pick, orient, and feed the scion K. Compatibility and the rootstock shoots to the grafting processor, performing As grafting is a composition of two different plants, some 750 grafts per hour with a 90% success rate. The new robot will beneficial or negative effects (besides the effect of soilborne be commercially available in a few years. pathogens), may arise after grafting. Graft incompatibility, as re- viewed by Andrews and Marquez (1993), is differentiated from I. Acclimatization graft failure that often results from environmental factors or lack Proper environmental conditions are important to facilitate of skill of the grafter. When grafting conditions have been suc- rootstock and scion union for some grafting methods. Some cessfully ensured, graft incompatibility could be attributed to nurseries have chambers that maintain temperature above 20◦C, ◦ other factors like failure of rootstock and scion to effect a strong or for the tongue approach method, at around 25 C, and low union, failure of the grafted plant to grow, or premature death light intensity for the first five to seven days. Relative humidity of either rootstock or scion after grafting. Also, physiological should be maintained between 85% to 100% (Miguel, 1997). incompatibility may occur due to lack of cellular recognition, Most nurseries acclimatize grafted plants in small plastic tun- wounding responses, presence of growth regulators, or incom- nels inside greenhouses where it is possible to maintain a high patibility toxins. relative humidity. Three to eight days after grafting, plants are Incompatibility induces undergrowth or overgrowth of scion acclimated to the natural conditions of the greenhouse by slowly (Figure 6), which can lead to decreased water and nutrient flow dropping humidity (Miguel, 1997; Lee and Oda, 2003; Hassell through the graft union and cause wilting of the plant. Generally, and Memmott, 2008). grafting compatibility is related to taxonomic affinity but there are significant exceptions. For example, luffa and melon have J. Production of Rootstock and Scion higher compatibility with netted melon (Cucumis melo var. retic- Cucurbits are usually grafted after the first true leaf appears, ulatus) compared to Chinese pumpkin (Cucurbita moschata) but before it is fully developed in both the rootstock and scion and wax gourd (Wei et al., 2006). Grafting incompatibility usu- seedlings. This means that planting dates must be optimized ally occurs at early stages as vascular connections are forming, for both the scion and the rootstock. Uniformity in both ger- but incompatibility can appear as late as the fruiting stage, when mination and growth of the rootstock and scion are critical for a high demand for nutrients and water is placed on the plant. grafting survival. Optimum seedling age varies for species and Cucumber and trellised muskmelon plants grafted onto Cu- different grafting methods. Difficult seeds to germinate, such as curbita rootstocks may collapse even in disease-free soils. This triploid watermelon seeds, should be watered lightly and main- wilt was observed slightly more often in cucumber grafted onto tained around 30◦C for consistent germination rates (Hassell figleaf gourd (Yamamoto, 1979). This phenomenon appears dur- and Schulthesis, 2002). If seedlings are too young, they are too ing the harvest period and was a serious issue in the 1970s in delicate to handle during the grafting process, and if too old, Japan and Israel (Cohen et al., 2007; Sakata et al., 2008). In may cause unwanted meristematic regrowth of rootstock tissue the major watermelon production areas, a similar sudden wilt of (Hassell and Memmott, 2008). Some grafting facilities rinse leaf and stem occurred as early as the 1950s throughout Japan. the seedlings with clean water, treated with fungicides or disin- Wilting occurred from the fruiting stages until harvest (Tamada, fectant (e.g., Physan 20 or peroxyacetic acid/ hydrogen perox- 1989). It seems that this is a physiological disorder caused by Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008

FIG. 6. Grafting compatibility between scion and rootstock. 68 A. R. DAVIS ET AL.

an imbalance of growth between the scion and the rootstock VI. CONCLUSION (Hamaya and Ogawa, 1973). Plants collapse because tylosis de- For decades, grafting has been successfully practiced in many velops leading to a disrupted water supply and a rapid drop in Asian countries, and is becoming increasingly popular in Eu- carbohydrates in shoots and roots as a result of a lack of solar ra- rope. Grafting is routinely employed for cucumbers, melons, diation or severe pruning (Takahashi and Shiraki, 1976; Kondo, oriental melons, squash, and watermelon. Identification of com- 1978). Fruit load subjects plants to a progressive increase of patible multi-disease-resistant rootstocks with tolerance to abi- water stress (Pivonia et al., 2002). Trellised grafted plants with otic stresses is a basic requirement for continued success. Ad- high fruit load cannot always keep up with the water demand ditionally, the availability of efficient grafting machines, and during hot periods. These plants are exposed to solar irradia- grafting robots will encourage cultivation of grafted cucurbits tion from all directions, whereas prostrate plants are irradiated worldwide (Lee and Oda, 2003). Automatic grafting machines only in their upper canopy (Cohen et al., 2007). To avoid this can increase grafting speed and increase the survival rate of physiological sudden wilt, the promotion of root development grafted plants (Gu, 2006). They may also increase grafted cu- and improved watering management is important. curbit crop production, and in turn, increase yield, and decrease Watermelons do not have compatibility problems with the chemical usage. usual rootstocks, mainly squash interspecific hybrids and Citrul- The low rate of grafting success results in high costs, reducing lus spp. (Miguel, 2004). However, problems have been reported the appeal of grafting in developed countries. Increased graft- with some rootstocks of Cucurbita moschata (Miguel, 1997) ing success requires close contact between scion and rootstock and burr cucumber (Miguel et al., 2005). Yetisir and Sari (2003) vascular bundles, rootstock and scion compatibility, and proper tested 10 rootstocks (Cucurbita moschata, Cucurbita maxima, environmental conditions to facilitate rootstock and scion union. bottle gourd, and a squash interspecific hybrid). They found that Grafted plants with a good rootstock / scion combination have the watermelon scion had a higher survival rate (95%) on bottle disease resistance, better abiotic stress tolerance, and higher gourd type rootstock than on the Cucurbita spp. rootstock (65%). yield. Unfortunately, the range of commercial rootstocks is lim- In melon, the cultivars of Spanish types (Cucumis melo ited, and the effect of unexplored rootstocks on fruit quality is var.saccharinus)have serious compatibility problems with the still not clear. squash interspecific hybrids (Miguel, 2004). However, the Several problems commonly associated with grafting have ‘Galia’ and Cantaloupe types, and some Cucumis melo var. flex- been reported such as: a) additional cost for rootstock seeds; uosus (Miguel, 2004), have no compatibility problems with the b) labor for grafting and seedling maintenance; c) inadequate squash interspecific hybrids. Morra (1997) demonstrated the low experience and technique for grafting and cultivation of grafted affinity of melon with L. siceraria, Cucurbita ficifolia, and Cu- plants; and d) physiological disorders associated with grafting curbita moschata but had good affinity with squash interspecific (Lee, 1994). Despite these problems, enormous benefits are real- hybrids and Cucumis melo. ized from grafting, namely: a) avoidance of soilborne diseases; Cucumber adapts well to grafting and has few compatibility b) added income from increased yield and premium price from problems with the usual rootstocks (Hoyos, 2001). Oda et al. off-season production; c) lower cost of fertilizers and irrigation (1993) performed experiments with horizontal grafting of cu- water due to the rootstocks extensive root systems; d) extended cumber seedlings onto Cucurbita spp. rootstocks. Along with harvest periods; e) avoidance of soil salinity; f) reduced cost for Yetisir and Sari (2004), they demonstrated that the survival rate soil fumigation; and g) a means to achieve organic vegetable wasinversely correlated with difference in the scion and root- production without fumigation (Lee and Oda, 2003). Further re- stock hypocotyl diameters. The number of vascular bundles did search needs to focus on rootstock development, more efficient not significantly affect survival rate, but did positively affect

Downloaded By: [USDA National Agricultural Library] At: 11:18 13 August 2008 grafting robots, and development of acclimatization facilities. the growth rate of grafted watermelon plants—in general, bot- This research should considerably reduce the cost of grafted tle gourd type rootstocks had a higher survival rate than other seedling production in the future. rootstocks. However, results from Edelstein et al. (2004) do not concur. Their studies showed that stem diameter and number of rootstock vascular bundles did not correlate with melon scion ACKNOWLEDGEMENTS fresh plant weight with 22 Cucurbita spp. rootstocks. We would like to thank Amy Helms, Antoine Bastien van Most cucurbit scions can be grafted onto several rootstock der Meer, Jim McCreight, Yun-Chan Huh, and Jung-Myung species and incompatibility can be circumvented by using appro- Lee for valuable additional information and support. We also priate grafting methods and growing environments (Ko, 1999). thank Richard Hassell and Amnon Levi for critical reviews of Rojas and Rivero (2001) showed that grafting method and vari- the manuscript. ety used signiﬁcantly affected graft survivability, but scion age (one to four weeks) did not. Moreover, Tamada (1969) pointed REFERENCES out that speciﬁc accessions and seed lots should be used con- Ahn, S. J., Im, Y.J., Chung, G. C., Cho, B. H., and Suh, S. R. 1999. Physiological sistently, as compatibility of each accession and lot differ, even responses of grafted-cucumber leaves and rootstock roots affected by low root within cultivars. temperature. Scientia Hort. 81: 397–408. CUCURBIT GRAFTING 69

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